Hostname: page-component-5c6d5d7d68-lvtdw Total loading time: 0 Render date: 2024-08-16T10:23:26.987Z Has data issue: false hasContentIssue false
  • English
  • Français

The sarcoplasmic Ca2+-ATPase: design of a perfect chemi-osmotic pump

Published online by Cambridge University Press:  01 September 2010

Jesper V. Møller ,
Claus Olesen ,
Anne-Marie L. Winther  and
Poul Nissen
Jesper V. Møller*
Affiliation:
Centre for Membrane Pumps in Cells and Disease – PUMPKIN, Danish National Research Foundation, Denmark Department of Physiology and Biophysics, Aarhus University, Ole Worms Alle 6, 1180, DK-8000 Aarhus C, Denmark
Claus Olesen*
Affiliation:
Centre for Membrane Pumps in Cells and Disease – PUMPKIN, Danish National Research Foundation, Denmark Department of Physiology and Biophysics, Aarhus University, Ole Worms Alle 6, 1180, DK-8000 Aarhus C, Denmark
Anne-Marie L. Winther
Affiliation:
Centre for Membrane Pumps in Cells and Disease – PUMPKIN, Danish National Research Foundation, Denmark Department of Molecular Biology, Aarhus University, Gustav Wieds Vej 10C, DK-8000 Aarhus C, Denmark
Poul Nissen
Affiliation:
Centre for Membrane Pumps in Cells and Disease – PUMPKIN, Danish National Research Foundation, Denmark Department of Molecular Biology, Aarhus University, Gustav Wieds Vej 10C, DK-8000 Aarhus C, Denmark
*
*Authors for correspondence: Jesper V. Møller and Claus Olesen. Email: jvm@biophys.au.dk and co@biophys.au.dk
*Authors for correspondence: Jesper V. Møller and Claus Olesen. Email: jvm@biophys.au.dk and co@biophys.au.dk
Get access Rights & Permissions [Opens in a new window]

Abstract

The sarcoplasmic (SERCA 1a) Ca2+-ATPase is a membrane protein abundantly present in skeletal mucles where it functions as an indispensable component of the excitation–contraction coupling, being at the expense of ATP hydrolysis involved in Ca2+/H+ exchange with a high thermodynamic efficiency across the sarcoplasmic reticulum membrane. The transporter serves as a prototype of a whole family of cation transporters, the P-type ATPases, which in addition to Ca2+ transporting proteins count Na+, K+-ATPase and H+, K+-, proton- and heavy metal transporting ATPases as prominent members. The ability in recent years to produce and analyze at atomic (2·3–3 Å) resolution 3D-crystals of Ca2+-transport intermediates of SERCA 1a has meant a breakthrough in our understanding of the structural aspects of the transport mechanism. We describe here the detailed construction of the ATPase in terms of one membraneous and three cytosolic domains held together by a central core that mediates coupling between Ca2+-transport and ATP hydrolysis. During turnover, the pump is present in two different conformational states, E1 and E2, with a preference for the binding of Ca2+ and H+, respectively. We discuss how phosphorylated and non-phosphorylated forms of these conformational states with cytosolic, occluded or luminally exposed cation-binding sites are able to convert the chemical energy derived from ATP hydrolysis into an electrochemical gradient of Ca2+ across the sarcoplasmic reticulum membrane. In conjunction with these basic reactions which serve as a structural framework for the transport function of other P-type ATPases as well, we also review the role of the lipid phase and the regulatory and thermodynamic aspects of the transport mechanism.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 43 , Issue 4 , November 2010 , pp. 501 - 566
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

7. References

Abrahams, J. P., Leslie, A. G., Lutter, R. & Walker, J. E. (1994). Structure at 2·8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628.CrossRefGoogle ScholarPubMed
Abu-Abed, M., Mal, T. K., Kainosho, M., Maclennan, D. H. & Ikura, M. (2002). Characterization of the ATP-binding domain of the sarco(endo)plasmic reticulum Ca2+-ATPase: probing nucleotide binding by multidimensional NMR. Biochemistry 41, 1156–1164.CrossRefGoogle ScholarPubMed
Accardi, A. & Miller, C. (2004). Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels. Nature 427, 803–807.CrossRefGoogle ScholarPubMed
Andersen, J. P. (1995a). Dissection of the functional domains of the sarcoplasmic reticulum Ca2+-ATPase by site-directed mutagenesis. Bioscience Reports 15, 243–261.CrossRefGoogle ScholarPubMed
Andersen, J. P. (1995b). Functional consequences of alterations to amino acids at the M5S5 boundary of the Ca2+-ATPase of sarcoplasmic reticulum. Mutation Tyr763–>Gly uncouples ATP hydrolysis from Ca2+ transport. Journal of Biological Chemistry 270, 908–914.CrossRefGoogle ScholarPubMed
Andersen, J. P., Fellmann, P., Moller, J. V. & Devaux, P. F. (1981). Immobilization of a spin-labeled fatty acid chain covalently attached to Ca2+-ATPase from sarcoplasmic reticulum suggests an oligomeric structure. Biochemistry 20, 4928–4936.CrossRefGoogle ScholarPubMed
Andersen, J. P., Jorgensen, P. L. & Moller, J. V. (1985a). Direct demonstration of structural changes in soluble, monomeric Ca2+-ATPase associated with Ca2+ release during the transport cycle. Proceedings of the National Academy of Sciences USA 82, 4573–4577.CrossRefGoogle ScholarPubMed
Andersen, J. P., Lassen, K. & Moller, J. V. (1985b). Changes in Ca2+ affinity related to conformational transitions in the phosphorylated state of soluble monomeric Ca2+-ATPase from sarcoplasmic reticulum. Journal of Biological Chemistry 260, 371–380.CrossRefGoogle ScholarPubMed
Andersen, J. P., Le Maire, M., Kragh-Hansen, U., Champeil, P. & Moller, J. V. (1983). Perturbation of the structure and function of a membranous Ca2+-ATPase by non-solubilizing concentrations of a non-ionic detergent. European Journal of Biochemistry 134, 205–214.CrossRefGoogle ScholarPubMed
Andersen, J. P., Vilsen, B., Nielsen, H. & Moller, J. V. (1986). Characterization of detergent-solubilized sarcoplasmic reticulum Ca2+-ATPase by high-performance liquid chromatography. Biochemistry 25, 6439–6447.CrossRefGoogle ScholarPubMed
Andersson, J., Hauser, K., Karjalainen, E. L. & Barth, A. (2008). Protonation and hydrogen bonding of Ca2+ site residues in the E2P phosphoenzyme intermediate of sarcoplasmic reticulum Ca2+-ATPase studied by a combination of infrared spectroscopy and electrostatic calculations. Biophysical Journal 94, 600–611.CrossRefGoogle ScholarPubMed
Anthonisen, A. N., Clausen, J. D. & Andersen, J. P. (2006). Mutational analysis of the conserved TGES loop of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 281, 31572–31582.CrossRefGoogle ScholarPubMed
Antonny, B. & Chabre, M. (1992). Characterization of the aluminum and beryllium fluoride species which activate transducin. Analysis of the binding and dissociation kinetics. Journal of Biological Chemistry 267, 6710–6718.CrossRefGoogle ScholarPubMed
Aravind, L., Galperin, M. Y. & Koonin, E. V. (1998). The catalytic domain of the P-type ATPase has the haloacid dehalogenase fold. Trends in Biochemical Sciences 23, 127–129.CrossRefGoogle ScholarPubMed
Asahi, M., Kurzydlowski, K., Tada, M. & Maclennan, D. H. (2002). Sarcolipin inhibits polymerization of phospholamban to induce superinhibition of sarco(endo)plasmic reticulum Ca2+-ATPases (SERCAs). Journal of Biological Chemistry 277, 26725–26728.CrossRefGoogle ScholarPubMed
Asahi, M., Sugita, Y., Kurzydlowski, K., De Leon, S., Tada, M., Toyoshima, C. & Maclennan, D. H. (2003). Sarcolipin regulates sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) by binding to transmembrane helices alone or in association with phospholamban. Proceedings of the National Academy of Sciences USA 100, 5040–5045.CrossRefGoogle ScholarPubMed
Axelsen, K. B. & Palmgren, M. G. (1998). Evolution of substrate specificities in the P-type ATPase superfamily. Journal of Molecular Evolution 46, 84–101.CrossRefGoogle ScholarPubMed
Barata, H. & De Meis, L. (2002). Uncoupled ATP hydrolysis and thermogenic activity of the sarcoplasmic reticulum Ca2+-ATPase: coupling effects of dimethyl sulfoxide and low temperature. Journal of Biological Chemistry 277, 16868–16872.CrossRefGoogle ScholarPubMed
Bellsolell, L., Prieto, J., Serrano, L. & Coll, M. (1994). Magnesium binding to the bacterial chemotaxis protein CheY results in large conformational changes involving its functional surface. Journal of Molecular Biology 238, 489–495.CrossRefGoogle Scholar
Bigelow, D. J. & Inesi, G. (1992). Contributions of chemical derivatization and spectroscopic studies to the characterization of the Ca2+ transport ATPase of sarcoplasmic reticulum. Biochimica et Biophysica Acta 1113, 323–338.CrossRefGoogle Scholar
Bishop, J. E. & Al-Shawi, M. K. (1988). Inhibition of sarcoplasmic reticulum Ca2+-ATPase by Mg2+ at high pH. Journal of Biological Chemistry 263, 1886–1892.CrossRefGoogle ScholarPubMed
Brandl, C. J., Green, N. M., Korczak, B. & Maclennan, D. H. (1986). Two Ca2+ ATPase genes: homologies and mechanistic implications of deduced amino acid sequences. Cell 44, 597–607.CrossRefGoogle ScholarPubMed
Carafoli, E. (2002). Calcium signaling: a tale for all seasons. Proceedings of the National Academy of Sciences USA 99, 1115–1122.CrossRefGoogle ScholarPubMed
Castellani, L., Hardwicke, P. M. & Vibert, P. (1985). Dimer ribbons in the three-dimensional structure of sarcoplasmic reticulum. Journal of Molecular Biology 185, 579–594.CrossRefGoogle ScholarPubMed
Chabre, M. (1990). Aluminofluoride and beryllofluoride complexes: a new phosphate analogs in enzymology. Trends in Biochemical Sciences 15, 6–10.CrossRefGoogle ScholarPubMed
Champeil, P., Le Maire, M., Andersen, J. P., Guillain, F., Gingold, M., Lund, S. & Moller, J. V. (1986). Kinetic characterization of the normal and detergent-perturbed reaction cycles of the sarcoplasmic reticulum calcium pump. Rate-limiting step(s) under different conditions. Journal of Biological Chemistry 261, 16372–16384.CrossRefGoogle ScholarPubMed
Champeil, P., Menguy, T., Soulie, S., Juul, B., De Gracia, A. G., Rusconi, F., Falson, P., Denoroy, L., Henao, F., Le Maire, M. & Moller, J. V. (1998). Characterization of a protease-resistant domain of the cytosolic portion of sarcoplasmic reticulum Ca2+-ATPase. Nucleotide- and metal-binding sites. Journal of Biological Chemistry 273, 6619–6631.CrossRefGoogle ScholarPubMed
Champeil, P., Riollet, S., Orlowski, S., Guillain, F., Seebregts, C. J. & Mcintosh, D. B. (1988). ATP regulation of sarcoplasmic reticulum Ca2+-ATPase. Metal-free ATP and 8-bromo-ATP bind with high affinity to the catalytic site of phosphorylated ATPase and accelerate dephosphorylation. Journal of Biological Chemistry 263, 12288–12294.CrossRefGoogle Scholar
Cheong, G. W., Young, H. S., Ogawa, H., Toyoshima, C. & Stokes, D. L. (1996). Lamellar stacking in three-dimensional crystals of Ca2+-ATPase from sarcoplasmic reticulum. Biophysical Journal 70, 1689–1699.CrossRefGoogle ScholarPubMed
Clausen, J. D. & Andersen, J. P. (2003). Roles of Leu249, Lys252, and Leu253 in membrane segment M3 of sarcoplasmic reticulum Ca2+-ATPase in control of Ca2+ migration and long-range intramolecular communication. Biochemistry 42, 2585–2594.CrossRefGoogle ScholarPubMed
Clausen, J. D. & Andersen, J. P. (2004). Functional consequences of alterations to Thr247, Pro248, Glu340, Asp813, Arg819, and Arg822 at the interfaces between domain P, M3, and L6–7 of sarcoplasmic reticulum Ca2+-ATPase. Roles in Ca2+ interaction and phosphoenzyme processing. Journal of Biological Chemistry 279, 54426–54437.CrossRefGoogle ScholarPubMed
Clausen, J. D., Mcintosh, D. B., Anthonisen, A. N., Woolley, D. G., Vilsen, B. & Andersen, J. P. (2007). ATP-binding modes and functionally important interdomain bonds of sarcoplasmic reticulum Ca2+-ATPase revealed by mutation of glycine 438, glutamate 439, and arginine 678. Journal of Biological Chemistry 282, 20686–20697.CrossRefGoogle ScholarPubMed
Clausen, J. D., Mcintosh, D. B., Vilsen, B., Woolley, D. G. & Andersen, J. P. (2003). Importance of conserved N-domain residues Thr441, Glu442, Lys515, Arg560, and Leu562 of sarcoplasmic reticulum Ca2+-ATPase for MgATP binding and subsequent catalytic steps. Plasticity of the nucleotide-binding site. Journal of Biological Chemistry 278, 20245–20258.CrossRefGoogle ScholarPubMed
Clausen, J. D., Mcintosh, D. B., Woolley, D. G. & Andersen, J. P. (2001). Importance of Thr-353 of the conserved phosphorylation loop of the sarcoplasmic reticulum Ca2+-ATPase in MgATP binding and catalytic activity. Journal of Biological Chemistry 276, 35741–35750.CrossRefGoogle ScholarPubMed
Clausen, J. D., Mcintosh, D. B., Woolley, D. G. & Andersen, J. P. (2008). Critical interaction of actuator domain residues arginine 174, isoleucine 188, and lysine 205 with modulatory nucleotide in sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 283, 35703–35714.CrossRefGoogle ScholarPubMed
Clausen, J. D., Vilsen, B., Mcintosh, D. B., Einholm, A. P. & Andersen, J. P. (2004). Glutamate-183 in the conserved TGES motif of domain A of sarcoplasmic reticulum Ca2+-ATPase assists in catalysis of E2/E2P partial reactions. Proceedings of the National Academy of Sciences USA 101, 2776–2781.CrossRefGoogle Scholar
Coan, C., Ji, J. Y. & Amaral, J. A. (1994). Ca2+ binding to occluded sites in the CrATP-ATPase complex of sarcoplasmic reticulum: evidence for two independent high-affinity sites. Biochemistry 33, 3722–3731.CrossRefGoogle ScholarPubMed
Collet, J. F., Gerin, I., Rider, M. H., Veiga-Da-cunha, M. & Van Schaftingen, E. (1997). Human L-3-phosphoserine phosphatase: sequence, expression and evidence for a phosphoenzyme intermediate. FEBS Letters 408, 281–284.CrossRefGoogle ScholarPubMed
Cornelius, F. & Moller, J. V. (1991). Electrogenic pump current of sarcoplasmic reticulum Ca2+-ATPase reconstituted at high lipid/protein ratio. FEBS Letters 284, 46–50.CrossRefGoogle ScholarPubMed
Daiho, T., Yamasaki, K., Danko, S. & Suzuki, H. (2007). Critical role of Glu40-Ser48 loop linking actuator domain and 1st transmembrane helix of Ca2+-ATPase in Ca2+ deocclusion and release from ADP-insensitive phosphoenzyme. Journal of Biological Chemistry 282, 34429–34447.CrossRefGoogle Scholar
Daiho, T., Yamasaki, K., Wang, G., Danko, S., Iizuka, H. & Suzuki, H. (2003). Deletions of any single residues in Glu40-Ser48 loop connecting a domain and the first transmembrane helix of sarcoplasmic reticulum Ca2+-ATPase result in almost complete inhibition of conformational transition and hydrolysis of phosphoenzyme intermediate. Journal of Biological Chemistry 278, 39197–39204.CrossRefGoogle ScholarPubMed
Dalton, K. A., Pilot, J. D., Mall, S., East, J. M. & Lee, A. G. (1999). Anionic phospholipids decrease the rate of slippage on the Ca2+-ATPase of sarcoplasmic reticulum. Biochemical Journal 342, 431–438.CrossRefGoogle ScholarPubMed
Danko, S., Daiho, T., Yamasaki, K., Liu, X. & Suzuki, H. (2009). Formation of the stable structural analog of ADP-sensitive phosphoenzyme of Ca2+-ATPase with occluded Ca2+ by beryllium fluoride: structural changes during phosphorylation and isomerization. Journal of Biological Chemistry 284, 22722–22735.CrossRefGoogle ScholarPubMed
Danko, S., Yamasaki, K., Daiho, T. & Suzuki, H. (2004). Distinct natures of beryllium fluoride-bound, aluminum fluoride-bound, and magnesium fluoride-bound stable analogues of an ADP-insensitive phosphoenzyme intermediate of sarcoplasmic reticulum Ca2+-ATPase: changes in catalytic and transport sites during phosphoenzyme hydrolysis. Journal of Biological Chemistry 279, 14991–14998.CrossRefGoogle ScholarPubMed
Dawson, R. J. & Locher, K. P. (2006). Structure of a bacterial multidrug ABC transporter. Nature 443, 180–185.CrossRefGoogle ScholarPubMed
De Foresta, B., Henao, F. & Champeil, P. (1992). Kinetic characterization of the perturbation by dodecylmaltoside of sarcoplasmic reticulum Ca2+-ATPase. European Journal of Biochemistry 209, 1023–1034.CrossRefGoogle Scholar
De Foresta, B., Henao, F. & Champeil, P. (1994). Cancellation of the cooperativity of Ca2+ binding to sarcoplasmic reticulum Ca2+-ATPase by the non-ionic detergent dodecylmaltoside. European Journal of Biochemistry 223, 359–369.CrossRefGoogle ScholarPubMed
De Foresta, B., Legros, N., Plusquellec, D., Le Maire, M. & Champeil, P. (1996). Brominated detergents as tools to study protein-detergent interactions. European Journal of Biochemistry 241, 343–354.CrossRefGoogle ScholarPubMed
De Meis, L. (1981). In The Sarcoplasmic Reticulum: Transport and Energy Transduction (ed. Bittar, J.). New York:Wiley.Google Scholar
De Meis, L., Arruda, A. P. & Carvalho, D. P. (2005). Role of sarco/endoplasmic reticulum Ca2+-ATPase in thermogenesis. Bioscience Reports 25, 181–190.CrossRefGoogle ScholarPubMed
De Meis, L. & Vianna, A. L. (1979). Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annual Review of Biochemistry 48, 275–292.CrossRefGoogle ScholarPubMed
Deamer, D. W. & Baskin, R. J. (1969). Ultrastructure of sarcoplasmic reticulum preparations. Journal of Cell Biology 42, 296–307.CrossRefGoogle ScholarPubMed
Denmeade, S. R. & Isaacs, J. T. (2005). The SERCA pump as a therapeutic target: making a “Smart Bomb” for prostate cancer. Cancer Biology and Therapy 4, 14–23.CrossRefGoogle ScholarPubMed
Denmeade, S. R., Jakobsen, C. M., Janssen, S., Khan, S. R., Garrett, E. S., Lilja, H., Christensen, S. B. & Isaacs, J. T. (2003). Prostate-specific antigen-activated thapsigargin prodrug as targeted therapy for prostate cancer. Journal of the National Cancer Institute 95, 990–1000.CrossRefGoogle ScholarPubMed
Ding, J., Starling, A. P., East, J. M. & Lee, A. G. (1994). Binding sites for cholesterol on Ca2+-ATPase studied by using a cholesterol-containing phospholipid. Biochemistry 33, 4974–4979.CrossRefGoogle ScholarPubMed
Dupont, Y. (1982). Low-temperature studies of the sarcoplasmic reticulum calcium pump. Mechanisms of calcium binding. Biochimica et Biophysica Acta 688, 75–87.Google Scholar
Dupont, Y. & Hasselbach, W. (1973). Structural changes in sarcoplasmic reticulum membrane induced by SH reagents. Nature New Biology 246, 41–44.CrossRefGoogle ScholarPubMed
Dupont, Y. & Pougeois, R. (1983). Evaluation of H2O activity in the free or phosphorylated catalytic site of Ca2+-ATPase. FEBS Letters 156, 93–98.CrossRefGoogle ScholarPubMed
Dux, L. & Martonosi, A. (1983). Two-dimensional arrays of proteins in sarcoplasmic reticulum and purified Ca2+-ATPase vesicles treated with vanadate. Journal of Biological Chemistry 258, 2599–2603.CrossRefGoogle ScholarPubMed
Dux, L., Pikula, S., Mullner, N. & Martonosi, A. (1987). Crystallization of Ca2+-ATPase in detergent-solubilized sarcoplasmic reticulum. Journal of Biological Chemistry 262, 6439–6442.CrossRefGoogle ScholarPubMed
East, J. M. & Lee, A. G. (1982). Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid. Biochemistry 21, 4144–4151.CrossRefGoogle ScholarPubMed
Einholm, A. P., Andersen, J. P. & Vilsen, B. (2007). Roles of transmembrane segment M1 of Na+, K+-ATPase and Ca2-ATPase, the gatekeeper and the pivot. Journal of Bioenergetics and Biomembranes 39, 357–366.CrossRefGoogle ScholarPubMed
Endo, M. (1977). Calcium release from the sarcoplasmic reticulum. Physiological Reviews 57, 71–108.Google Scholar
Falson, P., Menguy, T., Corre, F., Bouneau, L., De Gracia, A. G., Soulie, S., Centeno, F., Moller, J. V., Champeil, P. & Le Maire, M. (1997). The cytoplasmic loop between putative transmembrane segments 6 and 7 in sarcoplasmic reticulum Ca2+-ATPase binds Ca2+ and is functionally important. Journal of Biological Chemistry 272, 17258–17262.CrossRefGoogle ScholarPubMed
Feher, J. J. & Briggs, F. N. (1983). Determinants of calcium loading at steady state in sarcoplasmic reticulum. Biochimica et Biophysica Acta 727, 389–402.CrossRefGoogle Scholar
Forge, V., Mintz, E. & Guillain, F. (1993). Ca2+ binding to sarcoplasmic reticulum ATPase revisited. II. Equilibrium and kinetic evidence for a two-route mechanism. Journal of Biological Chemistry 268, 10961–10968.CrossRefGoogle ScholarPubMed
Gadsby, D. C. (2009). Ion channels versus ion pumps: the principal difference, in principle. Nature Reviews Molecular Cell Biology 10, 344–352.CrossRefGoogle ScholarPubMed
Gadsby, D. C., Rakowski, R. F. & De Weer, P. (1993). Extracellular access to the Na, K pump: pathway similar to ion channel. Science 260, 100–103.CrossRefGoogle Scholar
Garnett, C., Sumbilla, C., Belda, F. F., Chen, L. & Inesi, G. (1996). Energy transduction and kinetic regulation by the peptide segment connecting phosphorylation and cation binding domains in transport ATPases. Biochemistry 35, 11019–11025.CrossRefGoogle ScholarPubMed
Gerdes, U. & Møller, J. V. (1983). The Ca2+ permeability of sarcoplasmic reticulum vesicles. II. Ca2+ efflux in the energized state of the calcium pump. Biochimica et Biophysica Acta 734, 191–200.CrossRefGoogle ScholarPubMed
Greaser, M. L., Cassens, R. G., Hoekstra, W. G. & Briskey, E. J. (1969). Effects of diethyl ether and thymol on the ultrastructural and biochemical properties of purified sarcoplasmic reticulum fragments from skeletal muscle. Biochimica et Biophysica Acta 193, 73–81.CrossRefGoogle ScholarPubMed
Green, N. M. & Stokes, D. L. (1992). Structural modelling of P-type ion pumps. Acta Physiologica Scandinavica 607, 59–68.Google Scholar
Håkansson, K. O. (2003). The crystallographic structure of Na, K-ATPase N-domain at 2·6A resolution. Journal of Molecular Biology 332, 1175–1182.CrossRefGoogle ScholarPubMed
Hasselbach, W. & Elfvin, L. G. (1967). Structural and chemical asymmetry of the calcium-transporting membranes of the sarcotubular system as revealed by electron microscopy. Journal of Ultrastructure Research 17, 598–622.CrossRefGoogle ScholarPubMed
Hasselbach, W. & Oetliker, H. (1983). Energetics and electrogenicity of the sarcoplasmic reticulum calcium pump. Annual Review of Physiology 45, 325–339.CrossRefGoogle ScholarPubMed
Hauser, K. & Barth, A. (2007). Side-chain protonation and mobility in the sarcoplasmic reticulum Ca2+-ATPase: implications for proton countertransport and Ca2+ release. Biophysical Journal 93, 3259–3270.CrossRefGoogle ScholarPubMed
Heegaard, C. W., Le Maire, M., Gulik-Krzywicki, T. & Moller, J. V. (1990). Monomeric state and Ca2+ transport by sarcoplasmic reticulum Ca2+-ATPase, reconstituted with an excess of phospholipid. Journal of Biological Chemistry 265, 12020–12028.CrossRefGoogle ScholarPubMed
Herbette, L., Defoor, P., Fleischer, S., Pascolini, D., Scarpa, A. & Blasie, J. K. (1985). The separate profile structures of the functional calcium pump protein and the phospholipid bilayer within isolated sarcoplasmic reticulum membranes determined by X-ray and neutron diffraction. Biochimica et Biophysica Acta 817, 103–122.Google Scholar
Hesketh, T. R., Smith, G. A., Houslay, M. D., Mcgill, K. A., Birdsall, N. J., Metcalfe, J. C. & Warren, G. B. (1976). Annular lipids determine the ATPase activity of a calcium transport protein complexed with dipalmitoyllecithin. Biochemistry 15, 4145–4151.CrossRefGoogle ScholarPubMed
Hilge, M., Siegal, G., Vuister, G. W., Guntert, P., Gloor, S. M. & Abrahams, J. P. (2003). ATP-induced conformational changes of the nucleotide-binding domain of Na, K-ATPase . Nature Structural Biology 10, 468–474.CrossRefGoogle ScholarPubMed
Hinton, A., Bond, S. & Forgac, M. (2009). V-ATPase functions in normal and disease processes. Pflugers Arch 457, 589–598.CrossRefGoogle ScholarPubMed
Holdensen, A. N. & Andersen, J. P. (2009). The length of the A-M3 linker is a crucial determinant of the rate of the Ca2+ transport cycle of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 284, 12258–12265.Google Scholar
Hollenstein, K., Dawson, R. J. & Locher, K. P. (2007). Structure and mechanism of ABC transporter proteins. Current Opinion in Structural Biology 17, 412–418.CrossRefGoogle ScholarPubMed
Hua, S., Inesi, G., Nomura, H. & Toyoshima, C. (2002). Fe2+-catalyzed oxidation and cleavage of sarcoplasmic reticulum ATPase reveals Mg2+ and Mg2+-ATP sites. Biochemistry 41, 11405–11410.CrossRefGoogle Scholar
Hughes, E., Clayton, J. C., Kitmitto, A., Esmann, M. & Middleton, D. A. (2007). Solid-state NMR and functional measurements indicate that the conserved tyrosine residues of sarcolipin are involved directly in the inhibition of SERCA1. Journal of Biological Chemistry 282, 26603–26613.CrossRefGoogle ScholarPubMed
Ikemoto, N., Kitagawa, S., Nakamura, A. & Gergely, J. (1968). Electron microscopic investigations of actomyosin as a function of ionic strength. Journal of Cell Biology 39, 620–629.CrossRefGoogle ScholarPubMed
Imamura, Y. & Kawakita, M. (1989). Purification of limited tryptic fragments of Ca2+, Mg2+-adenosine triphosphatase of the sarcoplasmic reticulum and identification of conformation-sensitive cleavage sites. Journal of Biochemistry 105, 775–781.CrossRefGoogle ScholarPubMed
Inesi, G. & De Meis, L. (1989). Regulation of steady state filling in sarcoplasmic reticulum. Roles of back-inhibition, leakage, and slippage of the calcium pump. Journal of Biological Chemistry 264, 5929–5936.Google Scholar
Inesi, G., Kurzmack, M., Coan, C. & Lewis, D. E. (1980). Cooperative calcium binding and ATPase activation in sarcoplasmic reticulum vesicles. Journal of Biological Chemistry 255, 3025–3031.CrossRefGoogle ScholarPubMed
Inesi, G., Ma, H., Lewis, D. & Xu, C. (2004). Ca2+ occlusion and gating function of Glu309 in the ADP-fluoroaluminate analog of the Ca2+-ATPase phosphoenzyme intermediate. Journal of Biological Chemistry 279, 31629–31637.Google Scholar
James, P., Inui, M., Tada, M., Chiesi, M. & Carafoli, E. (1989). Nature and site of phospholamban regulation of the Ca2+ pump of sarcoplasmic reticulum. Nature 342, 90–92.Google Scholar
Jardetzky, O. (1966). Simple allosteric model for membrane pumps. Nature 211, 969–970.Google Scholar
Jensen, A. M., Sorensen, T. L., Olesen, C., Moller, J. V. & Nissen, P. (2006). Modulatory and catalytic modes of ATP binding by the calcium pump. EMBO Journal 25, 2305–2314.CrossRefGoogle ScholarPubMed
Jidenko, M., Nielsen, R. C., Sorensen, T. L., Moller, J. V., Le Maire, M., Nissen, P. & Jaxel, C. (2005). Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences USA 102, 11687–11691.CrossRefGoogle ScholarPubMed
Johannsson, A., Keightley, C. A., Smith, G. A., Richards, C. D., Hesketh, T. R. & Metcalfe, J. C. (1981). The effect of bilayer thickness and n-alkanes on the activity of the (Ca2++Mg2+)-dependent ATPase of sarcoplasmic reticulum. Journal of Biological Chemistry 256, 1643–1650.Google Scholar
Jorgensen, K. E., Lind, K. E., Roigaard-Petersen, H. & Moller, J. V. (1978). The functional unit of calcium-plus-magnesium-ion-dependent adenosine triphosphatase from sarcoplasmic reticulum. The aggregational state of the deoxycholate-solubilized protein in an enzymically active form. Biochemical Journal 169, 489–498.CrossRefGoogle Scholar
Jørgensen, P. L., Hakansson, K. O. & Karlish, S. J. (2003). Structure and mechanism of Na, K-ATPase: functional sites and their interactions. Annual Review of Physiology 65, 817–849.CrossRefGoogle ScholarPubMed
Junge, W., Sielaff, H. & Engelbrecht, S. (2009). Torque generation and elastic power transmission in the rotary F(O)F(1)-ATPase. Nature 459, 364–370.Google Scholar
Juul, B., Turc, H., Durand, M. L., Gomez De Gracia, A., Denoroy, L., Moller, J. V., Champeil, P. & Le Maire, M. (1995). Do transmembrane segments in proteolyzed sarcoplasmic reticulum Ca2+-ATPase retain their functional Ca2+ binding properties after removal of cytoplasmic fragments by proteinase K? Journal of Biological Chemistry 270, 20123–20134.CrossRefGoogle ScholarPubMed
Kabaleeswaran, V., Puri, N., Walker, J. E., Leslie, A. G. & Mueller, D. M. (2006). Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase. EMBO Journal 25, 5433–5442.CrossRefGoogle ScholarPubMed
Kagawa, Y. & Racker, E. (1966a). Partial resolution of the enzymes catalyzing oxidative phosphorylation. X. Correlation of morphology and function in submitochondrial particles. Journal of Biological Chemistry 241, 2475–2482.CrossRefGoogle ScholarPubMed
Kagawa, Y. & Racker, E. (1966b). Partial resolution of the enzymes catalyzing oxidative phosphorylation. IX. Reconstruction of oligomycin-sensitive adenosine triphosphatase. Journal of Biological Chemistry 241, 2467–2474.CrossRefGoogle ScholarPubMed
Karim, C. B., Marquardt, C. G., Stamm, J. D., Barany, G. & Thomas, D. D. (2000). Synthetic null-cysteine phospholamban analogue and the corresponding transmembrane domain inhibit the Ca-ATPase. Biochemistry 39, 10892–10897.CrossRefGoogle ScholarPubMed
Karjalainen, E. L., Hauser, K. & Barth, A. (2007). Proton paths in the sarcoplasmic reticulum Ca2+-ATPase. Biochimica et Biophysica Acta 1767, 1310–1318.Google Scholar
Khare, D., Oldham, M. L., Orelle, C., Davidson, A. L. & Chen, J. (2009). Alternating access in maltose transporter mediated by rigid-body rotations. Molecular Cell 33, 528–536.Google Scholar
Koonin, E. V. & Tatusov, R. L. (1994). Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. Journal of Biological Chemistry 244, 125–132.Google ScholarPubMed
Kühlbrandt, W. (2004). Biology, structure and mechanism of P-type ATPases. Nature Reviews Molecular Cell Biology 5, 282–295.CrossRefGoogle ScholarPubMed
Lacapere, J. J. & Guillain, F. (1993). The reaction mechanism of Ca2+-ATPase of sarcoplasmic reticulum. Direct measurement of the Mg.ATP dissociation constant gives similar values in the presence or absence of calcium. European Journal of Biochemistry 211, 117–126.CrossRefGoogle ScholarPubMed
Läuger, P. (1991). Electrogenic Pumps. Sunderland, MA: Sinauer Associates.Google Scholar
Laursen, M., Bublitz, M., Moncoq, K., Olesen, C., Møller, J. V., Young, H. S., Nissen, P. & Morth, J. P. (2009). Cyclopiazonic acid is complexed to a divalent metal ion when bound to the sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 284, 13513–13518.Google Scholar
Le Maire, M., Arnou, B., Olesen, C., Georgin, D., Ebel, C. & Møller, J. V. (2008). Gel chromatography and analytical ultracentrifugation to determine the extent of detergent binding and aggregation, and Stokes radius of membrane proteins using sarcoplasmic reticulum Ca2+-ATPase as an example. Nature Protocols 3, 1782–1795.CrossRefGoogle ScholarPubMed
Le Maire, M., Champeil, P. & Møller, J. V. (2000). Interaction of membrane proteins and lipids with solubilizing detergents. Biochimica et Biophysica Acta 1508, 86–111.CrossRefGoogle ScholarPubMed
Le Maire, M., Jorgensen, K. E., Roigaard-Petersen, H. & Møller, J. V. (1976). Properties of deoxycholate solubilized sarcoplasmic reticulum Ca2+-ATPase. Biochemistry 15, 5805–5812.CrossRefGoogle ScholarPubMed
Le Maire, M., Lund, S., Viel, A., Champeil, P. & Møller, J. V. (1990). Ca2+-induced conformational changes and location of Ca2+ transport sites in sarcoplasmic reticulum Ca2+-ATPase as detected by the use of proteolytic enzyme (V8). Journal of Biological Chemistry 265, 1111–1123.Google Scholar
Le Maire, M., Møller, J. V. & Tardieu, A. (1981). Shape and thermodynamic parameters of a Ca2+-dependent ATPase. A solution x-ray scattering and sedimentation equilibrium study. Journal of Molecular Biology 150, 273–296.Google Scholar
Lee, A. G. (1998). How lipids interact with an intrinsic membrane protein: the case of the calcium pump. Biochimica et Biophysica Acta 1376, 381–390.Google Scholar
Lee, A. G. (2003). Lipid-protein interactions in biological membranes: a structural perspective. Biochimica et Biophysica Acta 1612, 1–40.CrossRefGoogle ScholarPubMed
Lee, A. G. & East, J. M. (2001). What the structure of a calcium pump tells us about its mechanism. Biochemistry Journal 356, 665–683.Google Scholar
Lenoir, G., Picard, M., Gauron, C., Montigny, C., Le Marechal, P., Falson, P., Le Maire, M., Moller, J. V. & Champeil, P. (2004). Functional properties of sarcoplasmic reticulum Ca2+-ATPase after proteolytic cleavage at Leu119-Lys120, close to the A-domain. Journal of Biological Chemistry 279, 9156–9166.Google Scholar
Lepock, J. R., Rodahl, A. M., Zhang, C., Heynen, M. L., Waters, B. & Cheng, K. H. (1990). Thermal denaturation of the Ca2+-ATPase of sarcoplasmic reticulum reveals two thermodynamically independent domains. Biochemistry 29, 681–689.CrossRefGoogle ScholarPubMed
Levy, D., Seigneuret, M., Bluzat, A. & Rigaud, J. L. (1990). Evidence for proton countertransport by the sarcoplasmic reticulum Ca2+-ATPase during calcium transport in reconstituted proteoliposomes with low ionic permeability. Journal of Biological Chemistry 265, 19524–19534.CrossRefGoogle ScholarPubMed
Li, Y., Ge, M., Ciani, L., Kuriakose, G., Westover, E. J., Dura, M., Covey, D. F., Freed, J. H., Maxfield, F. R., Lytton, J. & Tabas, I. (2004). Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages. Journal of Biological Chemistry 279, 37030–37039.Google Scholar
Liu, M. & Barth, A. (2004). Phosphorylation of the sarcoplasmic reticulum Ca2+-ATPase from ATP and ATP analogs studied by infrared spectroscopy. Journal of Biological Chemistry 279, 49902–49909.Google Scholar
London, E. & Feigenson, G. W. (1981). Fluorescence quenching in model membranes. 2. Determination of local lipid environment of the calcium adenosinetriphosphatase from sarcoplasmic reticulum. Biochemistry 20, 1939–1948.Google Scholar
Long, S. B., Tao, X., Campbell, E. B. & Mackinnon, R. (2007). Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450, 376–382.CrossRefGoogle Scholar
Lund, S., Orlowski, S., De Foresta, B., Champeil, P., Le Maire, M. & Moller, J. V. (1989). Detergent structure and associated lipid as determinants in the stabilization of solubilized Ca2+-ATPase from sarcoplasmic reticulum. Journal of Biological Chemistry 264, 4907–4915.CrossRefGoogle ScholarPubMed
Lutsenko, S. & Kaplan, J. H. (1995). Organization of P-type ATPases: significance of structural diversity. Biochemistry 34, 15607–15613.Google Scholar
Maclennan, D. H., Asahi, M. & Tupling, A. R. (2003). The regulation of SERCA-type pumps by phospholamban and sarcolipin. Annals of the New York Academy of Sciences 986, 472–480.Google Scholar
Maclennan, D. H., Brandl, C. J., Korczak, B. & Green, N. M. (1985). Amino-acid sequence of a Ca2++Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature 316, 696–700.CrossRefGoogle ScholarPubMed
Maclennan, D. H. & Kranias, E. G. (2003). Phospholamban: a crucial regulator of cardiac contractility. Nature Reviews Molecular Cell Biology 4, 566–577.CrossRefGoogle ScholarPubMed
Maclennan, D. H., Rice, W. J. & Green, N. M. (1997). The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. Journal of Biological Chemistry 272, 28815–28818.Google Scholar
Maclennan, D. H., Yip, C. C., Iles, G. H., & Seeman, P. (1972). Isolation of sarcoplasmic reticulum proteins. Cold Spring Harbor Symposia on Quantitative Biology 37, 469–478.Google Scholar
Mahaney, J. E., Albers, R. W., Waggoner, J. R., Kutchai, H. C. & Froehlich, J. P. (2005). Intermolecular conformational coupling and free energy exchange enhance the catalytic efficiency of cardiac muscle SERCA2a following the relief of phospholamban inhibition. Biochemistry 44, 7713–7724.CrossRefGoogle ScholarPubMed
Mahaney, J. E., Thomas, D. D. & Froehlich, J. P. (2004). The time-dependent distribution of phosphorylated intermediates in native sarcoplasmic reticulum Ca2+-ATPase from skeletal muscle is not compatible with a linear kinetic model. Biochemistry 43, 4400–4416.Google Scholar
Mahmmoud, Y. A. (2008). Capsaicin stimulates uncoupled ATP hydrolysis by the sarcoplasmic reticulum calcium pump. Journal of Biological Chemistry 283, 21418–21426.Google Scholar
Mall, S., Broadbridge, R., Harrison, S. L., Gore, M. G., Lee, A. G. & East, J. M. (2006). The presence of sarcolipin results in increased heat production by Ca2+-ATPase. Journal of Biological Chemistry 281, 36597–36602.Google Scholar
Marchand, A., Lund Winther, A. M., Holm, P. J., Olesen, C., Montigny, C., Arnou, B., Champeil, P., Clausen, J. D., Vilsen, B., Andersen, J. P., Nissen, P., Jaxel, C., Moller, J. V. & Le Maire, M. (2008). Crystal structure of D351A and P312A mutant forms of the mammalian sarcoplasmic reticulum Ca2+-ATPase reveals key events in phosphorylation and Ca2+ release. Journal of Biological Chemistry 283, 14867–14882.Google Scholar
Marsh, D. & Horvath, L. I. (1998). Structure, dynamics and composition of the lipid-protein interface. Perspectives from spin-labelling. Biochimica et Biophysica Acta 1376, 267–296.Google Scholar
Marsh, D. & Pali, T. (2004). The protein-lipid interface: perspectives from magnetic resonance and crystal structures. Biochimica et Biophysica Acta 1666, 118–141.CrossRefGoogle ScholarPubMed
Mcintosh, D. B., Clausen, J. D., Woolley, D. G., Maclennan, D. H., Vilsen, B. & Andersen, J. P. (2004). Roles of conserved P domain residues and Mg2+ in ATP binding in the ground and Ca2+-activated states of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 279, 32515–32523.CrossRefGoogle ScholarPubMed
Mcintosh, D. B. & Ross, D. C. (1985). Role of phospholipid and protein-protein associations in activation and stabilization of soluble Ca2+-ATPase of sarcoplasmic reticulum. Biochemistry 24, 1244–1251.Google Scholar
Mcintosh, D. B. & Ross, D. C. (1988). Reaction cycle of solubilized monomeric Ca2+-ATPase of sarcoplasmic reticulum is the same as that of the membrane form. Journal of Biological Chemistry 263, 12220–12223.Google Scholar
Mcintosh, D. B., Woolley, D. G., Maclennan, D. H., Vilsen, B. & Andersen, J. P. (1999). Interaction of nucleotides with Asp(351) and the conserved phosphorylation loop of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 274, 25227–25236.Google Scholar
Menguy, T., Corre, F., Bouneau, L., Deschamps, S., Moller, J. V., Champeil, P., Le Maire, M. & Falson, P. (1998). The cytoplasmic loop located between transmembrane segments 6 and 7 controls activation by Ca2+ of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 273, 20134–20143.Google Scholar
Merino, J. M., Moller, J. V. & Gutierrez-Merino, C. (1994). Thermal unfolding of monomeric Ca(II), Mg(II)-ATPase from sarcoplasmic reticulum of rabbit skeletal muscle. FEBS Letters 343, 155–159.Google Scholar
Metcalfe, E. E., Zamoon, J., Thomas, D. D. & Veglia, G. (2004). H/N heteronuclear NMR spectroscopy shows four dynamic domains for phospholamban reconstituted in dodecylphosphocholine micelles. Biophysical Journal 87, 1205–1214.Google Scholar
Michel, H. (1990). Crystallization of Membrane Proteins. Boca Raton, FL: CRC Press.Google Scholar
Michelangeli, F., Grimes, E. A., East, J. M. & Lee, A. G. (1991). Effects of phospholipids on the function of (Ca2+-Mg2+)-ATPase. Biochemistry 30, 342–351.CrossRefGoogle ScholarPubMed
Mikkelsen, E. O., Thastrup, O. & Christensen, S. B. (1988). Effects of thapsigargin in isolated rat thoracic aorta. Pharmacology and Toxicology 62, 7–11.Google Scholar
Mintz, E. & Guillain, F. (1997). Ca2+ transport by the sarcoplasmic reticulum ATPase. Biochimica et Biophysica Acta 1318, 52–70.Google Scholar
Mitchinson, C., Wilderspin, A. F., Trinnaman, B. J. & Green, N. M. (1982). Identification of a labelled peptide after stoicheiometric reaction of fluorescein isothiocyanate with the Ca2+ -dependent adenosine triphosphatase of sarcoplasmic reticulum. FEBS Letters 146, 87–92.Google Scholar
Møller, J. & Falson, P. (2000). Na/K-ATPase and related ATPases. Excerpta Medica (eds. Taniguchi, K. & Kaya, S.), pp. 155–162. Amsterdam: Elsevier.Google Scholar
Møller, J. V., Andersen, J. P. & Le Maire, M. (1982). The sarcoplasmic reticulum Ca2+-ATPase. Molecular and Cellular Biochemistry 42, 83–107.CrossRefGoogle ScholarPubMed
Møller, J. V., Juul, B. & Le Maire, M. (1996). Structural organization, ion transport, and energy transduction of P-type ATPases. Biochimica et Biophysica Acta 1286, 1–51.Google Scholar
Møller, J. V., Lenoir, G., Marchand, C., Montigny, C., Le Maire, M., Toyoshima, C., Juul, B. S. & Champeil, P. (2002). Calcium transport by sarcoplasmic reticulum Ca2+-ATPase. Role of the A domain and its C-terminal link with the transmembrane region. Current Opinion in Structural Biology 277, 38647–38659.Google Scholar
Møller, J. V., Lind, K. E. & Andersen, J. P. (1980). Enzyme kinetics and substrate stabilization of detergent-solubilized and membraneous (Ca2++Mg2+)-activated ATPase from sarcoplasmic reticulum. Effect of protein-protein interactions. Journal of Biological Chemistry 255, 1912–1920.Google Scholar
Moller, J. V., Nissen, P., Sorensen, T. L. & Le Maire, M. (2005). Transport mechanism of the sarcoplasmic reticulum Ca2+ -ATPase pump. Current Opinion in Structural Biology 15, 387–393.Google Scholar
Møller, J. V., Olesen, C., Jensen, A. M. & Nissen, P. (2005). The structural basis for coupling of Ca2+ transport to ATP hydrolysis by the sarcoplasmic reticulum Ca2+-ATPase. Journal of Bioenergetics and Biomembranes 37, 359–364.Google Scholar
Moncoq, K., Trieber, C. A. & Young, H. S. (2007). The molecular basis for cyclopiazonic acid inhibition of the sarcoplasmic reticulum calcium pump. Journal of Biological Chemistry 282, 9748–9757.CrossRefGoogle ScholarPubMed
Montigny, C., Jaxel, C., Shainskaya, A., Vinh, J., Labas, V., Moller, J. V., Karlish, S. J. & Le Maire, M. (2004). Fe2+-catalyzed oxidative cleavages of Ca2+-ATPase reveal novel features of its pumping mechanism. Journal of Biological Chemistry 279, 43971–43981.Google Scholar
Morth, J. P., Pedersen, B. P., Toustrup-Jensen, M. S., Sorensen, T. L., Petersen, J., Andersen, J. P., Vilsen, B. & Nissen, P. (2007). Crystal structure of the sodium-potassium pump. Nature 450, 1043–1049.Google Scholar
Moutin, M. J., Rapin, C., Miras, R., Vincon, M., Dupont, Y. & Mcintosh, D. B. (1998). Autonomous folding of the recombinant large cytoplasmic loop of sarcoplasmic reticulum Ca2+-ATPase probed by affinity labeling and trypsin digestion. European Journal of Biochemistry 251, 682–690.Google Scholar
Nakamoto, R. K. & Inesi, G. (1984). Studies of the interactions of 2′,3′-O-(2,4,6-trinitrocyclohexyldienylidine)adenosine nucleotides with the sarcoplasmic reticulum (Ca2++Mg2+)-ATPase active site. Journal of Biological Chemistry 259, 2961–2970.Google Scholar
Nielsen, G., Malmendal, A., Meissner, A., Moller, J. V. & Nielsen, N. C. (2003). NMR studies of the fifth transmembrane segment of sarcoplasmic reticulum Ca2+-ATPase reveals a hinge close to the Ca2+-ligating residues. FEBS Letters 544, 50–56.Google Scholar
Nørby, J. G., Klodos, I. & Christiansen, N. O. (1983). Kinetics of Na-ATPase activity by the Na, K pump. Interactions of the phosphorylated intermediates with Na+, Tris+, and K+. Journal of General Physiology 82, 725–759.Google Scholar
Obara, K., Miyashita, N., Xu, C., Toyoshima, I., Sugita, Y., Inesi, G. & Toyoshima, C. (2005). Structural role of countertransport revealed in Ca2+ pump crystal structure in the absence of Ca2+. Proceedings of the National Academy of Sciences USA 102, 14489–14496.CrossRefGoogle ScholarPubMed
Odermatt, A., Becker, S., Khanna, V. K., Kurzydlowski, K., Leisner, E., Pette, D. & Maclennan, D. H. (1998). Sarcolipin regulates the activity of SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 273, 12360–12369.Google Scholar
Odermatt, A., Taschner, P. E., Scherer, S. W., Beatty, B., Khanna, V. K., Cornblath, D. R., Chaudhry, V., Yee, W. C., Schrank, B., Karpati, G., Breuning, M. H., Knoers, N. & Maclennan, D. H. (1997). Characterization of the gene encoding human sarcolipin (SLN), a proteolipid associated with SERCA1: absence of structural mutations in five patients with Brody disease. Genomics 45, 541–553.CrossRefGoogle ScholarPubMed
Ogawa, H., Stokes, D. L., Sasabe, H. & Toyoshima, C. (1998). Structure of the Ca2+ pump of sarcoplasmic reticulum: a view along the lipid bilayer at 9-A resolution. Biophysical Journal 75, 41–52.Google Scholar
Olesen, C., Picard, M., Winther, A. M., Gyrup, C., Morth, J. P., Oxvig, C., Møller, J. V. & Nissen, P. (2007). The structural basis of calcium transport by the calcium pump. Nature 450, 1036–1042.Google Scholar
Olesen, C., Sørensen, T. L., Nielsen, R. C., Møller, J. V. & Nissen, P. (2004). Dephosphorylation of the calcium pump coupled to counterion occlusion. Science 306, 2251–2255.Google Scholar
Orlowski, S. & Champeil, P. (1991a). The two calcium ions initially bound to nonphosphorylated sarcoplasmic reticulum Ca2+-ATPase can no longer be kinetically distinguished when they dissociate from phosphorylated ATPase toward the lumen. Biochemistry 30, 11331–11342.Google Scholar
Orlowski, S. & Champeil, P. (1991b). Kinetics of calcium dissociation from its high-affinity transport sites on sarcoplasmic reticulum ATPase. Biochemistry 30, 352–361.Google Scholar
Packer, L., Mehard, C. W., Meissner, G., Zahler, W. L. & Fleischer, S. (1974). The structural role of lipids in mitochondrial and sarcoplasmic reticulum membranes. Freeze-fracture electron microscopy studies. Biochimica et Biophysica Acta 363, 159–181.Google Scholar
Park, S., Ajtai, K. & Burghardt, T. P. (1999). Inhibition of myosin ATPase by metal fluoride complexes. Biochimica et Biophysica Acta 1430, 127–140.CrossRefGoogle ScholarPubMed
Patlak, C. S. (1957). Contributions to the theory of active transport: II. The gate type non-carrier mechanism and generalizations concerning tracer flow, efficiency, and measurement of energy expenditure. Bulletin of Mathematical Biophysics 19, 209–235.Google Scholar
Pedersen, B. P., Buch-Pedersen, M. J., Morth, J. P., Palmgren, M. G. & Nissen, P. (2007). Crystal structure of the plasma membrane proton pump. Nature 450, 1111–1114.Google Scholar
Pedersen, P. A., Rasmussen, J. H. & Jorgensen, P. L. (1996). Consequences of mutations to the phosphorylation site of the alpha-subunit of Na, K-ATPase for ATP binding and E1-E2 conformational equilibrium. Biochemistry 35, 16085–16093.Google Scholar
Pedersen, P. L. (2007). Transport ATPases into the year 2008: a brief overview related to types, structures, functions and roles in health and disease. Journal of Bioenergetics and Biomembranes 39, 349–355.CrossRefGoogle ScholarPubMed
Peeraer, Y., Rabijns, A., Verboven, C., Collet, J. F., Van Schaftingen, E. & De Ranter, C. (2003). High-resolution structure of human phosphoserine phosphatase in open conformation. Acta Crystallographica D, Biological Crystallography 59, 971–977.Google Scholar
Peinelt, C. & Apell, H. J. (2005). Kinetics of Ca2+ binding to the SR Ca-ATPase in the E1 state. Biophysical Journal 89, 2427–2433.Google Scholar
Picard, M., Jensen, A. M., Sorensen, T. L., Champeil, P., Moller, J. V. & Nissen, P. (2007). Ca2+ versus Mg2+ coordination at the nucleotide-binding site of the sarcoplasmic reticulum Ca2+-ATPase. Journal of Molecular Biology 368, 1–7.Google Scholar
Picard, M., Toyoshima, C. & Champeil, P. (2005). The average conformation at micromolar [Ca2+] of Ca2+-atpase with bound nucleotide differs from that adopted with the transition state analog ADP.AlFx or with AMPPCP under crystallization conditions at millimolar [Ca2+]. Journal of Biological Chemistry 280, 18745–18754.Google Scholar
Picard, M., Toyoshima, C. & Champeil, P. (2006). Effects of inhibitors on luminal opening of Ca2+ binding sites in an E2P-like complex of sarcoplasmic reticulum Ca2+-ATPase with Be2+-fluoride. Journal of Biological Chemistry 281, 3360–3369.Google Scholar
Pickart, C. M. & Jencks, W. P. (1984). Energetics of the calcium-transporting ATPase. Journal of Biological Chemistry 259, 1629–1643.Google Scholar
Pikula, S., Mullner, N., Dux, L. & Martonosi, A. (1988). Stabilization and crystallization of Ca2+-ATPase in detergent-solubilized sarcoplasmic reticulum. Journal of Biological Chemistry 263, 5277–5286.Google Scholar
Punzengruber, C., Prager, R., Kolassa, N., Winkler, F. & Suko, J. (1978). Calcium gradient-dependent and calcium gradient-independent phosphorylation of sarcoplasmic reticulum by orthophosphate. The role of magnesium. European Journal of Biochemistry 92, 349–359.Google Scholar
Rasmussen, U., Christensen, S. B. & Patkar, S. A. (1982). Structure and biological activity of sesquiterpene lactones from thapsia species and of analogue derivatives. Planta Medica 45, 157.Google Scholar
Rice, D. M., Meadows, M. D., Scheinman, A. O., Goni, F. M., Gomez-Fernandez, J. C., Moscarello, M. A., Chapman, D. & Oldfield, E. (1979). Protein-lipid interactions. A nuclear magnetic resonance study of sarcoplasmic reticulum Ca2+,Mg2+-ATPase, lipophilin, and proteolipid apoprotein-lecithin systems and a comparison with the effects of cholesterol. Biochemistry 18, 5893–5903.Google Scholar
Ridder, I. S. & Dijkstra, B. W. (1999). Identification of the Mg2+-binding site in the P-type ATPase and phosphatase members of the HAD (haloacid dehalogenase) superfamily by structural similarity to the response regulator protein CheY. Biochemical Journal 339, 223–226.Google Scholar
Rizzolo, L. J., Maire, M., Reynolds, J. A. & Tanford, C. (1976). Molecular weights and hydrophobicity of the polypeptide chain of sarcoplasmic reticulum calcium(II) adenosine triphosphatase and of its primary tryptic fragments. Biochemistry 15, 3433–3437.Google Scholar
Sagara, Y., Fernandez-Belda, F., De Meis, L. & Inesi, G. (1992). Characterization of the inhibition of intracellular Ca2+ transport ATPases by thapsigargin. Journal of Biological Chemistry 267, 12606–12613.Google Scholar
Sagara, Y. & Inesi, G. (1991). Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations. Journal of Biological Chemistry 266, 13503–13506.Google Scholar
Saroussi, S. & Nelson, N. (2009). Vacuolar H+-ATPase-an enzyme for all seasons. Pflugers Arch 457, 581–587.Google Scholar
Sasaki, T., Inui, M., Kimura, Y., Kuzuya, T. & Tada, M. (1992). Molecular mechanism of regulation of Ca2+ pump ATPase by phospholamban in cardiac sarcoplasmic reticulum. Effects of synthetic phospholamban peptides on Ca2+ pump ATPase. Journal of Biological Chemistry 267, 1674–1679.Google Scholar
Scales, D. J. & Inesi, G. (1976). Localization of ATPase protein in sarcoplasmic reticulum membrane. Archives of Biochemistry and Biophysics 176, 392–394.Google Scholar
Scarborough, G. A. (2002). Molecular mechanism of the P-type ATPases. Journal of Bioenergetics and Biomembranes 34, 235–250.Google Scholar
Schack, V. R., Morth, J. P., Toustrup-Jensen, M. S., Anthonisen, A. N., Nissen, P., Andersen, J. P. & Vilsen, B. (2008). Identification and function of a cytoplasmic K+ site of the Na+, K+ -ATPase. Journal of Biological Chemistry 283, 27982–27990.Google Scholar
Scofano, H. M. & De Meis, L. (1981). Ratio of hydrolysis and synthesis of ATP by the sarcoplasmic reticulum ATPase in the absence of a Ca2+ concentration gradient. Journal of Biological Chemistry 256, 4282–4285.Google Scholar
Scofano, H. M., Vieyra, A. & De Meis, L. (1979). Substrate regulation of the sarcoplasmic reticulum ATPase. Transient kinetic studies. Journal of Biological Chemistry 254, 10227–10231.Google Scholar
Seekoe, T., Peall, S. & Mcintosh, D. B. (2001). Thapsigargin and dimethyl sulfoxide activate medium P(i)<–>HOH oxygen exchange catalyzed by sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 276, 46737–46744.Google Scholar
Seelig, J., Tamm, L., Hymel, L. & Fleischer, S. (1981). Deuterium and phosphorus nuclear magnetic resonance and fluorescence depolarization studies of functional reconstituted sarcoplasmic reticulum membrane vesicles. Biochemistry 20, 3922–3932.Google Scholar
Shigekawa, M. & Dougherty, J. P. (1978). Reaction mechanism of Ca2+-dependent ATP hydrolysis by skeletal muscle sarcoplasmic reticulum in the absence of added alkali metal salts. III. Sequential occurrence of ADP-sensitive and ADP-insensitive phosphoenzymes. Journal of Biological Chemistry 253, 1458–1464.Google Scholar
Shigekawa, M. & Pearl, L. J. (1976). Activation of calcium transport in skeletal muscle sarcoplasmic reticulum by monovalent cations. Journal of Biological Chemistry 251, 6947–6952.Google Scholar
Shigekawa, M. & Wakabayashi, S. (1985). Sidedness of K+ activation of calcium transport in the reconstituted sarcoplasmic reticulum calcium pump. Journal of Biological Chemistry 260, 11679–11687.Google Scholar
Shinoda, T., Ogawa, H., Cornelius, F. & Toyoshima, C. (2009). Crystal structure of the sodium-potassium pump at 2·4 A resolution. Nature 459, 446–450.CrossRefGoogle ScholarPubMed
Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sugimura, T., Kurono, S., Tsujimoto, K., Mizushima, T., Yamashita, E., Tsukihara, T. & Yoshikawa, S. (2007). Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO Journal 26, 1713–1725.Google Scholar
Silvius, J. R., Mcmillen, D. A., Saley, N. D., Jost, P. C. & Griffith, O. H. (1984). Competition between cholesterol and phosphatidylcholine for the hydrophobic surface of sarcoplasmic reticulum Ca2+-ATPase. Biochemistry 23, 538–547.Google Scholar
Skriver, E., Maunsbach, A. B. & Jorgensen, P. L. (1981). Formation of two-dimensional crystals in pure membrane-bound Na+, K+-ATPase. FEBS Letters 131, 219–222.Google Scholar
Søhoel, H., Jensen, A. M., Moller, J. V., Nissen, P., Denmeade, S. R., Isaacs, J. T., Olsen, C. E. & Christensen, S. B. (2006). Natural products as starting materials for development of second-generation SERCA inhibitors targeted towards prostate cancer cells. Bioorganic and Medicinal Chemistry Letters 14, 2810–2815.Google Scholar
Sondek, J., Lambright, D. G., Noel, J. P., Hamm, H. E. & Sigler, P. B. (1994). GTPase mechanism of Gproteins from the 1·7-A crystal structure of transducin alpha-GDP-AIF-4. Nature 372, 276–279.Google Scholar
Sørensen, T. L. & Andersen, J. P. (2000). Importance of stalk segment S5 for intramolecular communication in the sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 275, 28954–28961.Google Scholar
Sørensen, T. L., Clausen, J. D., Jensen, A. M., Vilsen, B., Moller, J. V., Andersen, J. P. & Nissen, P. (2004a). Localization of a K+-binding site involved in dephosphorylation of the sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 279, 46355–46357.Google Scholar
Sørensen, T. L., Møller, J. V. & Nissen, P. (2004b). Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science 304, 1672–1675.Google Scholar
Sørensen, T. L., Olesen, C., Jensen, A. M., Møller, J. V. & Nissen, P. (2006). Crystals of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biotechnology 124, 704–716.Google Scholar
Soulie, S., Neumann, J. M., Berthomieu, C., Moller, J. V., Le Maire, M. & Forge, V. (1999). NMR conformational study of the sixth transmembrane segment of sarcoplasmic reticulum Ca2+-ATPase. Biochemistry 38, 5813–5821.CrossRefGoogle ScholarPubMed
Stahl, N. & Jencks, W. P. (1984). Adenosine 5′-triphosphate at the active site accelerates binding of calcium to calcium adenosinetriphosphatase. Biochemistry 23, 5389–5392.Google Scholar
Starling, A. P., East, J. M. & Lee, A. G. (1993). Effects of phosphatidylcholine fatty acyl chain length on calcium binding and other functions of the (Ca2+-Mg2+)-ATPase. Biochemistry 32, 1593–1600.Google Scholar
Stewart, P. S. & Maclennan, D. H. (1974). Surface particles of sarcoplasmic reticulum membranes. Structural features of the adenosine triphosphatase. Journal of Biological Chemistry 249, 985–993.Google Scholar
Stock, A. M., Martinez-Hackert, E., Rasmussen, B. F., West, A. H., Stock, J. B., Ringe, D. & Petsko, G. A. (1993). Structure of the Mg2+-bound form of CheY and mechanism of phosphoryl transfer in bacterial chemotaxis. Biochemistry 32, 13375–13380.Google Scholar
Stokes, D. L. & Green, N. M. (1990). Structure of CaATPase: electron microscopy of frozen-hydrated crystals at 6 A resolution in projection. Journal of Molecular Biology 213, 529–538.Google Scholar
Stokes, D. L. & Green, N. M. (2000). Modeling a dehalogenase fold into the 8-A density map for Ca2+-ATPase defines a new domain structure. Biophysical Journal 78, 1765–1776.Google Scholar
Stokes, D. L. & Green, N. M. (2003). Structure and function of the calcium pump. Annual Review of Biophysics and Biomolecular Structure 32, 445–468.Google Scholar
Stokes, D. L., Pomfret, A. J., Rice, W. J., Glaves, J. P. & Young, H. S. (2006). Interactions between Ca2+-ATPase and the pentameric form of phospholamban in two-dimensional co-crystals. Biophysical Journal 90, 4213–4223.Google Scholar
Sugita, Y., Miyashita, N., Ikeguchi, M., Kidera, A. & Toyoshima, C. (2005). Protonation of the acidic residues in the transmembrane cation-binding sites of the Ca2+ pump. Journal of the American Chemical Society 127, 6150–6151.Google Scholar
Sumbilla, C., Lewis, D., Hammerschmidt, T. & Inesi, G. (2002). The slippage of the Ca2+ pump and its control by anions and curcumin in skeletal and cardiac sarcoplasmic reticulum. Journal of Biological Chemistry 277, 13900–13906.Google Scholar
Tada, M., Yamamoto, T. & Tonomura, Y. (1978). Molecular mechanism of active calcium transport by sarcoplasmic reticulum. Physiological Reviews 58, 1–79.Google Scholar
Tadini-Buoninsegni, F., Bartolommei, G., Moncelli, M. R., Guidelli, R. & Inesi, G. (2006). Pre-steady state electrogenic events of Ca2+/H+ exchange and transport by the Ca2+-ATPase. Journal of Biological Chemistry 281, 37720–37727.Google Scholar
Takahashi, M., Kondou, Y. & Toyoshima, C. (2007). Interdomain communication in calcium pump as revealed in the crystal structures with transmembrane inhibitors. Proceedings of the National Academy of Sciences USA 104, 5800–5805.Google Scholar
Takakuwa, Y. & Kanazawa, T. (1982). Role of Mg2+ in the Ca2+-Ca2+ exchange mediated by the membrane-bound (Ca2+, Mg2+)-ATPase of sarcoplasmic reticulum vesicles. Journal of Biological Chemistry 257, 10770–10775.Google Scholar
Takeuchi, A., Reyes, N., Artigas, P. & Gadsby, D. C. (2008). The ion pathway through the opened Na+, K+-ATPase pump. Nature 456, 413–416.Google Scholar
Tanford, C. (1981). Equilibrium state of ATP-driven ion pumps in relation to physiological ion concentration gradients. Journal of General Physiology 77, 223–229.Google Scholar
Tanford, C. (1983). Translocation pathway in the catalysis of active transport. Proceedings of the National Academy of Sciences USA 80, 3701–3705.Google Scholar
Tanford, C. (1984). The sarcoplasmic reticulum calcium pump. Localization of free energy transfer to discrete steps of the reaction cycle. FEBS Letters 166, 1–7.CrossRefGoogle ScholarPubMed
Taylor, K. A., Dux, L. & Martonosi, A. (1986). Three-dimensional reconstruction of negatively stained crystals of the Ca2+-ATPase from muscle sarcoplasmic reticulum. Journal of Molecular Biology 187, 417–427.CrossRefGoogle ScholarPubMed
Thastrup, O., Cullen, P. J., Drobak, B. K., Hanley, M. R. & Dawson, A. P. (1990). Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase. Proceedings of the National Academy of Sciences USA 87, 2466–2470.Google Scholar
Thorley-Lawson, D. A. & Green, N. M. (1973). Studies on the location and orientation of proteins in the sarcoplasmic reticulum. European Journal of Biochemistry 40, 403–413.Google Scholar
Toyofuku, T., Curotto Kurzydlowski, K., Narayanan, N. & Maclennan, D. H. (1994a). Identification of Ser38 as the site in cardiac sarcoplasmic reticulum Ca2+-ATPase that is phosphorylated by Ca2+/calmodulin-dependent protein kinase. Journal of Biological Chemistry 269, 26492–26496.CrossRefGoogle ScholarPubMed
Toyofuku, T., Kurzydlowski, K., Tada, M. & Maclennan, D. H. (1994b). Amino acids Glu2 to Ile18 in the cytoplasmic domain of phospholamban are essential for functional association with the Ca2+-ATPase of sarcoplasmic reticulum. Journal of Biological Chemistry 269, 3088–3094.Google Scholar
Toyofuku, T., Kurzydlowski, K., Tada, M. & Maclennan, D. H. (1994c). Amino acids Lys-Asp-Asp-Lys-Pro-Val402 in the Ca2+-ATPase of cardiac sarcoplasmic reticulum are critical for functional association with phospholamban. Journal of Biological Chemistry 269, 22929–22932.Google Scholar
Toyoshima, C. (2008). Structural aspects of ion pumping by Ca2+-ATPase of sarcoplasmic reticulum. Archives of Biochemistry and Biophysics 476, 3–11.Google Scholar
Toyoshima, C., Asahi, M., Sugita, Y., Khanna, R., Tsuda, T. & Maclennan, D. H. (2003). Modeling of the inhibitory interaction of phospholamban with the Ca2+ ATPase. Proceedings of the National Academy of Sciences USA 100, 467–472.CrossRefGoogle ScholarPubMed
Toyoshima, C. & Inesi, G. (2004). Structural basis of ion pumping by Ca2+-ATPase of the sarcoplasmic reticulum. Annual Review of Biochemistry 73, 269–292.Google Scholar
Toyoshima, C. & Mizutani, T. (2004). Crystal structure of the calcium pump with a bound ATP analogue. Nature 430, 529–535.Google Scholar
Toyoshima, C., Nakasako, M., Nomura, H. & Ogawa, H. (2000). Crystal structure of the calcium pump of sarcoplasmic reticulum at 2·6 A resolution. Nature 405, 647–655.Google Scholar
Toyoshima, C. & Nomura, H. (2002). Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 418, 605–611.Google Scholar
Toyoshima, C., Nomura, H. & Tsuda, T. (2004). Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432, 361–368.Google Scholar
Toyoshima, C., Norimatsu, Y., Iwasawa, S., Tsuda, T. & Ogawa, H. (2007). How processing of aspartylphosphate is coupled to lumenal gating of the ion pathway in the calcium pump. Proceedings of the National Academy of Sciences USA 104, 19831–19836.CrossRefGoogle ScholarPubMed
Toyoshima, C., Sasabe, H. & Stokes, D. L. (1993). Three-dimensional cryo-electron microscopy of the calcium ion pump in the sarcoplasmic reticulum membrane. Nature 362, 467–471.Google Scholar
Troullier, A., Girardet, J. L. & Dupont, Y. (1992). Fluoroaluminate complexes are bifunctional analogues of phosphate in sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 267, 22821–22829.Google Scholar
Tupling, A. R., Asahi, M. & Maclennan, D. H. (2002). Sarcolipin overexpression in rat slow twitch muscle inhibits sarcoplasmic reticulum Ca2+ uptake and impairs contractile function. Journal of Theoretical Biology 277, 44740–44746.Google Scholar
Vidaver, G. A. (1966). Inhibition of parallel flux and augmentation of counter flux shown by transport models not involving a mobile carrier. Journal of Theoretical Biology 10, 301–306.Google Scholar
Villamil Giraldo, A. M., Castello, P. R., Gonzalez Flecha, F. L., Moeller, J. V., Delfino, J. M. & Rossi, J. P. (2006). Stoichiometry of lipid-protein interaction assessed by hydrophobic photolabeling. FEBS Letters 580, 607–612.Google Scholar
Vilsen, B. & Andersen, J. P. (1992). Interdependence of Ca2+ occlusion sites in the unphosphorylated sarcoplasmic reticulum Ca2+-ATPase complex with CrATP. Journal of Biological Chemistry 267, 3539–3550.Google Scholar
Vilsen, B. & Andersen, J. P. (1998). Mutation to the glutamate in the fourth membrane segment of Na+, K+-ATPase and Ca2+-ATPase affects cation binding from both sides of the membrane and destabilizes the occluded enzyme forms. Biochemistry 37, 10961–10971.Google Scholar
Vilsen, B., Andersen, J. P. & Maclennan, D. H. (1991). Functional consequences of alterations to hydrophobic amino acids located at the M4S4 boundary of the Ca2+-ATPase of sarcoplasmic reticulum. Journal of Biological Chemistry 266, 18839–18845.Google Scholar
Vorherr, T., Wrzosek, A., Chiesi, M. & Carafoli, E. (1993). Total synthesis and functional properties of the membrane-intrinsic protein phospholamban. Protein Science 2, 339–347.Google Scholar
Wakabayashi, S., Ogurusu, T. & Shigekawa, M. (1986). Factors influencing calcium release from the ADP-sensitive phosphoenzyme intermediate of the sarcoplasmic reticulum ATPase. Journal of Biological Chemistry 261, 9762–9769.Google Scholar
Wakabayashi, S. & Shigekawa, M. (1990). Mechanism for activation of the 4-nitrobenzo-2-oxa-1,3-diazole-labeled sarcoplasmic reticulum ATPase by Ca2+ and its modulation by nucleotides. Biochemistry 29, 7309–7318.Google Scholar
Wang, G., Yamasaki, K., Daiho, T. & Suzuki, H. (2005). Critical hydrophobic interactions between phosphorylation and actuator domains of Ca2+-ATPase for hydrolysis of phosphorylated intermediate. Journal of Biological Chemistry 280, 26508–26516.Google Scholar
Wang, W., Cho, H. S., Kim, R., Jancarik, J., Yokota, H., Nguyen, H. H., Grigoriev, I. V., Wemmer, D. E. & Kim, S. H. (2002). Structural characterization of the reaction pathway in phosphoserine phosphatase: crystallographic “snapshots” of intermediate states. Journal of Molecular Biology 319, 421–431.Google Scholar
Wang, W., Kim, R., Jancarik, J., Yokota, H. & Kim, S. H. (2001). Crystal structure of phosphoserine phosphatase from Methanococcus jannaschii, a hyperthermophile, at 1·8 A resolution. Structure 9, 65–71.Google Scholar
Warren, G. B., Houslay, M. D., Metcalfe, J. C. & Birdsall, N. J. (1975). Cholesterol is excluded from the phospholipid annulus surrounding an active calcium transport protein. Nature 255, 684–687.Google Scholar
Warren, G. B., Toon, P. A., Birdsall, N. J., Lee, A. G. & Metcalfe, J. C. (1974). Reconstitution of a calcium pump using defined membrane components. Proceedings of the National Academy of Sciences USA 71, 622–626.Google Scholar
Wilbrandt, W. & Rosenberg, T. (1961). The concept of carrier transport and its corollaries in pharmacology. Pharmacological Reviews 13, 109–183.Google Scholar
Xu, C., Rice, W. J., He, W. & Stokes, D. L. (2002). A structural model for the catalytic cycle of Ca2+-ATPase. Journal of Molecular Biology 316, 201–211.Google Scholar
Yamasaki, K., Wang, G., Daiho, T., Danko, S. & Suzuki, H. (2008). Roles of Tyr122-hydrophobic cluster and K+ binding in Ca2+ -releasing process of ADP-insensitive phosphoenzyme of sarcoplasmic reticulum Ca2+-ATPase. Journal of Biological Chemistry 283, 29144–29155.Google Scholar
Yoda, A. & Yoda, S. (1987). Two different phosphorylation-dephosphorylation cycles of Na, K-ATPase proteoliposomes accompanying Na+ transport in the absence of K+. Journal of Biological Chemistry 262, 110–115.Google Scholar
Yonekura, K., Stokes, D. L., Sasabe, H. & Toyoshima, C. (1997). The ATP-binding site of Ca2+-ATPase revealed by electron image analysis. Biophysical Journal 72, 997–1005.Google Scholar
Yu, X., Carroll, S., Rigaud, J. L. & Inesi, G. (1993). H+ countertransport and electrogenicity of the sarcoplasmic reticulum Ca2+ pump in reconstituted proteoliposomes. Biophysical Journal 64, 1232–1242.Google Scholar
Yu, X., Hao, L. & Inesi, G. (1994). A pK change of acidic residues contributes to cation countertransport in the Ca-ATPase of sarcoplasmic reticulum. Role of H+ in Ca2+-ATPase countertransport. Journal of Biological Chemistry 269, 16656–16661.Google Scholar
Zhang, P., Toyoshima, C., Yonekura, K., Green, N. M. & Stokes, D. L. (1998). Structure of the calcium pump from sarcoplasmic reticulum at 8-A resolution. Nature 392, 835–839.Google Scholar
Zhang, Z., Lewis, D., Sumbilla, C., Inesi, G. & Toyoshima, C. (2001). The role of the M6-M7 loop (L67) in stabilization of the phosphorylation and Ca2+ binding domains of the sarcoplasmic reticulum Ca2+-ATPase (SERCA). Journal of Biological Chemistry 276, 15232–15239.Google Scholar