Neuroglobin expression and oxidant/antioxidant balance after graded traumatic brain injury in the rat

Free Radical Biology and Medicine

Volumn 69, Issue , 2014, Pages 258-264

  Lazzarino, Giuseppe ^c   Di Pietro, Valentina ^a   Lazzarino, Giacomo ^b   Amorini, Angela Maria ^b   Tavazzi, Barbara ^b   D'urso, Serafina ^c   Longo, Salvatore ^b   Vagnozzi, Roberto ^d   Signoretti, Stefano ^e   Clementi, Elisabetta ^b   Giardina, Bruno ^b   Belli, Antonio ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b CATHOLIC UNIVERSITY   (Italy)

^c UNIVERSITY OF CATANIA   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e SAN CAMILLO FORLANINI HOSPITAL   (Italy)

Author keywords

Brain antioxidants; Free radicals; Neuroglobin; Neuroprotection; Nitrosative stress; Oxidative stress; Traumatic brain injury

Indexed keywords

BRAIN ANTIOXIDANTS; FREE RADICALS; NEUROGLOBIN; NEUROPROTECTION; NITROSATIVE STRESS; OXIDATIVE STRESS; TRAUMATIC BRAIN INJURY;

ANIMALS; ANTIOXIDANTS; BRAIN INJURIES; GLOBINS; GLUTATHIONE; NERVE TISSUE PROTEINS; NITROSATION; OXIDANTS; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84894436009     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.01.032     Document Type: Article

References (56)

1. S. Kakar, F.G. Hoffman, J.F. Storz, M. Fabian, and M.S. Hargrove Structure and reactivity of hexacoordinate hemoglobins Biophys. Chem. 152 2010 1 14
2. S. Dewilde, L. Kiger, T. Burmester, T. Hankeln, V. Baudin-Creuza, T. Aerts, M.C. Marden, R. Caubergs, and L. Moens Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family J. Biol. Chem. 276 2001 38949 38955
3. J.T. Trent 3rd, R.A. Watts, and M.S. Hargrove Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen J. Biol. Chem. 276 2001 30106 30110
4. 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
5. S. Hua, S.T. Antao, A. Corbett, and P.K. Witting The significance of neuroglobin in the brain Curr. Med. Chem. 17 2010 160 172
6. A. Shang, D. Zhou, L. Wang, Y. Gao, M. Fan, X. Wang, R. Zhou, and C. Zhang Increased neuroglobin levels in the cerebral cortex and serum after ischemia-reperfusion insults Brain Res. 1078 2006 219 226
7. Z. Yu, J. Liu, S. Guo, C. Xing, X. Fan, M. Ning, J.C. Yuan, E.H. Lo, and X. Wang Neuroglobin-overexpression alters hypoxic response gene expression in primary neuron culture following oxygen glucose deprivation Neuroscience 162 2009 396 403
8. 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)
9. M. Tiso, J. Tejero, S. Basu, I. Azarov, X. Wang, V. Simplaceanu, S. Frizzell, T. Jayaraman, L. Geary, C. Shapiro, C. Ho, S. Shiva, D.B. Kim-Shapiro, and M.T. Gladwin Human neuroglobin functions as a redox-regulated nitrite reductase J. Biol. Chem. 286 2011 18277 18289
10. S. Singh, M. Zhuo, F.M. Gorgun, and E.W. Englander Overexpressed neuroglobin raises threshold for nitric oxide-induced impairment of mitochondrial respiratory activities and stress signaling in primary cortical neurons Nitric Oxide 32 2013 21 28
11. 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
12. R.C. Li, M.W. Morris, S.K. Lee, F. Pouranfar, Y. Wang, and D. Gozal Neuroglobin protects PC12 cells against oxidative stress Brain Res. 1190 2008 159 166
13. Z. Yu, N. Liu, J. Liu, K. Yang, and X. Wang Neuroglobin, a novel target for endogenous neuroprotection against stroke and neurodegenerative disorders Int. J. Mol. Sci. 13 2012 6995 7014
14. S.Q. Li, W.B. Li, M. Zhang, Y.Z. Wu, and Y.Y. Hu The role of neuroglobin in the neuroprotection of limb ischemic preconditioning in rats Mol. Neurobiol. 47 2013 197 208
15. A. Shang, K. Liu, H. Wang, J. Wang, X. Hang, Y. Yang, Z. Wang, C. Zhang, and D. Zhou Neuroprotective effects of neuroglobin after mechanical injury Neurol. Sci. 33 2012 551 558
16. A. Shang, X. Feng, H. Wang, J. Wang, X. Hang, Y. Yang, Z. Wang, and D. Zhou Neuroglobin upregulation offers neuroprotection in traumatic brain injury Neurol. Res. 34 2012 588 594
17. S. Signoretti, G. Lazzarino, B. Tavazzi, and R. Vagnozzi The pathophysiology of concussion PM R 3 10 Suppl. 2 2011 S359 S368
18. C.C. Giza, and D.A. Hovda The neurometabolic cascade of concussion J. Athl. Train. 36 2001 228 235 (Pubitemid 33685230)
19. V.G. Coronado, L. Xu, S.V. Basavaraju, L.C. McGuire, M.M. Wald, M.D. Faul, B.R. Guzman, and J.D. Hemphill Surveillance for traumatic brain injury-related deaths - United States, 1997-2007 MMWR Surveill. Summ 60 2011 1 32
20. V.G. Coronado, L.C. McGuire, K. Sarmiento, J. Bell, M.R. Lionbarger, C.D. Jones, A.I. Geller, N. Khoury, and L. Xu Trends in traumatic brain injury in the U.S. and the public health response: 1995-2009 J. Saf. Res 43 2012 299 307
21. R. Sharma, and D.T. Laskowitz Biomarkers in traumatic brain injury Curr. Neurol. Neurosci. Rep. 12 2012 560 569
22. M. Reinert, B. Hoelper, E. Doppenberg, A. Zauner, and R. Bullock Substrate delivery and ionic balance disturbance after severe human head injury Acta Neurochir. Suppl. 76 2000 439 444
23. D.J. Titus, A. Sakurai, Y. Kang, C. Furones, S. Jergova, R. Santos, T.J. Sick, and C.M. Atkins Phosphodiesterase inhibition rescues chronic cognitive deficits induced by traumatic brain injury J. Neurosci. 33 2013 5216 5226
24. I.S. Balan, A.J. Saladino, B. Aarabi, R.J. Castellani, C. Wade, D.M. Stein, H.M. Eisenberg, H.H. Chen, and G. Fiskum Cellular alterations in human traumatic brain injury: changes in mitochondrial morphology reflect regional levels of injury severity J. Neurotrauma 30 2013 367 381
25. V. Di Pietro, D. Amin, S. Pernagallo, G. Lazzarino, B. Tavazzi, R. Vagnozzi, A. Pringle, and A. Belli Transcriptomics of traumatic brain injury gene expression and molecular pathways of different grades of insult in a rat organotypic hippocampal culture model J. Neurotrauma 27 2010 349 359
26. V. Di Pietro, A.M. Amorini, B. Tavazzi, D.A. Hovda, S. Signoretti, C.C. Giza, G. Lazzarino, R. Vagnozzi, G. Lazzarino, and A. Belli Potentially neuroprotective gene modulation in an in vitro model of mild traumatic brain injury Mol. Cell. Biochem. 375 2013 185 198
27. B. Tavazzi, S. Signoretti, G. Lazzarino, A.M. Amorini, R. Delfini, M. Cimatti, A. Marmarou, and R. Vagnozzi Cerebral oxidative stress and depression of energy metabolism correlate with severity of diffuse brain injury in rats Neurosurgery 56 2005 582 589
28. B. Tavazzi, R. Vagnozzi, S. Signoretti, A.M. Amorini, A. Belli, M. Cimatti, R. Delfini, V. Di Pietro, A. Finocchiaro, and G. Lazzarino Temporal window of metabolic brain vulnerability to concussions: oxidative and nitrosative stresses - part II Neurosurgery 61 2007 390 396 (Pubitemid 47357349)
29. K.H. Yamada, D.A. Kozlowski, S.E. Seidl, S. Lance, A.J. Wieschhaus, P. Sundivakkam, C. Tiruppathi, I. Chishti, I.M. Herman, S.M. Kuchay, and A.H. Chishti Targeted gene inactivation of calpain-1 suppresses cortical degeneration due to traumatic brain injury and neuronal apoptosis induced by oxidative stress J. Biol. Chem. 287 2012 13182 13193
30. P.M. Abdul-Muneer, H. Schuetz, F. Wang, M. Skotak, J. Jones, S. Gorantla, M.C. Zimmerman, N. Chandra, and J. Haorah Induction of oxidative and nitrosative damage leads to cerebrovascular inflammation in an animal model of mild traumatic brain injury induced by primary blast Free Radic. Biol. Med. 60 2013 282 291
31. E.D. Hall, R.A. Vaishnav, and A.G. Mustafa Antioxidant therapies for traumatic brain injury Neurotherapeutics 7 2010 51 61
32. A. Marmarou, M.A. Foda, W. van den Brink, J. Campbell, H. Kita, and K. Demetriadou A new model of diffuse brain injury in rats. Part I. Pathophysiology and biomechanics J. Neurosurg. 80 1994 291 300 (Pubitemid 24036501)
33. G. Lazzarino, M. Nuutinen, B. Tavazzi, D. Di Pierro, and B. Giardina A method for preparing freeze-clamped tissue samples for metabolite analyses Anal. Biochem. 181 1989 239 241
34. G. Lazzarino, A.M. Amorini, G. Fazzina, R. Vagnozzi, S. Signoretti, S. Donzelli, E. Di Stasio, B. Giardina, and B. Tavazzi Single-sample preparation for simultaneous cellular redox and energy state determination Anal. Biochem. 322 2003 51 59 (Pubitemid 37188556)
35. -ΔΔC(T) method Methods 25 2001 402 408 (Pubitemid 34164012)
36. B. Tavazzi, G. Lazzarino, P. Leone, A.M. Amorini, F. Bellia, C.G. Janson, V. Di Pietro, L. Ceccarelli, S. Donzelli, J.S. Francis, and B. Giardina Simultaneous high performance liquid chromatographic separation of purines, pyrimidines, N-acetylated amino acids, and dicarboxylic acids for the chemical diagnosis of inborn errors of metabolism Clin. Biochem. 38 2005 997 1008 (Pubitemid 41606797)
37. G. Lazzarino, D. Di Pierro, B. Tavazzi, L. Cerroni, and B. Giardina Simultaneous separation of malondialdehyde, ascorbic acid, and adenine nucleotide derivatives from biological samples by ion-pairing high-performance liquid chromatography Anal. Biochem. 197 1991 191 196
38. F. Romitelli, S.A. Santini, E. Chierici, D. Pitocco, B. Tavazzi, A.M. Amorini, G. Lazzarino, and E. Di Stasio Comparison of nitrite/nitrate concentration in human plasma and serum samples measured by the enzymatic batch Griess assay, ion-pairing HPLC and ion-trap GC-MS: the importance of a correct removal of proteins in the Griess assay J. Chromatogr. B 851 2007 257 267 (Pubitemid 46720148)
39. B. Haines, X. Mao, L. Xie, S. Spusta, X. Zeng, K. Jin, and D.A. Greenberg Neuroglobin expression in neurogenesis Neurosci. Lett. 549 2013 3 6
40. Z. Raida, C.A. Hundahl, J.R. Nyengaard, and A. Hay-Schmidt Neuroglobin over expressing mice: expression pattern and effect on brain ischemic infarct size PLoS One 8 2013 e76565
41. C. Lechauve, S. Augustin, H. Cwerman-Thibault, A. Bouaita, V. Forster, C. Célier, P. Rustin, M.C. Marden, J.A. Sahel, and M. Corral-Debrinski Neuroglobin involvement in respiratory chain function and retinal ganglion cell integrity Biochim. Biophys. Acta 1823 2012 2261 2273
42. Z. Yu, J. Xu, N. Liu, Y. Wang, X. Li, S. Pallast, K. van Leyen, and X. Wang Mitochondrial distribution of neuroglobin and its response to oxygen-glucose deprivation in primary-cultured mouse cortical neurons Neuroscience 218 2012 235 242
43. S.H. Bønding, K. Henty, A.J. Dingley, and T. Brittain The binding of cytochrome c to neuroglobin: a docking and surface plasmon resonance study Int. J. Biol. Macromol. 43 2008 295 299
44. T. Brittain, J. Skommer, K. Henty, N. Birch, and S. Raychaudhuri A role for human neuroglobin in apoptosis IUBMB Life 62 2010 878 885
45. Z. Raida, C.A. Hundahl, J. Kelsen, J.R. Nyengaard, and A. Hay-Schmidt Reduced infarct size in neuroglobin-null mice after experimental stroke in vivo Exp. Transl. Stroke Med. 4 2012 15
46. P.Y. Chuang, Y.P. Conley, S.M. Poloyac, D.O. Okonkwo, D. Ren, P.R. Sherwood, M. Hravnak, and S.A. Alexander Neuroglobin genetic polymorphisms and their relationship to functional outcomes after traumatic brain injury J Neurotrauma 27 2010 999 1006
47. K. Jin, Y. Mao, X. Mao, L. Xie, and D.A. Greenberg Neuroglobin expression in ischemic stroke Stroke 41 2010 557 559
48. K. Jin, X.O. Mao, L. Xie, and D.A. Greenberg Pharmacological induction of neuroglobin expression Pharmacology 87 2011 81 84
49. T.A. Lusardi, N.K. Lytle, C. Szybala, and D. Boison Caffeine prevents acute mortality after TBI in rats without increased morbidity Exp. Neurol. 234 2012 161 168
50. K. Eakin, and J.P. Miller Mild traumatic brain injury is associated with impaired hippocampal spatiotemporal representation in the absence of histological changes J. Neurotrauma 29 2012 1180 1187
51. Z. Yu, N. Liu, Y. Li, J. Xu, and X. Wang Neuroglobin overexpression inhibits oxygen-glucose deprivation-induced mitochondrial permeability transition pore opening in primary cultured mouse cortical neurons Neurobiol. Dis. 56 2013 95 103
52. W. Van Leuven, D. Van Dam, L. Moens, P.P. De Deyn, and S. Dewilde A behavioural study of neuroglobin-overexpressing mice under normoxic and hypoxic conditions Biochim. Biophys. Acta 1834 2013 1764 1771
53. C.A. Hundahl, J. Fahrenkrug, H. Luuk, A. Hay-Schmidt, and J. Hannibal Restricted expression of neuroglobin in the mouse retina and co-localization with melanopsin and tyrosine hydroxylase Biochem. Biophys. Res. Commun. 425 2012 100 106
54. 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
55. Z. Yu, J.L. Poppe, and X. Wang Mitochondrial mechanisms of neuroglobins neuroprotection Oxid. Med. Cell. Longevity 2013 2013 756989
56. E. Miñambres, M.A. Ballesteros, M. Mayorga, M.J. Marin, P. Muñoz, J. Figols, and M. López-Hoyos Cerebral apoptosis in severe traumatic brain injury patients: an in vitro, in vivo, and postmortem study J. Neurotrauma 25 2008 581 591 (Pubitemid 351918435)