An evolutionarily conserved mechanism for cAMP elicited axonal regeneration involves direct activation of the dual leucine zipper kinase DLK

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Hao, Yan ^a   Frey, Erin ^b   Yoon, Choya ^a   Wong, Hetty ^c   Nestorovski, Douglas ^a   Holzman, Lawrence B ^c   Giger, Roman J ^a,d   DiAntonio, Aaron ^b   Collins, Catherine ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DUAL LEUCINE ZIPPER KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE; UNCLASSIFIED DRUG; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE 12;

ADULT; ANIMAL EXPERIMENT; ANIMAL GENETICS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIPTERA; DROSOPHILA; GENE MUTATION; GLAUCOMA; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE FIBER REGENERATION; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; ENZYMOLOGY; METABOLISM; NERVE REGENERATION; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DROSOPHILA; HUMANS; MAP KINASE KINASE KINASES; MICE; NERVE REGENERATION;

EID: 84975229692     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14048     Document Type: Article

References (69)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhães TR, Goodman CS. 2002. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in drosophila. Neuron 33: 545-558. doi: 10.1016/S0896-6273(02)00589-5
2. Babetto E, Beirowski B, Russler EV, Milbrandt J, DiAntonio A. 2013. The phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell Reports 3: 1422-1429. doi: 10.1016/j.celrep.2013.04.013
3. Brace EJ, DiAntonio A. 2016. Models of axon regeneration in drosophila. Experimental Neurology. doi: 10.1016/j.expneurol.2016.03.014
4. Budnik V, Koh Y. H, Guan B, Hartmann B, Hough C, Woods D, Gorczyca M, Gorczyca M. 1996 Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron, 17, 62740. doi: 10.1016/s0896-6273(00)80196-8
5. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT. 1999. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a camp-dependent mechanism. Neuron 22: 89-101. doi: 10.1016/S0896-6273(00)80681-9
6. Cho Y, Shin JE, Ewan EE, Oh YM, Pita-Thomas W, Cavalli V. 2015. Activating injury-responsive genes with hypoxia enhances axon regeneration through neuronal hif-1a. Neuron 88: 720-734. doi: 10.1016/j.neuron.2015.09.050
7. Cho Y, Sloutsky R, Naegle KM, Cavalli V. 2013. Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell 155: 894-908. doi: 10.1016/j.cell.2013.10.004
8. Chung SH, Awal MR, Shay J, McLoed MM, Mazur E, Gabel CV. 2016. Novel DLK-independent neuronal regeneration in Caenorhabditis elegans shares links with activity-dependent ectopic outgrowth. Proceedings of the National Academy of Sciences of the United States of America 113: E2852-2860. doi: 10.1073/pnas.1600564113
9. Collins CA, Wairkar YP, Johnson SL, DiAntonio A. 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51: 57-69. doi: 10.1016/j.neuron.2006.05.026
10. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-157. doi: 10.1038/nature05954
11. Durkin JT, Holskin BP, Kopec KK, Reed MS, Spais CM, Steffy BM, Gessner G, Angeles TS, Pohl J, Ator MA, Meyer SL. 2004. Phosphoregulation of mixed-lineage kinase 1 activity by multiple phosphorylation in the activation loop. Biochemistry 43: 16348-16355. doi: 10.1021/bi049866y
12. Fagoe ND, Attwell CL, Kouwenhoven D, Verhaagen J, Mason MR, Mason MR. 2015. Overexpression of ATF3 or the combination of ATF3, c-jun, STAT3 and smad1 promotes regeneration of the central axon branch of sensory neurons but without synergistic effects. Human Molecular Genetics 24: 6788-6800. doi: 10.1093/hmg/ddv383
13. Fawcett JW, Schwab ME, Montani L, Brazda N, Müller HW. 2012. Defeating inhibition of regeneration by scar and myelin components. Handbook of Clinical Neurology 109: 503-522. doi: 10.1016/B978-0-444-52137-8.00031-0
14. Filbin MT. 2003. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nature Reviews. Neuroscience 4: 703-713. doi: 10.1038/nrn1195
15. Frey E, Valakh V, Karney-Grobe S, Shi Y, Milbrandt J, DiAntonio A. 2015. An in vitro assay to study induction of the regenerative state in sensory neurons. Experimental Neurology 263: 350-363. doi: 10.1016/j.expneurol.2014.10.012
16. Fujioka M, Lear BC, Landgraf M, Yusibova GL, Zhou J, Riley KM, Patel NH, Jaynes JB. 2003. Even-skipped, acting as a repressor, regulates axonal projections in drosophila. Development 130: 5385-5400. doi: 10.1242/dev.00770
17. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT. 2004. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44: 609-621. doi: 10.1016/j.neuron.2004.10.030
18. Ghosh AS, Wang B, Pozniak CD, Chen M, Watts RJ, Lewcock JW. 2011. DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. The Journal of Cell Biology 194: 751-764. doi: 10.1083/jcb.201103153
19. Ghosh-Roy A, Wu Z, Goncharov A, Jin Y, Chisholm AD. 2010. Calcium and cyclic AMP promote axonal regeneration in caenorhabditis elegans and require DLK-1 kinase. The Journal of Neuroscience 30: 3175-3183. doi: 10.1523/JNEUROSCI.5464-09.2010
20. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M. 2009. Axon regeneration requires a conserved MAP kinase pathway. Science 323: 802-806. doi: 10.1126/science.1165527
21. Hannila SS, Filbin MT. 2008. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Experimental Neurology 209: 321-332. doi: 10.1016/j.expneurol.2007.06.020
22. Holland SM, Collura KM, Ketschek A, Noma K, Ferguson TA, Jin Y, Gallo G, Thomas GM. 2016. Palmitoylation controls DLK localization, interactions and activity to ensure effective axonal injury signaling. Proceedings of the National Academy of Sciences of the United States of America 113: 763-768. doi: 10.1073/pnas.1514123113
23. Hollis ER, Zou Y. 2012. Reinduced wnt signaling limits regenerative potential of sensory axons in the spinal cord following conditioning lesion. Proceedings of the National Academy of Sciences of the United States of America 109: 14663-14668. doi: 10.1073/pnas.1206218109
24. 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. The Journal of Cell Biology 202: 747-763. doi: 10.1083/jcb.201303066
25. Leung IW, Lassam N. 2001. The kinase activation loop is the key to mixed lineage kinase-3 activation via both autophosphorylation and hematopoietic progenitor kinase 1 phosphorylation. The Journal of Biological Chemistry 276: 1961-1967. doi: 10.1074/jbc.M004092200
26. Lewcock JW, Genoud N, Lettieri K, Pfaff SL. 2007. The ubiquitin ligase phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56: 604-620. doi: 10.1016/j.neuron.2007.09.009
27. Li C, Hisamoto N, Matsumoto K. 2015. Axon Regeneration Is Regulated by Ets-C/EBP Transcription Complexes Generated by Activation of the cAMP/Ca2+ Signaling Pathways. PLoS Genetics 11: e1005603. doi: 10.1371/journal.pgen.1005603
28. Li W, Ohlmeyer JT, Lane ME, Kalderon D. 1995. Function of protein kinase A in hedgehog signal transduction and drosophila imaginal disc development. Cell 80: 553-562. doi: 10.1016/0092-8674(95)90509-X
29. Liu K, Tedeschi A, Park KK, He Z. 2011. Neuronal intrinsic mechanisms of axon regeneration. Annual Review of Neuroscience 34: 131-152. doi: 10.1146/annurev-neuro-061010-113723
30. Ma TC, Barco A, Ratan RR, Willis DE. 2014. cAMP-responsive element-binding protein (CREB) and camp co-regulate activator protein 1 (ap1)-dependent regeneration-associated gene expression and neurite growth. The Journal of Biological Chemistry 289: 32914-32925. doi: 10.1074/jbc.M114.582460
31. Mata M, Merritt SE, Fan G, Yu GG, Holzman LB. 1996. Characterization of dual leucine zipper-bearing kinase, a mixed lineage kinase present in synaptic terminals whose phosphorylation state is regulated by membrane depolarization via calcineurin. The Journal of Biological Chemistry 271: 16888-16896. doi: 10.1074/jbc.271.28.16888
32. Mathiasen JR, McKenna BA, Saporito MS, Ghadge GD, Roos RP, Holskin BP, Wu ZL, Trusko SP, Connors TC, Maroney AC, Thomas BA, Thomas JC, Bozyczko-Coyne D. 2004. Inhibition of mixed lineage kinase 3 attenuates mpp+-induced neurotoxicity in SH-SY5Y cells. Brain Research 1003: 86-97. doi: 10.1016/j.brainres.2003.11.073
33. Merrill RA, Dagda RK, Dickey AS, Cribbs JT, Green SH, Usachev YM, Strack S. 2011. Mechanism of neuroprotective mitochondrial remodeling by PKA/AKAP1. PLoS Biology 9: e1000612. doi: 10.1371/journal.pbio.1000612
34. Merritt SE, Mata M, Nihalani D, Zhu C, Hu X, Holzman LB. 1999. The mixed lineage kinase DLK utilizes MKK7 and not MKK4 as substrate. The Journal of Biological Chemistry 274: 10195-10202. doi: 10.1074/jbc.274.15.10195
35. Nakata K, Abrams B, Grill B, Goncharov A, Huang X, Chisholm AD, Jin Y. 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. doi: 10.1016/j.cell.2004.12.017
36. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI. 2002. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic camp elevation. Neuron 34: 885-893. doi: 10.1016/S0896-6273(02)00702-X
37. Neumann S, Woolf CJ. 1999. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23: 83-91. doi: 10.1016/S0896-6273(00)80755-2
38. Nihalani D, Merritt S, Holzman LB. 2000. Identification of structural and functional domains in mixed lineage kinase dual leucine zipper-bearing kinase required for complex formation and stress-activated protein kinase activation. The Journal of Biological Chemistry 275: 7273-7279. doi: 10.1074/jbc.275.10.7273
39. Omura T, Omura K, Tedeschi A, Riva P, Painter MW, Rojas L, Martin J, Lisi V, Huebner EA, Latremoliere A, Yin Y, Barrett LB, Singh B, Lee S, Crisman T, Gao F, Li S, Kapur K, Geschwind DH, Kosik KS, et al. 2015. Robust axonal regeneration occurs in the injured cast/ei mouse CNS. Neuron 86: 1215-1227. doi: 10.1016/j.neuron.2015.05.005
40. Pierre SC, Häusler J, Birod K, Geisslinger G, Scholich K. 2004. PAM mediates sustained inhibition of camp signaling by sphingosine-1-phosphate. The EMBO Journal 23: 3031-3040. doi: 10.1038/sj.emboj.7600321
41. Pozniak CD, 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. The Journal of Experimental Medicine 210: 2553-2567. doi: 10.1084/jem.20122832
42. Qiu J, Cafferty WB, McMahon SB, Thompson SW. 2005. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. The Journal of Neuroscience 25: 1645-1653. doi: 10.1523/JNEUROSCI.3269-04.2005
43. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. 2002. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34: 895-903. doi: 10.1016/S0896-6273(02)00730-4
44. Richardson PM, Issa VMK. 1984. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309: 791-793. doi: 10.1038/309791a0
45. Ritzenthaler S, Suzuki E, Chiba A. 2000. Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nature Neuroscience 3: 1012-1017. doi: 10.1038/79833
46. Shin JE, 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. doi: 10.1016/j.neuron.2012.04.028
47. Shin JE, DiAntonio A. 2011. Highwire regulates guidance of sister axons in the drosophila mushroom body. The Journal of Neuroscience 31: 17689-17700. doi: 10.1523/JNEUROSCI.3902-11.2011
48. Silver J, Schwab ME, Popovich PG. 2015. Central nervous system regenerative failure: Role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harbor Perspectives in Biology 7: a020602. doi: 10.1101/cshperspect.a020602
49. Spira ME, Oren R, Dormann A, Ilouz N, Lev S. 2001. Calcium, protease activation, and cytoskeleton remodeling underlie growth cone formation and neuronal regeneration. Cellular and Molecular Neurobiology 21: 591-604. doi: 10.1023/A: 1015135617557
50. Sun F, He Z. 2010. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Current Opinion in Neurobiology 20: 510-518. doi: 10.1016/j.conb.2010.03.013
51. Taskén K, Aandahl EM. 2004. Localized effects of camp mediated by distinct routes of protein kinase A. Physiological Reviews 84: 137-167. doi: 10.1152/physrev.00021.2003
52. Tedeschi A, Bradke F. 2013. The DLK signalling pathway-a double-edged sword in neural development and regeneration. EMBO Reports 14: 605-614. doi: 10.1038/embor.2013.64
53. Valakh V, Frey E, Babetto E, Diantonio A. 2015. Cytoskeletal disruption activates the dlk/jnk pathway, which promotes axonal regeneration and mimics a preconditioning injury. Neurobiol Dis 77: 13-25. doi: 10.1016/j.nbd.2015.02.014
54. Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS. 2000. Highwire regulates synaptic growth in drosophila. Neuron 26: 313-329. doi: 10.1016/S0896-6273(00)81166-6
55. Wang X, Kim JH, Bazzi M, Robinson S, Ye B. 2013. Bimodal control of dendritic and axonal growth by the dual leucine zipper kinase pathway. PLoS Biol 11: e1001572. doi: 10.1371/journal.pbio.1001572
56. Watkins TA, 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. Proceedings of the National Academy of Sciences of the United States of America 110: 4039-4044. doi: 10.1073/pnas.1211074110
57. Welsbie DS, Yang Z, Ge Y, Mitchell KL, Zhou X, Martin SE, Berlinicke CA, Hackler L, 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. Proceedings of the National Academy of Sciences of the United States of America 110: 4045-4050. doi: 10.1073/pnas.1211284110
58. Wong CO, Palmieri M, Li J, Akhmedov D, Chao Y, Broadhead GT, Zhu MX, Berdeaux R, Collins CA, Sardiello M, Venkatachalam K. 2015. Diminished mtorc1-dependent JNK activation underlies the neurodevelopmental defects associated with lysosomal dysfunction. Cell Reports 12: 2009-2020. doi: 10.1016/j.celrep.2015.08.047
59. Wong W, Scott JD. 2004. AKAP signalling complexes: Focal points in space and time. Nature Reviews. Molecular Cell Biology 5: 959-970. doi: 10.1038/nrm1527
60. Xiao Y, Tian W, López-Schier H. 2015. Optogenetic stimulation of neuronal repair. Current Biology 25: R1068-1069. doi: 10.1016/j.cub.2015.09.038
61. Xiong X, Collins CA. 2012. A conditioning lesion protects axons from degeneration via the wallenda/dlk map kinase signaling cascade. J Neurosci 32: 610-615. doi: 10.1523/JNEUROSCI.3586-11.2012
62. Xiong X, Hao Y, Sun K, Li J, Li X, Mishra B, Soppina P, Wu C, Hume RI, Collins CA. 2012. The highwire ubiquitin ligase promotes axonal degeneration by tuning levels of nmnat protein. PLoS Biology 10-e1001440. doi: 10.1371/journal.pbio.1001440
63. 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. The Journal of Cell Biology 191: 211-223. doi: 10.1083/jcb.201006039
64. Xue Y, Ren J, Gao X, Jin C, Wen L, Yao X. 2008. GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Molecular & Cellular Proteomics 7: 1598-1608. doi: 10.1074/mcp.M700574-MCP200
65. Xue Y, Zhou F, Zhu M, Ahmed K, Chen G, Yao X. 2005. GPS: A comprehensive www server for phosphorylation sites prediction. Nucleic Acids Research 33: W184-187. doi: 10.1093/nar/gki393
66. Yan D, Jin Y. 2012. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76: 534-548. doi: 10.1016/j.neuron.2012.08.043
67. Yan D, Wu Z, Chisholm AD, Jin Y. 2009. The DLK-1 kinase promotes mrna stability and local translation in C. elegans synapses and axon regeneration. Cell 138: 1005-1018. doi: 10.1016/j.cell.2009.06.023
68. Ylera B, Ertürk A, Hellal F, Nadrigny F, Hurtado A, Tahirovic S, Oudega M, Kirchhoff F, Bradke F. 2009. Chronically cns-injured adult sensory neurons gain regenerative competence upon a lesion of their peripheral axon. Current Biology 19: 930-936. doi: 10.1016/j.cub.2009.04.017
69. Zou H, Ho C, Wong K, Tessier-Lavigne M. 2009. Axotomy-induced smad1 activation promotes axonal growth in adult sensory neurons. The Journal of Neuroscience 29: 7116-7123. doi: 10.1523/JNEUROSCI.5397-08.2009