DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity

Journal of Cell Biology

Volumn 194, Issue 5, 2011, Pages 751-764

  Ghosh, Arundhati Sengupta ^a   Wang, Bei ^a   Pozniak, Christine D ^a   Chen, Mark ^a   Watts, Ryan J ^a   Lewcock, Joseph W ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL LEUCINE ZIPPER KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FLUORESCENCE MICROSCOPY; HOMEOSTASIS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL DEGENERATION; NERVE FIBER DEGENERATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; AXONS; CASPASE 3; CASPASE 9; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; EMBRYO, MAMMALIAN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GANGLIA, SPINAL; HOMEODOMAIN PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE GROWTH FACTOR; NERVE TISSUE PROTEINS; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-JUN; RNA, SMALL INTERFERING; SPINAL CORD; TRANSCRIPTION FACTORS;

MUS;

EID: 80052636605     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201103153     Document Type: Article

References (54)

1. Arber, S., B. Han, M. Mendelsohn, M. Smith, T.M. Jessell, and S. Sockanathan. 1999. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron. 23:659-674.
2. Behrens, A., M. Sibilia, J.P. David, U. Möhle-Steinlein, F. Tronche, G. Schütz, and E.F. Wagner. 2002. Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver. EMBO J. 21:1782-1790.
3. Besirli, C.G., E.F. Wagner, and E.M. Johnson Jr. 2005. The limited role of NH2-terminal c-Jun phosphorylation in neuronal apoptosis: identification of the nuclear pore complex as a potential target of the JNK pathway. J. Cell Biol. 170:401-411.
4. Björkblom, B., N. Ostman, V. Hongisto, V. Komarovski, J.J. Filén, T.A. Nyman, T. Kallunki, M.J. Courtney, and E.T. Coffey. 2005. Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J. Neurosci. 25:6350-6361.
5. Björkblom, B., J.C. Vainio, V. Hongisto, T. Herdegen, M.J. Courtney, and E.T. Coffey. 2008. All JNKs can kill, but nuclear localization is critical for neuronal death. J. Biol. Chem. 283:19704-19713.
6. Bogoyevitch, M.A. 2006. The isoform-specific functions of the c-Jun N-terminal Kinases (JNKs): differences revealed by gene targeting. Bioessays. 28: 923-934.
7. Brandon, E.P., W. Lin, K.A. D'Amour, D.P. Pizzo, B. Dominguez, Y. Sugiura, S. Thode, C.P. Ko, L.J. Thal, F.H. Gage, and K.F. Lee. 2003. Aberrant patterning of neuromuscular synapses in choline acetyltransferasedeficient mice. J. Neurosci. 23:539-549.
8. Campenot, R.B. 1977. Local control of neurite development by nerve growth factor. Proc. Natl. Acad. Sci. USA. 74:4516-4519.
9. Cavalli, V., P. Kujala, J. Klumperman, and L.S. Goldstein. 2005. Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 168:775-787.
10. Chang, L., Y. Jones, M.H. Ellisman, L.S. Goldstein, and M. Karin. 2003. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell. 4:521-533.
11. Coffey, E.T., V. Hongisto, M. Dickens, R.J. Davis, and M.J. Courtney. 2000. Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J. Neurosci. 20:7602-7613.
12. Collins, C.A., Y.P. Wairkar, S.L. Johnson, and A. DiAntonio. 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron. 51:57-69.
13. Crowley, C., S.D. Spencer, M.C. Nishimura, K.S. Chen, S. Pitts-Meek, M.P. Armanini, L.H. Ling, S.B. McMahon, D.L. Shelton, A.D. Levinson, et al. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 76:1001-1011.
14. Deckwerth, T.L., J.L. Elliott, C.M. Knudson, E.M. Johnson Jr., W.D. Snider, and S.J. Korsmeyer. 1996. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron. 17:401-411.
15. Donovan, N., E.B. Becker, Y. Konishi, and A. Bonni. 2002. JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery. J. Biol. Chem. 277:40944-40949.
16. Garcia, I., I. Martinou, Y. Tsujimoto, and J.C. Martinou. 1992. Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science. 258:302-304.
17. Gdalyahu, A., I. Ghosh, T. Levy, T. Sapir, S. Sapoznik, Y. Fishler, D. Azoulai, and O. Reiner. 2004. DCX, a new mediator of the JNK pathway. EMBO J. 23:823-832.
18. Goedert, M., M. Hasegawa, R. Jakes, S. Lawler, A. Cuenda, and P. Cohen. 1997. Phosphorylation of microtubule-associated protein tau by stress-activated protein kinases. FEBS Lett. 409:57-62.
19. Gorin, P.D., and E.M. Johnson. 1979. Experimental autoimmune model of nerve growth factor deprivation: effects on developing peripheral sympathetic and sensory neurons. Proc. Natl. Acad. Sci. USA. 76:5382-5386.
20. Gupta, S., T. Barrett, A.J. Whitmarsh, J. Cavanagh, H.K. Sluss, B. Dérijard, and R.J. Davis. 1996. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15:2760-2770.
21. Ham, J., C. Babij, J. Whitfield, C.M. Pfarr, D. Lallemand, M. Yaniv, and L.L. Rubin. 1995. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron. 14:927-939.
22. Hammarlund, M., P. Nix, L. Hauth, E.M. Jorgensen, and M. Bastiani. 2009. Axon regeneration requires a conserved MAP kinase pathway. Science. 323:802-806.
23. Hirai, S., A. Kawaguchi, J. Suenaga, M. Ono, D.F. Cui, and S. Ohno. 2005. Expression of MUK/DLK/ZPK, an activator of the JNK pathway, in the nervous systems of the developing mouse embryo. Gene Expr. Patterns. 5:517-523.
24. Hirai, S., F. Cui, T. Miyata, M. Ogawa, H. Kiyonari, Y. Suda, S. Aizawa, Y. Banba, and S. Ohno. 2006. The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J. Neurosci. 26:11992-12002.
25. Hunot, S., M. Vila, P. Teismann, R.J. Davis, E.C. Hirsch, S. Przedborski, P. Rakic, and R.A. Flavell. 2004. JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. USA. 101:665-670.
26. Ito, M., K. Yoshioka, M. Akechi, S. Yamashita, N. Takamatsu, K. Sugiyama, M. Hibi, Y. Nakabeppu, T. Shiba, and K.I. Yamamoto. 1999. JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway. Mol. Cell. Biol. 19:7539-7548.
27. Itoh, A., M. Horiuchi, K. Wakayama, J. Xu, P. Bannerman, D. Pleasure, and T. Itoh. 2011. ZPK/DLK, a mitogen-activated protein kinase kinase kinase, is a critical mediator of programmed cell death of motoneurons. J. Neurosci. 31:7223-7228.
28. Lee, S.K., L.W. Jurata, J. Funahashi, E.C. Ruiz, and S.L. Pfaff. 2004. Analysis of embryonic motoneuron gene regulation: derepression of general activators function in concert with enhancer factors. Development. 131:3295-3306.
29. Levi-Montalcini, R., and B. Booker. 1960. Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein. Proc. Natl. Acad. Sci. USA. 46:384-391.
30. Lewcock, J.W., N. Genoud, K. Lettieri, and S.L. Pfaff. 2007. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron. 56:604-620.
31. Luo, L., and D.D. O'Leary. 2005. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28:127-156.
32. Mack, T.G., M. Reiner, B. Beirowski, W. Mi, M. Emanuelli, D. Wagner, D. Thomson, T. Gillingwater, F. Court, L. Conforti, et al. 2001. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4:1199-1206.
33. Maroney, A.C., M.A. Glicksman, A.N. Basma, K.M. Walton, E. Knight Jr., C.A. Murphy, B.A. Bartlett, J.P. Finn, T. Angeles, Y. Matsuda, et al. 1998. Motoneuron apoptosis is blocked by CEP-1347 (KT 7515), a novel inhibitor of the JNK signaling pathway. J. Neurosci. 18:104-111.
34. Middlemas, A., J.D. Delcroix, N.M. Sayers, D.R. Tomlinson, and P. Fernyhough. 2003. Enhanced activation of axonally transported stress-activated protein kinases in peripheral nerve in diabetic neuropathy is prevented by neurotrophin-3. Brain. 126:1671-1682.
35. Miller, B.R., C. Press, R.W. Daniels, Y. Sasaki, J. Milbrandt, and A. DiAntonio. 2009. A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat. Neurosci. 12:387-389.
36. Mok, S.A., K. Lund, and R.B. Campenot. 2009. A retrograde apoptotic signal originating in NGF-deprived distal axons of rat sympathetic neurons in compartmented cultures. Cell Res. 19:546-560.
37. Nakata, K., B. Abrams, B. Grill, A. Goncharov, X. Huang, A.D. Chisholm, and Y. Jin. 2005. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell. 120:407-420.
38. Nikolaev, A., T. McLaughlin, D.D. O'Leary, and M. Tessier-Lavigne. 2009. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature. 457:981-989.
39. Oppenheim, R.W. 1991. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:453-501.
40. Palmada, M., S. Kanwal, N.J. Rutkoski, C. Gustafson-Brown, R.S. Johnson, R. Wisdom, and B.D. Carter. 2002. c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J. Cell Biol. 158:453-461.
41. Putcha, G.V., S. Le, S. Frank, C.G. Besirli, K. Clark, B. Chu, S. Alix, R.J. Youle, A. LaMarche, A.C. Maroney, and E.M. Johnson Jr. 2003. JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron. 38:899-914.
42. Schoenmann, Z., E. Assa-Kunik, S. Tiomny, A. Minis, L. Haklai-Topper, E. Arama, and A. Yaron. 2010. Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J. Neurosci. 30:6375-6386.
43. Tararuk, T., N. Ostman, W. Li, B. Björkblom, A. Padzik, J. Zdrojewska, V. Hongisto, T. Herdegen, W. Konopka, M.J. Courtney, and E.T. Coffey. 2006. JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J. Cell Biol. 173:265-277.
44. Vohra, B.P., Y. Sasaki, B.R. Miller, J. Chang, A. DiAntonio, and J. Milbrandt. 2010. Amyloid precursor protein cleavage-dependent and -independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J. Neurosci. 30:13729-13738.
45. Waetzig, V., and T. Herdegen. 2005. Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol. Sci. 26:455-461.
46. Watts, R.J., E.D. Hoopfer, and L. Luo. 2003. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron. 38:871-885.
47. White, F.A., I. Silos-Santiago, D.C. Molliver, M. Nishimura, H. Phillips, M. Barbacid, and W.D. Snider. 1996. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J. Neurosci. 16:4662-4672.
48. White, F.A., C.R. Keller-Peck, C.M. Knudson, S.J. Korsmeyer, and W.D. Snider. 1998. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18:1428-1439.
49. Whitfield, J., S.J. Neame, L. Paquet, O. Bernard, and J. Ham. 2001. Dominantnegative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron. 29:629-643.
50. Whitmarsh, A.J. 2006. The JIP family of MAPK scaffold proteins. Biochem. Soc. Trans. 34:828-832.
51. Widmann, C., S. Gibson, M.B. Jarpe, and G.L. Johnson. 1999. Mitogenactivated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79:143-180.
52. Xiong, X., X. Wang, R. Ewanek, P. Bhat, A. Diantonio, and C.A. Collins. 2010. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 191:211-223.
53. Xu, Z., A.C. Maroney, P. Dobrzanski, N.V. Kukekov, and L.A. Greene. 2001. The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol. Cell. Biol. 21:4713-4724.
54. Yang, D.D., C.Y. Kuan, A.J. Whitmarsh, M. Rincón, T.S. Zheng, R.J. Davis, P. Rakic, and R.A. Flavell. 1997. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature. 389:865-870.