Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease

Nature Medicine

Volumn 5, Issue 12, 1999, Pages 1403-1409

  Liberatore, Gabriel T ^a   Jackson Lewis, Vernice ^a   Vukosavic, Slobodanka ^a   Mandir, Allen S ^b   Vila, Miquel ^a   Mcauliffe, W Geoffrey ^c   Dawson, Valina L ^b   Dawson, Ted M ^b   Przedborski, Serge ^a  

^a Columbia University ^*  (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; ENZYME ANALYSIS; HISTOPATHOLOGY; MALE; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; ENZYME INHIBITORS; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MPTP POISONING; NERVE DEGENERATION; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PARKINSON DISEASE; RNA, MESSENGER;

EID: 0032710609     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/70978     Document Type: Article

References (51)

1. Fahn, S. in Cecil's Textbook of Medicine vol. 18 (eds. Wyngaarden, J.B. & Smith, L.H.Jr.) 2143-2147 (Saunders, Philadelphia, 1988).
2. Pakkenberg, B., Moller, A., Gundersen, H.J.G., Mouritzen, A. & Pakkenberg, H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method. J. Neurol. Neurosurg. Psychiat. 54, 30-33 (1991).
3. Hornykiewicz, O. & Kish, S.J. in Parkinson's Ddisease (eds. Yahr, M. & Bergmann, K.J.) 19-34 (Raven, New York, 1987).
4. Kostic, V., Przedborski, S., Flaster, E. & Sternic, N. Early development of levodopa-induced dyskinesias and response fluctuations in young-onset Parkinson's disease. Neurology 41, 202-205 (1991).
5. Langston, J.W. & Irwin, I. MPTP: current concepts and controversies. Clin. Neuropharmacol. 9, 485-507 (1986).
6. Przedborski, S. & Jackson-Lewis, V. Mechanisms of MPTP toxicity. Mov. Disord. 13, 35-38 (1998).
7. Przedborski, S. & Jackson-Lewis, V. Experimental developments in movement disorders: update on proposed free radical mechanisms. Curr. Opin. Neurol 11, 335-339 (1998).
8. Dawson, T.M. & Dawson, V.L. Nitric oxide synthase: role as a transmitter/mediator in the brain and endocrine system. Annu. Rev. Med. 47, 219-227 (1996).
9. Bredt, D.S., Glatt, C.E., Huang, P.L., Fotuhi, M., Dawson, T.M. & Snyder, S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7, 615-624 (1991).
10. Huang, P.L., Dawson, T.M., Bredt, D.S., Snyder, S.H. & Fishman, M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75, 1273-1285 (1993).
11. Lowenstein, C.J., Glatt, C.S., Bredt, D.S. & Snyder, S.H. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc. Natl. Acad. Sci. USA 89, 6711-6715 (1992).
12. Keilhoff, G. et al. Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience 75, 1193-1201 (1996).
13. Simmons, M.L. & Murphy, S. Induction of nitric oxide synthase in glial cells. J. Neurochem. 59, 897-905 (1992).
14. Wallace, M.N. & Fredens, K. Activated astrocytes of the mouse hippocampus contain high levels of NADPH-diaphorase. Neuroreport 3, 953-956 (1992).
15. Iadecola, C., Xu, X., Zhang, F., el-Fakahany, E.E. & Ross, M.E. Marked induction of calcium-independent nitric oxide synthase activity after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 15, 52-59 (1995).
16. G-nitro-arginine autoradiography. Neuroscience 75, 881-890 (1996).
17. Dinerman, J.L., Dawson, T.M., Schell, M.J., Snowman, A. & Snyder, S.H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. USA 91, 4214-4218 (1994).
18. Dawson, T.M. & Dawson, V.L. in Nitric oxide Sources and Detection of NO; NO Synthase (ed. Packer, L.) 349-358 (Academic, New York, 1996).
19. Schulz, J.B., Matthews, R.T., Muqit, M.M.K., Browne, S.E. & Beal, M.F. Inhibition of neuronal nitric oxide synthase by 7-nitroindazole protects against MPTP-induced neurotoxicity in mice. J. Neurochem. 64, 936-939 (1995).
20. Przedborski, S. et al. Role of neuronal nitric oxide in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine)-induced dopaminergic neurotoxicity. Proc. Natl. Acad. Sci. USA 93, 4565-4571 (1996).
21. Hantraye, P. et al. Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nature Med. 2, 1017-1021 (1996).
22. Matthews, R.T., Yang, L.C. & Beal, M.F. S-methylthiocitrulline, a neuronal nitric oxide synthase inhibitor, protects against malonate and MPTP neurotoxicity. Exp. Neurol. 143, 282-286 (1997).
23. Hunot, S. et al. Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 72, 355-363 (1996).
24. Adamson, D.C. et al. Immunologic NO synthase: elevation in severe AIDS dementia and induction by HIV-1 gp41. Science 274, 1917-1921 (1996).
25. Nathan, C. & Xie, Q.W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269, 13725-13728 (1994).
26. Giovanni, A., Sieber, B.A., Heikkila, R.E. & Sonsalla, P.K. Correlation between the neostriatal content of the 1-methyl-4-phenylpyridinium species and dopaminergic neurotoxicity following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration to several strains of mice. J. Pharmacol. Exp. Ther. 257, 691-697 (1991).
27. Forno, L.S., DeLanney, L.E., Irwin, I., Di Monte, D. & Langston, J.W. Astrocytes and Parkinson's disease. Prog Brain Res. 94, 429-436 (1992).
28. Hirsch, E.C., Hunot, S., Damier, P. & Faucheux, B. Glial cells and inflammation in Parkinsons' disease: a role in neurodegeneration? Ann. Neurol. 44 (Suppl. 1), S115-5120(1998).
29. Ridet, J.L., Malhotra, S.K., Privat, A. & Gage, F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570-577 (1997).
30. Gonzalez-Scarano, F. & Baltuch, G. Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240 (1999).
31. Jackson-Lewis, V., Jakowec, M., Burke, R.E. & Przedborski, S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Neurodegeneration 4, 257-269 (1995).
32. Xia, Y. & Zweier, J.L. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages, Proc. Natl. Acad. Sci. USA 94, 6954-6958 (1997).
33. Murphy, S. et al. Synthesis of nitric oxide in CNS glial cells. Trends Neurosci. 16, 323-328 (1993).
34. Galea, E., Feinstein, D.L. & Reis, D.J. Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc Natl. Acad. Sci. USA 89, 10945-10949 (1992).
35. 1. Glia 22, 282-294 (1998).
36. Dugas, N. et al. Regulation by endogenous interleukin 10 of the expression of nitric oxide synthase induced after ligation of CD23 in human macrophages. Cytokine. 10, 680-689 (1998).
37. Hunot, S. et al. FcεRII/CD23 is expressed in Parkinson's disease and induces, in vitro, production of nitric oxide and tumor necrosis factor-alpha in glial cells. J. Neurosci. 19, 3440-3447 (1999).
38. MacMicking, J., Xie, Q.-W. & Nathan, C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350 (1997)
39. Halliwell, B. & Gutteridge, J.M. in Free Radicals in Biology and Medicine (Clarendon, Oxford, 1991).
40. MacMicking, J. et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81, 641-650 (1995).
41. Nathan, C. & Root, R.K. Hydrogen peroxide release from mouse peritoneal macrophages. Dependence on sequential activation and triggering. J. Exp. Med. 146, 1648-1662 (1977).
42. Leonard, C.S., Kerman, I., Blaha, G., Taveras, E. & Taylor, B. Interdigitation of nitric oxide synthase-, tyrosine hydroxylase-, and serotonin-containing neurons in and around the laterodorsal and pedunculopontine tegmental nuclei of the guinea pig. J. Comp. Neurol. 362, 411-432 (1995).
43. Dawson, T.M. & Snyder, S.H. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J. Neurosci. 14, 5147-5159 (1994).
44. Beckman, J.S. et al. Kinetics of superoxide dismutase-and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298, 438-445 (1992).
45. Ara, J. et al. Inactivation of tyrosine hydroxylase by nitration following exposure to peroxynitrite and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Proc. Natl. Acad. Sci. USA 95, 7659-7663 (1998).
46. Almer, G., Vukosavic, S., Romero, N. & Przedborski, S. Inducible nitric oxide synthase upregulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem, 72, 2415-2425 (1999).
47. Asmus, S.E. & Newman, S.W. Colocalization of tyrosine hydroxylase and Fos in the male Syrian hamster brain following different states of arousal. J. Neurobiol. 25, 156-168 (1994).
48. Mandir, A.S. et al. Poly (ADP-ribose) polymerase activation mediates MPTP-induced parkinsonism. Proc. Natl. Acad. Sci. USA 96, 5774-5779 (1999).
49. Coggeshall, R.E. & Lekan, H.A. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J. Comp. Neurol. 364, 6-15 (1996).
50. West, M.J. New stereological methods for counting neurons. Neurobiol. Aging 14, 275-285 (1993).
51. Ye, Y.Z., Strong, M., Huang, Z.-Q. & Beckman, J.S. in Nitric Oxide. Physiological and Pathological Processes (ed. Packer, L.) 201-209 (Acedemic, New York, 1996).