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Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Research Article

(-)-Epigallocatechin Gallate Attenuates Spinal Motoneuron Death Induced by Brachial Plexus Root Avulsion in Rats

Author(s): Fatai Lu, Guodong Zhang, Yingkang Zhu and Zunpeng Liu*

Volume 29, Issue 30, 2022

Published on: 15 June, 2022

Page: [5139 - 5154] Pages: 16

DOI: 10.2174/0929867329666220509204151

Price: $65


Background: Recent studies have indicated that epigallocatechin gallate (EGCG) benefits a variety of neurological insults. This study was performed to investigate the neuroprotective effect of EGCG after brachial plexus root avulsion in SD rats.

Methods: One hundred twenty SD rats were randomized into the following three groups: an EGCG group, an Avulsion group, and a Sham group. There were 40 rats in each group. EGCG (100 mg/kg, i.p.) or normal saline was administered to rats immediately following the injuries. The treatment was continued from day 1 to day 7, and the animals were sacrificed on days 3, 7, 14, and 28 post-surgery for the harvesting of spinal cord samples for Nissl staining, immunohistochemistry (caspase-3, p-JNK, p-c-Jun), and western blot analysis (p-JNK, JNK, p-c-Jun, c-Jun).

Results: EGCG treatment caused significant increases in the percentage of surviving motoneurons on days 14 and 28 (p<0.05) compared to the control animals. On days 3 and 7 after avulsion, the numbers of caspase-3-positive motoneurons in the EGCG-treated animals were significantly fewer than in the control animals (p<0.05). The numbers of p- JNK-positive motoneurons and the ratio of p-JNK/JNK were no significant differences between the Avulsion group and the EGCG-treated group after injury at any time point. The numbers of p-c-Jun-positive motoneurons and the ratio of p-c-Jun/c-Jun were significantly lower in the EGCG-treated group compared with the Avulsion group at 3d and 7d after injury (p<0.05).

Conclusion: Our results indicated that motoneurons were protected by EGCG against the cell death induced by brachial plexus root avulsion, and this effect was correlated with inhibiting c-Jun phosphorylation.

Keywords: Root avulsion, brachial plexus, epigallocatechin gallate, c-Jun phosphorylation, motoneuron death, EGCG.

« Previous
Midha, R. Epidemiology of brachial plexus injuries in a multitrauma population. Neurosurgery, 1997, 40(6), 1182-1188.
[] [PMID: 9179891]
Carlstedt, T. Nerve root replantation. Neurosurg. Clin. N. Am., 2009, 20(1), 39-50, vi.
[] [PMID: 19064178]
Eggers, R.; Tannemaat, M.R.; De Winter, F.; Malessy, M.J.; Verhaagen, J. Clinical and neurobiological advances in promoting regeneration of the ventral root avulsion lesion. Eur. J. Neurosci., 2016, 43(3), 318-335.
[] [PMID: 26415525]
El-Gammal, T.A.; Fathi, N.A. Outcomes of surgical treatment of brachial plexus injuries using nerve grafting and nerve transfers. J. Reconstr. Microsurg., 2002, 18(1), 7-15.
[] [PMID: 11917959]
Carlstedt, T.P.; Hallin, R.G.; Hedström, K.G.; Nilsson-Remahl, I.A. Functional recovery in primates with brachial plexus injury after spinal cord implantation of avulsed ventral roots. J. Neurol. Neurosurg. Psychiatry, 1993, 56(6), 649-654.
[] [PMID: 8509779]
Terzis, J.K.; Vekris, M.D.; Soucacos, P.N. Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast. Reconstr. Surg., 1999, 104(5), 1221-1240.
[] [PMID: 10513901]
Narakas, A.O. [Injuries of the brachial plexus and neighboring peripheral nerves in vertebral fractures and other trauma of the cervical spine. Orthopade, 1987, 16(1), 81-86.
[PMID: 3574946]
Zhang, X.; Liu, X.D.; Xian, Y.F.; Zhang, F.; Huang, P.Y.; Tang, Y.; Yuan, Q.J.; Lin, Z.X. Berberine enhances survival and axonal regeneration of motoneurons following spinal root avulsion and re-implantation in rats. Free Radic. Biol. Med., 2019, 143, 454-470.
[] [PMID: 31472247]
Teixeira, M.J.; da Paz, M.G.; Bina, M.T.; Santos, S.N.; Raicher, I.; Galhardoni, R.; Fernandes, D.T.; Yeng, L.T.; Baptista, A.F.; de Andrade, D.C. Neuropathic pain after brachial plexus avulsion--central and peripheral mechanisms. BMC Neurol., 2015, 15, 73.
[] [PMID: 25935556]
Jerome, J.T.; Rajmohan, B. Axillary nerve neurotization with the anterior deltopectoral approach in brachial plexus injuries. Microsurgery, 2012, 32(6), 445-451.
[] [PMID: 22434572]
Gu, H.Y.; Chai, H.; Zhang, J.Y.; Yao, Z.B.; Zhou, L.H.; Wong, W.M.; Bruce, I.C.; Wu, W.T. Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp. Neurol., 2005, 192(1), 89-99.
[] [PMID: 15698622]
Carlstedt, T.; Aldskogius, H.; Hallin, R.G.; Nilsson-Remahl, I. Novel surgical strategies to correct neural deficits following experimental spinal nerve root lesions. Brain Res. Bull., 1993, 30(3-4), 447-451.
[] [PMID: 8457894]
Carlstedt, T.; Grane, P.; Hallin, R.G.; Norén, G. Return of function after spinal cord implantation of avulsed spinal nerve roots. Lancet, 1995, 346(8986), 1323-1325.
[] [PMID: 7475770]
Kimura, M.; Umegaki, K.; Kasuya, Y.; Sugisawa, A.; Higuchi, M. The relation between single/double or repeated tea catechin ingestions and plasma antioxidant activity in humans. Eur. J. Clin. Nutr., 2002, 56(12), 1186-1193.
[] [PMID: 12494303]
Mielgo-Ayuso, J.; Barrenechea, L.; Alcorta, P.; Larrarte, E.; Margareto, J.; Labayen, I. Effects of dietary supplementation with epigallocatechin-3-gallate on weight loss, energy homeostasis, cardiometabolic risk factors and liver function in obese women: Randomised, double-blind, placebo-controlled clinical trial. Br. J. Nutr., 2014, 111(7), 1263-1271.
[] [PMID: 24299662]
Mukhtar, H.; Ahmad, N. Tea polyphenols: Prevention of cancer and optimizing health. Am. J. Clin. Nutr., 2000, 71(6)(Suppl.), 1698S-1702S.
[] [PMID: 10837321]
Granja, A.; Frias, I.; Neves, A.R.; Pinheiro, M.; Reis, S. Therapeutic potential of epigallocatechin gallate nanodelivery systems. BioMed Res. Int., 2017, (2017), 5813793.
[] [PMID: 28791306]
Lin, Y.L.; Lin, J.K. (-)-Epigallocatechin-3-gallate blocks the induction of nitric oxide synthase by down-regulating lipopolysaccharide-induced activity of transcription factor nuclear factor-kappaB. Mol. Pharmacol., 1997, 52(3), 465-472.
[] [PMID: 9281609]
Suganuma, M.; Okabe, S.; Oniyama, M.; Tada, Y.; Ito, H.; Fujiki, H. Wide distribution of [3H](-)-epigallocatechin gallate, a cancer preventive tea polyphenol, in mouse tissue. Carcinogenesis, 1998, 19(10), 1771-1776.
[] [PMID: 9806157]
Lin, L.C.; Wang, M.N.; Tseng, T.Y.; Sung, J.S.; Tsai, T.H. Pharmacokinetics of (-)-epigallocatechin-3-gallate in conscious and freely moving rats and its brain regional distribution. J. Agric. Food Chem., 2007, 55(4), 1517-1524.
[] [PMID: 17256961]
van Acker, S.A.; Tromp, M.N.; Haenen, G.R.; van der Vijgh, W.J.; Bast, A. Flavonoids as scavengers of nitric oxide radical. Biochem. Biophys. Res. Commun., 1995, 214(3), 755-759.
[] [PMID: 7575540]
Diao, Y.; Zhao, W.; Li, Y. Radiolabeling of EGCG with 125I and its biodistribution in mice. J. Radioanal. Nucl. Chem., 2014, 301(1), 167-173.
Zhang, B.; Rusciano, D.; Osborne, N.N. Orally administered epigallocatechin gallate attenuates retinal neuronal death in vivo and light-induced apoptosis in vitro . Brain Res., 2008, 1198, 141-152.
[] [PMID: 18255049]
Zhang, B.; Safa, R.; Rusciano, D.; Osborne, N.N. Epigallocatechin gallate, an active ingredient from green tea, attenuates damaging influences to the retina caused by ischemia/reperfusion. Brain Res., 2007, 1159, 40-53.
[] [PMID: 17573045]
Xie, J.; Jiang, L.; Zhang, T.; Jin, Y.; Yang, D.; Chen, F. Neuroprotective effects of Epigallocatechin-3-gallate (EGCG) in optic nerve crush model in rats. Neurosci. Lett., 2010, 479(1), 26-30.
[] [PMID: 20471452]
Wei, I.H.; Tu, H.C.; Huang, C.C.; Tsai, M.H.; Tseng, C.Y.; Shieh, J.Y. (-)-Epigallocatechin gallate attenuates NADPH-d/nNOS expression in motor neurons of rats following peripheral nerve injury. BMC Neurosci., 2011, 12, 52.
[] [PMID: 21627848]
Khalatbary, A.R.; Tiraihi, T.; Boroujeni, M.B.; Ahmadvand, H.; Tavafi, M.; Tamjidipoor, A. Effects of epigallocatechin gallate on tissue protection and functional recovery after contusive spinal cord injury in rats. Brain Res., 2010, 1306, 168-175.
[] [PMID: 19815005]
Khalatbary, A.R.; Ahmadvand, H. Anti-inflammatory effect of the epigallocatechin gallate following spinal cord trauma in rat. Iran. Biomed. J., 2011, 15(1-2), 31-37.
[PMID: 21725497]
Pervin, M.; Unno, K.; Takagaki, A.; Isemura, M.; Nakamura, Y. Function of green tea catechins in the brain: epigallocatechin gallate and its metabolites. Int. J. Mol. Sci., 2019, 20(15), E3630.
[] [PMID: 31349535]
Chen, S.; Hou, Y.; Zhao, Z.; Luo, Y.; Lv, S.; Wang, Q.; Li, J.; He, L.; Zhou, L.; Wu, W. Neuregulin-1 accelerates functional motor recovery by improving motoneuron survival after brachial plexus root avulsion in mice. Neuroscience, 2019, 404, 510-518.
[] [PMID: 30731156]
Ge, R.; Zhu, Y.; Diao, Y.; Tao, L.; Yuan, W.; Xiong, X.C. Anti-edema effect of epigallocatechin gallate on spinal cord injury in rats. Brain Res., 2013, 1527, 40-46.
[] [PMID: 23831998]
Wu, W. Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp. Neurol., 1993, 120(2), 153-159.
[] [PMID: 7684000]
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(1), 84-92.
[] [PMID: 16246329]
Zhou, L.H.; 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(6), 920-927.
[] [PMID: 16774476]
Zhou, L.H.; Han, S.; Xie, Y.Y.; Wang, L.L.; Yao, Z.B. Differences in c-jun and nNOS expression levels in motoneurons following different kinds of axonal injury in adult rats. Brain Cell Biol., 2008, 36(5-6), 213-227.
[] [PMID: 19238548]
Li, X.; Huo, X.; Zhang, C.; Ma, X.; Han, F.; Wang, G. Role of continuous high thoracic epidural anesthesia in hippocampal apoptosis after global cerebral ischemia in rats. Cell. Physiol. Biochem., 2014, 34(4), 1227-1240.
[] [PMID: 25277843]
Manabe, Y.; Nagano, I.; Gazi, M.S.; Murakami, T.; Shiote, M.; Shoji, M.; Kitagawa, H.; Abe, K. Glial cell line-derived neurotrophic factor protein prevents motor neuron loss of transgenic model mice for amyotrophic lateral sclerosis. Neurol. Res., 2003, 25(2), 195-200.
[] [PMID: 12635522]
Cheng, X.; Liu, F.L.; Zhang, J.; Wang, L.L.; Li, F.L.; Liu, S.; Zhou, L.H. EGb761 protects motoneurons against avulsion-induced oxidative stress in rats. J. Brachial Plex. Peripher. Nerve Inj., 2010, 5, 12.
[PMID: 20497551]
Wu, W.; Li, L. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci. Lett., 1993, 153(2), 121-124.
[] [PMID: 7687046]
Narakas, A.O. The treatment of brachial plexus injuries. Int. Orthop., 1985, 9(1), 29-36.
[] [PMID: 4018968]
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(2), 190-200.
[] [PMID: 8812152]
Cheng, X.; Fu, R.; Gao, M.; Liu, S.; Li, Y.Q.; Song, F.H.; Bruce, I.C.; Zhou, L.H.; Wu, W. Intrathecal application of short interfering RNA knocks down c-jun expression and augments spinal motoneuron death after root avulsion in adult rats. Neuroscience, 2013, 241, 268-279.
[] [PMID: 23506737]
Aldskogius, H.; Barron, K.D.; Regal, R. Axon reaction in hypoglossal and dorsal motor vagal neurons of adult rat: Incorporation of [3H]leucine. Exp. Neurol., 1984, 85(1), 139-151.
[] [PMID: 6203773]
Zhong, L.Y.; Wang, A.P.; Hong, L.; Chen, S.H.; Wang, X.Q.; Lv, Y.C.; Peng, T.H. Microanatomy of the brachial plexus roots and its clinical significance. Surg. Radiol. Anat., 2017, 39(6), 601-610.
[] [PMID: 27866248]
Clifton, W.E. Delayed myelopathy in patients with traumatic preganglionic brachial plexus avulsion injuries. World Neurosurgery, 2019, 122, e1562-e1569.
Li, L.; Wu, W.; Lin, L.F. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA, 1995, 92(21), 9771-9775.
[] [PMID: 7568215]
Wu, Q.; Jing, Y.; Yuan, X.; Zhang, X.; Li, B.; Liu, M.; Wang, B.; Li, H.; Liu, S.; Xiu, R. Melatonin treatment protects against acute spinal cord injury-induced disruption of blood spinal cord barrier in mice. J. Mol. Neurosci., 2014, 54(4), 714-722.
[] [PMID: 25303856]
Novikov, L.; Novikova, L.; Kellerth, J.O. Brain-derived neurotrophic factor promotes survival and blocks nitric oxide synthase expression in adult rat spinal motoneurons after ventral root avulsion. Neurosci. Lett., 1995, 200(1), 45-48.
[] [PMID: 8584263]
Araújo, M.R.; Kyrylenko, S.; Spejo, A.B.; Castro, M.V.; Ferreira Junior, R.S.; Barraviera, B.; Oliveira, A.L.R. Transgenic human embryonic stem cells overexpressing FGF2 stimulate neuroprotection following spinal cord ventral root avulsion. Exp. Neurol., 2017, 294, 45-57.
[] [PMID: 28450050]
Barbizan, R.; Castro, M.V.; Barraviera, B.; Ferreira, R.S., Jr; Oliveira, A.L. Influence of delivery method on neuroprotection by bone marrow mononuclear cell therapy following ventral root reimplantation with fibrin sealant. PLoS One, 2014, 9(8), e105712.
[] [PMID: 25157845]
Oliveira, A.L.; Thams, S.; Lidman, O.; Piehl, F.; Hökfelt, T.; Kärre, K.; Lindå, H.; Cullheim, S. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc. Natl. Acad. Sci. USA, 2004, 101(51), 17843-17848.
[] [PMID: 15591351]
Gomes-Leal, W.; Corkill, D.J.; Freire, M.A.; Picanço-Diniz, C.W.; Perry, V.H. Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp. Neurol., 2004, 190(2), 456-467.
[] [PMID: 15530884]
Galloway, D.A.; Williams, J.B.; Moore, C.S. Effects of fumarates on inflammatory human astrocyte responses and oligodendrocyte differentiation. Ann. Clin. Transl. Neurol., 2017, 4(6), 381-391.
[] [PMID: 28589165]
Spejo, A.B.; Chiarotto, G.B.; Ferreira, A.D.F.; Gomes, D.A.; Ferreira, R.S., Jr; Barraviera, B.; Oliveira, A.L.R. Neuroprotection and immunomodulation following intraspinal axotomy of motoneurons by treatment with adult mesenchymal stem cells. J. Neuroinflammation, 2018, 15(1), 230.
[] [PMID: 30107848]
Tom, V.J.; Steinmetz, M.P.; Miller, J.H.; Doller, C.M.; Silver, J. Studies on the development and behavior of the dystrophic growth cone, the hallmark of regeneration failure, in an in vitro model of the glial scar and after spinal cord injury. J. Neurosci., 2004, 24(29), 6531-6539.
[] [PMID: 15269264]
Wang, D.D.; Bordey, A. The astrocyte odyssey. Prog. Neurobiol., 2008, 86(4), 342-367.
[PMID: 18948166]
Eggers, R.; Tannemaat, M.R.; Ehlert, E.M.; Verhaagen, J. A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation. Exp. Neurol., 2010, 223(1), 207-220.
[] [PMID: 19646436]
Hallin, R.G.; 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(3), 304-310.
[] [PMID: 9989436]
Doubell, T.P.; Woolf, C.J. Growth-associated protein 43 immunoreactivity in the superficial dorsal horn of the rat spinal cord is localized in atrophic C-fiber, and not in sprouted A-fiber, central terminals after peripheral nerve injury. J. Comp. Neurol., 1997, 386(1), 111-118.
[<111::AID-CNE10>3.0.CO;2-N] [PMID: 9303528]
Bertelli, J.A.; Ghizoni, M.F. Nerve root grafting and distal nerve transfers for C5-C6 brachial plexus injuries. J. Hand Surg. Am., 2010, 35(5), 769-775.
[] [PMID: 20346595]
Wang, L.; Zhao, X.; Gao, K.; Lao, J.; Gu, Y.D. Reinnervation of thenar muscle after repair of total brachial plexus avulsion injury with contralateral C7 root transfer: Report of five cases. Microsurgery, 2011, 31(4), 323-326.
[] [PMID: 21557307]
Fox, I.K.; Brenner, M.J.; Johnson, P.J.; Hunter, D.A.; Mackinnon, S.E. Axonal regeneration and motor neuron survival after microsurgical nerve reconstruction. Microsurgery, 2012, 32(7), 552-562.
[] [PMID: 22806696]
Fournier, H.D.; Mercier, P.; Menei, P. Repair of avulsed ventral nerve roots by direct ventral intraspinal implantation after brachial plexus injury. Hand Clin., 2005, 21(1), 109-118.
[] [PMID: 15668071]
Carlstedt, T.; Norén, G. Repair of ruptured spinal nerve roots in a brachial plexus lesion. Case report. J. Neurosurg., 1995, 82(4), 661-663.
[] [PMID: 7897534]
Wang, S.; Yiu, H.W.; Li, P.; 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(3), 183-188.
[] [PMID: 22002908]
Cullheim, S.; Wallquist, W.; Hammarberg, H.; Lindå, 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(1-3), 309-316.
[] [PMID: 12589929]
Yamada, S.; Lonser, R.R.; Colohan, A.R.; Yamada, S.M.; Won, D.J. Bypass coaptation for cervical root avulsion: Indications for optimal outcome. Neurosurgery, 2009, 65(4)(Suppl.), A203-A211.
[] [PMID: 19927070]
Pintér, S.; Gloviczki, B.; Szabó, A.; Márton, G.; Nógrádi, A. Increased survival and reinnervation of cervical motoneurons by riluzole after avulsion of the C7 ventral root. J. Neurotrauma, 2010, 27(12), 2273-2282.
[] [PMID: 20939695]
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(3), 308-318.
[] [PMID: 11819038]
Frisén, J.; Fried, K.; Sjögren, A.M.; Risling, M. Growth of ascending spinal axons in CNS scar tissue. Int. J. Dev. Neurosci., 1993, 11(4), 461-475.
[] [PMID: 7694445]
Kim, T.H.; Lim, J.M.; Kim, S.S.; Kim, J.; Park, M.; Song, J.H. Effects of (-) epigallocatechin-3-gallate on Na(+) currents in rat dorsal root ganglion neurons. Eur. J. Pharmacol., 2009, 604(1-3), 20-26.
[] [PMID: 19111536]
Deng, H.M.; Yin, S.T.; Yan, D.; Tang, M.L.; Li, C.C.; Chen, J.T.; Wang, M.; Ruan, D.Y. Effects of EGCG on voltage-gated sodium channels in primary cultures of rat hippocampal CA1 neurons. Toxicology, 2008, 252(1-3), 1-8.
[] [PMID: 18706964]
Renno, W.M.; Al-Khaledi, G.; Mousa, A.; Karam, S.M.; Abul, H.; Asfar, S. (-)-Epigallocatechin-3-gallate (EGCG) modulates neurological function when intravenously infused in acute and, chronically injured spinal cord of adult rats. Neuropharmacology, 2014, 77, 100-119.
[] [PMID: 24071567]
Yao, C.; Zhang, J.; Liu, G.; Chen, F.; Lin, Y. Neuroprotection by (-)-epigallocatechin-3-gallate in a rat model of stroke is mediated through inhibition of endoplasmic reticulum stress. Mol. Med. Rep., 2014, 9(1), 69-76.
[] [PMID: 24193141]
Renno, W.M.; Al-Maghrebi, M.; Alshammari, A.; George, P. (-)-Epigallocatechin-3-gallate (EGCG) attenuates peripheral nerve degeneration in rat sciatic nerve crush injury. Neurochem. Int., 2013, 62(3), 221-231.
[] [PMID: 23313191]
Silva, K.C.; Rosales, M.A.; Hamassaki, D.E.; Saito, K.C.; Faria, A.M.; Ribeiro, P.A.; Faria, J.B.; Faria, J.M. Green tea is neuroprotective in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci., 2013, 54(2), 1325-1336.
[] [PMID: 23299475]
Itoh, T.; Tabuchi, M.; Mizuguchi, N.; Imano, M.; Tsubaki, M.; Nishida, S.; Hashimoto, S.; Matsuo, K.; Nakayama, T.; Ito, A.; Munakata, H.; Satou, T. Neuroprotective effect of (-)-epigallocatechin-3-gallate in rats when administered pre- or post-traumatic brain injury. J. Neural Transm. (Vienna), 2013, 120(5), 767-783.
[] [PMID: 23180302]
Raivich, G. c-Jun expression, activation and function in neural cell death, inflammation and repair. J. Neurochem., 2008, 107(4), 898-906.
[] [PMID: 18793328]
Bogoyevitch, M.A.; Arthur, P.G. Inhibitors of c-Jun N-terminal kinases: JuNK no more? Biochim. Biophys. Acta, 2008, 1784(1), 76-93.
[] [PMID: 17964301]
Vogel, J.; Anand, V.S.; Ludwig, B.; Nawoschik, S.; Dunlop, J.; Braithwaite, S.P. The JNK pathway amplifies and drives subcellular changes in tau phosphorylation. Neuropharmacology, 2009, 57(5-6), 539-550.
[] [PMID: 19628001]
Barnat, M.; Enslen, H.; Propst, F.; Davis, R.J.; Soares, S.; Nothias, F. Distinct roles of c-Jun N-terminal kinase isoforms in neurite initiation and elongation during axonal regeneration. J. Neurosci., 2010, 30(23), 7804-7816.
[] [PMID: 20534829]
Herdegen, T.; Waetzig, V. AP-1 proteins in the adult brain: Facts and fiction about effectors of neuroprotection and neurodegeneration. Oncogene, 2001, 20(19), 2424-2437.
[] [PMID: 11402338]
Sommer, C.; Gass, P.; Kiessling, M. Selective c-JUN expression in CA1 neurons of the gerbil hippocampus during and after acquisition of an ischemia-tolerant state. Brain Pathol., 1995, 5(2), 135-144.
[] [PMID: 7670654]
McTigue, D.M.; Horner, P.J.; Stokes, B.T.; Gage, F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci., 1998, 18(14), 5354-5365.
[] [PMID: 9651218]
Raivich, G.; Bohatschek, M.; Da Costa, C.; Iwata, O.; Galiano, M.; Hristova, M.; Nateri, A.S.; Makwana, M.; Riera-Sans, L.; Wolfer, D.P.; Lipp, H.P.; Aguzzi, A.; Wagner, E.F.; Behrens, A. The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron, 2004, 43(1), 57-67.
[] [PMID: 15233917]
Wu, W.; Li, L.; Yick, L.W.; Chai, H.; Xie, Y.; Yang, Y.; Prevette, D.M.; Oppenheim, R.W. GDNF and BDNF alter the expression of neuronal NOS, c-Jun, and p75 and prevent motoneuron death following spinal root avulsion in adult rats. J. Neurotrauma, 2003, 20(6), 603-612.
[] [PMID: 12906744]
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(4), 347-352.
[] [PMID: 8326831]
Ploia, C.; Antoniou, X.; Sclip, A.; Grande, V.; Cardinetti, D.; Colombo, A.; Canu, N.; Benussi, L.; Ghidoni, R.; Forloni, G.; Borsello, T. JNK plays a key role in tau hyperphosphorylation in Alzheimer’s disease models. J. Alzheimers Dis., 2011, 26(2), 315-329.
[] [PMID: 21628793]
Wang, L.L.; Zhao, X.C.; Yan, L.F.; Wang, Y.Q.; Cheng, X.; Fu, R.; Zhou, L.H. C-jun phosphorylation contributes to down regulation of neuronal nitric oxide synthase protein and motoneurons death in injured spinal cords following root-avulsion of the brachial plexus. Neuroscience, 2011, 189, 397-407.
[] [PMID: 21596101]
Wu, D.; Li, Q.; Zhu, X.; Wu, G.; Cui, S. Valproic acid protection against the brachial plexus root avulsion-induced death of motoneurons in rats. Microsurgery, 2013, 33(7), 551-559.
[] [PMID: 23843283]
Herdegen, T.; Leah, J.D.; 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(2-3), 643-654.
[] [PMID: 1908067]
Palmada, M.; Kanwal, S.; Rutkoski, N.J.; Gustafson-Brown, C.; Johnson, R.S.; Wisdom, R.; Carter, B.D. c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J. Cell Biol., 2002, 158(3), 453-461.
[] [PMID: 12163468]
Yuan, Q.; Hu, B.; Wu, Y.; Chu, T.H.; Su, H.; Zhang, W.; So, K.F.; Lin, Z.; Wu, W. Induction of c-Jun phosphorylation in spinal motoneurons in neonatal and adult rats following axonal injury. Brain Res., 2010, 1320, 7-15.
[] [PMID: 20096669]

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