Protein carbonylation after traumatic brain injury: Cell specificity, regional susceptibility, and gender differences

Free Radical Biology and Medicine

Volumn 78, Issue , 2015, Pages 89-100

  Lazarus, Rachel C ^a   Buonora, John E ^a,b   Jacobowitz, David M ^a   Mueller, Gregory P ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b BAYLOR UNIVERSITY   (United States)

Author keywords

Astrocytes; Carbonylation; Dorsal third ventricle; Ependymal cells; Free radicals; Median eminence; Reactive carbonyl species; Reactive oxygen species; Traumatic brain injury

Indexed keywords

DIHYDROPYRIMIDASE RELATED PROTEIN 2; FREE RADICAL; FRUCTOSE BISPHOSPHATE ALDOLASE; GLIAL FIBRILLARY ACIDIC PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CRMP2 PROTEIN, RAT; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN THIRD VENTRICLE; CARBONYLATION; CELL TYPE; CONTROLLED STUDY; EPENDYMA CELL; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MEDIAN EMINENCE; MICROGLIA; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PROTEIN CARBONYLATION; RAT; SEX DIFFERENCE; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY; CELL CULTURE; CYTOLOGY; ENZYME IMMUNOASSAY; EPENDYMA; METABOLISM; PROTEOMICS; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

RATTUS;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; BRAIN INJURIES; CELLS, CULTURED; EPENDYMA; FEMALE; FRUCTOSE-BISPHOSPHATE ALDOLASE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOENZYME TECHNIQUES; MALE; MICROGLIA; NERVE TISSUE PROTEINS; NEURONS; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS;

EID: 84913570394     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.10.507     Document Type: Article

References (61)

1. M. Faul, L. Xu, M.M. Wald, V. Coronado, and A.M. Dellinger Traumatic brain injury in the United States: national estimates of prevalence and incidence, 2002-2006 Inj. Prev. 16 2010
2. C.S. Piao, B.A. Stoica, J. Wu, B. Sabirzhanov, Z. Zhao, R. Cabatbat, D.J. Loane, and A.I. Faden Combined inhibition of cell death induced by apoptosis inducing factor and caspases provides additive neuroprotection in experimental traumatic brain injury Neurobiol. Dis. 46 2013 745 758
3. W.O. Opii, V.N. Nukal, R. Sultana, J.D. Pandya, K.M. Day, M.L. Marchant, J.B. Klein, and P.G.; B., D.A. Sullivan Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury J. Neurotrauma 24 2007 772 789
4. A.F. Schindler, E.C. Olson, N.C. Spitzer, and M. Montal Mitochondrial dysfunction is a primary event in glutamate neurotoxicity J. Neurosci. 16 1996 6125 6133
5. L. Devi, B.M. Prabhu, D.F. Galati, N.G. Avadhani, and H.K. Anandatheerthavarada Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction Neuroscience 26 2006 9057 9068
6. F. Clausen Delayed cell death after traumatic brain injury: role of reactive oxygen species Acta Universitatis Upsaliensis: Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 77 2004 S. Academiae Ubsaliensis Uppsala
7. V.A. Tyurin, Y.Y. Tyurina, G.G. Borisenko, T.V. Sokolova, V.B. Ritov, P.J. Quinn, M. Rose, P. Kochanek, S.H. Graham, and V.E. Kagan Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates J. Neurochem. 75 2000 2178 2189
8. J. Zheng, and O.A. Bizzozero Accumulation of protein carbonyls within cerebellar astrocytes in murine experimental autoimmune encephalomyelitis J. Neurosci. Res. 88 2010 3376 3385
9. I. Dalle-Donne, G. Aldini, M. Carini, R. Colombo, R. Rossi, and A. Milzani Protein carbonylation, cellular dysfunction, and disease progression J. Cell. Mol. Med. 10 2006 389 406
10. O.A. Bizzozero, G. DeJesus, K. Callahan, and A. Paruszyn Elevated protein carbonylation in the brain white matter and gray matter of patients with multiple sclerosis J. Neurosci. Res. 81 2005 687 695
11. R. Sultana, and D.A. Butterfield Role of oxidative stress in the progression of Alzheimer's disease J. Alzheimers Dis. 19 2010 341 353
12. A. Rodríguez-Rodríguez, J.J. Egea-Guerrero, F. Murillo-Cabezas, and A. Carrillo-Vico Oxidative stress in traumatic brain injury Curr. Med. Chem. 21 2014 1201 1211
13. C.C. Conrad, J.M. Talent, C.A. Malakowsky, and R.W. Gracy Post-electrophoretic identification of oxidized proteins Biol. Proced. Online 2 1999 39 45
14. R.L. Roof, and E.D. Hall Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats J. Neurotrauma 17 2000 1155 1169
15. H. Bayir, D.W. Marion, A.M. Puccio, S.R. Wisniewski, K.L. Janesko, R.S.B. Clark, and P.M. Kochanek Marked gender effect on lipid peroxidation after severe traumatic brain injury in adult patients J. Neurotrauma 21 2004 1 8
16. D.A. Butterfield, M. Perluigi, T. Reed, T. Muharib, C.P. Hughes, R.A.S. Robinson, and R. Sultana Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications Antioxid. Redox Signaling 17 2012 1610 1655
17. H.S. Kavakli, O. Erel, O. Karakayali, S. Neceluoglu, F. Tanriverdi, F. Coskun, and A.F. Kahraman Oxidative stress in isolated blunt traumatic brain injury Sci. Res. Essays 5 2010 2832 2836
18. Z. Goswasser, M. Cohen, and O. Keren Female TBI patients recover better than males Brain Inj. 12 1998 805 808
19. C. Werner, and K. Engelhard Pathophysiology of traumatic brain injury Br. J. Anaesth. 99 2007 4 9
20. A.A. Starkov, C. Chinopulos, and G. Fiskum Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury Cell Calcium 36 2004 257 264
21. T.X. Shao, K.N. Roberts, W.R. Markesbery, S.W. Scheff, and M.A. Lovell Oxidative stress in head trauma in aging Free Radic. Biol. Med. 41 2006 77 85
22. H.M. Semchyshyn, and V.L. Luschchak Interplay between oxidative and carbonyl stresses: molecular mechanisms, biological effects and therapeutic strategies of protection H.M. Semchyshyn, V.L. Luschchak, Oxidative Stress - Molecular Mechanisms and Biological Effects. Ivano-Frankivsk 2012 Vassyl Stefanuk Precarpathian National University Ukraine
23. M.V. Sofroniew, and H.V. Vinters Astrocytes: biology and pathology Acta Neuropathol. 119 2010 7 35
24. S. Peuchen, J.P. Bolanos, S.J.R. Heales, A. Almeida, M.R. Duchen, and J.B. Clark Interrelationships between astrocyte function, oxidative stress and antioxidant status within the central nervous system Prog. Neurobiol. 52 1997 261 281
25. S. Desagher, J. Glowinski, and J. Premont Astrocytes protect neurons from hydrogen peroxide toxicity J. Neurosci. 16 1996 2553 2562
26. P.G. Noble, J.P. Antel, and V.W. Yong Astrocytes and catalase prevent the toxicity of catecholamines to oligodendrocytes Brain Res. 1-2 1994 83 90
27. M.C. Papadopoulos, I.L. Koumenis, T.Y. Yuan, and R.G. Giffard Increased vulnerability of astrocytes to oxidative injury with age despite constant antioxidant defenses Neuroscience 82 1998 915 925
28. Y. Chen, and R.A. Swanson Astrocytes and brain injury J. Cereb. Blood Flow Metab. 23 2003 137 149
29. M. Kernt, N. Arend, A. Buerger, T. Mann, C. Haritoglou, M.W. Ulbig, A. Kampik, and C. Hirneiss Idebenone prevents human optic nerve head astrocytes from oxidative stress, apoptosis, and senescence by stabilizing BAX/Bcl-2 ratio J. Glaucoma 22 2013 404 412
30. M.R. Del Bigio Ependymal cells: biology and pathology Acta Neuropathol. 119 2010 55 73
31. M. Carini, and M. Orioli Mass spectrometric strategies for identification and characterization of carbonylated peptides and proteins G. Aldini, K.J. Yeum, E. Niki, R.M. Russell, Biomarkers for Antioxidant Defense and Oxidative Damage: Principles and Practical Applications 2010 Wiley-Blackwell New York 173 197
32. E.P. Simpson, Y.K. Henry, J.S. Henkel, R.G. Smith, and S.H. Appel Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden Neurology 62 2004 1758 1765
33. M.S. Selley (E)-4-hydroxy-2-nonenal may be involved in the pathogenesis of Parkinson's disease Free Radic. Biol. Med. 25 1998 169 174
34. C. Johanson, E. Stopa, P. McMillan, D. Roth, J. l. Funk, and G. Krinke The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread Toxicol. Pathol. 39 2011 186 212
35. P. Barrett, E. Ivanova, E.S. Graham, A.W. Ross, D. Wilson, H. Ple, J.G. Mercer, F.J. Ebling, S. Schuhler, S.M. Dupre, A. Loudon, and P.J. Morgan Photoperiodic regulation of cellular retinoic acid-binding protein 1, GPR50 and nestin in tanycytes of the third ventricle ependymal layer of the Siberian hamster J. Endocrinol. 191 2006 687 698
36. B. Peruzzo, F.E. Pastor, J.L. Blazquez, P. Amat, and E.M. Rodrigues Polarized endocytosis and transcytosis in the hypothalamic tanycytes of the rat Cell Tissue Res. 317 2004 147 164
37. D.A. Lee, J.L. Bedont, T. Pak, H. Wang, J. Song, A. Miranda-Angulo, V. Takiar, V. Charubhumi, F. Balordi, H. Takebayahi, S. Aja, E. Ford, G. Fishell, and S. Blackshaw Tanycytes of the hypothalamic median eminence for a diet-responsive neurogenic niche Nat. Neurosci. 15 2012 700 702
38. E.M. Rodrigues, J.L. Blazquez, F.E. Pastor, B. Pelaez, P. Pena, B. Peruzzo, and P. Amat Hypothalamic tanycytes: a key component of brain-endocrine interaction Int. Rev. Cytol. 247 2005 89 164
39. A. Novarro, J. Tolivia, and M. Alvarez-Uria Ultrastructural study of a special type of ependymal cell at paraventricular level of the golden hamster third ventricle Histol. Histopathol. 10 1995 861 868
40. C. Berry, E.J. Ley, A. Tillou, G. Cryer, D.R. Marguilies, and A. Salim The effect of gender on patients with moderate to severe head injuries J. Trauma: Inj., Infect., Crit. Care 67 2009 950 953
41. R.W. Irwin, J. Yao, R.T. Hamilton, E. Cadenas, R.D. Brinton, and J. Nilsen Progesterone and estrogen regulate oxidative metabolism in brain mitochondria Endocrinology 149 2008 3167 3175
42. D.G. Stein, D.W. Wright, and A.L. Kellermann Does progesterone have neuroprotective properties? Ann. Emerg. Med. 51 2008 164 172
43. N. Sugino, T. Shimamura, H. Tamura, M. Ono, Y. Nakamura, K. Ogino, and H. Kato Progesterone inhibits superoxide radical production by mononuclear phagocytes in pseudopregnant rats Endocrinology 137 1996 749 754
44. J.I. Luoma, B.G. Kelley, and P.G. Mermelstein Progesterone inhibition of voltage-gated calcium channels is a potential neuroprotective mechanism against excitotoxicity Steroids 76 2011 845 855
45. R.L. Roof, S.W. Hoffamn, and D.G. Stein Progesterone protects against lipid peroxidation following traumatic brain injury in rats Mol. Clin. Neuropathol. 31 1997 1 11
46. R.D. Readnower, M. Chavko, S. Adeeb, M.D. Conroy, J.R. Pauly, R.M. McCarron, and P.G. Sullivan Increase in blood brain barrier permeability, oxidative stress, and activated microglia in a rat model of blast induced traumatic brain injury J. Neurosci. Res. 88 2010 3530 3539
47. C. Van Den Heuvel, and R. Vink Recent advances in the development of multifactorial therapies for the treatment of traumatic brain injury Expert Opin. Invest. Drugs 13 2004 1263 1274
48. O. Ates, S. Cayli, E. Altinoz, I. Gurses, N. Yucel, M. Sener, A. Kocak, and S. Yologlu Neuroprotection by resveratrol against traumatic brain in jury in rats Mol. Cell. Biol. 294 2006 137 144
49. T. Kent, and J. Tour Mission Connect Mild TBI Translational Research Consortium. Annual Report 1, August 2008-July 2009 2009 Baylor College of Medicine Houston
50. B.A. Rzigalinski, K. Meehan, M.D. Whiting, C.E. Dillon, K. Hockey, and M. Brewer Antioxidant nanoparticles R.J. Hunter, V.R. Preedy, Nanomedicine in Health and Disease. London: Taylor & Francis/ 2011 CRC Press 100 121
51. O. Azimzadeh, H. Scherthan, H. Sarioglu, Z. Barjaktarovic, M. Conrad, A. Vogt, J. Calzada-Wack, F. Neff, M. Aubele, C. Buske, M.J. Atkinson, and S. Tapio Rapid proteomic remodeling of cardiac tissue caused by total body ionizing radiation Proteomics 11 2011 3299 3311
52. Assessments of Oxidative Damage and Lipid Peroxidation after Traumatic Brain Injury and Spinal Cord Injury J.M. Bosken, J.A. Wang, and E.D. Hall Springer Protocols Handbooks 2012 Humana Press New York
53. G.M. Mackay, C.M. Forrest, N. Stoy, J. Christofides, M. Egerton, T.W. Stone, and L.G. Darlington Tryptophan metabolism and oxidative stress in patients with chronic brain injury Eur. J. Neurol. 13 2006 30 42
54. R. Beschorner, D. Adjodah, J.M. Schwab, M. Mittelbronn, I. Pedal, R. Mattern, H.J. Schluesener, and R. Metermann Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans Acta Neuropathol. 100 2000 377 384
55. A. Castegna, M. Aksenov, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery, and D.A. Butterfield Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II. Dihydropyrimidinase-related protein 2, α-enolase and heat shock cognate 71 J. Neurochem. 82 2002 1524 1532
56. S. Oikawa, H. Kobayashi, Y. Kitamura, H. Zhu, K. Obata, Y. Minabe, M. Dazortsava, K. Ohashi, S. Tada-Oikawa, H. Takahashi, K. Yata, M. Murata, and T. Yamashima Proteomic analysis of carbonylated proteins in the monkey substantia nigra after ischemia-reperfusion Free Radic. Res. 48 2014 694 705
57. K. Ikegami, and M. Setou Unique post-translational modifications in specialized microtubule architecture Cell Struct. Funct. 35 2010 15 22
58. M. Merkulova, A. Hurtado-Lorenzo, H. Hosokawa, Z. Zhuang, D. Brown, D.A. Ausiello, and V. Marshansky Aldolase directly interacts with ARNO and modulates cell morphology and acidic vesicle distribution Am. J. Physiol. Cell Physiol 300 2011 C1442 C1455
59. Rangarajan, E. S.; Park, H.; Fortin, E.; Sygusch, J.; Izard, T. Mechanism of aldolase control of sorting nexin 9 function in endocytosis. J. Biol. Chem. 285:11983-11990.
60. L.F. Eng Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes J. Neuroimmunol. 8 1985 203 214
61. Y. Suzuki, S. Nakagomi, K. Namikawa, S. Kiryu-Seo, N. Inagaki, K. Kaibuchi, H. Aizawa, K. Kikuchi, and H. Kiyama Collapsin response mediator protein-2 accelerates axon regeneration of nerve-injured motor neurons of rat J. Neurochem. 86 2003 1042 1050