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12 - The role of nitric oxide and PARP in neuronal cell death

from Part I - Basic aspects of neurodegeneration

Published online by Cambridge University Press:  04 August 2010

M. Flint Beal ,
Anthony E. Lang  and
Albert C. Ludolph
By
Mika Shimoji ,
Valina L. Dawson  and
Ted M. Dawson
M. Flint Beal
Affiliation:
Cornell University, New York
Anthony E. Lang
Affiliation:
University of Toronto
Albert C. Ludolph
Affiliation:
Universität Ulm, Germany
Mika Shimoji
Affiliation:
Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Valina L. Dawson
Affiliation:
Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Ted M. Dawson
Affiliation:
Department of Neurology, Johns Hopkins University School of Medicine, 600 N Wolfe Street, Pathol 2-210, Baltimore, MD 21205, USA
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Summary

Nitric oxide

Nitric oxide (NO) is a novel neuronal messenger molecule that is not confined to the synaptic cleft and can mediate rapid signaling by diffusing freely in three dimensions to act throughout local regions of neural tissue (Dawson & Dawson, 1998). NO can be generated in most tissues in the body and was first identified as endothelium-derived relaxing factor (EDRF) in blood vessels where it is the major regulator of vascular tone (Furchgott & Zawadzki, 1980; Palmer et al., 1987; Kilbourn & Belloni, 1990; Ignarro, 1991). NO is produced by the enzymatic conversion of L-arginine to L-citrulline by nitric oxide synthase (NOS). In the NO biosynthetic scheme, L-arginine is first oxygenated to the intermediate NG-hydroxy-L-arginine, which is then oxygenated to produce NO and L-citrulline. NO has a short half-life due to the pervasive action of superoxide (Palmer et al., 1987). There are three isoforms of NOS. Two isoforms are expressed constitutively (neuronal; nNOS, endothelial; eNOS) and one that expressed only after induction (inducible; iNOS) (Fujisawa et al., 1994; Chartrain et al., 1994; Marsden et al., 1993). Both the constitutive and inducible forms are tetrahydrobiopterin (BH4) dependent (Tayeh & Marletta, 1989; Kwon et al., 1989). The constitutive isoforms, nNOS and eNOS are Ca2+/calmodulin regulated and thus NO generation is dependent on calcium signaling events. However, iNOS is Ca2+/calmodulin independent and therefore NO is generated from iNOS upon protein expression. NO generation from iNOS is regulated by the duration of mRNA expression for iNOS (Dawson & Dawson, 1998).

Type
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Information
Neurodegenerative Diseases
Neurobiology, Pathogenesis and Therapeutics
 , pp. 146 - 156
Publisher: Cambridge University Press
Print publication year: 2005

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References

Aarts, M., Liu, Y., Liu, L.et al. (2002). Treatment of ischemic brain damage by perturbing NMDA receptor– PSD-95 protein interactions. Science, 298, 846–50CrossRefGoogle ScholarPubMed
Adamson, D. C., Wildemann, B., Sasaki, M.et al. (1996). Immunologic NO synthase: elevation in severe AIDS dementia and induction by HIV-1 gp41. Science, 274, 1917–21CrossRefGoogle ScholarPubMed
Adamson, D. C., McArthur, J. C., Dawson, T. M. & Dawson, V. L. (1999a). Course of HIV-Associated Dementia: Correlation's with gp41, iNOS and Macrophage/Microglial Activation. Mol. Med., 5, 98–109Google Scholar
Adamson, D. C., Kopnisky, K. L., Dawson, T. M. & Dawson, V. L. (1999b). Mechanisms and structural determinants of HIV-1 coat protein, gp41-induced neurotoxicity. J. Neurosci., 19, 64–71CrossRefGoogle Scholar
Alderton, W. K., Cooper, C. E. & Knowles, R. G. (2001). Nitric oxide synthases: structure, function and inhibition. Biochem. J., 357, 593–615CrossRefGoogle Scholar
Alkhatib, H. M., Chen, D. F., Cherney, B.et al. (1987). Cloning and expression of cDNA for human poly(ADP-ribose) polymerase. Proc. Nat. Acad. Sci., USA, 84, 1224–8CrossRefGoogle ScholarPubMed
Atwood, W. J., Berger, J. R., Kaderman, R., Tornatore, C. S. & Major, E. O. (1993). Human immunodeficiency virus type 1 infection of the brain. Clin. Microbiol. Rev., 6, 339–66CrossRefGoogle Scholar
Bagasra, O., Michaels, F. H., Zheng, et al. (1995). Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl Acad. Sci., USA, 92, 12041–5CrossRefGoogle ScholarPubMed
Beckman, J. S., Chen, J., Crow, J. P. & Ye, Y. Z. (1994a). Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog. Brain. Res., 103, 371–80CrossRefGoogle Scholar
Beckman, J. S., Chen, J., Ischiropoulos, H. & Crow, J. P. (1994b). Oxidative chemistry of peroxynitrite. Methods Enzymol., 233, 229–40CrossRefGoogle Scholar
Berger, N. A. (1985). Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res., 101, 4–15CrossRefGoogle ScholarPubMed
Bo, L., Dawson, T. M., Wesselingh, S.et al. (1994). Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann. Neurol., 36, 778–86CrossRefGoogle ScholarPubMed
Burns, R. S., Chiueh, C. C., Markey, S. R., Ebert, M. H., Jacobowitz, D. M., & Kopin, I. J. (1983). A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. Proc. Natl Acad. Sci. USA, 80 (14), 4546–50CrossRefGoogle ScholarPubMed
Burtscher, H. J., Auer, B., Klocker, H., Schweiger, M. & Hirsch-Kauffmann, M. (1986). Isolation of ADP-ribosyltransferase by affinity chromatography. Anal. Biochem., 152, 285–90CrossRefGoogle ScholarPubMed
Burtscher, H. J., Klocker, H., Schneider, R., Auer, B., Hirsch-Kauffmann, M. & Schweiger, M. (1987). ADP-ribosyltransferase from Helix pomatia. Purification and characterization. Biochem. J., 248, 859–64CrossRefGoogle ScholarPubMed
Butterfield, D. A., Griffin, S., Munch, G. & Pasinetti, G. M. (2002). Amyloid beta-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer's disease brain exists. J. Alzheimers Dis., 4, 193–201CrossRefGoogle ScholarPubMed
Carson, D. A., Seto, S., Wasson, D. B. & Carrera, C. J. (1986). DNA strand breaks, NAD metabolism, and programmed cell death. Exp. Cell. Res., 164, 273–81CrossRefGoogle ScholarPubMed
Chambon, P., Weill, J. D. & Mandel, P. (1963). Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun., 11, 39–43CrossRefGoogle ScholarPubMed
Chartrain, N. A., Geller, D. A., Koty, P. P.et al. (1994). Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem., 269, 6765–72Google ScholarPubMed
Chatterjee, S., Berger, S. J. & Berger, N. A. (1999). Poly(ADP-ribose) polymerase: a guardian of the genome that facilitates DNA repair by protecting against DNA recombination. Mol. Cell. Biochem., 193, 23–30CrossRefGoogle ScholarPubMed
Cherney, B. W., McBride, O. W., Chen, D. F.et al. (1987). cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc. Natl Acad. Sci., USA, 84, 8370–4CrossRefGoogle ScholarPubMed
Chiba, K., Trevor, A. & Castagnoli, N. Jr. (1984). Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem. Biophys. Res. Commun., 120, 574–8CrossRefGoogle ScholarPubMed
Chiba, K., Trevor, A. J. & Castagnoli, N. Jr. (1985). Active uptake of MPP+, a metabolite of MPTP, by brain synaptosomes. Biochem. Biophys. Res. Commun., 128, 1228–32CrossRefGoogle ScholarPubMed
Christopherson, K. S., Hillier, B. J., Lim, W. A. & Bredt, D. S. (1999). PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J. Biol. Chem., 274, 27467–73CrossRefGoogle Scholar
Cross, A. H., Manning, P. T., Stern, M. K. & Misko, T. P. (1997). Evidence for the production of peroxynitrite in inflammatory CNS demyelination. J. Neuroimmunol., 80, 121–30CrossRefGoogle ScholarPubMed
Dalkara, T. & Moskowitz, M. A. (1997). Neurotoxic and neuroprotective roles of nitric oxide in cerebral ischaemia. Int. Rev. Neurobiol., 40, 319–36CrossRefGoogle ScholarPubMed
Daugas, E., Susin, S. A., Zamzami, N.et al. (2000). Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J., 14, 729–39CrossRefGoogle ScholarPubMed
Dawson, V. L. & Dawson, T. M. (1998). Nitric oxide in neurodegeneration. Prog. Brain Res., 118, 215–29CrossRefGoogle ScholarPubMed
Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S. & Snyder, S. H. (1991). Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl Acad. Sci., USA, 88, 6368–71CrossRefGoogle ScholarPubMed
Dawson, V. L., Dawson, T. M., Bartley, D. A., Uhl, G. R. & Snyder, S. H. (1993a). Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci., 13, 2651–61CrossRefGoogle Scholar
Dawson, V. L., Dawson, T. M., Uhl, G. R. & Snyder, S. H. (1993b). Human immunodeficiency virus type 1 coat protein neurotoxicity mediated by nitric oxide in primary cortical cultures. Proc. Natl Acad. Sci., USA, 90, 3256–9CrossRefGoogle Scholar
Dawson, V. L., Brahmbhatt, H. P., Mong, J. A. & Dawson, T. M. (1994). Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal-glial cortical cultures. Neuropharmacology, 33, 1425–30CrossRefGoogle ScholarPubMed
Groot, C. J., Ruuls, S. R., Theeuwes, J. W., Dijkstra, C. D. & Valk, P. (1997). Immunocytochemical characterization of the expression of inducible and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions. J. Neuropathol. Exp. Neurol., 56, 10–20CrossRefGoogle ScholarPubMed
Murcia, G., Huletsky, A., Lamarre, D.et al. (1986). Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J. Biol. Chem., 261, 7011–7Google ScholarPubMed
Murcia, G. & Menissier de Murcia, J. (1994). Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci., 19, 172–6CrossRefGoogle ScholarPubMed
Murcia, J. M., Niedergang, C.Trucco, C.et al. (1997). Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl Acad. Sci., USA, 94, 7303–7CrossRefGoogle ScholarPubMed
Eliasson, M. J., Sampei, K., Mandir, A. S.et al. (1997). Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med., 3, 1089–95CrossRefGoogle ScholarPubMed
Ferri, K. F. & Kroemer, G. (2001). Organelle-specific initiation of cell death pathways. Nat. Cell. Biol., 3, E255–63CrossRefGoogle ScholarPubMed
Floyd, R. A. (1999). Antioxidants, oxidative stress, and degenerative neurological disorders. Proc. Soc. Exp. Biol. Med., 222, 236–45CrossRefGoogle ScholarPubMed
Frechette, A., Huletsky, A., Aubin, R. J.et al. (1985). Poly(ADP-ribosyl)ation of chromatin: kinetics of relaxation and its effect on chromatin solubility. Can. J. Biochem. Cell. Biol., 63, 764–73CrossRefGoogle ScholarPubMed
Fujisawa, H., Ogura, T., Kurashima, Y., Yokoyama, T., Yamashita, J. & Esumi, H. (1994). Expression of two types of nitric oxide synthase mRNA in human neuroblastoma cell lines. J. Neurochem., 63, 140–5CrossRefGoogle ScholarPubMed
Furchgott, R. F. & Zawadzki, J. V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature, 288, 373–6CrossRefGoogle ScholarPubMed
Giasson, B. I., Duda, J. E., Murray, I. V.et al. (2000). Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science, 290, 985–9CrossRefGoogle ScholarPubMed
Gold, D. P., Schroder, K., Powell, H. C. & Kelly, C. J. (1997). Nitric oxide and the immunomodulation of experimental allergic encephalomyelitis. Eur. J. Immunol., 27, 2863–9CrossRefGoogle ScholarPubMed
Hara, H.Huang, P. L.Panahian, N.Fishman, M. C. & Moskowitz, M. A. (1996). Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J. Cereb. Blood Flow Metab., 16 (4), 605–11CrossRefGoogle ScholarPubMed
Heneka, M. T., Wiesinger, H., Dumitrescu-Ozimek, L., Riederer, P., Feinstein, D. L. & Klockgether, T. (2001). Neuronal and glial coexpression of argininosuccinate synthetase and inducible nitric oxide synthase in Alzheimer disease. J. Neuropathol. Exp. Neurol., 60, 906–16CrossRefGoogle ScholarPubMed
Huang, Z., Huang, P. L., Panahian, N., Dalkara, T., Fishman, M. C. & Moskowitz, M. A. (1994). Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science, 265, 1883–5CrossRefGoogle ScholarPubMed
Huang, Z., Huang, P. L., Ma, J.et al. (1996). Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J. Cereb. Blood Flow Metab., 16, 981–7CrossRefGoogle ScholarPubMed
Ignarro, L. J. (1991). Signal transduction mechanisms involving nitric oxide. Biochem. Pharmacol., 41, 485–90CrossRefGoogle ScholarPubMed
Javitch, J. A., D'Amato, R. J., Strittmatter, S. M. & Snyder, S. H. (1985). Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridi ne by dopamine neurons explains selective toxicity. Proc. Natl Acad. Sci., USA, 82, 2173–7CrossRefGoogle Scholar
Joza, N., Susin, S. A., Daugas, E.et al. (2001). Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature, 410, 549–54CrossRefGoogle ScholarPubMed
Kilbourn, R. G. & Belloni, P. (1990). Endothelial cell production of nitrogen oxides in response to interferon gamma in combination with tumor necrosis factor, interleukin-1, or endotoxin. J. Natl Cancer Inst., 82, 772–6CrossRefGoogle ScholarPubMed
Koppenol, W. H., Moreno, J. J., Pryor, W. A., Ischiropoulos, H. & Beckman, J. S. (1992). Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol., 5, 834–42CrossRefGoogle ScholarPubMed
Krupitza, G. & Cerutti, P. (1989). Poly(ADP-ribosylation) of histones in intact human keratinocytes. Biochemistry, 28, 4054–60CrossRefGoogle ScholarPubMed
Kurosaki, T., Ushiro, H., Mitsuuchi, Y.et al. (1987). Primary structure of human poly(ADP-ribose) synthetase as deduced from cDNA sequence. J. Biol. Chem., 262, 15990–7Google ScholarPubMed
Kwon, N. S., Nathan, C. F. & Stuehr, D. J. (1989). Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages. J. Biol. Chem., 264, 20496–501Google ScholarPubMed
Langston, J. W., Ballard, P. A., Tetrud, J. W. & Irwin, I. (1983). Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science, 219, 979–80CrossRefGoogle ScholarPubMed
Lau, Y. S., Trobough, K. L., Crampton, J. M. & Wilson, J. A. (1990). Effects of probenecid on striatal dopamine depletion in acute and long-term 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-treated mice. Gen. Pharmacol., 21 (2), 181–7CrossRefGoogle ScholarPubMed
Lautier, D., Lagueux, J., Thibodeau, J., Menard, L. & Poirier, G. G. (1993). Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol. Cell. Biochem., 122, 171–93CrossRefGoogle ScholarPubMed
Liberatore, G. T., Jackson-Lewis, V., Vukosavic, S.et al. (1999). Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med., 5, 1403–9CrossRefGoogle ScholarPubMed
Lin, R. F., Lin, T. S., Tilton, R. G. & Cross, A. H. (1993). Nitric oxide localized to spinal cords of mice with experimental allergic encephalomyelitis: an electron paramagnetic resonance study. J. Exp. Med., 178, 643–8CrossRefGoogle ScholarPubMed
Lipton, S. A. (1992). Memantine prevents HIV coat protein-induced neuronal injury in vitro. Neurology, 42, 1403–5CrossRefGoogle ScholarPubMed
Liu, J. S., Zhao, M. L., Brosnan, C. F. & Lee, S. C. (2001). Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am. J. Pathol., 158, 2057–66CrossRefGoogle ScholarPubMed
Love, S., Barber, R. & Wilcock, G. K. (1999a). Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer's disease. Brain, 122 (2), 247–53CrossRefGoogle Scholar
Love, S., Barber, R. & Wilcock, G. K. (1999b). Neuronal accumulation of poly(ADP-ribose) after brain ischaemia. Neuropathol. Appl. Neurobiol., 25, 98–103CrossRefGoogle Scholar
Lowenstein, C. J., Alley, E. W., Raval, P.et al. (1993). Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl Acad. Sci., USA, 90, 9730–4CrossRefGoogle ScholarPubMed
Ludwig, A., Behnke, B., Holtlund, J. & Hilz, H. (1988). Immunoquantitation and size determination of intrinsic poly(ADP-ribose) polymerase from acid precipitates. An analysis of the in vivo status in mammalian species and in lower eukaryotes. J. Biol. Chem., 263, 6993–9Google ScholarPubMed
Luth, H. J., Holzer, M., Gartner, U., Staufenbiel, M. & Arendt, T. (2001). Expression of endothelial and inducible NOS-isoforms is increased in Alzheimer's disease, in APP23 transgenic mice and after experimental brain lesion in rat: evidence for an induction by amyloid pathology. Brain Res., 913, 57–67CrossRefGoogle ScholarPubMed
MacMillan-Crow, L. A., Crow, J. P., Kerby, J. D., Beckman, J. S. & Thompson, J. A. (1996). Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl Acad. Sci., USA, 93, 11853–8CrossRefGoogle ScholarPubMed
Mandir, A. S., Przedborski, S., Jackson-Lewis, V.et al. (1999). Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrid ine (MPTP)-induced parkinsonism. Proc. Natl Acad. Sci., USA, 96, 5774–9CrossRefGoogle Scholar
Markey, S. P., Johannessen, J. N., Chiueh, C. C., Burns, R. S. & Herkenham, M. A. (1984). Intraneuronal generation of a pyridinium metabolite may cause drug-induced parkinsonism. Nature, 311, 464–7CrossRefGoogle ScholarPubMed
Marsden, P. A., Heng, H. H., Scherer, S. W.et al. (1993). Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J. Biol. Chem., 268, 17478–88Google ScholarPubMed
Marshall, H. E., Merchant, K. & Stamler, J. S. (2000). Nitrosation and oxidation in the regulation of gene expression. FASEB J., 14, 1889–900CrossRefGoogle ScholarPubMed
Mazen, A., Menissier-de Murcia, J., Molinete, M.et al. (1989). Poly(ADP-ribose)polymerase: a novel finger protein. Nucl. Acids Res., 17, 4689–98CrossRefGoogle ScholarPubMed
Merrill, J. E., Ignarro, L. J., Sherman, M. P., Melinek, J. & Lane, T. E. (1993). Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol., 151, 2132–41Google ScholarPubMed
Morrison, C., Smith, G. C., Stingl, L., Jackson, S. P., Wagner, E. F. & Wang, Z. Q. (1997). Genetic interaction between PARP and DNA-PK in V(D)J recombination and tumorigenesis. Nat. Genet., 17, 479–82CrossRefGoogle Scholar
Moskowitz, M. A. & Dalkara, T. (1996). Nitric oxide and cerebral ischemia. Adv. Neurol., 71, 365–7; discussion 367–9Google ScholarPubMed
Navia, B. A., Jordan, B. D. & Price, R. W. (1986). The AIDS dementia complex: I. Clinical features. Ann. Neurol., 19, 517–24CrossRefGoogle ScholarPubMed
Nicklas, W. J., Vyas, I. & Heikkila, R. E. (1985). Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyrid ine. Life Sci., 36, 2503–8CrossRefGoogle Scholar
Niedergang, C. P., Murcia, G., Ittel, M. E., Pouyet, J. & Mandel, P. (1985). Time course of polynucleosome relaxation and ADP-ribosylation. Correlation between relaxation and histone H1 hyper-ADP-ribosylation.Eur. J. Biochem., 146, 185–91CrossRefGoogle ScholarPubMed
Ohashi, Y., Itaya, A., Tanaka, Y., Yoshihara, K., Kamiya, T. & Matsukage, A. (1986). Poly(ADP-ribosyl)ation of DNA polymerase beta in vitro. Biochem. Biophys. Res. Commun., 140, 666–73CrossRefGoogle ScholarPubMed
Oleinick, N. L. & Evans, H. H. (1985). Poly(ADP-ribose) and the response of cells to ionizing radiation. Radiat. Res., 101, 29–46CrossRefGoogle ScholarPubMed
Palmer, R. M., Ferrige, A. G. & Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature, 327, 524–6CrossRefGoogle ScholarPubMed
Panahian, N., Yoshida, T., Huang, P. L.et al. (1996). Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience, 72 (2), 343–54CrossRefGoogle ScholarPubMed
Parkinson, J. F., Mitrovic, B. & Merrill, J. E. (1997). The role of nitric oxide in multiple sclerosis. J. Mol. Med., 75, 174–86CrossRefGoogle ScholarPubMed
Petroske, E., Meredith, G. E., Callen, S., Totterdell, S. & Lau, Y. S. (2001). Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP; probenecid treatment. Neuroscience, 106 (3), 589–601CrossRefGoogle ScholarPubMed
Pieper, A. A., Brat, D. J., Krug, D. K.et al. (1999a). Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc. Natl Acad. Sci., USA, 96, 3059–64CrossRefGoogle Scholar
Pieper, A. A., Verma, A., Zhang, J. & Snyder, S. H. (1999b). Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol. Sci., 20, 171–81CrossRefGoogle Scholar
Power, C. & Johnson, R. T. (1995). HIV-1 associated dementia: clinical features and pathogenesis. Can. J. Neurol. Sci., 22, 92–100CrossRefGoogle ScholarPubMed
Przedborski, S., Jackson-Lewis, V., Yokoyama, R., Shibata, T., Dawson, V. L. & Dawson, T. M. (1996). Role of neuronal nitric oxide in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrid ine (MPTP)-induced dopaminergic neurotoxicity. Proc. Natl Acad. Sci., USA, 93, 4565–71CrossRefGoogle Scholar
Przedborski, S., Chen, Q., Vila, M.et al. (2001). Oxidative post-translational modifications of alpha-synuclein in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrid ine (MPTP) mouse model of Parkinson's disease. J. Neurochem., 76, 637–40CrossRefGoogle Scholar
Ramsay, R. R., Krueger, M. J., Youngster, S. K., Gluck, M. R., Casida, J. E. & Singer, T. P. (1991). Interaction of 1-methyl-4-phenylpyridinium ion (MPP+) and its analogs with the rotenone/piericidin binding site of NADH dehydrogenase. J. Neurochem., 56, 1184–90CrossRefGoogle ScholarPubMed
Ramsay, R. R. & Singer, T. P. (1992). Relation of superoxide generation and lipid peroxidation to the inhibition of NADH-Q oxidoreductase by rotenone, piericidin A, and MPP+. Biochem. Biophys. Res. Commun., 189, 47–52CrossRefGoogle ScholarPubMed
Rickwood, D. & Osman, M. S. (1979). Characterisation of poly(ADP-Rib) polymerase activity in nuclei from the slime mould Dictyostelium discoideum. Mol. Cell. Biochem., 27, 79–84CrossRefGoogle ScholarPubMed
Ruf, A., Mennissier de Murcia, J., Murcia, G. & Schulz, G. E. (1996). Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. Proc. Natl Acad. Sci., USA, 93, 7481–5CrossRefGoogle ScholarPubMed
Ruscetti, T., Lehnert, B. E., Halbrook, J.et al. (1998). Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J. Biol. Chem., 273, 14461–7CrossRefGoogle ScholarPubMed
Samdani, A. F., Dawson, T. M. & Dawson, V. L. (1997). Nitric oxide synthase in models of focal ischemia. Stroke, 28, 1283–8CrossRefGoogle ScholarPubMed
Sattler, R., Xiong, Z., Lu, W. Y., Hafner, M., MacDonald, J. F. & Tymianski, M. (1999). Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science, 284, 1845–8CrossRefGoogle ScholarPubMed
Scovassi, A. I., Mariani, C., Negroni, M., Negri, C. & Bertazzoni, U. (1993). ADP-ribosylation of nonhistone proteins in HeLa cells: modification of DNA topoisomerase II. Exp. Cell. Res., 206, 177–81CrossRefGoogle ScholarPubMed
Shall, S. & Murcia, G. (2000). Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?Mutat. Res., 460, 1–15CrossRefGoogle ScholarPubMed
Singer, T. P., Castagnoli, N. Jr., Ramsay, R. R. & Trevor, A. J. (1987). Biochemical events in the development of parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrid ine. J. Neurochem., 49, 1–8CrossRefGoogle Scholar
Smith, S. (2001). The world according to PARP. Trends Biochem. Sci., 26, 174–9CrossRefGoogle ScholarPubMed
Souza, J. M., Giasson, B. I., Chen, Q., Lee, V. M. & Ischiropoulos, H. (2000). Dityrosine cross-linking promotes formation of stable alpha -synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J. Biol. Chem., 275, 18344–9CrossRefGoogle ScholarPubMed
Stamler, J. S., Lamas, S. & Fang, F. C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell, 106, 675–83CrossRefGoogle ScholarPubMed
Sun, D., Coleclough, C., Cao, L., Hu, X., Sun, S. & Whitaker, J. N. (1998). Reciprocal stimulation between TNF-alpha and nitric oxide may exacerbate CNS inflammation in experimental autoimmune encephalomyelitis. J. Neuroimmunol., 89, 122–30CrossRefGoogle ScholarPubMed
Susin, S. A., Lorenzo, H. K., Zamzami, N.et al. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 397, 441–6CrossRefGoogle ScholarPubMed
Szabo, C. & Dawson, V. L. (1998). Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol. Sci., 19, 287–98CrossRefGoogle ScholarPubMed
Takahashi, K., Wesselingh, S. L., Griffin, D. E., McArthur, J. C., Johnson, R. T. & Glass, J. D. (1996). Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann. Neurol., 39, 705–11CrossRefGoogle ScholarPubMed
Takahashi, K., Pieper, A. A., Croul, S. E., Zhang, J., Snyder, S. H. & Greenberg, J. H. (1999). Post-treatment with an inhibitor of poly(ADP-ribose) polymerase attenuates cerebral damage in focal ischemia. Brain Res., 829, 46–54CrossRefGoogle ScholarPubMed
Tanuma, S., Yagi, T. & Johnson, G. S. (1985). Endogenous ADP ribosylation of high mobility group proteins 1 and 2 and histone H1 following DNA damage in intact cells. Arch. Biochem. Biophys., 237, 38–42CrossRefGoogle ScholarPubMed
Tayeh, M. A. & Marletta, M. A. (1989). Macrophage oxidation of L-arginine to nitric oxide, nitrite, and nitrate. Tetrahydrobiopterin is required as a cofactor. J. Biol. Chem., 264, 19654–8Google ScholarPubMed
Tsai, Y. J., Aoki, T., Maruta, H.et al. (1992). Mouse mammary tumor virus gene expression is suppressed by oligomeric ellagitannins, novel inhibitors of poly(ADP-ribose) glycohydrolase. J. Biol. Chem., 267, 14436–42Google ScholarPubMed
Uchida, K. & Miwa, M. (1994). Poly(ADP-ribose) polymerase: structural conservation among different classes of animals and its implications. Mol. Cell. Biochem., 138, 25–32CrossRefGoogle ScholarPubMed
Uchida, K., Morita, T., Sato, T.et al. (1987). Nucleotide sequence of a full-length cDNA for human fibroblast poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun., 148, 617–22CrossRefGoogle ScholarPubMed
Ushiro, H., Yokoyama, Y. & Shizuta, Y. (1987). Purification and characterization of poly (ADP-ribose) synthetase from human placenta. J. Biol. Chem., 262, 2352–7Google ScholarPubMed
Wang, Z. Q., Stingl, L., Morrison, C.et al. (1997). PARP is important for genomic stability but dispensable in apoptosis. Genes Dev., 11, 2347–58CrossRefGoogle ScholarPubMed
Werner, E., Sohst, S., Gropp, F., Simon, D., Wagner, H. & Kroger, H. (1984). Presence of poly (ADP-ribose) polymerase and poly (ADP-ribose) glycohydrolase in the dinoflagellate Crypthecodinium cohnii. Eur. J. Biochem., 139, 81–6CrossRefGoogle ScholarPubMed
Wesierska-Gadek, J., Bugajska-Schretter, A. & Cerni, C. (1996a). ADP-ribosylation of p53 tumor suppressor protein: mutant but not wild-type p53 is modified. J. Cell. Biochem., 62, 90–1013.0.CO;2-J>CrossRefGoogle Scholar
Wesierska-Gadek, J., Schmid, G. & Cerni, C. (1996b). ADP-ribosylation of wild-type p53 in vitro: binding of p53 protein to specific p53 consensus sequence prevents its modification. Biochem. Biophys. Res. Commun., 224, 96–102CrossRefGoogle Scholar
Wiley, C. A., Schrier, R. D., Nelson, J. A., Lampert, P. W. & Oldstone, M. B. (1986). Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl Acad. Sci., USA, 83, 7089–93CrossRefGoogle ScholarPubMed
Yamanaka, H., Penning, C. A., Willis, E. H., Wasson, D. B. & Carson, D. A. (1988). Characterization of human poly(ADP-ribose) polymerase with autoantibodies. J. Biol. Chem., 263, 3879–83Google ScholarPubMed
Yoshihara, K., Itaya, A., Tanaka, Y.et al. (1985). Inhibition of DNA polymerase alpha, DNA polymerase beta, terminal deoxynucleotidyl transferase, and DNA ligase II by poly(ADP-ribosyl)ation reaction in vitro. Biochem. Biophys. Res. Commun., 128, 61–7CrossRefGoogle ScholarPubMed
Yu, S. W., Wang, H., Poitras, M. F.et al. (2002). Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science, 297, 259–63CrossRefGoogle ScholarPubMed
Zhang, J., Dawson, V. L., Dawson, T. M. & Snyder, S. H. (1994). Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science, 263, 687–9CrossRefGoogle ScholarPubMed
Zhang, J., Pieper, A. & Snyder, S. H. (1995). Poly(ADP-ribose) synthetase activation: an early indicator of neurotoxic DNA damage. J. Neurochem., 65, 1411–14CrossRefGoogle ScholarPubMed
Zhang, X., Morera, S., Bates, P. A.et al. (1998). Structure of an XRCC1 BRCT domain: a new protein-protein interaction module. EMBO J., 17, 6404–11CrossRefGoogle Scholar

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