Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T23:02:52.933Z Has data issue: false hasContentIssue false
  • English
  • Français

S-Adenosyl-l-methionine restores photoreceptor function following acute retinal ischemia

Published online by Cambridge University Press:  18 November 2009

LEITH MOXON-LESTER ,
KEI TAKAMOTO ,
PAUL B. COLDITZ  and
NIGEL L. BARNETT
LEITH MOXON-LESTER
Affiliation:
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia The University of Queensland, Perinatal Research Centre, Brisbane, Australia
KEI TAKAMOTO
Affiliation:
The University of Queensland, Perinatal Research Centre, Brisbane, Australia
PAUL B. COLDITZ
Affiliation:
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia The University of Queensland, Perinatal Research Centre, Brisbane, Australia
NIGEL L. BARNETT*
Affiliation:
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia The University of Queensland, Perinatal Research Centre, Brisbane, Australia
*
*Address correspondence and reprint requests to: Nigel L. Barnett, The University of Queensland, Centre for Clinical Research, Royal Brisbane and Women’s Hospital, Herston, Queensland 4029, Australia. E-mail: n.barnett@uq.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The survival and function of retinal neurons is dependent on mitochondrial energy generation and its intracellular distribution by creatine kinase. Post ischemic disruption of retinal creatine synthesis, creatine kinase activity, or transport of creatine into neurons may impair retinal function. S-adenosyl-l-methionine (SAMe) is required for creatine synthesis, phosphatidylcholine and glutathione synthesis, and transducin methylation. These reactions are essential for photoreceptor function but may be downregulated after ischemia due to a reduction in SAMe. Our aim was to determine whether administration of SAMe after ischemia could improve retinal function. Unilateral retinal ischemia was induced in adult rats by increasing the intraocular pressure to 110 mm Hg for 60 min. Immediately after the ischemic insult, SAMe was injected into the vitreous (100 μm), followed by oral administration (69 mg/kg/day) for 5 or 10 days. Retinal function (electroretinography), histology, and creatine transporter (CRT-1) expression were analyzed. Photoreceptoral responses (RmP3, S), rod and cone bipolar cell responses (PII), and oscillatory potentials were reduced by the ischemia/reperfusion insult. Although SAMe treatment ameliorated the ischemia-induced histological damage by day 5, there was no improvement in retinal function and the intensity of CRT-1 labeling in ischemic retinas was markedly reduced. However, 10 days after ischemia, a recovery in CRT-1 immunolabeling was evident and SAMe supplementation significantly restored photoreceptor function and rod PII responses. In conclusion, these data suggest that creatine transport and methylation reactions, such as creatine synthesis, may be compromised by an ischemic insult contributing to retinal dysfunction and injury. Oral SAMe supplementation after retinal ischemia may provide an effective, safe, and accessible neuroprotective strategy.

Keywords

RetinaIschemiaPhotoreceptorsS-adenosyl-L-methionine (SAMe)NeuroprotectionCreatine
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 5-6 , November 2009 , pp. 429 - 441
Copyright
Copyright © Cambridge University Press 2009

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

Acosta, M.L., Kalloniatis, M. & Christie, D.L. (2005). Creatine transporter localization in developing and adult retina: Importance of creatine to retinal function. American Journal of Physiology. Cell Physiology 289, C1015–C1023.CrossRefGoogle ScholarPubMed
Aslan, M., Cort, A. & Yucel, I. (2008). Oxidative and nitrative stress markers in glaucoma. Free Radical Biology & Medicine 45, 367–376.CrossRefGoogle ScholarPubMed
Baric, I. (2009). Inherited disorders in the conversion of methionine to homocysteine. Journal of Inherited Metabolic Disease 32, 459–471.CrossRefGoogle ScholarPubMed
Barnett, N.L. & Grozdanic, S.D. (2004). Glutamate transporter localization does not correspond to the temporary functional recovery and late degeneration after acute ocular ischemia in rats. Experimental Eye Research 79, 513–524.CrossRefGoogle ScholarPubMed
Barnett, N.L., Pow, D.V. & Bull, N.D. (2001). Differential perturbation of neuronal and glial glutamate transport systems in retinal ischaemia. Neurochemistry International 39, 291–299.CrossRefGoogle ScholarPubMed
Birch, D.G., Hood, D.C., Nusinowitz, S. & Pepperberg, D.R. (1995). Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Investigative Ophthalmology & Visual Science 36, 1603–1614.Google ScholarPubMed
Bottiglieri, T. (2002). S-Adenosyl-L-methionine (SAMe): From the bench to the bedside–molecular basis of a pleiotrophic molecule. The American Journal of Clinical Nutrition 76, 1151S–1157S.CrossRefGoogle Scholar
Bui, B.V., Armitage, J.A. & Vingrys, A.J. (2002). Extraction and modelling of oscillatory potentials. Documenta Ophthalmologica 104, 17–36.CrossRefGoogle ScholarPubMed
Bui, B.V., Kalloniatis, M. & Vingrys, A.J. (2004). Retinal function loss after monocarboxylate transport inhibition. Investigative Ophthalmology & Visual Science 45, 584–593.CrossRefGoogle ScholarPubMed
Burstedt, M.S., Ristoff, E., Larsson, A. & Wachtmeister, L. (2009). Rod-cone dystrophy with maculopathy in genetic glutathione synthetase deficiency: A morphologic and electrophysiologic study. Ophthalmology 116, 324–331.CrossRefGoogle ScholarPubMed
Castagnet, P.I., Roque, M.E., Pasquare, S.J. & Giusto, N.M. (1998). Phosphorylation of rod outer segment proteins modulates phosphatidylethanolamine N-methyltransferase and phospholipase A2 activities in photoreceptor membranes. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 120, 683–691.CrossRefGoogle ScholarPubMed
Chan, A., Tchantchou, F., Rogers, E.J. & Shea, T.B. (2009). Dietary deficiency increases presenilin expression, gamma-secretase activity, and Abeta levels: potentiation by ApoE genotype and alleviation by S-adenosyl methionine. Journal of Neurochemistry 110, 831–836.CrossRefGoogle ScholarPubMed
Chen, K., Zhang, Q., Wang, J., Liu, F., Mi, M., Xu, H., Chen, F. & Zeng, K. (2009). Taurine protects transformed rat retinal ganglion cells from hypoxia-induced apoptosis by preventing mitochondrial dysfunction. Brain Research 1279, 131–138.CrossRefGoogle ScholarPubMed
Cheong, J.L., Cady, E.B., Penrice, J., Wyatt, J.S., Cox, I.J. & Robertson, N.J. (2006). Proton MR spectroscopy in neonates with perinatal cerebral hypoxic-ischemic injury: Metabolite peak-area ratios, relaxation times, and absolute concentrations. American Journal of Neuroradiology 27, 1546–1554.Google ScholarPubMed
Christen, W.G., Glynn, R.J., Chew, E.Y., Albert, C.M. & Manson, J.E. (2009). Folic acid, pyridoxine, and cyanocobalamin combination treatment and age-related macular degeneration in women: The Women’s Antioxidant and Folic Acid Cardiovascular Study. Archives of Internal Medicine 169, 335–341.CrossRefGoogle ScholarPubMed
Danishpajooh, I.O., Gudi, T., Chen, Y., Kharitonov, V.G., Sharma, V.S. & Boss, G.R. (2001). Nitric oxide inhibits methionine synthase activity in vivo and disrupts carbon flow through the folate pathway. The Journal of Biological Chemistry 276, 27296–27303.CrossRefGoogle ScholarPubMed
de Brouwer, A.P., Williams, K.L., Duley, J.A., van Kuilenburg, A.B., Nabuurs, S.B., Egmont-Petersen, M., Lugtenberg, D., Zoetekouw, L., Banning, M.J., Roeffen, M., Hamel, B.C., Weaving, L., Ouvrier, R.A., Donald, J.A., Wevers, R.A., Christodoulou, J. & van Bokhoven, H. (2007). Arts syndrome is caused by loss-of-function mutations in PRPS1. American Journal of Human Genetics 81, 507–518.CrossRefGoogle ScholarPubMed
De La Cruz, J.P., Villalobos, M.A., Cuerda, M.A., Guerrero, A., Gonzalez-Correa, J.A. & Sanchez De La Cuesta, F. (2002). Effects of S-adenosyl-L-methionine on lipid peroxidation and glutathione levels in rat brain slices exposed to reoxygenation after oxygen-glucose deprivation. Neuroscience Letters 318, 103–107.CrossRefGoogle ScholarPubMed
Dodd, J.R. & Christie, D.L. (2001). Cysteine 144 in the third transmembrane domain of the creatine transporter is located close to a substrate-binding site. The Journal of Biological Chemistry 276, 46983–46988.CrossRefGoogle ScholarPubMed
Finkelstein, J.D. (2007). Metabolic regulatory properties of S-adenosylmethionine and S-adenosylhomocysteine. Clinical Chemistry and Laboratory Medicine 45, 1694–1699.CrossRefGoogle ScholarPubMed
Friedburg, C., Thomas, M.M. & Lamb, T.D. (2001). Time course of the flash response of dark- and light-adapted human rod photoreceptors derived from the electroretinogram. The Journal of Physiology 534, 217–242.CrossRefGoogle ScholarPubMed
Fulton, A.B., Akula, J.D., Mocko, J.A., Hansen, R.M., Benador, I.Y., Beck, S.C., Fahl, E., Seeliger, M.W., Moskowitz, A. & Harris, M.E. (2009). Retinal degenerative and hypoxic ischemic disease. Documenta Ophthalmologica 118, 55–61.CrossRefGoogle ScholarPubMed
Glick, N. (2006). Dramatic reduction in self-injury in Lesch-Nyhan disease following S-adenosylmethionine administration. Journal of Inherited Metabolic Disease 29, 687.CrossRefGoogle ScholarPubMed
Goodyear, M.J., Crewther, S.G. & Junghans, B.M. (2009). A role for aquaporin-4 in fluid regulation in the inner retina. Visual Neuroscience 26, 159–165.CrossRefGoogle ScholarPubMed
Goren, J.L., Stoll, A.L., Damico, K.E., Sarmiento, I.A. & Cohen, B.M. (2004). Bioavailability and lack of toxicity of S-adenosyl-L-methionine (SAMe) in humans. Pharmacotherapy 24, 1501–1507.CrossRefGoogle ScholarPubMed
Green, D.G. & Kapousta-Bruneau, N.V. (1999). A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs. Visual Neuroscience 16, 727–741.CrossRefGoogle ScholarPubMed
Grillo, M.A. & Colombatto, S. (2008). S-Adenosylmethionine and its products. Amino Acids 34, 187–193.CrossRefGoogle ScholarPubMed
Hangai, M., Yoshimura, N., Hiroi, K., Mandai, M. & Honda, Y. (1996). Inducible nitric oxide synthase in retinal ischemia-reperfusion injury. Experimental Eye Research 63, 501–509.CrossRefGoogle ScholarPubMed
Harada, T., Harada, C., Nakamura, K., Quah, H.M., Okumura, A., Namekata, K., Saeki, T., Aihara, M., Yoshida, H., Mitani, A. & Tanaka, K. (2007). The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. The Journal of Clinical Investigation 117, 1763–1770.CrossRefGoogle ScholarPubMed
Hayreh, S.S. (2005). Prevalent misconceptions about acute retinal vascular occlusive disorders. Progress in Retinal and Eye Research 24, 493–519.CrossRefGoogle ScholarPubMed
Hemmer, W., Riesinger, I., Wallimann, T., Eppenberger, H.M. & Quest, A.F. (1993). Brain-type creatine kinase in photoreceptor cell outer segments: Role of a phosphocreatine circuit in outer segment energy metabolism and phototransduction. Journal of Cell Science 106, 671–683.CrossRefGoogle ScholarPubMed
Hermes, M., Osswald, H. & Kloor, D. (2007). Role of S-adenosylhomocysteine hydrolase in adenosine-induced apoptosis in HepG2 cells. Experimental Cell Research 313, 264–283.CrossRefGoogle ScholarPubMed
Holcombe, D.J., Lengefeld, N., Gole, G.A. & Barnett, N.L. (2008). The effects of acute intraocular pressure elevation on rat retinal glutamate transport. Acta Ophthalmologica 86, 408–414.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1990). A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Visual Neuroscience 5, 379–387.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1992). A computational model of the amplitude and implicit time of the b-wave of the human ERG. Visual Neuroscience 8, 107–126.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1993). Light adaptation of human rod receptors: The leading edge of the human a-wave and models of rod receptor activity. Vision Research 33, 1605–1618.CrossRefGoogle Scholar
Johnson, J.E. Jr, Perkins, G.A., Giddabasappa, A., Chaney, S., Xiao, W., White, A.D., Brown, J.M., Waggoner, J., Ellisman, M.H. & Fox, D.A. (2007). Spatiotemporal regulation of ATP and Ca2+ dynamics in vertebrate rod and cone ribbon synapses. Molecular Vision 13, 887–919.Google ScholarPubMed
Juhaszova, M., Wang, S., Zorov, D.B., Nuss, H.B., Gleichmann, M., Mattson, M.P. & Sollott, S.J. (2008). The identity and regulation of the mitochondrial permeability transition pore: Where the known meets the unknown. Annals of the New York Academy of Sciences 1123, 197–212.CrossRefGoogle ScholarPubMed
Kakkar, P. & Singh, B.K. (2007). Mitochondria: A hub of redox activities and cellular distress control. Molecular and Cellular Biochemistry 305, 235–253.CrossRefGoogle ScholarPubMed
Kang Derwent, J.J. & Linsenmeier, R.A. (2001). Hypoglycemia increases the sensitivity of the cat electroretinogram to hypoxemia. Visual Neuroscience 18, 983–993.CrossRefGoogle ScholarPubMed
Kapousta-Bruneau, N.V. (1999). Effects of sodium pentobarbital on the components of electroretinogram in the isolated rat retina. Vision Research 39, 3498–3512.CrossRefGoogle ScholarPubMed
Kharbanda, K.K. (2007). Role of transmethylation reactions in alcoholic liver disease. World Journal of Gastroenterology 13, 4947–4954.CrossRefGoogle ScholarPubMed
Kikuchi, M., Kashii, S., Honda, Y., Tamura, Y., Kaneda, K. & Akaike, A. (1997). Protective effects of methylcobalamin, a vitamin B12 analog, against glutamate-induced neurotoxicity in retinal cell culture. Investigative Ophthalmology & Visual Science 38, 848–854.Google ScholarPubMed
Kloor, D., Delabar, U., Muhlbauer, B., Luippold, G. & Osswald, H. (2002). Tissue levels of S-adenosylhomocysteine in the rat kidney: Effects of ischemia and homocysteine. Biochemical Pharmacology 63, 809–815.CrossRefGoogle ScholarPubMed
Kloor, D. & Osswald, H. (2004). S-Adenosylhomocysteine hydrolase as a target for intracellular adenosine action. Trends in Pharmacological Sciences 25, 294–297.CrossRefGoogle ScholarPubMed
Kozuka, M. & Iwata, N. (1989). S-Adenosyl-L-methionine ameliorates ischemic brain metabolism in spontaneously hypertensive rats. Japanese Journal of Pharmacology 49, 173–179.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Pugh, E.N. Jr. (2004). Dark adaptation and the retinoid cycle of vision. Progress in Retinal and Eye Research 23, 307–380.CrossRefGoogle ScholarPubMed
Lang, F., Bohmer, C., Palmada, M., Seebohm, G., Strutz-Seebohm, N. & Vallon, V. (2006). (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiological Reviews 86, 1151–1178.CrossRefGoogle ScholarPubMed
Lawler, J.M., Barnes, W.S., Wu, G., Song, W. & Demaree, S. (2002). Direct antioxidant properties of creatine. Biochemical and Biophysical Research Communications 290, 47–52.CrossRefGoogle ScholarPubMed
Lee, J., Ryu, H., Ferrante, R.J., Morris, S.M. Jr & Ratan, R.R. (2003). Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proceedings of the National Academy of Sciences of the United States of America 100, 4843–4848.CrossRefGoogle ScholarPubMed
Lipton, S.A. (1999). Redox sensitivity of NMDA receptors. Methods in Molecular Biology 128, 121–130.Google ScholarPubMed
Maher, P. & Hanneken, A. (2005). The molecular basis of oxidative stress-induced cell death in an immortalized retinal ganglion cell line. Investigative Ophthalmology & Visual Science 46, 749–757.CrossRefGoogle Scholar
Majano, P.L., Garcia-Monzon, C., Garcia-Trevijano, E.R., Corrales, F.J., Camara, J., Ortiz, P., Mato, J.M., Avila, M.A. & Moreno-Otero, R. (2001). S-Adenosylmethionine modulates inducible nitric oxide synthase gene expression in rat liver and isolated hepatocytes. Journal of Hepatology 35, 692–699.CrossRefGoogle ScholarPubMed
Monge, C., Beraud, N., Kuznetsov, A.V., Rostovtseva, T., Sackett, D., Schlattner, U., Vendelin, M. & Saks, V.A. (2008). Regulation of respiration in brain mitochondria and synaptosomes: Restrictions of ADP diffusion in situ, roles of tubulin, and mitochondrial creatine kinase. Molecular and Cellular Biochemistry 318, 147–165.CrossRefGoogle ScholarPubMed
Moxon-Lester, L., Sinclair, K., Burke, C., Cowin, G.J., Rose, S.E. & Colditz, P. (2007). Increased cerebral lactate during hypoxia may be neuroprotective in newborn piglets with intrauterine growth restriction. Brain Research 1179, 79–88.CrossRefGoogle ScholarPubMed
Mudd, S.H., Brosnan, J.T., Brosnan, M.E., Jacobs, R.L., Stabler, S.P., Allen, R.H., Vance, D.E. & Wagner, C. (2007). Methyl balance and transmethylation fluxes in humans. The American Journal of Clinical Nutrition 85, 19–25.CrossRefGoogle ScholarPubMed
Nagase, K., Tomi, M., Tachikawa, M. & Hosoya, K. (2006). Functional and molecular characterization of adenosine transport at the rat inner blood-retinal barrier. Biochimica et Biophysica Acta 1758, 13–19.CrossRefGoogle ScholarPubMed
Nakashima, T., Tomi, M., Katayama, K., Tachikawa, M., Watanabe, M., Terasaki, T. & Hosoya, K. (2004). Blood-to-retina transport of creatine via creatine transporter (CRT) at the rat inner blood-retinal barrier. Journal of Neurochemistry 89, 1454–1461.CrossRefGoogle ScholarPubMed
Nakashima, T., Tomi, M., Tachikawa, M., Watanabe, M., Terasaki, T. & Hosoya, K. (2005). Evidence for creatine biosynthesis in Muller glia. Glia 52, 47–52.CrossRefGoogle ScholarPubMed
Nishida, Y., Nagata, T., Takahashi, Y., Sugahara-Kobayashi, M., Murata, A. & Asai, S. (2004). Alteration of serum/glucocorticoid regulated kinase-1 (sgk-1) gene expression in rat hippocampus after transient global ischemia. Brain Research Molecular Brain Research 123, 121–125.CrossRefGoogle ScholarPubMed
Nixon, P.J., Bui, B.V., Armitage, J.A. & Vingrys, A.J. (2001). The contribution of cone responses to rat electroretinograms. Clinical & Experimental Ophthalmology 29, 193–196.CrossRefGoogle ScholarPubMed
Nusinowitz, S., Nguyen, L., Radu, R., Kashani, Z., Farber, D. & Danciger, M. (2003). Electroretinographic evidence for altered phototransduction gain and slowed recovery from photobleaches in albino mice with a MET450 variant in RPE65. Experimental Eye Research 77, 627–638.CrossRefGoogle ScholarPubMed
Okawa, H., Sampath, A.P., Laughlin, S.B. & Fain, G.L. (2008). ATP consumption by mammalian rod photoreceptors in darkness and in light. Current Biology 18, 1917–1921.CrossRefGoogle ScholarPubMed
Osborne, N.N. (2008). Pathogenesis of ganglion “cell death” in glaucoma and neuroprotection: Focus on ganglion cell axonal mitochondria. Progress in Brain Research 173, 339–352.CrossRefGoogle ScholarPubMed
Peachey, N.S. & Ball, S.L. (2003). Electrophysiological analysis of visual function in mutant mice. Documenta Ophthalmologica 107, 13–36.CrossRefGoogle ScholarPubMed
Perez-Sala, D., Gilbert, B.A., Tan, E.W. & Rando, R.R. (1992). Prenylated protein methyltransferases do not distinguish between farnesylated and geranylgeranylated substrates. Biochemical Journal 284, 835–840.CrossRefGoogle Scholar
Perez-Sala, D., Tan, E.W., Canada, F.J. & Rando, R.R. (1991). Methylation and demethylation reactions of guanine nucleotide-binding proteins of retinal rod outer segments. Proceedings of the National Academy of Sciences of the United States of America 88, 3043–3046.CrossRefGoogle ScholarPubMed
Persa, C., Osmotherly, K., Chao-Wei Chen, K., Moon, S. & Lou, M.F. (2006). The distribution of cystathionine beta-synthase (CBS) in the eye: Implication of the presence of a trans-sulfuration pathway for oxidative stress defense. Experimental Eye Research 83, 817–823.CrossRefGoogle ScholarPubMed
Persa, C., Pierce, A., Ma, Z., Kabil, O. & Lou, M.F. (2004). The presence of a transsulfuration pathway in the lens: A new oxidative stress defense system. Experimental Eye Research 79, 875–886.CrossRefGoogle Scholar
Phipps, J.A., Fletcher, E.L. & Vingrys, A.J. (2004). Paired-flash identification of rod and cone dysfunction in the diabetic rat. Investigative Ophthalmology & Visual Science 45, 4592–4600.CrossRefGoogle ScholarPubMed
Pow, D.V. (2001). Visualising the activity of the cystine-glutamate antiporter in glial cells using antibodies to aminoadipic acid, a selectively transported substrate. Glia 34, 27–38.CrossRefGoogle ScholarPubMed
Prudova, A., Bauman, Z., Braun, A., Vitvitsky, V., Lu, S.C. & Banerjee, R. (2006). S-Adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. Proceedings of the National Academy of Sciences of the United States of America 103, 6489–6494.CrossRefGoogle ScholarPubMed
Reichenbach, A., Wurm, A., Pannicke, T., Iandiev, I., Wiedemann, P. & Bringmann, A. (2007). Muller cells as players in retinal degeneration and edema. Graefe’s Archives for Clinical and Experimental Ophthalmology 245, 627–636.CrossRefGoogle ScholarPubMed
Roque, M.E. & Giusto, N.M. (1995). Phosphatidylethanolamine N-methyltransferase activity in isolated rod outer segments from bovine retina. Experimental Eye Research 60, 631–643.CrossRefGoogle ScholarPubMed
Rumpel, H., Lim, W.E., Chang, H.M., Chan, L.L., Ho, G.L., Wong, M.C. & Tan, K.P. (2003). Is myo-inositol a measure of glial swelling after stroke? A magnetic resonance study. Journal of Magnetic Resonance Imaging 17, 11–19.CrossRefGoogle ScholarPubMed
Saha, R.N. & Pahan, K. (2006). Regulation of inducible nitric oxide synthase gene in glial cells. Antioxidants & Redox Signaling 8, 929–947.CrossRefGoogle ScholarPubMed
Sangiovanni, J.P. & Chew, E.Y. (2005). The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Progress in Retinal and Eye Research 24, 87–138.CrossRefGoogle ScholarPubMed
Sato, H., Hariyama, H. & Moriguchi, K. (1988). S-Adenosyl-L-methionine protects the hippocampal CA1 neurons from the ischemic neuronal death in rat. Biochemical and Biophysical Research Communications 150, 491–496.CrossRefGoogle ScholarPubMed
Sato, H., Nakano, M., Horita, I., Takahashi, J. & Moriguchi, K. (1987 a). [Effect of S-adenosyl-L-methionine sulfate tosylate (FO-1561) on functional recovery after transient cerebral ischemia in rats]. Nippon Yakurigaku Zasshi 90, 91–95.CrossRefGoogle ScholarPubMed
Sato, H., Tobita, M., Ohtomo, H., Izumiyama, M. & Kogure, K. (1987 b). [Effects of S-adenosyl-L-methionine on the cerebral energy metabolism and microcirculation in the rats subjected to transient forebrain ischemia]. No To Shinkei 39, 1151–1156.Google ScholarPubMed
Sarris, J., Schoendorfer, N. & Kavanagh, D.J. (2009). Major depressive disorder and nutritional medicine: a review of monotherapies and adjuvant treatments. Nutrition Reviews 67, 125–131.CrossRefGoogle ScholarPubMed
Schlattner, U., Tokarska-Schlattner, M. & Wallimann, T. (2006). Mitochondrial creatine kinase in human health and disease. Biochimica et Biophysica Acta—Molecular Basis of Disease 1762, 164–180.CrossRefGoogle ScholarPubMed
Schober, M.S., Chidlow, G., Wood, J.P. & Casson, R.J. (2008). Bioenergetic-based neuroprotection and glaucoma. Clinical & Experimental Ophthalmology 36, 377–385.CrossRefGoogle ScholarPubMed
Schubert, H.L., Blumenthal, R.M. & Cheng, X. (2003). Many paths to methyltransfer: A chronicle of convergence. Trends in Biochemical Sciences 28, 329–335.CrossRefGoogle ScholarPubMed
Sennlaub, F., Courtois, Y. & Goureau, O. (2002). Inducible nitric oxide synthase mediates retinal apoptosis in ischemic proliferative retinopathy. The Journal of Neuroscience 22, 3987–3993.CrossRefGoogle ScholarPubMed
Sestili, P., Martinelli, C., Bravi, G., Piccoli, G., Curci, R., Battistelli, M., Falcieri, E., Agostini, D., Gioacchini, A.M. & Stocchi, V. (2006). Creatine supplementation affords cytoprotection in oxidatively injured cultured mammalian cells via direct antioxidant activity. Free Radical Biology & Medicine 40, 837–849.CrossRefGoogle ScholarPubMed
Silveri, M.M., Parow, A.M., Villafuerte, R.A., Damico, K.E., Goren, J., Stoll, A.L., Cohen, B.M. & Renshaw, P.F. (2003). S-Adenosyl-L-methionine: Effects on brain bioenergetic status and transverse relaxation time in healthy subjects. Biological Psychiatry 54, 833–839.CrossRefGoogle ScholarPubMed
Stachowiak, O., Dolder, M., Wallimann, T. & Richter, C. (1998). Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. The Journal of Biological Chemistry 273, 16694–16699.CrossRefGoogle ScholarPubMed
Strutz-Seebohm, N., Shojaiefard, M., Christie, D., Tavare, J., Seebohm, G. & Lang, F. (2007). PIKfyve in the SGK1 mediated regulation of the creatine transporter SLC6A8. Cellular Physiology and Biochemistry 20, 729–734.CrossRefGoogle ScholarPubMed
Sun, D., Bui, B.V., Vingrys, A.J. & Kalloniatis, M. (2007 a). Alterations in photoreceptor-bipolar cell signaling following ischemia/reperfusion in the rat retina. The Journal of Comparative Neurology 505, 131–146.CrossRefGoogle ScholarPubMed
Sun, D., Vingrys, A.J. & Kalloniatis, M. (2007 b). Metabolic and functional profiling of the ischemic/reperfused rat retina. The Journal of Comparative Neurology 505, 114–130.CrossRefGoogle ScholarPubMed
Suzuki, M., Kamei, M., Itabe, H., Yoneda, K., Bando, H., Kume, N. & Tano, Y. (2007). Oxidized phospholipids in the macula increase with age and in eyes with age-related macular degeneration. Molecular Vision 13, 772–778.Google ScholarPubMed
Tan, S., Schubert, D. & Maher, P. (2001). Oxytosis: A novel form of programmed cell death. Current Topics in Medicinal Chemistry 1, 497–506.Google ScholarPubMed
Tan, S.V. & Guiloff, R.J. (1998). Hypothesis on the pathogenesis of vacuolar myelopathy, dementia, and peripheral neuropathy in AIDS. Journal of Neurology, Neurosurgery and Psychiatry 65, 23–28.CrossRefGoogle ScholarPubMed
Trovarelli, G., De Medio, G.E., Porcellati, S., Stramentinoli, G. & Porcellati, G. (1983). The effect of S-Adenosyl-L-methionine on ischemia-induced disturbances of brain phospholipid in the gerbil. Neurochemical Research 8, 1597–1609.CrossRefGoogle ScholarPubMed
Uckermann, O., Kutzera, F., Wolf, A., Pannicke, T., Reichenbach, A., Wiedemann, P., Wolf, S. & Bringmann, A. (2005). The glucocorticoid triamcinolone acetonide inhibits osmotic swelling of retinal glial cells via stimulation of endogenous adenosine signaling. The Journal of Pharmacology and Experimental Therapeutics 315, 1036–1045.CrossRefGoogle ScholarPubMed
Wallimann, T., Wegmann, G., Moser, H., Huber, R. & Eppenberger, H.M. (1986). High content of creatine kinase in chicken retina: Compartmentalized localization of creatine kinase isoenzymes in photoreceptor cells. Proceedings of the National Academy of Sciences of the United States of America 83, 3816–3819.CrossRefGoogle ScholarPubMed
Warrant, E.J. (2009). Mammalian vision: Rods are a bargain. Current Biology 19, R69–R71.CrossRefGoogle ScholarPubMed
Wegmann, G., Huber, R., Zanolla, E., Eppenberger, H.M. & Wallimann, T. (1991). Differential expression and localization of brain-type and mitochondrial creatine kinase isoenzymes during development of the chicken retina: Mi-CK as a marker for differentiation of photoreceptor cells. Differentiation 46, 77–87.CrossRefGoogle ScholarPubMed
Wensel, T.G. (2008). Signal transducing membrane complexes of photoreceptor outer segments. Vision Research 48, 2052–2061.CrossRefGoogle ScholarPubMed
Winkler, B.S. (2008). An hypothesis to account for the renewal of outer segments in rod and cone photoreceptor cells: Renewal as a surrogate antioxidant. Investigative Ophthalmology & Visual Science 49, 3259–3261.CrossRefGoogle ScholarPubMed
Wright, A.D., Martin, N. & Dodson, P.M. (2008). Homocysteine, folates, and the eye. Eye 22, 989–993.CrossRefGoogle ScholarPubMed
Wyss, M. & Kaddurah-Daouk, R. (2000). Creatine and creatinine metabolism. Physiological Reviews 80, 1107–1213.CrossRefGoogle ScholarPubMed
Young, S.N. & Shalchi, M. (2005). The effect of methionine and S-adenosylmethionine on S-adenosylmethionine levels in the rat brain. Journal of Psychiatry & Neuroscience 30, 44–48.Google ScholarPubMed