Divergent effects of the MEKK-1/JNK pathway on NB2a/d1 differentiation: Some activity is required for outgrowth and stabilization of neurites but overactivation inhibits both phenomena

Brain Research

Volumn 1123, Issue 1, 2006, Pages 20-26

  DeFuria, Jason ^a   Chen, Po ^a   Shea, Thomas B ^a  

^a UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

Axonal transport; JNK; MEKK 1; Mitogen activated protein kinase; Neuritogenesis; Neurofilament; Phosphorylation; Stress activated protein kinase

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; NERVE CELL; NERVE FIBER GROWTH; NEUROFILAMENT; PERIKARYON; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASE 1; MICE; NEURITES; NEUROBLASTOMA; NEUROFIBRILS; NEURONS; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 33751164429     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.09.036     Document Type: Article

References (63)

1. Abe K., Aoyagi A., and Saito H. Sustained phosphorylation of mitogen-activated protein kinase is required for basic fibroblast growth factor-mediated axonal branch formation in cultured rat hippocampal neurons. Neurochem. Int. 38 (2001) 309-315
2. Ackerley S., Grierson A.J., Banner S., Perkinton M.S., Brownlees J., Byers H.L., Ward M., Thornhill P., Hussain K., Waby J.S., Anderton B.H., Cooper J.D., Dingwall C., Leigh P.N., Shaw C.E., and Miller C.C. p38alpha stress-activated protein kinase phosphorylates neurofilaments and is associated with neurofilament pathology in amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 26 (2005) 354-364
3. Anderton B.H., Breinburg D., Downes M.J., Green P.J., Tomlinson B.E., Ulrich J., Wood J.N., and Kahn J. Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants. Nature 298 (1982) 84-86
4. Bennette B.L., and Goss G.C. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. 98 (2001) 13681
5. Bogoyevitch M.A., Boehm I., Oakley A., Ketterman A.J., and Barr R.K. Targeting the JNK MAPK cascade for inhibition: basic science and therapeutic potential. Biochim. Biophys. Acta 1697 (2004) 89-101
6. Brecht S., Kirchhof R., Chromik A., Willesen M., Nicolaus T., Raivich G., Wessig J., Waetzig V., Goetz M., Claussen M., Pearse D., Kuan C.Y., Vaudano E., Behrens A., Wagner E., Flavell R.A., Davis R.J., and Herdegen T. Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. (2005) 363-377
7. Cano E., and Mahadevan L.C. Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci. 20 (1995) 117-122
8. Chan W.K.-C., Dickerson A., Otriz D., Pimenta A., Moran C., Malik K., Motil J., Snyder S., Pant H.C., and Shea T.B. Mitogen activated protein kinase regulates neurofilament axonal transport. J. Cell. Sci. 117 (2004) 4629-4642
9. Cobb M.H. MAP kinase pathways. Prog. Biophys. Mol. Biol. 71 (1999) 479-500
10. Cuenda A., Rouse J., Doza Y.N., Meier R., Cohen P., Gallagher T.F., Young P.R., and Lee J.C. SB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364 (1995) 229-233
11. D'Ambrosio C., Arena S., Fulcoli G., Scheinfeld M.H., Zhou D., D'Adamio L., and Scaloni A. Hyperphosphorylation of proteins associated with Alzheimer's disease: the case of JNK-interacting protein 1. Mol. Cell. Proteomics (2005) (Electronic publication ahead of print)
12. Eom D.S., Choi W.S., and Oh Y.J. Bcl-2 enhances neurite extension via activation of c-Jun N-terminal kinase. Biochem. Biophys. Res. Commun. 314 (2004) 377-381
13. Eom D.S., Choi W.S., Ji S., Cho J.W., and Oh Y.J. Activation of c-Jun N-terminal kinase is required for neurite outgrowth of dopaminergic neuronal cells. NeuroReport 16 (2005) 823-828
14. Filomeni G., Aquilano K., Civitareale P., Rotilio G., and Ciriolo M.R. Activation of c-Jun-N-terminal kinase is required for apoptosis triggered by glutathione disulfide in neuroblastoma cells. Free Radical Biol. Med. 39 (2005) 345-354
15. Gelderblom M., Eminel S., Herdegen T., and Waetzig V. c-Jun N-terminal kinases (JNKs) and the cytoskeleton-Functions beyond neurodegeneration. Int. J. Dev. Neurosci. 22 (2004) 559-564
16. Giasson B.I., and Mushynski W.E. Aberrant stress-induced phosphorylation of perikaryal neurofilaments. J. Biol. Chem. 271 (1996) 30404-30409
17. Giasson B.I., and Mushynski W.E. Study of proline-directed protein kinases involved in phosphorylation of the heavy neurofilament subunit. J. Neurosci. 17 (1997) 9466-9472
18. Guo Q. When good Cdk5 turns bad. Sci. Aging Knowledge Environ. 5 (2006) (Feb. 8)
19. Hargreaves A.J., Fowler M.J., Sachana M., Flaskos J., Bountouri M., Coutts I.C., Glynn P., Harris W., and Graham McLean W. Inhibition of neurite outgrowth in differentiating mouse N2a neuroblastoma cells by phenyl saligenin phosphate: effects on MAP kinase (ERK 1/2) activation, neurofilament heavy chain phosphorylation and neuropathy target esterase activity. Biochem. Pharmacol. 71 (2006) 1240-1247
20. Harper S.J., and LoGrasso P. Signalling for survival and death in neurones: the role of stress-activated kinases, JNK and p38. Cell. Signal. 13 (2001) 299-310
21. Holasek S.S., Wengenack T.M., Kandimalla K.K., Montano C., Gregor D.M., Curran G.L., and Poduslo J.F. Activation of the stress-activated MAP kinase, p38, but not JNK in cortical motor neurons during early presymptomatic stages of amyotrophic lateral sclerosis in transgenic mice. Brain Res. 1045 (2005) 185-198
22. Johnson G.L., and Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298 (2002) 1911-1912
23. Julien J.P., and Mushynski W.E. Neurofilaments in health and disease. Prog. Nucleic Acid Res. Mol. Biol. 61 (1998) 1-23
24. Jung C., Yabe J., Wang F.-S., and Shea T.B. Neurofilaments are present within axonal neurites before incorporation into Triton-insoluble structures. Cell Motil. Cytoskelet. 40 (1998) 44-58
25. Kawauchi T., Chihama K., Nabeshima Y., and Hoshino M. The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J. (2003) 4190-4201
26. Kawauchi T., Chihama K., Nishimura Y.V., Nabeshima Y., and Hoshino M. MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem. Biophys. Res. Commun. 331 (2005) 50-55
27. Kholodenko B.N. MAP kinase cascade signaling and endocytic trafficking: a marriage of convenience?. Trends Cell Biol. 12 (2002) 173-177
28. Kim H.S., Yumkham S., Kim S.H., Yea K., Shin Y.C., Ryu S.H., and Suh P.G. Secretin induces neurite outgrowth of PC12 through cAMP-mitogen-activated protein kinase pathway. Exp. Mol. Med. 38 (2006) 85-93
29. Kyriakis J.M., and Avruch J. Protein kinase cascades activated by stress and inflammatory cytokines. BioEssays 18 (1996) 567-577
30. Masaki R., Saito T., Yamada K., and Ohtani-Kaneko R. Accumulation of phosphorylated neurofilaments and increase in apoptosis-specific protein and phosphorylated c-Jun induced by proteasome inhibitors. J. Neurosci. Res.. 62 (2001) 75-83
31. Mielke K., Damm A., Yang D.D., and Herdegen T. Selective expression of JNK isoforms and stress-specific JNK activity in different neural cell lines. Mol. Brain Res. 75 (2000) 128-137
32. Miller C.C.J., Ackerley S., Brownlees J., Grierson A.J., Jacobsen N.J.O., and Thornhill P. Axonal transport of neurofilaments in normal and disease states. Cell. Mol. Life Sci. 59 (2002) 323-330
33. Moran C.M., Donnelly M., Daniela Ortiz D., Pant H.C., Mandelkow E.-M.P., and Shea T.B. Cdk5 inhibits anterograde axonal transport of neuorfilaments but not that of tau by inhibition of mitogen activated protein kinase activity. Mol. Brain Res. 134 (2005) 338-344
34. Obara Y., Aoki T., Kusano M., and Ohizumi Y. Beta-eudesmol induces neurite outgrowth in rat pheochromocytoma cells accompanied by an activation of mitogen-activated protein kinase. J. Pharmacol. Exp. Ther. 3 (2002) 803-811
35. Pant H.C., and Veeranna. Neurofilament phosphorylation. Biochem. Cell. Biol. 73 (1995) 575-592
36. Park K.S., Lee R.D., Kang S.K., Han S.Y., Park K.L., Yang K.H., Song Y.S., Park H.J., Lee Y.M., Yun Y.P., Oh K.W., Kim D.J., Yun Y.W., Hwang S.J., Lee S.E., and Hong J.T. Neuronal differentiation of embryonic midbrain cells by upregulation of peroxisome proliferator-activated receptor-gamma via the JNK-dependent pathway. Exp. Cell Res. 297 (2004) 424-433
37. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., and Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22 (2001) 153-183
38. Price S.A., Hounsom L., Purves-Tyson T.D., Fernyhough P., and Tomlinson D.R. Activation of JNK in sensory neurons protects against sensory neuron cell death in diabetes and on exposure to glucose/oxidative stress in vitro. Ann. N. Y. Acad. Sci. 1010 (2003) 95-99
39. Raingeaud J., Gupta S., Rogers J.S., Dickens M., Han J., Ulevitch R.J., and Davis R.J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270 (1995) 7420-7426
40. Rosso S.B., Sussman D., Wynshaw-Boris A., and Salinas P.C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 8 (2005) 34-42
41. Sang C., Kobayashi Y., Du J., Katsumo M., Adachi H., Doyu M., and Sobue G. c-Jun N-terminal kinase pathway mediates Lactacystin-induced cell death in a neuronal differentiated Neuro2a cell line. Mol. Brain Res. 20108 (2002) 7-17
42. Sasaki T., Gotow T., Shiozaki M., Sakaue F., Saito T., Julien J.P., Uchiyama Y., and Hisanaga S. Aggregate formation and phosphorylation of neurofilament-L Pro22 Charcot-Marie-Tooth disease mutants. Hum. Mol. Genet. 15 (2006) 943-952
43. Shea T.B., and Beermann M.L. Respective roles of neurofilaments, microtubules, MAP1B and tau in the outgrowth and stabilization of axonal neurites. Mol. Biol. Cell 5 (1994) 863-875
44. Shea T.B., Yabe J.T., Ortiz D., Pimenta A., Loomis P., Goldman R.D., Amin N., and Pant H.C. CDK5 regulates axonal transport and phosphorylation of neurofilaments in cultured neurons. J. Cell. Sci. 117 (2004) 933-941
45. Shin M., and Boyd D. An inhibitor of c-Jun aminoterminal kinase (SP600125) repressed c-Jun activation, DNA-binding and PMA-inducible 92-kDa type IV collagenase expression. Biochim. Biophys. Acta 589 (2002) 311-316
46. Tararuk T., Ostman N., Li W., Bjorkblom B., Padzik A., Zdrojewska J., Hongisto V., Herdegen T., Konopka W., Courtney M.J., and Coffey E.T. JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J. Cell Biol. 173 2 (2006) 265-277 (Apr 24)
47. Vaillant A.R., Zanassi P., Walsh G.S., Aumont A., Alonso A., and Miller F.D. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 34 (2002) 985-998
48. van der Heide L.P., Hoekman M.F., Biessels G.J., and Gispen W.H. Insulin inhibits extracellular regulated kinase 1/2 phosphorylation in a phosphatidylinositol 3-kinase (PI3) kinase-dependent manner in Neuro2a cells. J. Neurochem. 86 (2003) 86-91
49. Waetzig V., and Herdegen T. 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
50. Waetzig V., and Herdegen T. Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol. Sci. 26 (2005) 455-461
51. Waetzig V., and Herdegen T. MEKK1 controls neurite regrowth after experimental injury by balancing ERK1/2 and JNK2 signaling. Mol. Cell. Neurosci. 30 (2005) 67-78
52. Xiao J., and Liu Y. 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
53. Xiao J., Zhou Q., and Liu Y. Variant PC12 cell line that spontaneously differentiates and extends neuritic processes. J. Neurosci. Res.. 69 (2002) 104-109
54. Xiao J., Pradhan A., and Liu Y. Functional role of JNK in neuritogenesis of PC12-N1 cells. Neurosci. Lett. (2005) Oct 6; [Electronic publication ahead of print]
55. Xu Z., Kukekov N.V., and Greene L.A. Regulation of apoptotic c-Jun N-terminal kinase signaling by a stabilization-based feed-forward loop. Mol. Cell. Biol. 25 (2005) 9949-9959
56. Yabe J.T., Pimenta A.F., and Shea T.B. Kinesin mediates axonal transport of non-filamentous neurofilament oligomers. J. Cell. Sci. 112 (1999) 3799-3814
57. Yabe J.T., Chylinski T.M., Wang F.-S., Pimenta A.F., Kattar S.D., Linsley M.-D., Chan W.K.-H., and Shea T.B. Neurofilaments consist of distinct populations that can be distinguished by C-terminal phosphorylation, bundling and axonal transport rate in growing axonal neurites. J. Neurosci. 21 (2001) 2195-2205
58. Yoon S., Choi J., Yoon J., Huh J.W., and Kim D. Okadaic acid induces JNK activation, bim overexpression and mitochondrial dysfunction in cultured rat cortical neurons. Neurosci. Lett. (2005) Oct 28; [Electronic publication ahead of print]
59. Yu Y.M., Han P.L., and Lee J.K. JNK pathway is required for retinoic acid-induced neurite outgrowth of human neuroblastoma, SH-SY5Y. NeuroReport 14 (2003) 941-945
60. Yujiri T., and Joghson G.L. Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by the targeted gene disruption. Science 282 (1998) 1911-1914
61. Yujiri T., and Joghson G.L. Biophys. Acta 1589 3 (1998) 311-316
62. Zentrich E., Han S.Y., Pessoa-Brandao L., Butterfield L., and Heasley L.E. 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
63. Zhang L., and Xia Y. MEK kinase1 regulates c-Jun phosphorylation in the control of corneal morphogenesis. Mol. Vis. 9 (2003) 584-593