Valproic acid protection against the brachial plexus root avulsion-induced death of motoneurons in rats

Microsurgery

Volumn 33, Issue 7, 2013, Pages 551-559

  Wu, Dianxiu ^a   Li, Qiang ^a   Zhu, Xiaojuan ^b   Wu, Guangzhi ^a   Cui, Shusen ^a  

^a JILIN UNIVERSITY   (China)

^b NORTHEAST NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; PROTEIN C JUN; VALPROIC ACID; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRACHIAL PLEXUS; DRUG MECHANISM; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MOTONEURON; NICK END LABELING; NISSL STAINING; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; ANALYSIS OF VARIANCE; ANIMAL; BRACHIAL PLEXUS NEUROPATHIES; CELL CULTURE; CELL DEATH; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; INJURIES; PATHOLOGY; RANDOMIZATION; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY; SPINAL CORD INJURIES; TUNEL ASSAY; ULTRASTRUCTURE; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; BRACHIAL PLEXUS; BRACHIAL PLEXUS NEUROPATHIES; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MICROSCOPY, ELECTRON; MOTOR NEURONS; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION; RATS; RATS, WISTAR; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY; SPINAL CORD INJURIES; VALPROIC ACID;

EID: 84886915189     PISSN: 07381085     EISSN: 10982752     Source Type: Journal    
DOI: 10.1002/micr.22130     Document Type: Article

References (69)

1. Bertelli JA, Ghizoni MF,. Nerve root grafting and distal nerve transfers for C5-C6 brachial plexus injuries. J Hand Surg Am 2010; 35: 769-775.
2. Wang L, Zhao X, Gao K, Lao J, Gu YD,. Reinnervation of thenar muscle after repair of total brachial plexus avulsion injury with contralateral C7 root transfer: Report of five cases. Microsurgery 2011; 31: 323-326.
3. Jerome JT, Rajmohan B,. Axillary nerve neurotization with the anterior deltopectoral approach in brachial plexus injuries. Microsurgery 2012; 32: 445-451.
4. Fox IK, Brenner MJ, Johnson PJ, Hunter DA, Mackinnon SE,. Axonal regeneration and motor neuron survival after microsurgical nerve reconstruction. Microsurgery 2012; 32: 552-562.
5. Koliatsos VE, Price WL, Pardo CA, Price DL,. Ventral root avulsion: An experimental model of death of adult motor neurons. J Comp Neurol 1994; 342: 35-44.
6. Wu W, Li L,. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci Lett 1993; 153: 121-124.
7. Gu Y, Spasic Z, Wu W,. The effects of remaining axons on motoneuron survival and NOS expression following axotomy in the adult rat. Dev Neurosci 1997; 19: 255-259.
8. McKay Hart A, Brannstrom T, Wiberg M, Terenghi G,. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat-timecourse of cell death and elimination. Exp Brain Res 2002; 142: 308-318.
9. Novikov L, Novikova L, Kellerth JO,. Brain-derived neurotrophic factor promotes axonal regeneration and long-term survival of adult rat spinal motoneurons in vivo. Neuroscience 1997; 79: 765-774.
10. Fu SY, Gordon T,. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 1997; 14: 67-116.
11. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M,., Tessler A, Fischer L,. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 1999; 19: 4370-4387.
12. Oliveira AL, Risling M, Negro A, Langone F, Cullheim S,. Apoptosis of spinal Interneurons induced by sciatic nerve axotomy in the neonatal rat is counteracted by nerve growth factor and ciliary neurotrophic factor. J Comp Neurol 2002; 447: 381-393.
13. Pardridge WM,. CNS drug design based on principles of blood-brain barrier transport. J Neurochem 1998; 70: 1781-1792.
14. Pardridge WM, Wu D, Sakane T,. Combined use of carboxyl-directed protein pegylation and vector-mediated blood-brain barrier drug delivery system optimizes brain uptake of brain-derived neurotrophic factor following intravenous administration. Pharm Res 1998; 15: 576-582.
15. Weihl CC, Connolly AM, Pestronk A,. Valproate may improve strength and function in patients with type III/IV spinal muscle atrophy. Neurology 2006; 67: 500-501.
16. Dragunow M, Greenwood JM, Cameron RE, Narayan PJ, O'Carroll SJ, Pearson AG, Gibbons HM,. Valproic acid induces caspase3-mediated apoptosis in microglial cells. Neuroscience 2006; 140: 1149-1156.
17. Smith AM, Gibbons HM, Dragunow M,. Valproic acid enhances microglial phagocytosis of amyloid-beta (1-42). Neuroscience 2010; 169: 505-515.
18. Gibbons HM, Smith AM, Teoh HH, Bergin PM, Mee EW, Faull RL, Dragunow M,. Valproic acid induces microglial dysfunction, not apoptosis, in human glial cultures. Neurobiol Dis 2011; 41: 96-103.
19. Santos AR Jr, Wada ML, Langone F, Oliveira AL,. Differential schwann cell migration in adult and old mice: An in vitro study. Brain Res 2000; 881: 73-76.
20. Yuan PX, Huang LD, Jiang YM, Gutkind JS, Manji HK, Chen G,. The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth. J Biol Chem 2001; 276: 31674-31683.
21. Pan T, Li X, Xie W, Jankovic J, Le W,. Valproic acid-mediated Hsp70 induction and anti-apoptotic neuroprotection in SH-SY5Y cells. FEBS Lett 2005; 579: 6716-6720.
22. Johannessen CU,. Mechanisms of action of valproate: A commentatory. Neurochem Int 2000; 37: 103-110.
23. Boeckeler K, Adley K, Xu X, Jenkins A, Jin T, Williams RS,. The neuroprotective agent, valproic acid, regulates the mitogen-activated protein kinase pathway through modulation of protein kinase A signaling in Dictyostelium discoideum. Eur J Cell Biol 2006; 85: 1047-1057.
24. Herdegen T, Leah JD, Manisali A, Bravo R, Zimmermann M,. c-JUN-like immunoreactivity in the CNS of the adult rat: Basal and transynaptically induced expression of an immediate-early gene. Neuroscience 1991; 41: 643-654.
25. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL,. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 1995; 14: 927-939.
26. Tsujimoto Y, Croce CM,. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci U S A 1986; 83: 5214-5218.
27. Chen DF, Schneider GE, Martinou JC, Tonegawa S,. Bcl-2 promotes regeneration of severed axons in mammalian CNS. Nature 1997; 385: 434-439.
28. Szupera Z, Mezei Z, Kis B, Gecse A, Vécsei L, Telegdy G,. The effects of valproate on the arachidonic acid metabolism of rat brain microvessels and of platelets. Eur J Pharmacol 2000; 387: 205-210.
29. Zhou LH, Wu W,. Survival of injured spinal motoneurons in adult rat upon treatment with glial cell line-derived neurotrophic factor at 2 weeks but not at 4 weeks after root avulsion. J Neurotrauma 2006; 23: 920-927.
30. Zhou L, Wu W,. Antisense oligos to neuronal nitric oxide synthase aggravate motoneuron death induced by spinal root avulsion in adult rat. Exp Neurol 2006; 197: 84-92.
31. Cheng X, Liu FL, Zhang J, Wang LL, Li FL, Liu S, Zhou LH,. EGb761 protects motoneurons against avulsion-induced oxidative stress in rats. J Brachial Plex Peripher Nerve Inj 2010; 5: 12.
32. Li L, Oppenheim RW, Lei M, Houenou LJ,. Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J Neurobiol 1994; 25: 759-766.
33. Li L, Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ,. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci U S A 1995; 92: 9771-9775.
34. Wu W,. Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp Neurol 1993; 120: 153-159.
35. Bergerot A, Shortland PJ, Anand P, Hunt SP, Carlstedt T,. Co-treatment with riluzole and GDNF is necessary for functional recovery after ventral root avulsion injury. Exp Neurol 2004; 187: 359-366.
36. Kishino A, Ishige Y, Tatsuno T, Nakayama C, Noguchi H,. BDNF prevents and reverses adult rat motor neuron degeneration and induces axonal outgrowth. Exp Neurol 1997; 144: 273-286.
37. Gregory J, Cowey A, Jones M, Pickard S, Ford D,. The anatomy, investigations and management of adult brachial plexus injuries. Orthop Trauma 2009; 23: 420-432.
38. Carlstedt T, Noren G,. Repair of ruptured spinal nerve roots in a brachial plexus lesion. J Neurosurg 1995; 82: 661-663.
39. Fournier HD, Mercier P, Menei P,. Repair of avulsed ventral nerve roots by direct ventral intraspinal in implantation after brachial plexus injury. Hand Clin 2005; 21: 109-118.
40. Wang S, Yiu HW, Li Y, Wang H, Pan Y,. Contralateral C7 nerve root transfer to neurotize the upper trunk via a modified prespinal route in repair of brachial plexus avulsion injury. Microsurgery 2012; 32: 183-188.
41. Leffert RD, Seddon H,. Infraclavicular brachial plexus injuries. J Bone Joint Surg Br 1965; 49B: 9-22.
42. Amr SM, Moharram AN,. Repair of brachial plexus lesions by end-to-side side-to-side grafting neurorrhaphy: Experience based on 11 cases. Microsurgery 2005; 25: 126-146.
43. Bertelli JA, Ghizoni MFÁ, Loure lro Chaves DP,. Sensory disturbances and pain complaints after brachial plexus root injury: A prospective study involving 150 adult patients. Microsurgery 2011; 31: 93-97.
44. Cullheim S, Wallquist W, Hammarberg H, Lind å H, Piehl F, Carlstedt T, Risling M,. Properties of motoneurons underlying their regenerative capacity after axon lesions in the ventral funiculus or at the surface of the spinal cord. Brain Res Brain Res Rev 2002; 40: 309-316.
45. Hallin RG, Carlstedt T, Nilsson-Remahl I, Risling M,. Spinal cord implantation of avulsed ventral roots in primates; correlation between restored motor function and morphology. Exp Brain Res 1999; 124: 304-310.
46. Gu HY, Chai H, Zhang ZB, Yao LH, Zhou LH, Wong WM, Bruce IC, Wu WT,. Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp Neurol 2005; 192: 89-99.
47. Chen ZY, Chai YF, Cao L, Lu CL, He C,. Glial cell line-derived neurotrophic factor enhances axonal regeneration following sciatic nerve transection in adult rats. Brain Res 2001; 902: 272-276.
48. Tuszynski MH, Gabriel K, Gage FH, Suhr S, Meyer S, Rosetti A,. Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neuritis after adult spinal cord injury. Exp Neurol 1996; 137: 157-173.
49. Yin Q, Kemp GK, Yu LG, Wagstaff SC, Frostick SP,. Neurotrophin-4 delivered by fibrin glue promotes peripheral nerve regeneration. Muscle Nerve 2001; 24: 345-351.
50. ALS CNTF Treatment group. A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neuro-trophic factor (rHCNTF) in amyotrophic lateral sclerosis. Neurology 1996; 46: 1244-1249.
51. Scism JL, Powers KM, Artru AA, Chambers AC, Lewis L, Adkison KK, Kalhorn TF, Shen DD,. Effects of probenecid on brain-cerebrospinal fluid-blood distribution kinetics of E-Delta2-valproic acid in rabbits. Drug Metab Dispos 1997; 25: 1337-1346.
52. Yamauchi J, Miyamoto Y, Kusakawa S, Torii T, Mizutani R, Sanbe A, Nakajima H, Kiyokawa N, Tanoue A,. Neurofibromatosis 2 tumor suppressor, the gene induced by valproic acid, mediates neurite outgrowth through interaction with paxillin. Exp cell Res 2008; 314: 2279-2288.
53. Fei W, Aixi Y, Danmou X, Wusheng K, Zhengren P, Ting R,. The mood stabilizer valproic acid induces proliferation and myelination of rat Schwann cells. Neurosci Res 2011; 70: 383-390.
54. Cui SS, Yang CP, Bowen RC, Bai O, Li XM, Jiang W, Zhang X,. Valproic acid enhances axonal regeneration and recovery of motor function after sciatic nerve axotomy in adult rats. Brain Res 2003; 975: 229-236.
55. Leng Y, Marinova Z, Reis-Fernandes MA, Nau H, Chuang DM,. Potent neuroprotective effects of novel structural derivatives of valproic acid: Potential roles of HDAC inhibition and HSP70 induction. Neurosci Lett 2010; 476: 127-132.
56. Lv L, Sun Y, Han X, Xu CC, Tang YP, Dong Q,. Valproic acid improves outcome after rodent spinal cord injury: Potential roles of histone deacetylase inhibition. Brain Res 2011; 1396: 60-68.
57. Lv L, Han X, Sun Y, Wang X, Dong Q,. Valproic acid improves locomotion in vivo after SCI and axonal growth of neurons in vitro. Exp Neurol 2012; 233: 783-790.
58. Raivich G, Bohatschek M, Da Costa C, Iwata O, Galiano M, Hristova M, Nateri AS, Makwana M, Riera-Sans L, Wolfer DP, Lipp HP, Aguzzi A, Wagner EF, Behrens A,. The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 2004; 43: 57-67.
59. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM Jr,. Altered gene expression in neurons during programmed cell death: Identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 1994; 127: 1717-1727.
60. Dragunow M, Young D, Hughes P, MacGibbon G, Lawlor P, Singleton K, Sirimanne E, Beilharz E, Gluckman P,. Is c-Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Brain Res Mol Brain Res 1993; 18: 347-352.
61. Houle JD, Schramm P, Herdeqen T,. Trophic factor modulation of c-Jun expression in supraspinal neurons after chronic spinal cord injury. Exp Neurol 1998; 154: 602-611.
62. Wu W,. Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: A comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp Neurol 1996; 141: 190-200.
63. Kroemer G,. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 1997; 3: 614-620.
64. 2+ fluxes. Proc Natl Acad Sci U S A 1994; 91: 6569-6573.
65. Clark RS, Chen J, Watkins SC, Kochanek PM, Chen M, Stetle RA, Loeffert JE, Graham SH,. Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J Neurosci 1997; 17: 9172-9182.
66. Yamada M, Natsume A, Mata M, Oligino T, Goss J, Glorioso J, Fink DJ,. Herpes simplex virus vector-mediated expression of Bcl-2 protects spinal motor neurons from degeneration following root avulsion. Exp Neurol 2001; 168: 225-230.
67. Wang ZM, Dai CF, Kanoh N, Chi FL, Li KY,. Apoptosis and expression of Bcl-2 in facial motoneurons after facial nerve injury. Otol Neurotol 2002; 23: 397-404.
68. Chen G, Zeng WZ, Yuan PX, Huang LD, Jiang YM, Zhao ZH, Manji HK,. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 1999; 72: 879-882.
69. Lin H, Wang H, Chen D, Gu Y,. A dose-effect relationship of Ginkgo biloba extract to nerve regeneration in a rat model. Microsurgery 2007; 27: 673-677.