ZPK/DLK and MKK4 form the critical gateway to axotomy-induced motoneuron death in neonates

Journal of Neuroscience

Volumn 34, Issue 32, 2014, Pages 10729-10742

  Itoh, Takayuki ^a,b   Horiuchi, Makoto ^a,b   Ikeda Jr , Raymond H ^b   Xu, Jie ^b   Bannerman, Peter ^a,b   Pleasure, David ^a,b   Penninger, Josef M ^c   Tournier, Cathy ^d   Itoh, Aki ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

^c INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Injury response; Mitogen activated protein kinase; Programmed cell death

Indexed keywords

INJURY RESPONSE; MITOGEN-ACTIVATED PROTEIN KINASE; PROGRAMMED CELL DEATH;

ANIMALS; ANIMALS, NEWBORN; AXOTOMY; CALCIUM-BINDING PROTEINS; CELL DEATH; CENTRAL NERVOUS SYSTEM; CHOLINE O-ACETYLTRANSFERASE; DEXTRANS; DISEASE MODELS, ANIMAL; FACIAL NERVE INJURIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MAP KINASE KINASE 4; MAP KINASE KINASE KINASES; MICE; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; NESTIN; PHOSPHOPYRUVATE HYDRATASE; PROTO-ONCOGENE PROTEINS C-JUN; RHODAMINES; SIGNAL TRANSDUCTION;

EID: 84905693915     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0539-14.2014     Document Type: Article

References (63)

1. Abe N, Cavalli V (2008) Nerve injury signaling. Curr Opin Neurobiol 18: 276-283. CrossRef Medline
2. Arber S., Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S (1999) Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23:659-674. CrossRef Medline
3. Ashwell K. W, Watson CR (1983) The development of facial motoneurones in the mouse-neuronal death and the innervation of the facial muscles. J Embryol Exp Morphol 77:117-141. Medline
4. Bloom A. J, Miller BR, Sanes JR, DiAntonio A (2007) The requirement for Phr1 in CNS axon tract formation reveals the corticostriatal boundary as a choice point for cortical axons. Genes Dev 21:2593-2606. CrossRef Medline
5. Brancho D., Tanaka N, Jaeschke A, Ventura JJ, Kelkar N, Tanaka Y, Kyuuma M, Takeshita T, Flavell RA, Davis RJ (2003) Mechanism of p38 MAP kinase activation in vivo. Genes Dev 17:1969-1978. CrossRef Medline
6. Buss R. R, Sun W, Oppenheim RW (2006) Adaptive roles of programmedcell death during nervous system development. Annu Rev Neurosci 29:1-35. CrossRef Medline
7. Casanovas A., Ribera J, Hager G, Kreutzberg GW, Esquerda JE (2001) c-Jun regulation in rat neonatal motoneurons postaxotomy. J Neurosci Res 63:469-479. CrossRef Medline
8. Chandrasekhar A. (2004) Turning heads: development of vertebrate branchiomotor neurons. Dev Dyn 229:143-161. CrossRef Medline
9. Clarke P. G, Oppenheim RW (1995) Neuron death in vertebrate development: in vitro methods. Methods Cell Biol 46:277-321. CrossRef Medline
10. Coffey E. T, Hongisto V, Dickens M, Davis RJ, Courtney MJ (2000) Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci 20:7602-7613. Medline
11. Dekkers J., Bayley P, Dick JR, Schwaller B, Berchtold MW, Greensmith L (2004) Over-expression of parvalbumin in transgenic mice rescues motoneurons from injury-induced cell death. Neuroscience 123:459-466. CrossRef Medline
12. Dubois-Dauphin M., Frankowski H, Tsujimoto Y, Huarte J, Martinou JC (1994) Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc Natl Acad Sci U S A 91:3309-3313. CrossRef Medline
13. Ericson J., Thor S, Edlund T, Jessell TM, Yamada T (1992) Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256:1555-1560. CrossRef Medline
14. Ganiatsas S., Kwee L, Fujiwara Y, Perkins A, Ikeda T, Labow MA, Zon LI (1998) SEK1 deficiency reveals mitogen-activated protein kinase cascade crossregulation and leads to abnormal hepatogenesis. Proc Natl Acad Sci U S A 95:6881-6886. CrossRef Medline
15. Ghosh A. S, Wang B, Pozniak CD, Chen M, Watts RJ, Lewcock JW (2011) DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J Cell Biol 194:751-764. CrossRef Medline
16. Ghosh-Roy A., Wu Z, Goncharov A, Jin Y, Chisholm AD (2010) Calcium and cyclic AMP promote axonal regeneration inCaenorhabditis elegans and require DLK-1 kinase. J Neurosci 30:3175-3183. CrossRef Medline
17. Gould T. W, Oppenheim RW (2011) Motor neuron trophic factors: therapeutic use in ALS? Brain Res Rev 67:1-39. CrossRef Medline
18. Haase G., Pettmann B, Raoul C, Henderson CE (2008) Signaling by death receptors in the nervous system. Curr Opin Neurobiol 18:284-291. CrossRef Medline
19. Hafezparast M., Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S., Lalli G, Witherden AS, Hummerich H, Nicholson S, Morgan PJ, Oozageer R., Priestley JV, Averill S, King VR, Ball S, Peters J, Toda T, Yamamoto A., Hiraoka Y, et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812. CrossRef Medline
20. Hirai S. i, Katoh M, Terada M, Kyriakis JM, Zon LI, Rana A, Avruch J, Ohno S (1997) MST/MLK2, a member of the mixed lineage kinase family, directly phosphorylates and activates SEK1, an activator of c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 272: 15167-15173. CrossRef Medline
21. Hirai S., Kawaguchi A, Hirasawa R, Baba M, Ohnishi T, Ohno S (2002) MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo. Development 129: 4483-4495. Medline
22. Horiuchi M., Itoh A, Pleasure D, Itoh T (2006) MEK-ERK signaling is involved in interferon-gamma-induced death of oligodendroglial progenitor cells. J Biol Chem 281:20095-20106. CrossRef Medline
23. Huntwork-Rodriguez S., Wang B, Watkins T, Ghosh AS, Pozniak CD, Bustos D, Newton K, Kirkpatrick DS, Lewcock JW (2013) JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J Cell Biol 202:747-763. CrossRef Medline
24. Ito M., Yoshioka K, Akechi M, Yamashita S, Takamatsu N, Sugiyama K, Hibi M, Nakabeppu Y, Shiba T, Yamamoto KI (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. Medline
25. Itoh A., Horiuchi M, Bannerman P, Pleasure D, Itoh T (2009) Impaired regenerative response of primary sensory neurons in ZPK/DLK gene-trap mice. Biochem Biophys Res Commun 383:258-262. CrossRef Medline
26. Itoh A., Horiuchi M, Wakayama K, Xu J, Bannerman P, Pleasure D, Itoh T (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. CrossRef Medline
27. Iwasaki Y., Ikeda K, Shiojima T, Kinoshita M (1995) CNQX prevents spinal motor neuron death following sciatic nerve transection in newborn rats. J Neurol Sci 134:21-25. CrossRef Medline
28. Kanungo A. K, Hao Z, Elia AJ, Mak TW, Henderson JT (2008) Inhibition of apoptosome activation protects injured motor neurons from cell death. J Biol Chem 283:22105-22112. CrossRef Medline
29. Keramaris E., Vanderluit JL, Bahadori M, Mousavi K, Davis RJ, Flavell R, Slack RS, Park DS (2005) c-Jun N-terminal kinase 3 deficiency protects neurons from axotomy-induced death in vivo through mechanisms independent of c-Jun phosphorylation. J Biol Chem 280:1132-1141. CrossRef Medline
30. Kishimoto H., Nakagawa K, Watanabe T, Kitagawa D, Momose H, Seo J, Nishitai G., Shimizu N, Ohata S, Tanemura S, Asaka S, Goto T, Fukushi H, Yoshida H., Suzuki A, Sasaki T, Wada T, Penninger JM, Nishina H, Katada T (2003) Different properties of SEK1 and MKK7 in dual phosphorylation of stress-induced activated protein kinase SAPK/JNK in embryonic stem cells. J Biol Chem 278:16595-16601. CrossRef Medline
31. Koliatsos V. E, Price WL, Pardo CA, Price DL (1994) Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol 342:35-44. CrossRef Medline
32. Lawson S. J, Lowrie MB (1998) The role of apoptosis and excitotoxicity in the death of spinal motoneurons and interneurons after neonatal nerve injury. Neuroscience 87:337-348. CrossRef Medline
33. Li L., Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ (1995) Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci U S A 92:9771-9775. CrossRef Medline
34. Lowrie M. B, Vrbová G (1992) Dependence of postnatal motoneurones on their targets: review and hypothesis. Trends Neurosci 15:80-84. CrossRef Medline
35. Merritt S. E, Mata M, Nihalani D, Zhu C, Hu X, Holzman LB (1999) The mixed lineage kinase DLK utilizes MKK7 and not MKK4 as substrate. J Biol Chem 274:10195-10202. CrossRef Medline
36. Miller B. R, Press C, Daniels RW, Sasaki Y, Milbrandt J, DiAntonio A (2009) A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat Neurosci 12:387-389. CrossRef Medline
37. Mooney L. M, Whitmarsh AJ (2004) Docking interactions in the c-Jun N-terminal kinase pathway. J Biol Chem 279:11843-11852. CrossRef Medline
38. Moran L. B, Graeber MB (2004) The facial nerve axotomy model. Brain Res Brain Res Rev 44:154-178. CrossRef Medline
39. Nihalani D., Meyer D, Pajni S, Holzman LB (2001) Mixed lineage kinasedependent JNK activation is governed by interactions of scaffold protein JIP with MAPK module components. EMBO J 20:3447-3458. CrossRef Medline
40. Olsson T., Kristensson K (1979) Uptake and retrograde axonal transport of horseradish peroxidase in normal and axotomized motor neurons during postnatal development. Neuropathol Appl Neurobiol 5:377-387. CrossRef Medline
41. Osterloh J. M, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, Sheehan AE, Avery MA, Hackett R, Logan MA, MacDonald JM, Ziegenfuss JS, Milde S., Hou YJ, Nathan C, Ding A, Brown RH Jr, Conforti L, Coleman M, Tessier-Lavigne M, et al. (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337:481-484. CrossRef Medline
42. Pozniak C. D, Sengupta Ghosh A, Gogineni A, Hanson JE, Lee SH, Larson JL, Solanoy H., Bustos D, Li H, Ngu H, Jubb AM, Ayalon G, Wu J, Scearce-Levie K, Zhou Q, Weimer RM, Kirkpatrick DS, Lewcock JW (2013) Dual leucine zipper kinase is required for excitotoxicity-induced neuronal degeneration. J Exp Med 210:2553-2567. CrossRef Medline
43. Raivich G., Bohatschek M, Da Costa C, Iwata O, Galiano M, Hristova M, Nateri A. S, Makwana M, Riera-Sans L, Wolfer DP, Lipp HP, Aguzzi A, Wagner E. F, Behrens A (2004) The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43:57-67. CrossRef Medline
44. Ribera J., Ayala V, Casas C (2007) Involvement of c-Jun-JNK pathways in the regulation of programmed cell death of developing chick embryo spinal cord motoneurons. Dev Neurosci 29:438-451. CrossRef Medline
45. Ruff C. A, Staak N, Patodia S, Kaswich M, Rocha-Ferreira E, Da Costa C, Brecht S., Makwana M, Fontana X, Hristova M, Rumajogee P, Galiano M, Bohatschek M., Herdegen T, Behrens A, Raivich G (2012) Neuronal c-Jun is required for successful axonal regeneration, but the effects of phosphorylation of its N-terminus are moderate. J Neurochem 121:607-618. CrossRef Medline
46. Schramek D., Kotsinas A, Meixner A, Wada T, Elling U, Pospisilik JA, Neely GG, Zwick RH, Sigl V, Forni G, Serrano M, Gorgoulis VG, Penninger JM (2011) The stress kinase MKK7 couples oncogenic stress to p53 stability and tumor suppression. Nat Genet 43:212-219. CrossRef Medline
47. Sendtner M., Pei G, Beck M, Schweizer U, Wiese S (2000) Developmental motoneuron cell death and neurotrophic factors. Cell Tissue Res 301:71-84. CrossRef Medline
48. Shin J. E, Cho Y, Beirowski B, Milbrandt J, Cavalli V, DiAntonio A (2012) Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74:1015-1022. CrossRef Medline
49. Snider W. D, Elliott JL, Yan Q (1992) Axotomy-induced neuronal death during development. J Neurobiol 23:1231-1246. CrossRef Medline
50. Sun W., Gould TW, Newbern J, Milligan C, Choi SY, Kim H, Oppenheim RW (2005) Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J Neurosci 25:5595-5603. CrossRef Medline
51. Thaler J., Harrison K, Sharma K, Lettieri K, Kehrl J, Pfaff SL (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23:675-687. CrossRef Medline
52. Vanderhaeghen P., Cheng HJ (2010) Guidance molecules in axon pruning and cell death. Cold Spring Harb Perspect Biol 2:a001859. CrossRef Medline
53. Wada T., Joza N, Cheng HY, Sasaki T, Kozieradzki I, Bachmaier K, Katada T, Schreiber M., Wagner EF, Nishina H, Penninger JM (2004) MKK7 couples stress signalling to G2/M cell-cycle progression and cellular senescence. Nat Cell Biol 6:215-226. CrossRef Medline
54. Wang X., Destrument A, Tournier C (2007a) Physiological roles of MKK4 and MKK7: insights from animal models. Biochim Biophys Acta 1773: 1349-1357. CrossRef Medline
55. Wang X., Nadarajah B, Robinson AC, McColl BW, Jin JW, Dajas-Bailador F, Boot-Handford R. P, Tournier C (2007b) Targeted deletion of the mitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death. Mol Cell Biol 27:7935-7946. CrossRef Medline
56. Watkins T. A, Wang B, Huntwork-Rodriguez S, Yang J, Jiang Z, Eastham-Anderson J, Modrusan Z, Kaminker JS, Tessier-Lavigne M, Lewcock JW (2013) DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. Proc Natl Acad Sci U S A 110:4039-4044. CrossRef Medline
57. Welsbie D. S, Yang Z, Ge Y, Mitchell KL, Zhou X, Martin SE, Berlinicke CA, Hackler L. Jr, Fuller J, Fu J, Cao LH, Han B, Auld D, Xue T, Hirai S, Germain L., Simard-Bisson C, Blouin R, Nguyen JV, Davis CH, et al. (2013) Functional genomic screening identifies dual leucine zipper kinase as a key mediator of retinal ganglion cell death. Proc Natl Acad Sci U S A 110:4045-4050. CrossRef Medline
58. Whitmarsh A. J (2006) The JIP family of MAPK scaffold proteins. Biochem Soc Trans 34:828-832. CrossRef Medline
59. Xiong X., Wang X, Ewanek R, Bhat P, Diantonio A, Collins CA (2010) Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J Cell Biol 191:211-223. CrossRef Medline
60. Xu Z., Maroney AC, Dobrzanski P, Kukekov NV, Greene LA (2001) The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol Cell Biol 21:4713-4724. CrossRef Medline
61. Yamasaki T., Kawasaki H, Arakawa S, Shimizu K, Shimizu S, Reiner O, Okano H, Nishina S, Azuma N, Penninger JM, Katada T, Nishina H (2011) Stress-activated protein kinase MKK7 regulates axon elongation in the developing cerebral cortex. J Neurosci 31:16872-16883. CrossRef Medline
62. Yan D., Jin Y (2012) Regulation of DLK-1 kinase activity by calciummediated dissociation from an inhibitory isoform. Neuron 76:534-548. CrossRef Medline
63. Yasuda J., Whitmarsh AJ, Cavanagh J, Sharma M, Davis RJ (1999) The JIP group of mitogen-activated protein kinase scaffold proteins. Mol Cell Biol 19:7245-7254. Medline