Ethyl pyruvate promotes spinal cord repair by ameliorating the glial microenvironment

British Journal of Pharmacology

Volumn 166, Issue 2, 2012, Pages 749-763

  Yuan, Yimin ^a   Su, Zhida ^a   Pu, Yingyan ^a   Liu, Xiujie ^a   Chen, Jingjing ^a   Zhu, Feng ^a   Zhu, Yanling ^a   Zhang, Han ^a   He, Cheng ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

astrogliosis; axon regeneration; ethyl pyruvate; glial scar; neuroinflammation; spinal cord injury

Indexed keywords

CD11B ANTIGEN; PYRUVIC ACID DERIVATIVE; PYRUVIC ACID ETHYL ESTER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG DOSE COMPARISON; FUNCTIONAL ASSESSMENT; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY;

EID: 84859883497     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01804.x     Document Type: Article

References (66)

1. Aamodt S, (2007). Focus on glia and disease. Nat Neurosci 10: 1349. (Pubitemid 350014668)
2. Barres BA, (2008). The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60: 430-440.
3. Basso DM, Beattie MS, Bresnahan JC, (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12: 1-21.
4. Cao L, Liu L, Chen ZY, Wang LM, Ye JL, Qiu HY, et al,. (2004). Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127: 535-549. (Pubitemid 38295471)
5. Cao L, Zhu YL, Su ZD, Lv BL, Huang ZH, Mu LF, et al,. (2007). Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia 55: 897-904. (Pubitemid 46903990)
6. Choi JS, Lee MS, Jeong JW, (2010). Ethyl pyruvate has a neuroprotective effect through activation of extracellular signal-regulated kinase in Parkinson's disease model. Biochem Biophys Res Commun 394: 854-858.
7. Cuzzocrea S, Genovese T, Mazzon E, Esposito E, Di Paola R, Muià C, (2008). Effect of 17beta-estradiol on signal transduction pathways and secondary damage in experimental spinal cord trauma. Shock 29: 362-371. (Pubitemid 351271708)
8. Das UN, (2006). Pyruvate is an endogenous anti-inflammatory and anti-oxidant molecule. Med Sci Monit 12: RA79-RA84.
9. Dusart I, Schwab ME, (1993). Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6: 712-724. (Pubitemid 24143919)
10. Fink MP, (2003). Ethyl pyruvate: a novel anti-inflammatory agent. Crit Care Med 31 (Suppl. 1): S51-S56. (Pubitemid 36157299)
11. Fink MP, (2007). Ethyl pyruvate: a novel anti-inflammatory agent. J Intern Med 261: 349-362. (Pubitemid 46474763)
12. Fitch MT, Silver J, (2008). CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209: 294-301. (Pubitemid 351174127)
13. Fleming JC, Norenberg MD, Ramsay DA, Dekaban GA, Marcillo AE, Saenz AD, et al,. (2006). The cellular inflammatory response in human spinal cords after injury. Brain 129: 3249-3269. (Pubitemid 44871440)
14. Goldshmit Y, Galea MP, Wise G, Bartlett PF, Turnley AM, (2004). Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J Neurosci 24: 10064-10073. (Pubitemid 39492030)
15. Graeber MB, Streit WJ, (2010). Microglia: biology and pathology. Acta Neuropathol 119: 89-105.
16. Gris D, Marsh DR, Oatway MA, Chen Y, Hamilton EF, Dekaban GA, et al,. (2004). Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J Neurosci 24: 4043-4051. (Pubitemid 38544230)
17. Gupta SK, Rastogi S, Prakash J, Joshi S, Gupta YK, Awor L, et al,. (2000). Antiinflammatory activity of sodium pyruvate-a physiological antioxidant. Indian J Physiol Pharmacol 44: 101-104. (Pubitemid 30090042)
18. Han Y, Englert JA, Yang R, Delude RL, Fink MP, (2005). Ethyl pyruvate inhibits nuclear factor-kappaB-dependent signaling by directly targeting p65. J Pharmacol Exp Ther 312: 1097-1105. (Pubitemid 40293769)
19. Hanisch UK, Kettenmann H, (2007). Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394. (Pubitemid 350014685)
20. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, et al,. (2008). STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28: 7231-7243.
21. Hinoi E, Takarada T, Tsuchihashi Y, Fujimori S, Moriguchi N, Wang L, et al,. (2006). A molecular mechanism of pyruvate protection against cytotoxicity of reactive oxygen species in osteoblasts. Mol Pharmacol 70: 925-935. (Pubitemid 44268449)
22. Huh SH, Chung YC, Piao Y, Jin MY, Son HJ, Yoon NS, et al,. (2011). Ethyl pyruvate rescues nigrostriatal dopaminergic neurons by regulating glial activation in a mouse model of Parkinson's disease. J Immunol 187: 960-969.
23. (2) mediated apoptosis in human neuroblastoma cell line-SK-NMC. J Chem Neuroanat 26: 109-118. (Pubitemid 37346283)
24. Kao KK, Fink MP, (2010). The biochemical basis for the anti-inflammatory and cytoprotective actions of ethyl pyruvate and related compounds. Biochem Pharmacol 80: 151-159.
25. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG, (2006). Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26: 3377-3389.
26. Kim HS, Cho IH, Kim JE, Shin YJ, Jeon JH, Kim Y, et al,. (2008). Ethyl pyruvate has an anti-inflammatory effect by inhibiting ROS-dependent STAT signaling in activated microglia. Free Radic Biol Med 45: 950-963.
27. Kim JB, Yu YM, Kim SW, Lee JK, (2005). Anti-inflammatory mechanism is involved in ethyl pyruvate-mediated efficacious neuroprotection in the postischemic brain. Brain Res 1060: 188-192.
28. Kim SU, de Vellis J, (2005). Microglia in health and disease. J Neurosci Res 81: 302-313. (Pubitemid 41359284)
29. von Korff RW, (1964). Pyruvate-C14, purity and stability. Anal Biochem 8: 171-178.
30. Lee JY, Kim YH, Koh JY, (2001). Protection by pyruvate against transient forebrain ischemia in rats. J Neurosci 21: RC171.
31. Mongan PD, Capacchione J, Fontana JL, West S, Bünger R, (2001). Pyruvate improves cerebral metabolism during hemorrhagic shock. Am J Physiol Heart Circ Physiol 281: H854-H864.
32. Moro N, Sutton RL, (2010). Beneficial effects of sodium or ethyl pyruvate after traumatic brain injury in the rat. Exp Neurol 225: 391-401.
33. Ndubaku U, de Bellard ME, (2008). Glial cells: old cells with new twists. Acta Histochem 110: 182-195.
34. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki T, Ishii K, et al,. (2006). Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12: 829-834. (Pubitemid 44050074)
35. Pekny M, Nilsson M, (2005). Astrocyte activation and reactive gliosis. Glia 50: 427-434. (Pubitemid 40780846)
36. Popovich PG, Hickey WF, (2001). Bone marrow chimeric rats reveal the unique distribution of resident and recruited macrophages in the contused rat spinal cord. J Neuropathol Exp Neurol 60: 676-685. (Pubitemid 32619790)
37. Popovich PG, Wei P, Stokes BT, (1997). The cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 377: 443-464. (Pubitemid 27016650)
38. Robel S, Berninger B, Götz M, (2011). The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12: 88-104.
39. Rolls A, Shechter R, Schwartz M, (2009). The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10: 235-241.
40. Ruitenberg MJ, Levison DB, Lee SV, Verhaagen J, Harvey AR, Plant GW, (2005). NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 128: 839-853. (Pubitemid 40516921)
41. Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH, (1999). Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci 11: 3648-3658. (Pubitemid 29484261)
42. Schubert KO, Naumann T, Schnell O, Zhi Q, Steup A, Hofmann HD, et al,. (2005). Activation of STAT3 signaling in axotomized neurons and reactive astrocytes after fimbria-fornix transaction. Exp Brain Res 165: 520-531. (Pubitemid 41224993)
43. Shen HX, Hu XM, Liu C, Wang SP, Zhang WT, Gao H, et al,. (2010). Ethyl pyruvate protects against hypoxic-ischemic brain injury via anti-cell death and anti-inflammatory mechanisms. Neurobiol Dis 37: 711-722.
44. Sims CA, Wattanasirichaigoon S, Menconi MJ, Ajami AM, Fink MP, (2001). Ringer's ethyl pyruvate solution ameliorates ischemia/reperfusion induced intestinal mucosal injury in rats. Crit Care Med 29: 1513-1518. (Pubitemid 32762329)
45. Sofroniew MV, (2009). Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647.
46. Sofroniew MV, Vinters HV, (2010). Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
47. Song M, Kellum JA, Kaldas H, Fink MP, (2004). Evidence that glutathione depletion is a mechanism responsible for the anti-inflammatory effects of ethyl pyruvate in cultured LPS-stimulated RAW 264.7 cells. J Pharmacol Exp Ther 308: 307-316. (Pubitemid 38090732)
48. Sriram K, Benkovic SA, Hebert MA, Miller DB, O'Callaghan JP, (2004). Induction of gp130-related cytokines and activation of JAK2/STAT3 pathway in astrocytes precedes up-regulation of glial fibrillary acidic protein in the 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of neurodegeneration. J Biol Chem 279: 19936-19947. (Pubitemid 38623436)
49. Stoll G, Jander S, Schroeter M, (2002). Detrimental and beneficial effects of injury-induced inflammation and cytokine expression in the nervous system. Adv Exp Med Biol 513: 87-113. (Pubitemid 36332404)
50. Su ZD, Yuan YM, Cao L, Zhu YL, Gao L, He C, (2010). Triptolide promotes spinal cord repair by inhibiting astrogliosis and inflammation. Glia 58: 901-915.
51. Tederko P, Krasuski M, Kiwerski J, Nyka I, BiaÅoszewski D, (2009). Strategies for neuroprotection following spinal cord injury. Ortop Traumatol Rehabil 11: 103-110.
52. Tian DS, Yu ZY, Xie MJ, Bu BT, Witte OW, Wang W, (2006). Suppression of astroglial scar formation and enhanced axonal regeneration associated with functional recovery in a spinal cord injury rat model by the cell cycle inhibitor olomoucine. J Neurosci Res 84: 1053-1063. (Pubitemid 44521050)
53. Tian DS, Dong Q, Pan DJ, He Y, Yu ZY, Xie MJ, et al,. (2007). Attenuation of astrogliosis by suppressing of microglial proliferation with the cell cycle inhibitor olomoucine in rat spinal cord injury model. Brain Res 1154: 206-214. (Pubitemid 46856341)
54. Tian DS, Liu JL, Xie MJ, Zhan Y, Qu WS, Yu ZY, et al,. (2009). Tamoxifen attenuates inflammatory-mediated damage and improves functional outcome after spinal cord injury in rats. J Neurochem 109: 1658-1667.
55. Tokumaru O, Kuroki C, Yoshimura N, Sakamoto T, Takei H, Ogata K, et al,. (2009). Neuroprotective effects of ethyl pyruvate on brain energy metabolism after ischemia-reperfusion injury: a 31P-nuclear magnetic resonance study. Neurochem Res 34: 775-785.
56. Vander Heiden MG, Cantley LC, Thompson CB, (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
57. Vavrek R, Girgis J, Tetzlaff W, Hiebert GW, Fouad K, (2006). BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 129: 1534-1545. (Pubitemid 43999385)
58. Wang DD, Bordey A, (2008). The astrocyte odyssey. Prog Neurobiol 86: 342-367.
59. Wang Q, van Hoecke M, Tang XN, Lee H, Zheng Z, Swanson RA, et al,. (2009). Pyruvate protects against experimental stroke via an anti-inflammatory mechanism. Neurobiol Dis 36: 223-231.
60. Wang X, Perez E, Liu R, Yan LJ, Mallet RT, Yang SH, (2007). Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells. Brain Res 1132: 1-9. (Pubitemid 46096455)
61. -/- mice. Stem Cells 25: 2619-2627. (Pubitemid 47582755)
62. Wilhelmsson U, Li L, Pekna M, Berthold CH, Blom S, Eliasson C, et al,. (2004). Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J Neurosci 24: 5016-5021. (Pubitemid 38697835)
63. Yiu G, He ZG, (2006). Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7: 617-627. (Pubitemid 44106744)
64. Yu ACH, Lee YL, Eng LF, (1993). Astrogliosis in culture. I. The model and the effect of antisense oligonucleotides on glial fibrillary acidic protein synthesis. J Neurosci Res 34: 295-303. (Pubitemid 23060114)
65. Yu YM, Kim JB, Lee KW, Kim SY, Han PL, Lee JK, (2005). Inhibition of the cerebral ischemic injury by ethyl pyruvate with a wide therapeutic window. Stroke 36: 2238-2243. (Pubitemid 41429253)
66. Zeng J, Liu J, Yang GY Kelly MJ, James TL, Litt L, (2007). Exogenous ethyl pyruvate versus pyruvate during metabolic recovery after oxidative stress in neonatal rat cerebrocortical slices. Anesthesiology 107: 630-640. (Pubitemid 47480570)