JNK2 and JNK3 are major regulators of axonal injury-induced retinal ganglion cell death

Neurobiology of Disease

Volumn 46, Issue 2, 2012, Pages 393-401

  Fernandes, Kimberly A ^a   Harder, Jeffrey M ^a   Fornarola, Laura B ^a   Freeman, Robert S ^a   Clark, Abbot F ^b   Pang, Iok Hou ^c   John, Simon W M ^d,e,f   Libby, Richard T ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^c Alcon Research Inc   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e JACKSON LABORATORY   (United States)

^f TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Axonal injury; CJUN; Glaucoma; JNK; Mouse; Neurodegeneration; Neuroprotection; Retinal ganglion cell

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; TRANSCRIPTION FACTOR POU4F2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AXONAL INJURY; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; AXONS; CELL DEATH; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 10; MITOGEN-ACTIVATED PROTEIN KINASE 9; OPTIC NERVE INJURIES; RETINAL GANGLION CELLS; TRANSCRIPTIONAL ACTIVATION;

EID: 84859502988     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.02.003     Document Type: Article

References (82)

1. Abe N., Cavalli V. Nerve injury signaling. Curr. Opin. Neurobiol. 2008, 18:276-283.
2. Anderson D.R., Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest. Ophthalmol. 1974, 13:771-783.
3. Angel P., et al. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 1988, 55:875-885.
4. Badea T.C., et al. Distinct roles of transcription factors brn3a and brn3b in controlling the development, morphology, and function of retinal ganglion cells. Neuron 2009, 61:852-864.
5. Behrens A., et al. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 1999, 21:326-329.
6. Behrens A., et al. Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver. EMBO J. 2002, 21:1782-1790.
7. Bogoyevitch M.A., Kobe B. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 2006, 70:1061-1095.
8. Brecht S., et al. Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. 2005, 21:363-377.
9. Buckingham B.P., et al. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J. Neurosci. 2008, 28:2735-2744.
10. Cavalli V., et al. Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 2005, 168:775-787.
11. Chidlow G., et al. The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta Neuropathol. 2011, 121:737-751.
12. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
13. Cui Q., et al. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol. Cell. Neurosci. 2003, 22:49-61.
14. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
15. Eilers A., et al. 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.
16. Furuta Y., et al. Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 2000, 26:130-132.
17. Gan L., et al. POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev. Biol. 1999, 210:469-480.
18. George E.B., et al. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 1995, 15:6445-6452.
19. Ham J., et al. c-Jun and the transcriptional control of neuronal apoptosis. Biochem. Pharmacol. 2000, 60:1015-1021.
20. Hanz S., Fainzilber M. Retrograde signaling in injured nerve-the axon reaction revisited. J. Neurochem. 2006, 99:13-19.
21. Harder J.M., Libby R.T. BBC3 (PUMA) regulates developmental apoptosis but not axonal injury induced death in the retina. Mol. Neurodegener. 2011, 6:50.
22. Hibi M., et al. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 1993, 7:2135-2148.
23. Hilberg F., et al. c-jun is essential for normal mouse development and hepatogenesis. Nature 1993, 365:179-181.
24. Howell G.R., et al. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007, 179:1523-1537.
25. Howell G.R., et al. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J. Clin. Investig. 2011, 121:1429-1444.
26. Huang X., et al. Distortion of axonal cytoskeleton: an early sign of glaucomatous damage. Investig. Ophthalmol. Vis. Sci. 2011, 52:2879-2888.
27. Isenmann S., Bahr M. Expression of c-Jun protein in degenerating retinal ganglion cells after optic nerve lesion in the rat. Exp. Neurol. 1997, 147:28-36.
28. Jeon C.J., et al. The major cell populations of the mouse retina. J. Neurosci. 1998, 18:8936-8946.
29. Johnson R.S., et al. A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev. 1993, 7:1309-1317.
30. Johnson E.C., et al. Neurotrophin roles in retinal ganglion cell survival: lessons from rat glaucoma models. Exp. Eye Res. 2009, 88:808-815.
31. Kielczewski J.L., et al. The effect of experimental glaucoma and optic nerve transection on amacrine cells in the rat retina. Investig. Ophthalmol. Vis. Sci. 2005, 46:3188-3196.
32. Knoferle J., et al. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6064-6069.
33. Kuan C.Y., et al. A critical role of neural-specific JNK3 for ischemic apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15184-15189.
34. Kwong J.M., Caprioli J. Expression of phosphorylated c-Jun N-terminal protein kinase (JNK) in experimental glaucoma in rats. Exp. Eye Res. 2006, 82:576-582.
35. Lebrun-Julien F., et al. ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3817-3822.
36. Lee J.K., et al. Distinct localization of SAPK isoforms in neurons of adult mouse brain implies multiple signaling modes of SAPK pathway. Brain Res. Mol. Brain Res. 1999, 70:116-124.
37. Leppa S., Bohmann D. Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 1999, 18:6158-6162.
38. Levkovitch-Verbin H., et al. The transcription factor c-jun is activated in retinal ganglion cells in experimental rat glaucoma. Exp. Eye Res. 2005, 80:663-670.
39. Li Y., et al. Experimental induction of retinal ganglion cell death in adult mice. Investig. Ophthalmol. Vis. Sci. 1999, 40:1004-1008.
40. Li Y., et al. Bax-dependent and independent pathways of retinal ganglion cell death induced by different damaging stimuli. Exp. Eye Res. 2000, 71:209-213.
41. Li Y., et al. Dominant inheritance of retinal ganglion cell resistance to optic nerve crush in mice. BMC Neurosci. 2007, 8:19.
42. Libby R.T., et al. Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage. PLoS Genet. 2005, 1:17-26.
43. Lindwall C., Kanje M. Retrograde axonal transport of JNK signaling molecules influence injury induced nuclear changes in p-c-Jun and ATF3 in adult rat sensory neurons. Mol. Cell. Neurosci. 2005, 29:269-282.
44. Lingor P., et al. Down-regulation of apoptosis mediators by RNAi inhibits axotomy-induced retinal ganglion cell death in vivo. Brain 2005, 128:550-558.
45. Liu H., et al. Interference of the apoptotic signaling pathway in RGC stress response by SP600125 in moderate ocular hypertensive rats. Chin. J. Physiol. 2011, 54:124-132.
46. Lukas T.J., et al. Early cellular signaling responses to axonal injury. Cell Commun. Signaling: CCS 2009, 7:5.
47. Ma C., et al. dp5/HRK is a c-Jun target gene and required for apoptosis induced by potassium deprivation in cerebellar granule neurons. J. Biol. Chem. 2007, 282:30901-30909.
48. Martin J.H., et al. Developmental expression in the mouse nervous system of the p493F12 SAP kinase. Brain Res. Mol. Brain Res. 1996, 35:47-57.
49. Miller B.R., et al. A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat. Neurosci. 2009, 12:387-389.
50. Mok S.A., et al. A retrograde apoptotic signal originating in NGF-deprived distal axons of rat sympathetic neurons in compartmented cultures. Cell Res. 2009, 19:546-560.
51. Morfini G.A., et al. Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci. 2009, 12:864-871.
52. Morishima Y., et al. Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J. Neurosci. 2001, 21:7551-7560.
53. Moshiri A., et al. Near complete loss of retinal ganglion cells in the math5/brn3b double knockout elicits severe reductions of other cell types during retinal development. Dev. Biol. 2008, 316:214-227.
54. Muller G.J., et al. A role for mixed lineage kinases in granule cell apoptosis induced by cytoskeletal disruption. J. Neurochem. 2006, 96:1242-1252.
55. Munemasa Y., et al. Pro-apoptotic role of c-Jun in NMDA-induced neurotoxicity in the rat retina. J. Neurosci. Res. 2006, 83:907-918.
56. Natoli G., et al. Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science 1997, 275:200-203.
57. Oliver G., et al. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 1995, 121:4045-4055.
58. Pan L., et al. Functional equivalence of Brn3 POU-domain transcription factors in mouse retinal neurogenesis. Development 2005, 132:703-712.
59. Park K.K., et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
60. Pelzel H.R., et al. Histone H4 deacetylation plays a critical role in early gene silencing during neuronal apoptosis. BMC Neurosci. 2010, 11:62.
61. Perrin V., et al. Implication of the JNK pathway in a rat model of Huntington's disease. Exp. Neurol. 2009, 215:191-200.
62. Pirianov G., et al. Deletion of the c-Jun N-terminal kinase 3 gene protects neonatal mice against cerebral hypoxic-ischaemic injury. J. Cereb. Blood Flow Metab. 2007, 27:1022-1032.
63. Pulverer B.J., et al. Phosphorylation of c-jun mediated by MAP kinases. Nature 1991, 353:670-674.
64. Quigley H.A., et al. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am. J. Ophthalmol. 1983, 95:673-691.
65. Quigley H.A., et al. Lack of neuroprotection against experimental glaucoma in c-Jun N-terminal kinase 3 knockout mice. Exp. Eye Res. 2011, 92:299-305.
66. Raivich G., Behrens A. Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain. Prog. Neurobiol. 2006, 78:347-363.
67. Ries V., et al. JNK2 and JNK3 combined are essential for apoptosis in dopamine neurons of the substantia nigra, but are not required for axon degeneration. J. Neurochem. 2008, 107:1578-1588.
68. Robinson G.A., Madison R.D. Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vis. Res. 2004, 44:2667-2674.
69. Roth S., et al. Mitogen-activated protein kinases and retinal ischemia. Invest. Ophthalmol. Vis. Sci. 2003, 44:5383-5395.
70. Schenkel J. Activation of the c-Jun transcription factor following neurodegeneration in vivo. Neurosci. Lett. 2004, 361:36-39.
71. Schlamp C.L., et al. Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci. 2006, 7:66.
72. Sun H., et al. Protective effect of a JNK inhibitor against retinal ganglion cell loss induced by acute moderate ocular hypertension. Mol. Vis. 2011, 17:864-875.
73. Tezel G., et al. TNF-alpha and TNF-alpha receptor-1 in the retina of normal and glaucomatous eyes. Investig. Ophthalmol. Vis. Sci. 2001, 42:1787-1794.
74. Tezel G., et al. Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest. Ophthalmol. Vis. Sci. 2003, 44:3025-3033.
75. Tezel G., et al. Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Res. 2004, 996:202-212.
76. Wang S.W., et al. Retinal ganglion cell differentiation in cultured mouse retinal explants. Methods 2002, 28:448-456.
77. Weishaupt J.H., et al. Axotomy-induced early down-regulation of POU-IV class transcription factors Brn-3a and Brn-3b in retinal ganglion cells. J. Mol. Neurosci.: MN. 2005, 26:17-25.
78. Whitfield J., et al. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 2001, 29:629-643.
79. Xia X.G., et al. 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.
80. Yang D.D., et al. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997, 389:865-870.
81. Yang X., et al. Phosphorylation-dependent interaction with 14-3-3 in the regulation of bad trafficking in retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2008, 49:2483-2494.
82. Yoshida K., et al. Amino-terminal phosphorylation of c-Jun regulates apoptosis in the retinal ganglion cells by optic nerve transection. Invest. Ophthalmol. Vis. Sci. 2002, 43:1631-1635.