Mitigation of peroxynitrite-mediated nitric oxide (NO) toxicity as a mechanism of induced adaptive NO resistance in the CNS

Journal of Neurochemistry

Volumn 109, Issue 1, 2009, Pages 74-84

  Bishop, Amy ^a   Gooch, Renea ^a   Eguchi, Asuka ^a   Jeffrey, Stephanie ^a   Smallwood, Lorraine ^a   Anderson, James ^b   Estevez, Alvaro G ^c  

^a UNIVERSITY OF ALABAMA IN HUNTSVILLE   (United States)

^b Department of Biological Sciences   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Heme oxygenase 1; Motor neurons; Nitric oxide; Nitrotyrosine; Peroxynitrite; Resistance

Indexed keywords

HEME OXYGENASE 1; HEME OXYGENASE INHIBITOR; NITRIC OXIDE; PEROXYNITRITE;

ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENOTYPE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL DEATH; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASES; FEMALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MOTOR NEURONS; NITRIC OXIDE; PEROXYNITROUS ACID; PREGNANCY; REACTIVE NITROGEN SPECIES;

MUS;

EID: 61849184107     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05884.x     Document Type: Article

References (53)

1. Akins R. Jr., McLaughlin T., Boyce R., Gilmour L. Gratton K. (2004) Exogenous metalloporphyrins alter the organization and function of cultured neonatal rat heart cells via modulation of heme oxygenase activity. J. Cell. Physiol. 201, 26 34.
2. Beckman J. S. (1996) Oxidative damage and tyrosine nitration from peroxynitrite. Chem. Res. Toxicol. 9, 836 844.
3. Bishop A. Anderson James (2005) NO signaling in the CNS: from the physiological to the pathological. Toxicology 208, 193 205.
4. Bishop A. Cashman Neil R. (2003) Induced adaptive resistance to oxidative stress in the CNS: discussion of possible mechanisms and their therapeutic potential. Curr. Drug Metab. 4, 171 184.
5. Bishop A., Marquis J. C., Cashman N. R. Demple B. (1999) Adaptive resistance to nitric oxide in motor neurons. Free Radic. Biol. Med. 26, 978 986.
6. Bishop A., Shaw Fung-Yet., Mark J. Perrella, Arthur M. Lee., Cashman Neil R. Demple Bruce (2004) Decreased resistance to nitric oxide in motor neurons of HO-1 null mice. BBRC 325, 3 9.
7. Bouton C. Demple B. (2000) Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J. Biol. Chem. 275, 32688 32693.
8. Brenman J. E. Bredt D. S. (1996) Nitric oxide signaling in the nervous system. Meth. Enzymol. 269, 119 129.
9. Cashman N. R., Durham H. D., Blusztajn J. K., Oda K., Tabira T., Shaw I. T., Dahrouge S. Antel J. P. (1992) Neuroblastoma × spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dynamics 194, 209 221.
10. Cassina P., Peluffo H., Pehar M., Martinez-Palma L., Ressia A., Beckman J. S., Estevez A. G. Barbeito L. (2002) Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J. Neurosci. Res. 67, 21 29.
11. Clough G. F., Bennett A. R. Church M. K. (1998) Measurement of nitric oxide concentration in human skin in vivo using dermal microdialysis. Exp. Physiol. 83, 431 434.
12. Cornish A. S., Jijon H., Yachimec C. Madsen K. L. (2002) Peroxynitrite enhances the ability of Salmonella dublin to invade T84 monolayers. Shock 18, 93 96.
13. Dickhout J. G., Hossain G. S., Pozza L. M., Zhou J., Lhoták S. Austin R. C. (2005) Vascular endothelium: implications in atherogenesis. Arterioscler. Thromb. Vasc. Biol. 25, 2623 2629.
14. Durham H. D., Dahrouge S. Cashman N. R. (1993) Evaluation of the spinal cord neuron X neuroblastoma hybrid cell line NSC-34 as a model for neurotoxicity testing. Neurotoxicology 14, 387 395.
15. Eggett C. J., Crosier S., Manning P., Cookson M. R., Menzies F. M., McNeil C. J. Shaw P. J. (2000) Development and characterisation of a glutamate-sensitive motor neuron cell line. J. Neurochem. 74, 1895 1902.
16. Espey M. G., Xavier S., Thomas D. D., Miranda K. M. Wink W. D. (2002) Direct real-time evaluation of nitration with green fluorescent protein in solution and within human cells reveals the impact of nitrogen dioxide vs. peroxynitrite mechanisms. Proc. Natl Acad. Sci. USA 99, 3481 3486.
17. Estevez A. G., Spear N., Manuel S. M., Radi R., Henderson C. E., Barbieto L. Beckman J. S. (1998) Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18, 923 931.
18. Estevez A. G., Sampson J. B., Zhuang Y.-X., Spear N., Richardson G. J., Crow J. P., Tarpey M. M., Barbeito L. Beckman J. S. (2000) Liposome-delivered superoxide dismutase prevents nitric oxide dependent motor neuron death induced by trophic factor withdrawal. Free Radic. Biol. Med. 28, 437 446.
19. Feelisch M., te Poel M., Zamora R., Deussen A. Moncada S. (1994) Understanding the controversy over the identity of EDRF. Nature 368, 62 65.
20. Fung-Yet S., Perrella M. A., Layne M. D., Hsieh C. M., Maemura K., Kobzik L., Weisel P., Christou H., Kourembanas S. Lee Mu-En (Arthur) (1999) Hypoxia induces severe right ventricular dilation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103, R23 R29.
21. Garcia-Nogales P., Angeles A. Bolanos J. P. (2003) Peroxynitrite protects neurons against nitric oxide-mediated apoptosis: a key role for glucose-6-phospate dehydrogenase activity in neuroprotection. J. Biol. Chem. 278, 864 874.
22. Hall E. D., Oostveen J. A. Gurney M. E. (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23, 249 256.
23. Hobbs A. J. Ignarro L. J. (1996) Nitric oxide-cyclic GMP signal transduction system. Meth. Enzymol. 269, 134 148.
24. Hooper D. C., Scott G. S., Zborek A., Mikheeva T., Kean R. B., Koprowski H. Spitsin S. V. (2000) Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes, and tissue damage in a mouse model of MS. FASEB J. 14, 691 698.
25. Huk I., Brovkovych V., Nanobash Vili J., Weigel G., Neumayer Ch., Partyka L., Patton S. Malinski T. (1998) Bioflavonoid quercetin scavenges superoxide and increases nitric oxide concentration in ischaemia-reperfusion injury: an experimental study. Br. J. Surg. 85, 1080 1085.
26. Ischiropoulos H. Beckman J. S. (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J. Clin. Invest. 111, 163 169.
27. Juckett M., Zheng Y., Yuan H., Pastor T., Antholine W., Weber M. Vercellotti G. (1998) Heme and the endothelium. Effects of nitric oxide on catalytic iron and heme degradation by heme oxygenase. J. Biol. Chem. 273, 23388 23397.
28. Kawase M., Kinouchi H., Kato I., Akabane A., Kondo T., Arai S., Fujimura M., Okamoto H. Yoshimoto T. (1996) Inducible nitric oxide synthase following hypoxia in rat cultured glial cell. Brain Res. 738, 319 322.
29. Kitamura Y., Ishida Y., Takata K. et al. (2003) Hyperbilirubinemia protects against focal ischemia in rats. J. Neurosci. Res. 71, 544 550.
30. Kuljis R. O. Schelper R. L. (1996) Alterations in nitrogen monoxide-synthesizing cortical neurons in amyotrophic lateral sclerosis with dementia. J. Neuropathol. Exp. Neurol. 55, 25 35.
31. Leonard C. S., Michaelis E. K. Mitchell K. M. (2001) Activity-dependent nitric oxide concentration dynamics in the laterodorsal tegmental nucleus in vitro. J. Neurophysiol. 86, 2159 2172.
32. MacMicking J., Xie Q. W. Nathan C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323 350.
33. Maines M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517 554.
34. Matsumoto A., Yoshino H., Yuki N., Hara Y., Cashman N. R., Handa S. Miyatake T. (1995) Ganglioside characterization of a cell line displaying motor neuron-like phenotype: GM2 as a possible major ganglioside in motor neurons. J. Neurol. Sci. 131, 111 118.
35. McDonald J. W. and the Research Consortium of the Christopher Reeve Paralysis Foundation (1999) Repairing the damaged spinal cord. Sci. Am. 281, 64 73.
36. Pacher P., Beckman J. S. Liaudet L. (2007) Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315 424.
37. Packer M. A., Stasiv Y., Benraiss A., Chmieinicki E., Grinberg A., Westphal H., Goldman S. A. Enikolopov G. (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl Acad. Sci. USA 100, 9566 9571.
38. Panahian N. Maines M. D. (2001) Site of injury-directed induction of heme oxygenase-1 and -2 in experimental spinal cord injury: differential functions in neuronal defense mechanisms? J. Neurochem. 76, 539 554.
39. Pfeiffer S., Leopold E., Hemmens B., Schmidt K., Werner E. R. Mayer B. (1997) Interference of carboxy-PTIO with nitric oxide- and peroxynitrite- mediated reactions. Free Radic. Biol. Med. 22, 787 794.
40. Schipper H. M., Cisse S. Stopa E. (1995) Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann. Neurol. 37, 758 768.
41. Schnaar R. I. Schaffner A. E. (1981) Separation of cell types from embryonic chicken and rat spinal cord: characterization of motoneuron-enriched fractions. J. Neurosci. 1, 204 217.
42. Scorziello A., Santillo M., Adornetto A., Dell'Aversano C., Sirabella R., Damiano S., Canzoniero L. M. T., Di Renzo G. F. Annunziato L. (2007) NO-induced neuroprotection in ischemic preconditioning stimulates mitochondrial Mn-SOD activity and expression via RAS/ERK1/2 pathway. J. Neurochem. 103, 1472 1480.
43. Sharma H. S., Westman J., Olsson Y. Alm P. (1996) Involvement of nitric oxide in acute spinal cord injury: an immunocytochemical study using light and electron microscopy in the rat. Neurosci. Res. 24, 373 384.
44. Soares M. P., Usheva A., Brouard S., Berberat P. O., Gunther L., Tobiasch E. Bach F. H. (2002) Modulation of endothelial cell apoptosis by heme oxygenase-1-derived carbon monoxide. Antioxid. Redox Signal. 4, 321 329.
45. Stamler J. S., Jia L., Eu J. P., Mcmahon T. J., Demchenko I. T., Bonaventura J., Gernert K. Piantadosi C. A. (1997) Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276, 2034 2037.
46. Stuehr D. J. (1999) Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1411, 217 230.
47. Tamir S., Lewis R. S., de Rojas Walker T., Deen W. M., Wishnok J. S. Tannenbaum S. R. (1993) The influence of delivery rate on the chemistry and biological effects of nitric oxide. Chem. Res. Toxicol. 6, 895 899.
48. Tamir S., Burney S. Tannenbaum S. R. (1996) DNA damage by nitric oxide. Chem. Res. Toxicol. 9, 821 827.
49. - reaction. Proc. Natl Acad. Sci. USA 99, 12691 12696.
50. Tominaga T., Sato S., Ohnishi T. Ohnishi S. T. (1994) Electron paramagnetic resonance (EPR) detection of nitric oxide produced during forebrain ischemia of the rat. J. Cereb. Blood Flow Metab. 14, 715 722.
51. Vaziri N. D., Lee Y. S., Lin C. Y., Lin V. W. Sindhu R. K. (2004) NAD(P)H oxidase, superoxide dismutase, catalase, glutathione peroxidase and nitric oxide synthase expression in subacute spinal cord injury. Brain Res. 995, 76 83.
52. Yang G., Nguyen X., Ou J., Rekulapelli P., Stevenson D. K. Dennery P. A. (2001) Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood. 97, 1306 1313.
53. Zimmermann A., Leffler C. W., Tcheranova D., Fedinec A. L. Parfenova H. (2007) Cerebroprotective effects of the CO-releasing molecule CORM-A1 against seizure-induced neonatal vascular injury. Am. J. Physiol. Heart Circ. Physiol. 293, H2501 H2507.