Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N- terminal kinases after neuronal injury

Journal of Neuroscience

Volumn 18, Issue 14, 1998, Pages 5124-5135

  Herdegen, Thomas ^a,b,d   Claret, Francois Xavier ^a,e   Kallunki, Tuula ^a   Martin Villalba, Ana ^b   Winter, Christine ^b   Hunter, Tony ^c   Karin, Michael ^a  

^a San Diego   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d UNIVERSITY OF KIEL   (Germany)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Apoptosis; Axotomy; c Jun; Focal ischemia reperfusion; Medial forebrain bundle; Substantia nigra

Indexed keywords

CELL SURFACE RECEPTOR; FAS ANTIGEN; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR AP 1; URIDINE TRIPHOSPHATE;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ACTIVATION; MALE; MEDIAL FOREBRAIN BUNDLE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NONHUMAN; ONCOGENE C JUN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; SUBSTANTIA NIGRA;

EID: 0032527879     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-14-05124.1998     Document Type: Article

References (67)

1. Anderson AJ, Cummings BJ, Cotman CW (1994) Increased immunoreactivity for Jun- and Fos-related proteins in Alzheimer's disease: association with pathology. Exp Neurol 125:286-295.
2. Arias J, Alberts AS, Brindle P, Claret FX, Smeal T, Karin M, Feramisco J, Montminy M (1994) Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370:226-229.
3. Asanuma M, Nishibayashi S, Kondo Y, Iwata E, Tsuda M, Ogawa N (1995) Effects of single cyclosporin A pretreatment on pentylenetetrazol-induced convulsion and on TRE-binding activity in the rat brain. Mol Brain Res 33:29-36.
4. Blottner D, Herdegen T (1997) Neuroprotective FGF-2 down-regulates the c-Jun transcription factor in axotomized sympathetic preganglionic neurons of adult rats. Neuroscience 82:283-292.
5. Bossy-Wetzel E, Bakiri L, Yaniv M (1997) Induction of apoptosis by the transcription factor c-Jun. EMBO J 16:1695-1709.
6. Brecht S, Buschmann T, Grimm S, Zimmermann M, Herdegen T (1997) Persisting expression of galanin in axotomized mamillary and septal neurons of adult rats labeled for c-Jun and NADPH-diaphorase. Mol Brain Res 48:7-16.
7. Broude E, Bregman B (1996) Supply of neurotrophic factors and peripheral nerve grafts enhances the expression of c-Jun in axotomized rubrospinal neurons. Soc Neurosci Abstr 22:1018.
8. Carletti R, Tacconi S, Bettini E, Ferraguti F (1995) Stress activated protein kinases, a novel family of mitogen-activated protein kinases, are heterogeneously expressed in the adult rat brain and differentially distributed from extracellular-signal-regulated protein kinase. Neuroscience 69:1103-1110.
9. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719.
10. Chen YR, Wang X, Templeton D, Davis RJ, Tan TH (1996) The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. J Biol Chem 271:31929-31936.
11. Claret F-X, Hibi M, Dhut S, Toda T, Karin M (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383:453-457.
12. de la Monte SM, Sohn YK, Wands JR (1997) Correlates of p53 and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J Neurol Sci 152:73-83.
13. Deng T, Karin M (1992) Construction and expression of a monomeric c-Jun protein that binds and activates transcription of AP-1-responsive genes. Proc Natl Acad Sci USA 89:8572-8576.
14. Dérijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
15. Devary Y, Gottlieb RA, Smeal T, Karin M (1992) The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71:1081-1091.
16. Eilers A, Whitfield J, Babij C, Rubin LL, Ham J (1998) Role of the Jun kinase pathway in the regulation of c-Jun expression and apoptosis in sympathetic neurons. J Neurosci 18:1713-1724.
17. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM (1994) Altered gene expression in neurons during programmed cell death identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127:1717-1727.
18. Ferrer I, Olive M, Ribera J, Planas AM (1996a) Naturally occurring (programmed) and radiation-induced apoptosis are associated with selective c-jun expression in the developing rat brain. Eur J Neurosci 8:1286-1298.
19. Ferrer I, Segui J, Olive M (1996b) Strong c-Jun immunoreactivity is associated with apoptotic cell death in human tumors of the central nervous system. Neurosci Lett 214:49-52.
20. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
21. Giehl KM, Tetzlaff W (1996) BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corticospinal neurons in vivo. Eur J Neurosci 8:1167-1175.
22. Goillot E, Raingeaud J, Ranger A, Tepper RI, Davis RJ, Harlow E, Sanchez I (1997) Mitogen-activated protein kinase-mediated Fas apoptotic signaling pathway. Proc Natl Acad Sci 94:3302-3307.
23. Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, Dérijard B, Davis R (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15:2760-2770.
24. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL (1995) A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14:927-939.
25. Herdegen T, Leah JD, Manisali A, Bravo R, Zimmermann M (1991) c-Jun-like immunoreactivity in the CNS of the adult rat: basal and transsynaptically induced expression of an immediate early gene. Neuroscience 41:643-654.
26. Herdegen T, Brecht S, Mayer W, Leah JD, Kummer W, Bravo R, Zimmermann M (1993) Long-lasting expression of Jun and Krox transcription factors and nitric oxide synthase in intrinsic neurons of the rat brain following axotomy. J Neurosci 13:4130-4145.
27. Herdegen T, Blume A, Buschmann T, Georgakopoulos E, Winter C, Schmid W, Hsieh TF, Zimmermann M, Gass P (1997a) Expression of ATF-2, SRF and CREB in the adult rat brain following generalized seizures, nerve fiber lesion and UV-irradiation. Neuroscience 81:199-212.
28. Herdegen T, Skene P, Bähr M (1997b) The c-Jun protein-transcriptional mediator of neuronal survival, regeneration and death. Trends Neurosci 20:227-231.
29. Hibi M, Lin A, Smeal T, Minden A, Karin M (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7:2135-2148.
30. Hilberg F, Aguzzi A, Howells N, Wagner EF (1993) c-jun is essential for normal mouse development and hepatogenesis. Nature 365:179-181.
31. Hoeger C, Galyean R, Boublik J, McClintock R, Rivier J (1987) Preparative reversed phase high performance liquid chromatography. II. Effects of buffer pH on the purification of synthetic peptides. Biochromatography 2:134-142.
32. Houlé J, Schramm P, Herdegen T (1997) Changes in the expression of inducible transcription factors with long term spinal cord injury. Soc Neurosci Abstr 23:676.2.
33. Hughes PE, Alexi T, Hefti F, Knusel B (1997) Axotomized septal cholinergic neurons rescued by the nerve growth factor or neurotrophin-4/5 fail to express the inducible transcription factor c-Jun. Neuroscience 78:1037-1049.
34. Kallunki T, Su B, Tsigelny I, Sluss HK, DÉrijard B, Moore G, Davis R, Karin M (1994) JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev 8:2996-3007.
35. Kallunki T, Deng TL, Hibi M, Karin M (1996) c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87:929-939.
36. Kamei Y, Xu L, Heinzel T, Torchia J, Kurokawa R, Gloss B, Lin SC, Heyman RA, Rose DW, Glass CK, Rosenfeld MG (1996) A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85:403-414.
37. Karin M (1995) The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem 270:16483-16486.
38. Karin M, Liu Z, Zandi E (1997) AP-1 function and regulation. Curr Opin Cell Biol 9:240-246.
39. Kasibhatla S, Brunner T, Genestier L, Echeverri F, Mahboubi A, Green DR (1998) DNA damaging agents induce expression of Fas-ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kB and AP-1. Mol Cell 1:543-551.
40. Kenney AM, Kocsis JD (1998) Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and JunD in adult rat dorsal root ganglia in vivo. J Neurosci 18:1318-1328.
41. Kovary K, Bravo R (1991) The Jun and Fos protein families are both required for cell cycle progression in fibroblasts. Mol Cell Biol 11:4466-4472.
42. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad M, Avruch J, Woodgett RJ (1994) The stress-activated protein kinase subfamily of c-Jun kinases, Nature 369:156-160.
43. Leah JD, Herdegen T, Murashov A, Dragunow M, Bravo R (1993) Expression of immediate early gene proteins following axotomy and inhibition of axonal transport in the rat central nervous system. Neuroscience 57:53-66.
44. Liu ZG, Hsu H, Goeddel DV, Karin M (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kB activation prevents cell death. Cell 87:565-576.
45. Martin G, Segui J, Diaz-Villoslada P, Montalban X, Planas AM, Ferrer I (1996) Jun expression is found in neurons located in the vicinity of subacute plaques in patients with multiple sclerosis. Neurosci Lett 212:95-98.
46. Matsuyama T, Hata R, Yamamoto Y, Tagaya M, Akita H, Uno H, Wanaka A, Furuyama J, Sugita M (1995) Localization of the Fas antigen mRNA induced in the postischemic murine forebrain by in situ hybridization. Mol Brain Res 34:166-172.
47. Minden A, Lin A, McMahon M, Lange-Carter C, Dérijard B, Davis RJ, Johnson GL, Karin M (1994a) Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
48. Minden A, Lin A, Smeal T, Dérijard B, Cobb M, Davis R, Karin M (1994b) c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol Cell Biol 14:6683-6688.
49. Mohit AA, Martin JH, Miller CA (1995) p493F12 kinase: a novel MAP kinase expressed in a subset of neurons in the human nervous system. Neuron 14:67-78.
50. Musti AM, Treier M, Bohmann D (1997) Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP-kinases. Science 275:400-402.
51. Nagata S, Goldstein P (1995) The Fas death factor. Science 267:1449-1456.
52. Nagata S (1997) Apoptosis by death factor. Cell 88:355-365.
53. Natoli G, Costanzo A, Ianni A, Templeton DJ, Woodgett JR, Balsano C, Levrero M (1997) Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science 275:200-203.
54. Otvos Jr L, Elekes I, Lee VM (1989) Solid-phase synthesis of phosphopeptides. Int J Pept Protein Res 34:129-133.
55. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, Woodgett JR (1991) Phosphorylation of c-jun mediated by MAP kinases. Nature 353:670-674.
56. Reimold AM, Grusby MJ, Kosaras B, Fries JWU, Mori R, Maniwa S, Clauss IM, Collins T, Sidman RL, Glimcher MJ, Glimcher LH (1996) Chondrodysplasia and neurological abnormalities in ATF-2 deficient mice. Nature 379:262-264.
57. Schaden H, Stürmer CAO, Bähr M (1994) GAP-43 immunoreactivity and axon regeneration in retinal ganglion cells of the rat. J Neurobiol 25:1570-1578.
58. Schlingensiepen KH, Wollnik F, Kunst M, Schlingensiepen R, Herdegen T, Brysch W (1993) The role of Jun transcription factor expression and phosphorylation in neuronal differentiation, neuronal cell death, and plastic adaptations in vivo. Cell Mol Neurobiol 14:487-505.
59. Smeal T, Binetruy B, Mercola DA, Birrer M, Karin M (1991) Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serine-63 and serine-73. Nature 354:494-496.
60. Smeal T, Hibi M, Karin M (1994) Altering the specificity of signal transduction cascades: positive regulation of c-Jun transcriptional activity by protein kinase A. EMBO J 13:6006-6010.
61. Sommer C, Gass P, Kiessling M (1995) Selective c-Jun expression in CA1 neurons of the gerbil hippocampus during and after acquisition of an ischemia-tolerant state. Brain Pathol 5:135-144.
62. Watson A, Eilers A, Lallemand D, Kyriakis J, Rubin LL, Ham J (1998) Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons. J Neurosci 18:751-762.
63. Westwick JK, Bielawska AE, Dbaibo G, Hannun YA, Brenner DA (1995) Ceramide activates the stress-activated protein kinases. J Biol Chem 270:22689-22692.
64. Xia ZG, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of Erk and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
65. Xu X, Raber J, Yang D, Su B, Mucke L (1997) Dynamic regulation of c-Jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 94:12655-12660.
66. Yang D, Kuan C-Y, Whitmarsh AJ, Rincon M, Zheng TS, Davis RJ, Rakic P, Flavell RA (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the JNK3 gene. Nature 289:865-870.
67. Yang X, Koshravi-Far R, Chang H, Baltimore D (1997) Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 27:1067-1076.