Overexpressed neuroglobin raises threshold for nitric oxide-induced impairment of mitochondrial respiratory activities and stress signaling in primary cortical neurons

Nitric Oxide - Biology and Chemistry

Volumn 32, Issue , 2013, Pages 21-28

  Singh, Shilpee ^a   Zhuo, Ming ^a   Gorgun, Falih M ^a   Englander, Ella W ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

ATP synthesis; Bioenergetics; Mitochondrial respiration; Neuroglobin transgene; Nitric oxide; Primary neurons

Indexed keywords

ADENOSINE TRIPHOSPHATE; BUFFER; HEME OXYGENASE 1; NEUROGLOBIN; NITRIC OXIDE; OXYGEN; PROTEIN C FOS; PROTON;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE CELL LESION; NITRATION; NITROSATIVE STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; CEREBRAL CORTEX; GLOBINS; HEME OXYGENASE-1; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; NERVE TISSUE PROTEINS; NEURONS; NITRIC OXIDE; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-FOS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84877075192     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.03.008     Document Type: Article

References (52)

1. T. Burmester, B. Weich, S. Reinhardt, and T. Hankeln A vertebrate globin expressed in the brain Nature 407 2000 520 523
2. J. Droge, A. Pande, E.W. Englander, and W. Makalowski Comparative genomics of neuroglobin reveals its early origins PLoS One 7 2012 e47972
3. T. Burmester, and T. Hankeln What is the function of neuroglobin? J. Exp. Biol. 212 2009 1423 1428
4. Y. Sun, K. Jin, A. Peel, X.O. Mao, L. Xie, and D.A. Greenberg Neuroglobin protects the brain from experimental stroke in vivo Proc. Natl. Acad. Sci. USA 100 2003 3497 3500 (Pubitemid 36356612)
5. A.A. Khan, Y. Wang, Y. Sun, X.O. Mao, L. Xie, E. Miles, J. Graboski, S. Chen, L.M. Ellerby, K. Jin, and D.A. Greenberg Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia Proc. Natl. Acad. Sci. USA 103 2006 17944 17948 (Pubitemid 44852265)
6. L. Kiger, L. Tilleman, E. Geuens, D. Hoogewijs, C. Lechauve, L. Moens, S. Dewilde, and M.C. Marden Electron transfer function versus oxygen delivery: a comparative study for several hexacoordinated globins across the animal kingdom PLoS One 6 2011 e20478
7. W. Li, Y. Wu, C. Ren, Y. Lu, Y. Gao, X. Zheng, and C. Zhang The activity of recombinant human neuroglobin as an antioxidant and free radical scavenger Proteins 79 2011 115 125
8. T. Brittain, and J. Skommer Does a redox cycle provide a mechanism for setting the capacity of neuroglobin to protect cells from apoptosis? IUBMB Life 64 2012 419 422
9. S. Watanabe, N. Takahashi, H. Uchida, and K. Wakasugi Human neuroglobin functions as an oxidative stress-responsive sensor for neuroprotection J. Biol. Chem. 287 2012 30128 30138
10. C.A. Hundahl, J. Fahrenkrug, A. Hay-Schmidt, B. Georg, B. Faltoft, and J. Hannibal Circadian behaviour in neuroglobin deficient mice PLoS One 7 2012 e34462
11. C.A. Hundahl, J. Kelsen, S. Dewilde, and A. Hay-Schmidt Neuroglobin in the rat brain (II): co-localisation with neurotransmitters Neuroendocrinology 88 2008 183 198
12. H.M. Lee, G.H. Greeley Jr., and E.W. Englander Transgenic overexpression of neuroglobin attenuates formation of smoke-inhalation-induced oxidative DNA damage, in vivo, in the mouse brain Free Radic. Biol. Med. 51 2011 2281 2287
13. H.M. Lee, J. Reed, G.H. Greeley Jr., and E.W. Englander Impaired mitochondrial respiration and protein nitration in the rat hippocampus after acute inhalation of combustion smoke Toxicol. Appl. Pharmacol. 235 2009 208 215
14. M. Brunori, A. Giuffre, K. Nienhaus, G.U. Nienhaus, F.M. Scandurra, and B. Vallone Neuroglobin, nitric oxide, and oxygen: functional pathways and conformational changes Proc. Natl. Acad. Sci. USA 102 2005 8483 8488 (Pubitemid 40862762)
15. S. Van Doorslaer, S. Dewilde, L. Kiger, S.V. Nistor, E. Goovaerts, M.C. Marden, and L. Moens Nitric oxide binding properties of neuroglobin. A characterization by EPR and flash photolysis J. Biol. Chem. 278 2003 4919 4925 (Pubitemid 36800999)
16. B.G. Hill, B.P. Dranka, S.M. Bailey, J.R. Lancaster Jr., and V.M. Darley-Usmar What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology J. Biol. Chem. 285 2010 19699 19704
17. J.C. Toledo Jr., and O. Augusto Connecting the chemical and biological properties of nitric oxide Chem. Res. Toxicol. 25 2012 975 989
18. S. Moncada, and J.P. Bolanos Nitric oxide, cell bioenergetics and neurodegeneration J. Neurochem. 97 2006 1676 1689 (Pubitemid 43873660)
19. C.A. Piantadosi, and H.B. Suliman Redox regulation of mitochondrial biogenesis Free Radic. Biol. Med. 53 2012 2043 2053
20. F.J. Larsen, T.A. Schiffer, E. Weitzberg, and J.O. Lundberg Regulation of mitochondrial function and energetics by reactive nitrogen oxides Free Radic. Biol. Med. 2012
21. A. Almeida, J. Almeida, J.P. Bolanos, and S. Moncada Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection Proc. Natl. Acad. Sci. USA 98 2001 15294 15299 (Pubitemid 34014008)
22. O. Kann, and R. Kovacs Mitochondria and neuronal activity Am. J. Physiol. Cell Physiol. 292 2007 C641 657
23. D.G. Nicholls Oxidative stress and energy crises in neuronal dysfunction Ann. NY Acad. Sci. 1147 2008 53 60
24. M.T. Wong-Riley Bigenomic regulation of cytochrome c oxidase in neurons and the tight coupling between neuronal activity and energy metabolism Adv. Exp. Med. Biol. 748 2012 283 304
25. G.J. Brewer, J.R. Torricelli, E.K. Evege, and P.J. Price Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination J. Neurosci. Res. 35 1993 567 576 (Pubitemid 23215708)
26. H. Li, R. Swiercz, and E.W. Englander Elevated metals compromise repair of oxidative DNA damage via the base excision repair pathway: implications of pathologic iron overload in the brain on integrity of neuronal DNA J. Neurochem. 110 2009 1774 1783
27. S. Singh, and E.W. Englander Nuclear depletion of apurinic/apyrimidinic endonuclease 1 (Ape1/Ref-1) is an indicator of energy disruption in neurons Free Radic. Biol. Med. 53 2012 1782 1790
28. T.D. Schmittgen, and K.J. Livak Analyzing real-time PCR data by the comparative C(T) method Nat. Protoc. 3 2008 1101 1108 (Pubitemid 351818697)
29. Y.H. Wang, and S.C. Borkan Prior heat stress enhances survival of renal epithelial cells after ATP depletion Am. J. Physiol. 270 1996 F1057 1065
30. E.W. Englander, and S.H. Wilson Protein binding elements in the human beta-polymerase promoter Nucleic Acids Res. 18 1990 919 928
31. Y. Abe, T. Sakairi, H. Kajiyama, S. Shrivastav, C. Beeson, and J.B. Kopp Bioenergetic characterization of mouse podocytes Am. J. Physiol. Cell Physiol. 299 2010 C464 476
32. M.D. Brand, and D.G. Nicholls Assessing mitochondrial dysfunction in cells Biochem. J. 435 2011 297 312
33. B.P. Dranka, G.A. Benavides, A.R. Diers, S. Giordano, B.R. Zelickson, C. Reily, L. Zou, J.C. Chatham, B.G. Hill, J. Zhang, A. Landar, and V.M. Darley-Usmar Assessing bioenergetic function in response to oxidative stress by metabolic profiling Free Radic. Biol. Med. 51 2011 1621 1635
34. K. Jin, X.O. Mao, L. Xie, A.A. Khan, and D.A. Greenberg Neuroglobin protects against nitric oxide toxicity Neurosci. Lett. 430 2008 135 137
35. A.A. Gerencser, A. Neilson, S.W. Choi, U. Edman, N. Yadava, R.J. Oh, D.A. Ferrick, D.G. Nicholls, and M.D. Brand Quantitative microplate-based respirometry with correction for oxygen diffusion Anal. Chem. 81 2009 6868 6878
36. J.P. Bolanos, A. Herrero-Mendez, S. Fernandez-Fernandez, and A. Almeida Linking glycolysis with oxidative stress in neural cells: a regulatory role for nitric oxide Biochem. Soc. Trans. 35 2007 1224 1227 (Pubitemid 350206467)
37. Z. Gu, T. Nakamura, and S.A. Lipton Redox reactions induced by nitrosative stress mediate protein misfolding and mitochondrial dysfunction in neurodegenerative diseases Mol. Neurobiol. 41 2010 55 72
38. J.D. Erusalimsky, and S. Moncada Nitric oxide and mitochondrial signaling: from physiology to pathophysiology Arterioscler Thromb Vasc. Biol. 27 2007 2524 2531 (Pubitemid 350158901)
39. P. Sarti, M. Arese, E. Forte, A. Giuffre, and D. Mastronicola Mitochondria and nitric oxide: chemistry and pathophysiology Adv. Exp. Med. Biol. 942 2012 75 92
40. J.R. Brorson, P.T. Schumacker, and H. Zhang Nitric oxide acutely inhibits neuronal energy production. The Committees on Neurobiology and Cell Physiology J. Neurosci. 19 1999 147 158 (Pubitemid 29028957)
41. U. Flogel, M.W. Merx, A. Godecke, U.K. Decking, and J. Schrader Myoglobin: a scavenger of bioactive NO Proc. Natl. Acad. Sci. USA 98 2001 735 740 (Pubitemid 32105112)
42. S. Herold, A. Fago, R.E. Weber, S. Dewilde, and L. Moens Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress J. Biol. Chem. 279 2004 22841 22847 (Pubitemid 38685584)
43. S. Orlowski, and W. Nowak Topology and thermodynamics of gaseous ligands diffusion paths in human neuroglobin Biosystems 94 2008 263 266
44. H.M. Lee, G.H. Greeley, D.N. Herndon, M. Sinha, B.A. Luxon, and E.W. Englander A rat model of smoke inhalation injury: influence of combustion smoke on gene expression in the brain Toxicol. Appl. Pharmacol. 208 2005 255 265 (Pubitemid 41460536)
45. Z. Ying-ying, M.K. Enci, C. Qiong, L. Eng-ang, Combustion smoke induced inflammation in the cerebellum and hippocampus of adult rats. Neuropathol Appli Neurobiol (2-12) Oct 29-epub ahead of print-doi:10.111/nan.12001.
46. N. Yadava, and D.G. Nicholls Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone J. Neurosci. 27 2007 7310 7317 (Pubitemid 47037569)
47. J. Alam, J. Cai, and A. Smith Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 5' sequences are required for induction by heme or heavy metals J. Biol. Chem. 269 1994 1001 1009
48. J.K. Cui, C.Y. Hsu, and P.K. Liu Suppression of postischemic hippocampal nerve growth factor expression by a c-fos antisense oligodeoxynucleotide J. Neurosci. 19 1999 1335 1344 (Pubitemid 29088916)
49. J. Cui, and P.K. Liu Neuronal NOS inhibitor that reduces oxidative DNA lesions and neuronal sensitivity increases the expression of intact c-fos transcripts after brain injury J. Biomed. Sci. 8 2001 336 341 (Pubitemid 32678940)
50. M. Murphy, U. Greferath, N. Nag, J. Nithianantharajah, and Y.M. Wilson Tracing functional circuits using c-Fos regulated expression of marker genes targeted to neuronal projections Front Biosci. 9 2004 40 47 (Pubitemid 38925437)
51. A. Contestabile Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells Prog. Neurobiol. 84 2008 317 328
52. C.A. Hundahl, H. Luuk, S. Ilmjarv, B. Falktoft, Z. Raida, J. Vikesaa, L. Friis-Hansen, and A. Hay-Schmidt Neuroglobin-deficiency exacerbates Hif1A and c-FOS response, but does not affect neuronal survival during severe hypoxia in vivo PLoS One 6 2011 e28160