Protective effects of erythropoietin in traumatic spinal cord injury by inducing the Nrf2 signaling pathway activation

Journal of Trauma and Acute Care Surgery

Volumn 76, Issue 5, 2014, Pages 1228-1234

  Jin, Wei ^a   Ming, Xing ^a   Hou, Xiaoshan ^a   Zhu, Tiansheng ^a   Yuan, Baoyu ^a   Wang, Jing ^a   Ni, Hongbin ^a   Jiang, Jian ^a   Wang, Handong ^b   Liang, Weibang ^a  

^a THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

Erythropoietin; nuclear factor erythroid 2 related factor 2; rats; spinal cord injury

Indexed keywords

GLUTATHIONE TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE ALPHA1; RECOMBINANT ERYTHROPOIETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; AUTORADIOGRAPHY; BLOOD BRAIN BARRIER; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVITY; LAMINECTOMY; LOCOMOTION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; UPREGULATION;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; GLUTATHIONE TRANSFERASE; IN SITU NICK-END LABELING; LOCOMOTION; MALE; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES;

EID: 84899848215     PISSN: 21630755     EISSN: 21630763     Source Type: Journal    
DOI: 10.1097/TA.0000000000000211     Document Type: Conference Paper

References (35)

1. Cadotte DW, Fehlings MG. Spinal cord injury: a systematic review of current treatment options. Clin Orthop Relat Res. 2011;469:732-741.
2. Choo AM, Liu J, Dvorak M, Tetzlaff W, Oxland TR. Secondary pathology following contusion, dislocation, and distraction spinal cord injuries. Exp Neurol. 2008;212:490-506.
3. Owuor ED, Kong AN. Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol. 2002;64:765-770.
4. Jain AK, Bloom DA, Jaiswal AK. Nuclear import and export signals in control of Nrf2. J Biol Chem. 2005;280:29158-29168.
5. Osburn WO, Wakabayashi N, Misra V, Misra V, Nille T, Biswal S, Trush MA, Kensler TW. Nrf2 regulates an adaptive response protecting against oxidative damage following diquat-mediated formation of superoxide anion. Arch Biochem Biophys. 2006;454:7-15.
6. Jin W, Wu J, Wang H, Kong J, Ni H, Liang W. Erythropoietin administration modulates pulmonary Nrf2 signaling pathway after traumatic brain injury in mice. J Trauma. 2011;71:680-686.
7. Jin W, Wang HD, Yan W, Zhu L, Hu ZG, Ding YS, Tang K. Role of Nrf2 in protection against traumatic brain injury in mice. J Neurotrauma. 2009;26:131-138.
8. Wang XL, de Rivero Vaccari JP,Wang H, Diaz P, German R, Marcillo AE, Keane RW. Activation of the nuclear factor E2-related factor 2/antioxidant response element pathway is neuroprotective after spinal cord injury. J Neurotrauma. 2012;29:936-945.
9. Ozturk E, Demirbilek S, Kadir But A, Saricicek V, Gulec M, Akyol O, Ozcan Ersoy M. Antioxidant properties of propofol and erythropoietin after closed head injury in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29:922-927.
10. Chen G, Shi JX, Hang CH, Xie W, Liu J, Liu X. Inhibitory effect on cerebral inflammatory agents that accompany traumatic brain injury in a rat model: a potential neuroprotective mechanism of recombinant human erythropoietin (rhEPO). Neurosci Lett. 2007;425:177-182.
11. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, Itri LM, Cerami A. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad SciUS A. 2000;97: 10526-10531.
12. Lu D, Mahmood A, Qu C, Goussev A, Schallert T, Chopp M. Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J Neurotrauma. 2005;22:1011-1017.
13. Celik M, Gokmen N, Erbayraktar S, Akhisaroglu M, Konakc S, Ulukus C, Genc S, Genc K, Sagiroglu E, Cerami A, et al. Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury. Proc Natl Acad Sci U S A. 2002;99:2258-2263.
14. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia andmetabolic stress. Proc Natl Acad Sci U S A. 2001;98:4044-4049.
15. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Brainderived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J. 2005;19:2026-2028.
16. Digicaylioglu M, Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature. 2001;412:641-647.
17. Zhu L, Wang HD, Yu XG, Jin W, Qiao L, Lu TJ, Hu ZL, Zhou J, Erythropoietin prevents zinc accumulation and neuronal death after traumatic brain injury in rat hippocampus: in vitro and in vivo studies. Brain Res. 2009;1289:96-105.
18. JinW, Kong J, Lu TY,Wang HD, Ni HB,Wu J, Dai YX, Jiang J, LiangWB. Erythropoietin prevents secondary brain injury induced by cortical lesion in mice: possible involvement of Nrf2 signaling pathway. Ann Clin Lab Sci. 2011;41:25-32.
19. Liang WB, Han QQ, Jin W, Xiao ZG, Huang J, Ni HB, Chen B, Kong J, Wu J, Dai JW. The promotion of neurological recovery in the rat spinal cord crushed injury model by collagen-binding BDNF. Biomaterials. 2010;31:8634-8641.
20. Yatsiv I, GrigoriadisN, Simeonidou C, Stahel PF, Schmidt OI,Alexandrovitch AG, Tsenter J, Shohami E. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J. 2005;19: 1701-1703.
21. Zhang J, Zhu Y, Zhou D, Wang Z, Chen G. Recombinant human erythropoietin (rhEPO) alleviates early brain injury following subarachnoid hemorrhage in rats: possible involvement of Nrf2-ARE pathway. Cytokine. 2010;52:252-257.
22. Jin W, Kong J, Wang HD, Wu J, Lu TY, Jiang J, Ni HB, Liang WB. Protective effect of tert-butylhydroquinone on cerebral inflammatory response following traumatic brain injury in mice. Injury. 2011;42:714-718.
23. Matis GK, Birbilis TA. Erythropoietin in spinal cord injury. Eur Spine J. 2009;18:314-323.
24. Ning B, Zhang A, Song H, GongW, Ding Y, Guo S, Zhao Y, Jiang J, Jia T. Recombinant human erythropoietin prevents motor neuron apoptosis in a rat model of cervical sub-acute spinal cord compression. Neurosci Lett. 2011;490:57-62.
25. Vitellaro-Zuccarello L, Mazzetti S, Madaschi L, Bosisio P, Fontana E, Gorio A, De Biasi S. Chronic erythropoietin-mediated effects on the expression of astrocyte markers in a rat model of contusive spinal cord injury. Neuroscience. 2008;151:452-466.
26. Gorio A, Madaschi L, Stefano Di, Carelli S, Di Giulio AM, De Biasi S, Coleman T, Cerami A, Brines M. Methylprednisolone neutralises the beneficial effects of erythropoietin in experimental spinal cord injury. Proc Natl Acad Sci U S A. 2005;102:16379-16384.
27. Jia Z, Zhu H, Li J, Wang X, Misra H, Li Y. Oxidative stress in spinal cord injury and antioxidant-based intervention. Spinal Cord. 2012;50:264-274.
28. StammersAT,Liu J,Kwon BK.Expression of inflammatory cytokines following acute spinal cord injury in a rodent model. J Neurosci Res. 2012;90:782-790.
29. Chen XL, Kunsch C. Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pham Des. 2004;10:879-891.
30. Mao L, Wang HD, Wang XL, Tian L, Xu JY. Disruption of Nrf2 exacerbated the damage after spinal cord injury in mice. J Trauma Acute Care Surg. 2012;72:189-198.
31. Katavetin P, Inagi R, Miyata T, Shao J, Sassa R, Adler S, Eto N, Kato H, Fujita T, Nangaku M. Erythropoietin induces heme oxygenase-1 expression and attenuates oxidative stress. Biochem Biophys Res Commun. 2007;359:928-934.
32. Genc K, Egrilmez MY, Genc S. Erythropoietin induces nuclear translocation of Nrf2 and heme oxygenase-1 expression in SH-SY5- cells. Cell Biochem Funct. 2010;28:197-201.
33. Yazihan N, Uzuner K, Salman B, Vural M, Koken T, Arslantas A. Erythropoietin improves oxidative stress following spinal cord trauma in rats. Injury. 2008;39:1408-1413.
34. Okutan O, Solaroglu I, Beskonakli E, Taskin Y. Recombinant human erythropoietin decreases myeloperoxidase and caspase-3 activity and improves early functional results after spinal cord injury in rats. J Clin Neurosci. 2007;14:364-368.
35. Kasper C. Erythropoietin. In: Thomson AW, Lotze MT (eds) The Cytokine Handbook. vol I. 4th edn. Elsevier, London, 2003;pp 149-166.