MEKK1 controls neurite regrowth after experimental injury by balancing ERK1/2 and JNK2 signaling

Molecular and Cellular Neuroscience

Volumn 30, Issue 1, 2005, Pages 67-78

  Waetzig, Vicki ^a   Herdegen, Thomas ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 1 INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE GROWTH FACTOR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN; CONTROLLED STUDY; NERVE CELL LESION; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; MAP KINASE KINASE 7; MAP KINASE KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 9; NERVE GROWTH FACTOR; NEURITES; PC12 CELLS; RATS; RNA, SMALL INTERFERING;

EID: 23644445386     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2005.06.001     Document Type: Article

References (68)

1. S. Brecht, R. Kirchhof, A. Chromik, M. Willesen, T. Nicolaus, G. Raivich, J. Wessig, V. Waetzig, M. Goetz, M. Claussen, D. Pearse, C.Y. Kuan, E. Vaudano, A. Behrens, E. Wagner, R.A. Flavell, R.J. Davis, and T. Herdegen Specific pathophysiological functions of JNK isoforms in the brain Eur. J. Neurosci. 21 2005 363 377
2. J. Brownlees, A. Yates, N.P. Bajaj, D. Davis, B.H. Anderton, P.N. Leigh, C.E. Shaw, and C.C. Miller Phosphorylation of neurofilament heavy chain side-arms by stress activated protein kinase-1b/Jun N-terminal kinase-3 J. Cell Sci. 113 2000 401 407
3. D.E. Burstein, and L.A. Greene Evidence for RNA synthesis-dependent and -independent pathways in stimulation of neurite outgrowth by nerve growth factor Proc. Natl. Acad. Sci. U. S. A. 75 1978 6059 6063
4. T. Buschmann, A. Martin-Villalba, J.D. Kocsis, S.G. Waxman, M. Zimmermann, and T. Herdegen Expression of Jun, Fos, and ATF-2 proteins in axotomized explanted and cultured adult rat dorsal root ganglia Neuroscience 84 1998 163 176
5. L. Butterfield, E. Zentrich, A. Beekman, and L.E. Heasley Stress- and cell type-dependent regulation of transfected c-Jun N-terminal kinase and mitogen-activated protein kinase kinase isoforms Biochem. J. 338 1999 681 686
6. L. Chang, Y. Jones, M.H. Ellisman, L.S. Goldstein, and M. Karin JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins Dev. Cell 4 2003 521 533
7. E.T. Coffey, V. Hongisto, M. Dickens, R.J. Davis, and M.J. Courtney Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons J. Neurosci. 20 2000 7602 7613
8. E.T. Coffey, G. Smiciene, V. Hongisto, J. Cao, S. Brecht, T. Herdegen, and M.J. Courtney c-Jun N-terminal protein kinase (JNK) 2/3 is specifically activated by stress, mediating c-Jun activation, in the presence of constitutive JNK1 activity in cerebellar neurons J. Neurosci. 22 2002 4335 4345
9. R.J. Davis Signal transduction by the c-Jun N-terminal kinase Biochem. Soc. Symp. 64 1999 1 12
10. X. Deng, L. Xiao, W. Lang, F. Gao, P. Ruvolo, and W.S. May Jr. Novel role for JNK as a stress-activated Bcl2 kinase J. Biol. Chem. 276 2001 23681 23688
11. N. Dietrich, J. Thastrup, C. Holmberg, M. Gyrd-Hansen, N. Fehrenbacher, U. Lademann, M. Lerdrup, T. Herdegen, M. Jaattela, and T. Kallunki JNK2 mediates TNF-induced cell death in mouse embryonic fibroblasts via regulation of both caspase and cathepsin protease pathways Cell Death Differ. 11 2004 301 313
12. E. Douville, and J. Downward EGF induced SOS phosphorylation in PC12 cells involves P90 RSK-2 Oncogene 15 1997 373 383
13. D.T. Dudley, L. Pang, S.J. Decker, A.J. Bridges, and A.R. Saltiel A synthetic inhibitor of the mitogen-activated protein kinase cascade Proc. Natl. Acad. Sci. U. S. A. 92 1995 7686 7689
14. S. Eminel, A. Klettner, L. Roemer, T. Herdegen, and V. Waetzig JNK2 translocates to the mitochondria and mediates cytochrome c release in PC12 cells in response to 6-hydroxydopamine J. Biol. Chem. 279 2004 55385 55392
15. M.F. Favata, K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, W.S. Feeser, D.E. Van Dyk, W.J. Pitts, R.A. Earl, F. Hobbs, R.A. Copeland, R.L. Magolda, P.A. Scherle, and J.M. Trzaskos Identification of a novel inhibitor of mitogen-activated protein kinase kinase J. Biol. Chem. 273 1998 18623 18632
16. F. Galbiati, D. Volonte, O. Gil, G. Zanazzi, J.L. Salzer, M. Sargiacomo, P.E. Scherer, J.A. Engelman, A. Schlegel, M. Parenti, T. Okamoto, and M.P. Lisanti Expression of caveolin-1 and -2 in differentiating PC12 cells and dorsal root ganglion neurons: caveolin-2 is up-regulated in response to cell injury Proc. Natl. Acad. Sci. U. S. A. 95 1998 10257 10262
17. B.I. Giasson, and W.E. Mushynski Study of proline-directed protein kinases involved in phosphorylation of the heavy neurofilament subunit J. Neurosci. 17 1997 9466 9472
18. J.S. Gill, A.E. Schenone, J.L. Podratz, and A.J. Windebank Autocrine regulation of neurite outgrowth from PC12 cells by nerve growth factor Brain Res. Mol. Brain Res. 57 1998 123 131
19. M.A. Glicksman, A.Y. Chiu, C.A. Dionne, M. Harty, M. Kaneko, C. Murakata, R.W. Oppenheim, D. Prevette, D.R. Sengelaub, J.L. Vaught, and N.T. Neff CEP-1347/KT7515 prevents motor neuronal programmed cell death and injury-induced dedifferentiation in vivo J. Neurobiol. 35 1998 361 370
20. L.A. Greene, and A.S. Tischler Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor Proc. Natl. Acad. Sci. U. S. A. 73 1976 2424 2428
21. T. Herdegen, and V. Waetzig The JNK and p38 signal transduction following axotomy Restor. Neurol. Neurosci. 19 2001 29 39
22. T. Herdegen, P. Skene, and M. Bahr The c-Jun transcription factor-bipotential mediator of neuronal death, survival and regeneration Trends Neurosci. 20 1997 227 231
23. T. Herdegen, F.X. Claret, T. Kallunki, A. Martin-Villalba, C. Winter, T. Hunter, and M. Karin Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury J. Neurosci. 18 1998 5124 5135
24. N. Hikawa, Y. Kiuchi, T. Maruyama, and T. Takenaka Delayed neurite regeneration and its improvement by nerve growth factor (NGF) in dorsal root ganglia from MRL-lpr/lpr mice in vitro J. Neurol. Sci. 149 1997 13 17
25. M.K. Jezierski, A.K. Sturm, M.M. Scarborough, and F. Sohrabji NGF stimulation increases JNK2 phosphorylation and reduces caspase-3 activity in the olfactory bulb of estrogen-replaced animals Endocrinology 142 2001 2401
26. M. Karandikar, S. Xu, and M.H. Cobb MEKK1 binds raf-1 and the ERK2 cascade components J. Biol. Chem. 275 2000 40120 40127
27. A.M. Kenney, and J.D. Kocsis 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 1998 1318 1328
28. S. Kiryu, N. Morita, K. Ohno, H. Maeno, and H. Kiyama Regulation of mRNA expression involved in Ras and PKA signal pathways during rat hypoglossal nerve regeneration Brain Res. Mol. Brain Res. 29 1995 147 156
29. Y. Kita, K.D. Kimura, M. Kobayashi, S. Ihara, K. Kaibuchi, S. Kuroda, M. Ui, H. Iba, H. Konishi, U. Kikkawa, S. Nagata, and Y. Fukui Microinjection of activated phosphatidylinositol-3 kinase induces process outgrowth in rat PC12 cells through the Rac-JNK signal transduction pathway J. Cell Sci. 111 1998 907 915
30. T. Kitahara, S. Kiryu, K. Ohno, N. Morita, T. Kubo, and H. Kiyama Up-regulation of ERK (MAP kinase) and MEK (MAP kinase kinase) transcription after rat facial nerve transection Neurosci. Res. 20 1994 275 280
31. M. Kobayashi, S. Nagata, Y. Kita, N. Nakatsu, S. Ihara, K. Kaibuchi, S. Kuroda, M. Ui, H. Iba, H. Konishi, U. Kikkawa, I. Saitoh, and Y. Fukui Expression of a constitutively active phosphatidylinositol 3-kinase induces process formation in rat PC12 cells. Use of Cre/loxP recombination system J. Biol. Chem. 272 1997 16089 16092
32. S. Leppa, R. Saffrich, W. Ansorge, and D. Bohmann Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation EMBO J. 17 1998 4404 4413
33. R.Y. Liu, and W.D. Snider Different signaling pathways mediate regenerative versus developmental sensory axon growth J. Neurosci. 21 2001 RC164
34. C. Lu, M. Shimaoka, A. Salas, and T.A. Springer The binding sites for competitive antagonistic, allosteric antagonistic, and agonistic antibodies to the I domain of integrin LFA-1 J. Immunol. 173 2004 3972 3978
35. N. Maki, P. Hafkemeyer, and S. Dey Allosteric modulation of human P-glycoprotein. Inhibition of transport by preventing substrate translocation and dissociation J. Biol. Chem. 278 2003 18132 18139
36. M. Matsuoka, H. Igisu, K. Nakagawa, T. Katada, and H. Nishina Requirement of MKK4 and MKK7 for CdCl2- or HgCl2-induced activation of c-Jun NH2-terminal kinase in mouse embryonic stem cells Toxicol. Lett. 152 2004 175 181
37. K. Mielke, and T. Herdegen JNK and p38 stresskinases-degenerative effectors of signal-transduction-cascades in the nervous system Prog. Neurobiol. 61 2000 45 60
38. A. Minden, and M. Karin Regulation and function of the JNK subgroup of MAP kinases Biochim. Biophys. Acta 1333 1997 F85 F104
39. T. Miura, S. Tanaka, A. Seichi, M. Arai, T. Goto, H. Katagiri, T. Asano, H. Oda, and K. Nakamura Partial functional recovery of paraplegic rat by adenovirus-mediated gene delivery of constitutively active MEK1 Exp. Neurol. 166 2000 115 126
40. T. Morooka, and E. Nishida Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells J. Biol. Chem. 273 1998 24285 24288
41. A.K. Murashov, I. Ul Haq, C. Hill, E. Park, M. Smith, X. Wang, D.J. Goldberg, and D.J. Wolgemuth Crosstalk between p38, Hsp25 and Akt in spinal motor neurons after sciatic nerve injury Brain Res. Mol. Brain Res. 93 2001 199 208
42. S. Nakahara, K. Yone, T. Sakou, S. Wada, T. Nagamine, T. Niiyama, and H. Ichijo Induction of apoptosis signal regulating kinase 1 (ASK1) after spinal cord injury in rats: possible involvement of ASK1-JNK and -p38 pathways in neuronal apoptosis J. Neuropathol. Exp. Neurol. 58 1999 442 450
43. M.S. Qui, and S.H. Green PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity Neuron 9 1992 705 717
44. G. Raivich, M. Bohatschek, C. Da Costa, O. Iwata, M. Galiano, M. Hristova, A.S. Nateri, M. Makwana, L. Riera-Sans, D.P. Wolfer, H.P. Lipp, A. Aguzzi, E.F. Wagner, and A. Behrens The AP-1 transcription factor c-Jun is required for efficient axonal regeneration Neuron 43 2004 57 67
45. A.J. Reynolds, I.A. Hendry, and S.E. Bartlett Anterograde and retrograde transport of active extracellular signal-related kinase 1 (ERK1) in the ligated rat sciatic nerve Neuroscience 105 2001 761 771
46. C. Rosette, and M. Karin Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors Science 274 1996 1194 1197
47. M.G. Sanna, J. da Silva Correia, Y. Luo, B. Chuang, L.M. Paulson, B. Nguyen, Q.L. Deveraux, and R.J. Ulevitch ILPIP, a novel anti-apoptotic protein that enhances XIAP-mediated activation of JNK1 and protection against apoptosis J. Biol. Chem. 277 2002 30454 30462
48. M.S. Saporito, B.A. Thomas, and R.W. Scott MPTP activates c-Jun NH(2)-terminal kinase (JNK) and its upstream regulatory kinase MKK4 in nigrostriatal neurons in vivo J. Neurochem. 75 2000 1200 1208
49. J.Y. Sheu, D.J. Kulhanek, and F.P. Eckenstein Differential patterns of ERK and STAT3 phosphorylation after sciatic nerve transection in the rat Exp. Neurol. 166 2000 392 402
50. H. Tian, G. Zhang, H. Li, and Q. Zhang Antioxidant NAC and AMPA/KA receptor antagonist DNQX inhibited JNK3 activation following global ischemia in rat hippocampus Neurosci. Res. 46 2003 191 197
51. A.S. Tischler, Y.C. Lee, V.W. Slayton, and S.R. Bloom Kinetics of regulation of neurotensin content in PC12 cells Life Sci. 33 1983 347 351
52. H. Tsuiki, M. Tnani, I. Okamoto, L.C. Kenyon, D.R. Emlet, M. Holgado-Madruga, I.S. Lanham, C.J. Joynes, K.T. Vo, and A.J. Wong Constitutively active forms of c-Jun NH2-terminal kinase are expressed in primary glial tumors Cancer Res. 63 2003 250 255
53. D. Vaudry, P.J. Stork, P. Lazarovici, and L.E. Eiden Signaling pathways for PC12 cell differentiation: making the right connections Science 296 2002 1648 1649
54. N.D. Veeranna Amin, N.G. Ahn, H. Jaffe, C.A. Winters, P. Grant, and H.C. Pant Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M J. Neurosci. 18 1998 4008 4021
55. T. Wada, K. Nakagawa, T. Watanabe, G. Nishitai, J. Seo, H. Kishimoto, D. Kitagawa, T. Sasaki, J.M. Penninger, H. Nishina, and T. Katada Impaired synergistic activation of stress-activated protein kinase SAPK/JNK in mouse embryonic stem cells lacking SEK1/MKK4: different contribution of SEK2/MKK7 isoforms to the synergistic activation J. Biol. Chem. 276 2001 30892 30897
56. V. Waetzig, and T. Herdegen A single c-Jun N-terminal kinase isoform (JNK3-p54) is an effector in both neuronaldifferentiation and cell death J. Biol. Chem. 278 2003 567 572
57. V. Waetzig, and T. Herdegen The concerted signaling of ERK1/2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins Mol. Cell. Neurosci. 24 2003 238 249
58. A.J. Whitmarsh, and R.J. Davis Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways J. Mol. Med. 74 1996 589 607
59. C. Widmann, S. Gibson, M.B. Jarpe, and G.L. Johnson Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human Physiol. Rev. 79 1999 143 180
60. J.A. Witowsky, and G.L. Johnson Ubiquitylation of MEKK1 inhibits its phosphorylation of MKK1 and MKK4 and activation of the ERK1/2 and JNK pathways J. Biol. Chem. 278 2003 1403 1406
61. J. Xiao, and Y. Liu Differential roles of ERK and JNK in early and late stages of neuritogenesis: a study in a novel PC12 model system J. Neurochem. 86 2003 1516 1523
62. S. Xu, and M.H. Cobb MEKK1 binds directly to the c-Jun N-terminal kinases/stress-activated protein kinases J. Biol. Chem. 272 1997 32056 32060
63. D.D. Yang, C.Y. Kuan, A.J. Whitmarsh, M. Rincon, T.S. Zheng, R.J. Davis, P. Rakic, and R.A. Flavell Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene Nature 389 1997 865 870
64. S.H. Yang, A.J. Whitmarsh, R.J. Davis, and A.D. Sharrocks Differential targeting of MAP kinases to the ETS-domain transcription factor Elk-1 EMBO J. 17 1998 1740 1749
65. Y. Yang, E.J. Mufson, and K. Herrup Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease J. Neurosci. 23 2003 2557 2563
66. R. Yao, M. Yoshihara, and H. Osada Specific activation of a c-Jun NH2-terminal kinase isoform and induction of neurite outgrowth in PC-12 cells by staurosporine J. Biol. Chem. 272 1997 18261 18266
67. T. Yujiri, S. Sather, G.R. Fanger, and G.L. Johnson Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption Science 282 1998 1911 1914
68. E. Zentrich, S.Y. Han, L. Pessoa-Brandao, L. Butterfield, and L.E. Heasley Collaboration of JNKs and ERKs in nerve growth factor regulation of the neurofilament light chain promoter in PC12 cells J. Biol. Chem. 277 2002 4110 4118