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

Volumn 189, Issue , 2011, Pages 397-407

  Wang, L L ^a   Zhao, X C ^a   Yan, L F ^a   Wang, Y Q ^a   Cheng, X ^a   Fu, R ^a   Zhou, L H ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

C jun phosphorylation; Motoneuron death; Neuronal nitric oxide synthase; Root avulsion

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; NITRIC OXIDE SYNTHASE; PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVULSION INJURY; BRACHIAL PLEXUS INJURY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; INHIBITION KINETICS; MALE; MOTONEURON; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD INJURY; SPINAL CORD VENTRAL HORN; UPREGULATION;

ANIMALS; BRACHIAL PLEXUS; CELL DEATH; DOWN-REGULATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MOTOR NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES;

EID: 79960903504     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.070     Document Type: Article

References (57)

1. 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, 30:7804-7816.
2. Barrette B., Calvo E., Vallieres N., Lacroix S. Transcriptional profiling of the injured sciatic nerve of mice carrying the Wld(S) mutant gene: identification of genes involved in neuroprotection, neuroinflammation, and nerve regeneration. Brain Behav Immun 2010, 24:1254-1267.
3. Bogoyevitch M.A., Arthur P.G. Inhibitors of c-Jun N-terminal kinases: JuNK no more?. Biochim Biophys Acta 2008, 1784:76-93.
4. Borsello T., Centeno C., Riederer I.M., Haefliger J.A., Riederer B.M. Phosphorylation-dependent dimerization and subcellular localization of islet-brain 1/c-Jun N-terminal kinase-interacting protein 1. J Neurosci Res 2007, 85:3632-3641.
5. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 1991, 7:615-624.
6. Casanovas A., Ribera J., Hager G., Kreutzberg G.W., Esquerda J.E. c-Jun regulation in rat neonatal motoneurons postaxotomy. J Neurosci Res 2001, 63:469-479.
7. Chai H., Wu W., So K.F., Yip H.K. Survival and regeneration of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Neuroreport 2000, 11:1249-1252.
8. Chan Y.M., Yick L.W., Yip H.K., So K.F., Oppenheim R.W., Wu W. Inhibition of caspases promotes long-term survival and reinnervation by axotomized spinal motoneurons of denervated muscle in newborn rats. Exp Neurol 2003, 181:190-203.
9. 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.
10. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
11. Deckwerth T.L., Easton R.M., Knudson C.M., Korsmeyer S.J., Johnson E.M. Placement of the BCL2 family member BAX in the death pathway of sympathetic neurons activated by trophic factor deprivation. Exp Neurol 1998, 152:150-162.
12. Derijard B., Hibi M., Wu I.H., Barrett T., Su B., Deng T., Karin M., Davis R.J. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 1994, 76:1025-1037.
13. Eilers A., Whitfield J., Shah B., Spadoni C., Desmond H., Ham J. Direct inhibition of c-Jun N-terminal kinase in sympathetic neurones prevents c-jun promoter activation and NGF withdrawal-induced death. J Neurochem 2001, 76:1439-1454.
14. Gao Y.J., Xu Z.Z., Liu Y.C., Wen Y.R., Decosterd I., Ji R.R. The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition. Pain 2010, 148:309-319.
15. 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, 192:89-99.
16. Guan Q.H., Pei D.S., Zhang Q.G., Hao Z.B., Xu T.L., Zhang G.Y. The neuroprotective action of SP600125, a new inhibitor of JNK, on transient brain ischemia/reperfusion-induced neuronal death in rat hippocampal CA1 via nuclear and non-nuclear pathways. Brain Res 2005, 1035:51-59.
17. Gupta S., Barrett T., Whitmarsh A.J., Cavanagh J., Sluss H.K., Derijard B., Davis R.J. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 1996, 15:2760-2770.
18. Herdegen T., Kummer W., Fiallos C.E., Leah J., Bravo R. Expression of c-JUN, JUN B and JUN D proteins in rat nervous system following transection of vagus nerve and cervical sympathetic trunk. Neuroscience 1991, 45:413-422.
19. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 1998, 28:370-490.
20. Ichikawa H., Kano M., Shimizu Y., Suzuki T., Sawada E., Ono W., Chu L.W., Cote P.D. Increase of c-Fos and c-Jun expression in spinal and cranial motoneurons of the degenerating muscle mouse (Scn8a(dmu)). Cell Mol Neurobiol 2010, 30:737-742.
21. Ikeda K., Aoki M., Kawazoe Y., Sakamoto T., Hayashi Y., Ishigaki A., Nagai M., Kamii R., Kato S., Itoyama Y., Watabe K. Motoneuron degeneration after facial nerve avulsion is exacerbated in presymptomatic transgenic rats expressing human mutant Cu/Zn superoxide dismutase. J Neurosci Res 2005, 82:63-70.
22. Jenkins R., Hunt S.P. Long-term increase in the levels of c-jun mRNA and jun protein-like immunoreactivity in motor and sensory neurons following axon damage. Neurosci Lett 1991, 129:107-110.
23. Kamada H., Nito C., Endo H., Chan P.H. Bad as a converging signaling molecule between survival PI3-K/Akt and death JNK in neurons after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2007, 27:521-533.
24. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001, 81:807-869.
25. Li L., Houenou L.J., Wu W., Lei M., Prevette D.M., Oppenheim R.W. Characterization of spinal motoneuron degeneration following different types of peripheral nerve injury in neonatal and adult mice. J Comp Neurol 1998, 396:158-168.
26. Li M., Wang L., Peng Y., Wang J.C., Zhou L.H. Knockdown of the neuronal nitric oxide synthase gene retard the development of the cerebellar granule neurons in vitro. Dev Dyn 2010, 239:474-481.
27. Lindwall C., Kanje M. The role of p-c-Jun in survival and outgrowth of developing sensory neurons. Neuroreport 2005, 16:1655-1659.
28. Nangle M.R., Keast J.R. Deafferentation and axotomy each cause neurturin-independent upregulation of c-Jun in rodent pelvic ganglia. Exp Neurol 2009, 215:271-280.
29. Newbern J., Taylor A., Robinson M., Lively M.O., Milligan C.E. c-Jun N-terminal kinase signaling regulates events associated with both health and degeneration in motoneurons. Neuroscience 2007, 147:680-692.
30. Okuno S., Saito A., Hayashi T., Chan P.H. The c-Jun N-terminal protein kinase signaling pathway mediates Bax activation and subsequent neuronal apoptosis through interaction with Bim after transient focal cerebral ischemia. J Neurosci 2004, 24:7879-7887.
31. Oo T.F., Henchcliffe C., James D., Burke R.E. Expression of c-fos, c-jun, and c-jun N-terminal kinase (JNK) in a developmental model of induced apoptotic death in neurons of the substantia nigra. J Neurochem 1999, 72:557-564.
32. Parsadanian A., Pan Y., Li W., Myckatyn T.M., Brakefield D. Astrocyte-derived transgene GDNF promotes complete and long-term survival of adult facial motoneurons following avulsion and differentially regulates the expression of transcription factors of AP-1 and ATF/CREB families. Exp Neurol 2006, 200:26-37.
33. Piehl F., Hammarberg H., Tabar G., Hokfelt T., Cullheim S. Changes in the mRNA expression pattern, with special reference to calcitonin gene-related peptide, after axonal injuries in rat motoneurons depends on age and type of injury. Exp Brain Res 1998, 119:191-204.
34. Piehl F., Tabar G., Cullheim S. Expression of NMDA receptor mRNAs in rat motoneurons is down-regulated after axotomy. Eur J Neurosci 1995, 7:2101-2110.
35. Pulverer B.J., Kyriakis J.M., Avruch J., Nikolakaki E., Woodgett J.R. Phosphorylation of c-jun mediated by MAP kinases. Nature 1991, 353:670-674.
36. Raivich G. c-Jun expression, activation and function in neural cell death, inflammation and repair. J Neurochem 2008, 107:898-906.
37. 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, 43:57-67.
38. Saporito M.S., Brown E.M., Miller M.S., Carswell S. CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons in vivo. J Pharmacol Exp Ther 1999, 288:421-427.
39. Saporito M.S., Thomas B.A., Scott R.W. MPTP activates c-Jun NH(2)-terminal kinase (JNK) and its upstream regulatory kinase MKK4 in nigrostriatal neurons in vivo. J Neurochem 2000, 75:1200-1208.
40. Silva R.M., Kuan C.Y., Rakic P., Burke R.E. Mixed lineage kinase-c-jun N-terminal kinase signaling pathway: a new therapeutic target in Parkinson's disease. Mov Disord 2005, 20:653-664.
41. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci 2000, 15:170-182.
42. Vlug A.S., Teuling E., Haasdijk E.D., French P., Hoogenraad C.C., Jaarsma D. ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur J Neurosci 2005, 22:1881-1894.
43. 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, 57:539-550.
44. Wang J., Yan L., Zhao X., Wu W., Zhou L.H. The diversity of nNOS gene expression in avulsion-injured spinal motoneurons among laboratory rodents. Nitric Oxide 2010, 22:37-42.
45. Wang W., Shi L., Xie Y., Ma C., Li W., Su X., Huang S., Chen R., Zhu Z., Mao Z., Han Y., Li M. SP600125, a new JNK inhibitor, protects dopaminergic neurons in the MPTP model of Parkinson's disease. Neurosci Res 2004, 48:195-202.
46. Whitmarsh A.J., Davis R.J. Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem Sci 1998, 23:481-485.
47. Wu W. Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry. Exp Neurol 1993, 120:153-159.
48. 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.
49. 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, 20:603-612.
50. Wu W., Li Y., Schinco F.P. Expression of c-jun and neuronal nitric oxide synthase in rat spinal motoneurons following axonal injury. Neurosci Lett 1994, 179:157-161.
51. Xia X.G., Harding T., Weller M., Bieneman A., Uney J.B., Schulz J.B. Gene transfer of the JNK interacting protein-1 protects dopaminergic neurons in the MPTP model of Parkinson's disease. Proc Natl Acad Sci U S A 2001, 98:10433-10438.
52. Yin K.J., Kim G.M., Lee J.M., He Y.Y., Xu J., Hsu C.Y. JNK activation contributes to DP5 induction and apoptosis following traumatic spinal cord injury. Neurobiol Dis 2005, 20:881-889.
53. Yuan Q., Hu B., Su H., So K.F., Lin Z., Wu W. GAP-43 expression correlates with spinal motoneuron regeneration following root avulsion. J Brachial Plex Peripher Nerve Inj 2009, 4:18.
54. 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.
55. 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.
56. 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, 36:213-227.
57. 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, 23:920-927.