Tumor necrosis factor alpha-mediated nitric oxide production enhances manganese superoxide dismutase nitration and mitochondrial dysfunction in primary neurons: an insight into the role of glial cells

Neuroscience

Volumn 151, Issue 2, 2008, Pages 622-629

  Tangpong, J ^a   Sompol, P ^b,d   Vore, M ^b   St Clair, W ^c   Butterfield, D A ^b   St Clair, D K ^b  

^a WALAILAK UNIVERSITY   (Thailand)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d MAHIDOL UNIVERSITY   (Thailand)

Author keywords

CNS toxicity; iNOSKO; mitochondrial dysfunction; MnSOD nitration; nitric oxide; tumor necrosis factor alpha

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MANGANESE SUPEROXIDE DISMUTASE; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL ACTIVATION; CELL ISOLATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GLIA CELL; IMMUNE SYSTEM; MICROGLIA; MOUSE; NERVE CELL; NERVE CELL CULTURE; NEUROENDOCRINE SYSTEM; NEUROTOXICITY; NITRATION; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEUROGLIA; NEURONS; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; SUPEROXIDE DISMUTASE; TETRAZOLIUM SALTS; THIAZOLES; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE;

EID: 37849010216     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.10.046     Document Type: Article

References (53)

1. Abe K., Pan L.H., Watanabe M., Kato T., and Itoyama Y. Induction of nitrotyrosine-like immunoreactivity in the lower motor neuron of amyotrophic lateral sclerosis. Neurosci Lett 20 (1995) 152-154
2. Abe K., Pan L.H., Watanabe M., Konno H., Kato T., and Itoyama Y. Upregulation of protein-tyrosine nitration in the anterior horn cells of amyotrophic lateral sclerosis. Neurol Res 19 2 (1997) 124-128
3. P264L/P264L double knock-in mouse model of Alzheimer's disease. Am J Pathol 168 5 (2006) 1608-1618
4. Beal M.F., Ferrante R.J., Browne S.E., Matthews R.T., Kowall N.W., and Brown Jr. R.H. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann Neurol 42 4 (1997) 644-654
5. Beckman J.S., and Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271 (1996) C1424-C1437
6. Brown G.C., and Cooper C.E. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 19 (1994) 295-298
7. Brown G.C. Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: implications for inflammatory, neurodegenerative and ischaemic pathologies [review]. Mol Cell Biochem 174 (1997) 189-192
8. Bruijn L.I., Beal M.F., Becher M.W., Schulz J.B., Wong P.C., Price D.L., and Cleveland D.W. Elevated free nitrotyrosine levels, but not protein-bound nitrotyrosine or hydroxyl radicals, throughout amyotrophic lateral sclerosis (ALS)-like disease implicate tyrosine nitration as an aberrant in vivo property of one familial ALS-linked superoxide dismutase 1 mutant. Proc Natl Acad Sci U S A 8 (1997) 7606-7611
9. Cassina A., and Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 15 (1996) 309-316
10. Castro L., Rodriguez M., and Radi R. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 25 (1994) 29409-29415
11. Chao C.C., Hu S., Molitor T.W., Shaskan E.G., and Peterson P.K. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 15 (1992) 2736-2741
12. Davis R.E., Miller S., Herrnstadt C., Ghosh S.S., Fahy E., Shinobu L.A., Galasko D., Thal L.J., Beal M.F., Howell N., and Parker Jr. W.D. Mutations in mitochondrial cytochrome c oxidase genes segregate with late-onset Alzheimer's disease. Proc Natl Acad Sci U S A 29 (1996) 4526-4531
13. Dickson D.W., Lee S.C., Mattiace L.A., Yen S.H., and Brosnan C. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7 1 (1993) 75-83
14. Espey M.G., Chernyshev O.N., Reinhard Jr. J.F., Namboodiri M.A., and Colton C.A. Activated human microglia produce the excitotoxin quinolinic acid. Neuroreport 20 (1997) 431-434
15. Estévez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., and Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 24 (1999) 2498-2500
16. Estévez A.G., Spear N., Manuel S.M., Radi R., Henderson C.E., Barbeito L., and Beckman J.S. Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J Neurosci 1 (1998) 923-931
17. Ferrante R.J., Shinobu L.A., Schulz J.B., Matthews R.T., Thomas C.E., Kowall N.W., Gurney M.E., and Beal M.F. Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann Neurol 42 3 (1997) 326-334
18. Ferrante R.J., Browne S.E., Shinobu L.A., Bowling A.C., Baik M.J., MacGarvey U., Kowall N.W., Brown Jr. R.H., and Beal M.F. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem 69 5 (1997) 2064-2074
19. Filipovic M.R., Stanic D., Raicevic S., Spasic M., and Niketic V. Consequences of MnSOD interactions with nitric oxide: nitric oxide dismutation and the generation of peroxynitrite and hydrogen peroxide. Free Radic Res 41 1 (2007) 62-72
20. Floden A.M., Li S., and Combs C.K. Beta-amyloid-stimulated microglia induce neuron death via synergistic stimulation of tumor necrosis factor alpha and NMDA receptors. J Neurosci 9 (2005) 2566-2575
21. Gao H.M., Jiang J., Wilson B., Zhang W., Hong J.S., and Lin B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 81 (2002) 1285-1297
22. Gerlier D., and Thomasset N. Use of MTT colorimetric assay to measure cell activation. J Immunol Methods 20 (1986) 57-63
23. Gomez-Chiarri M., Ortiz A., Lerma J.L., Lopez-Armada M.J., Mampaso F., Gonzalez E., and Egido J. Involvement of tumor necrosis factor and platelet-activating factor in the pathogenesis of experimental nephrosis in rats. Lab Invest 70 4 (1994) 449-459
24. Guo W., Adachi T., Matsui R., Xu S., Jiang B., Zou M.H., Kirber M., Lieberthal W., and Cohen R.A. Quantitative assessment of tyrosine nitration of manganese superoxide dismutase in angiotensin II-infused rat kidney. Am J Physiol Heart Circ Physiol 285 4 (2003) H1396-H1403
25. Hausladen A., and Fridovich I. Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J Biol Chem 26 (1994) 29405-29408
26. Hirose K., Longo D.L., Oppenheim J.J., and Matsushima K. Overexpression of mitochondrial manganese superoxide dismutase promotes the survival of tumor cells exposed to interleukin-1, tumor necrosis factor, selected anticancer drugs, and ionizing radiation. FASEB J 7 2 (1993) 361-368
27. Hirsch E.C., Breidert T., Rousselet E., Hunot S., Hartmann A., and Michel P.P. The role of glial reaction and inflammation in Parkinson's disease. Ann N Y Acad Sci 991 (2003) 214-228
28. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., and Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1 (1992) 431-437
29. Jones S.P., Hoffmeyer M.R., Sharp B.R., Ho Y.S., and Lefer D.J. PKA-dependent binding of mRNA to the mitochondrial AKAP121 protein. J Mol Biol 327 4 (2003) 885-897
30. Keller J.N., Kindy M.S., Holtsberg F.W., St. Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., and Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci 18 2 (1998) 687-697
31. Klivenyi P., St. Clair D., Wermer M., Yen H.C., Oberley T., Yang L., and Flint Beal M. Manganese superoxide dismutase overexpression attenuates MPTP toxicity. Neurobiol Dis 5 4 (1998) 253-258
32. Lebovitz R.M., Zhang H., Vogel H., Cartwright J., Dionne Jr. L., Lu N., Huang S., and Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci U S A 93 (1996) 9782-9787
33. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., Noble L.J., Yoshimura M.P., Berger C., Chan P.H., Wallace D.C., and Epstein C.J. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11 4 (1995) 376-381
34. Liao S.L., Chen W.Y., Raung S.L., Kuo J.S., and Chen C.J. Association of immune responses and ischemic brain infarction in rat. Neuroreport 12 (2001) 1943-1947
35. Liu B., Gao H.M., Wang J.Y., Jeohn G.H., Cooper C.L., and Hong J.S. Role of nitric oxide in inflammation-mediated neurodegeneration. Ann N Y Acad Sci 962 (2002) 700-715
36. Lovell M.A., Robertson J.D., Teesdale W.J., Campbell J.L., and Markesbery W.R. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 158 (1998) 47-52
37. MacMillan-Crow L.A., Crow J.P., Kerby J.D., Beckman J.S., and Thompson J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci U S A 93 (1996) 11853-11858
38. MacMillan-Crow L.A., and Thompson J.A. Tyrosine modifications and inactivation of active site manganese superoxide dismutase mutant (Y34F) by peroxynitrite. Arch Biochem Biophys 366 1 (1999) 82-88
39. Maragos W.F., Jakel R., Chesnut D., Pocernich C.B., Butterfield D.A., St. Clair D., and Cass W.A. Methamphetamine toxicity is attenuated in mice that overexpress human manganese superoxide dismutase. Brain Res 878 1-2 (2000) 218-222
40. Minghetti L., and Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 54 (1998) 99-125
41. Pfeiffer S., Leopold E., Hemmens B., Schmidt K., Werner E.R., and Mayer B. Interference of carboxy-PTIO with nitric oxide- and peroxynitrite-mediated reactions. Free Radic Biol Med 22 5 (1997) 787-794
42. Poljakovic M., Nygren J.M., and Persson K. Signalling pathways regulating inducible nitric oxide synthase expression in human kidney epithelial cells. Eur J Pharmacol 23 (2003) 21-28
43. St. Clair D.K., Oberley T.D., and Ho Y.S. Overproduction of human Mn-superoxide dismutase modulates paraquat-mediated toxicity in mammalian cells. FEBS Lett 18 (1991) 199-203
44. St. Clair D.K., Wan X.S., Oberley T.D., Muse K.E., and St. Clair W.H. Suppression of radiation-induced neoplastic transformation by overexpression of mitochondrial superoxide dismutase. Mol Carcinog 6 4 (1992) 238-242
45. Streit W.J. Microglial response to brain injury: a brief synopsis. Toxicol Pathol 28 (2000) 28-30
46. Sullivan P.G., Bruce-Keller A.J., Rabchevsky A.G., Christakos S., St. Clair D.K., Mattson M.P., and Scheff S.W. Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J Neurosci 19 15 (1999) 6248-6256
47. Tangpong J., Cole M.P., Sultana R., Joshi G., Estus S., Vore M., St. Clair W., Ratanachaiyavong S., St. Clair D.K., and Butterfield D.A. Adriamycin-induced, TNF-alpha-mediated central nervous system toxicity. Neurobiol Dis 23 1 (2006) 127-139
48. Tangpong J., Cole M.P., Sultana R., Estus S., Vore M., St. Clair W., Ratanachaiyavong S., St. Clair D.K., and Butterfield D.A. Adriamycin-mediated nitration of manganese superoxide dismutase in the central nervous system: insight into the mechanism of chemobrain. J Neurochem 100 1 (2007) 191-201
49. Tohgi H., Abe T., Yamazaki K., Murata T., Ishizaki E., and Isobe C. Increase in oxidized NO products and reduction in oxidized glutathione in cerebrospinal fluid from patients with sporadic form of amyotrophic lateral sclerosis. Neurosci Lett 5 (1999) 204-206
50. West M., Mhatre M., Ceballos A., Floyd R.A., Grammas P., Gabbita S.P., Hamdheydari L., Mai T., Mou S., Pye Q.N., Stewart C., West S., Williamson K.S., Zemlan F., and Hensley K. The arachidonic acid 5-lipoxygenase inhibitor nordihydroguaiaretic acid inhibits tumor necrosis factor alpha activation of microglia and extends survival of G93A-SOD1 transgenic mice. J Neurochem 91 (2004) 133-143
51. Wispe J.R., Warner B.B., Clark J.C., Dey C.R., Neuman J., Glasser S.W., Crapo J.D., Chang L.Y., and Whitsett J.A. Human Mn-superoxide dismutase in pulmonary epithelial cells of transgenic mice confers protection from oxygen injury. J Biol Chem 25 (1992) 23937-23941
52. Wong G.H., Elwell J.H., Oberley L.W., and Goeddel D.V. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 8 (1989) 923-931
53. Yen H.C., Oberley T.D., Vichitbandha S., Ho Y.S., and St. Clair D.K. The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice. J Clin Invest 98 5 (1996) 1253-1260