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Annual Review of Cell and Developmental Biology

Volume 35, 2019

Multitasking: Dual Leucine Zipper–Bearing Kinases in Neuronal Development and Stress Management

Abstract

The dual leucine zipper–bearing kinase (DLK) and leucine zipper–bearing kinase (LZK) are evolutionarily conserved MAPKKKs of the mixed-lineage kinase family. Acting upstream of stress-responsive JNK and p38 MAP kinases, DLK and LZK have emerged as central players in neuronal responses to a variety of acute and traumatic injuries. Recent studies also implicate their function in astrocytes, microglia, and other nonneuronal cells, reflecting their expanding roles in the multicellular response to injury and in disease. Of particular note is the potential link of these kinases to neurodegenerative diseases and cancer. It is thus critical to understand the physiological contexts under which these kinases are activated, as well as the signal transduction mechanisms that mediate specific functional outcomes. In this review we first provide a historical overview of the biochemical and functional dissection of these kinases. We then discuss recent findings on regulating their activity to enhance cellular protection following injury and in disease, focusing on but not limited to the nervous system.

Keyword(s): adipogenesis, Alzheimer disease models, astrocytes, axon degeneration, axon regeneration, cytoskeleton, DLK, DLK-1, HSV infection, insulin β-cells, JNK, LZK, MAP3K, neuronal death, neuronal development, p38, Wallenda
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/content/journals/10.1146/annurev-cellbio-100617-062644
2019-10-06
2024-04-18
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Literature Cited

  1. Andrusiak MG, Jin Y. 2016. Context specificity of stress-activated mitogen-activated protein (MAP) kinase signaling: the story as told by Caenorhabditis elegans. J. Biol. Chem 291:7796–804
     [Google Scholar]
  2. Asghari Adib E, Smithson LJ, Collins CA 2018. An axonal stress response pathway: degenerative and regenerative signaling by DLK. Curr. Opin. Neurobiol. 53:110–19
     [Google Scholar]
  3. Bloom AJ, 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 21:2593–606
     [Google Scholar]
  4. Blouin R, Beaudoin J, Bergeron P, Nadeau A, Grondin G 1996. Cell-specific expression of the ZPK gene in adult mouse tissues. DNA Cell Biol 15:631–42
     [Google Scholar]
  5. Borchers S, Babaei R, Klimpel C, Duque Escobar J, Schroder S et al. 2017. TNFα-induced DLK activation contributes to apoptosis in the beta-cell line HIT. Naunyn Schmiedebergs Arch. Pharmacol. 390:813–25
     [Google Scholar]
  6. Bounoutas A, Kratz J, Emtage L, Ma C, Nguyen KC, Chalfie M 2011. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. PNAS 108:3982–87
     [Google Scholar]
  7. Bounoutas A, O'Hagan R, Chalfie M 2009. The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation. Curr. Biol. 19:1362–67
     [Google Scholar]
  8. Brace EJ, DiAntonio A. 2017. Models of axon regeneration in Drosophila. Exp. Neurol 287:310–17
     [Google Scholar]
  9. Burda JE, Sofroniew MV. 2014. Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81:229–48
     [Google Scholar]
  10. Burgess RW, Peterson KA, Johnson MJ, Roix JJ, Welsh IC, O'Brien TP 2004. Evidence for a conserved function in synapse formation reveals Phr1 as a candidate gene for respiratory failure in newborn mice. Mol. Cell. Biol. 24:1096–105
     [Google Scholar]
  11. Camarena V, Kobayashi M, Kim JY, Roehm P, Perez R et al. 2010. Nature and duration of growth factor signaling through receptor tyrosine kinases regulates HSV-1 latency in neurons. Cell Host Microbe 8:320–30
     [Google Scholar]
  12. Chen CH, Lee A, Liao CP, Liu YW, Pan CL 2014. RHGF-1/PDZ-RhoGEF and retrograde DLK-1 signaling drive neuronal remodeling on microtubule disassembly. PNAS 111:16568–73
     [Google Scholar]
  13. Chen M, Geoffroy CG, Meves JM, Narang A, Li Y et al. 2018. Leucine zipper–bearing kinase is a critical regulator of astrocyte reactivity in the adult mammalian CNS. Cell Rep 22:3587–97
     [Google Scholar]
  14. Chen M, Geoffroy CG, Wong HN, Tress O, Nguyen MT et al. 2016. Leucine zipper–bearing kinase promotes axon growth in mammalian central nervous system neurons. Sci. Rep. 6:31482
     [Google Scholar]
  15. Chen X, Rzhetskaya M, Kareva T, Bland R, During MJ et al. 2008. Antiapoptotic and trophic effects of dominant-negative forms of dual leucine zipper kinase in dopamine neurons of the substantia nigra in vivo. J. Neurosci. 28:672–80
     [Google Scholar]
  16. Chuang M, Goncharov A, Wang S, Oegema K, Jin Y, Chisholm AD 2014. The microtubule minus-end-binding protein patronin/PTRN-1 is required for axon regeneration in C. elegans. Cell Rep 9:874–83
     [Google Scholar]
  17. Cliffe AR, Arbuckle JH, Vogel JL, Geden MJ, Rothbart SB et al. 2015. Neuronal stress pathway mediating a histone methyl/phospho switch is required for herpes simplex virus reactivation. Cell Host Microbe 18:649–58
     [Google Scholar]
  18. Collins CA, Wairkar YP, Johnson SL, DiAntonio A 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51:57–69
     [Google Scholar]
  19. Couture JP, Blouin R. 2011. The DLK gene is a transcriptional target of PPARγ. Biochem. J. 438:93–101
     [Google Scholar]
  20. Couture JP, Daviau A, Fradette J, Blouin R 2009. The mixed-lineage kinase DLK is a key regulator of 3T3-L1 adipocyte differentiation. PLOS ONE 4:3e4743
     [Google Scholar]
  21. Daviau A, Proulx R, Robitaille K, Di Fruscio M, Tanguay RM et al. 2006. Down-regulation of the mixed-lineage dual leucine zipper–bearing kinase by heat shock protein 70 and its co-chaperone CHIP. J. Biol. Chem. 281:31467–77
     [Google Scholar]
  22. Dickson HM, Zurawski J, Zhang H, Turner DL, Vojtek AB 2010. POSH is an intracellular signal transducer for the axon outgrowth inhibitor Nogo66. J. Neurosci. 30:13319–25
     [Google Scholar]
  23. Douziech M, Grondin G, Loranger A, Marceau N, Blouin R 1998. Zonal induction of mixed lineage kinase ZPK/DLK/MUK gene expression in regenerating mouse liver. Biochem. Biophys. Res. Commun. 249:927–32
     [Google Scholar]
  24. Douziech M, Laberge G, Grondin G, Daigle N, Blouin R 1999. Localization of the mixed-lineage kinase DLK/MUK/ZPK to the Golgi apparatus in NIH 3T3 cells. J. Histochem. Cytochem. 47:1287–96
     [Google Scholar]
  25. Edwards ZC, Trotter EW, Torres-Ayuso P, Chapman P, Wood HM et al. 2017. Survival of head and neck cancer cells relies upon LZK kinase–mediated stabilization of mutant p53. Cancer Res 77:4961–72
     [Google Scholar]
  26. Fukuyama K, Yoshida M, Yamashita A, Deyama T, Baba M et al. 2000. MAPK upstream kinase (MUK)-binding inhibitory protein, a negative regulator of MUK/dual leucine zipper–bearing kinase/leucine zipper protein kinase. J. Biol. Chem. 275:21247–54
     [Google Scholar]
  27. Gallo KA, Johnson GL. 2002. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell Biol. 3:663–72
     [Google Scholar]
  28. Geoffroy CG, Zheng B. 2014. Myelin-associated inhibitors in axonal growth after CNS injury. Curr. Opin. Neurobiol. 27C:31–38
     [Google Scholar]
  29. Gerdts J, Summers DW, Milbrandt J, DiAntonio A 2016. Axon self-destruction: new links among SARM1, MAPKs, and NAD+ metabolism. Neuron 89:449–60
     [Google Scholar]
  30. 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. J. Cell Biol. 194:751–64
     [Google Scholar]
  31. 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. J. Neurosci. 30:3175–83
     [Google Scholar]
  32. Grill B, Murphey RK, Borgen MA 2016. The PHR proteins: intracellular signaling hubs in neuronal development and axon degeneration. Neural Dev 11:8
     [Google Scholar]
  33. Hammarlund M, Jorgensen EM, Bastiani MJ 2007. Axons break in animals lacking beta-spectrin. J. Cell Biol. 176:269–75
     [Google Scholar]
  34. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M 2009. Axon regeneration requires a conserved MAP kinase pathway. Science 323:802–6
     [Google Scholar]
  35. Han H, Chen Y, Cheng L, Prochownik EV, Li Y 2016. microRNA-206 impairs c-Myc-driven cancer in a synthetic lethal manner by directly inhibiting MAP3K13. Oncotarget 7:16409–19
     [Google Scholar]
  36. Hao Y, Frey E, Yoon C, Wong H, Nestorovski D et al. 2016. An evolutionarily conserved mechanism for cAMP elicited axonal regeneration involves direct activation of the dual leucine zipper kinase DLK. eLife 5:e14048
     [Google Scholar]
  37. Hirai S, Cui DF, Miyata T, Ogawa M, Kiyonari H et al. 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. 26:11992–2002
     [Google Scholar]
  38. 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 129:4483–95
     [Google Scholar]
  39. Hirai S, Kawaguchi A, Suenaga J, Ono M, Cui DF, Ohno S 2005. Expression of MUK/DLK/ZPK, an activator of the JNK pathway, in the nervous systems of the developing mouse embryo. Gene Expr. Patterns 5:517–23
     [Google Scholar]
  40. Holland SM, Collura KM, Ketschek A, Noma K, Ferguson TA et al. 2016. Palmitoylation controls DLK localization, interactions and activity to ensure effective axonal injury signaling. PNAS 113:763–68
     [Google Scholar]
  41. Holtzman DM, Herz J, Bu G 2012. Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2:a006312
     [Google Scholar]
  42. Holzman LB, Merritt SE, Fan G 1994. Identification, molecular cloning, and characterization of dual leucine zipper bearing kinase: a novel serine/threonine protein kinase that defines a second subfamily of mixed lineage kinases. J. Biol. Chem. 269:30808–17
     [Google Scholar]
  43. Horiuchi D, Collins CA, Bhat P, Barkus RV, Diantonio A, Saxton WM 2007. Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr. Biol. 17:1313–17
     [Google Scholar]
  44. Huang YA, Zhou B, Wernig M, Sudhof TC 2017. ApoE2, ApoE3, and ApoE4 differentially stimulate APP transcription and Aβ secretion. Cell 168:427–41.e21
     [Google Scholar]
  45. Huntwork-Rodriguez S, Wang B, Watkins T, Ghosh AS, Pozniak CD et al. 2013. JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J. Cell Biol. 202:747–63
     [Google Scholar]
  46. Ikeda A, Hasegawa K, Masaki M, Moriguchi T, Nishida E et al. 2001a. Mixed lineage kinase LZK forms a functional signaling complex with JIP-1, a scaffold protein of the c-Jun NH2-terminal kinase pathway. J. Biochem. 130:773–81
     [Google Scholar]
  47. Ikeda A, Masaki M, Kozutsumi Y, Oka S, Kawasaki T 2001b. Identification and characterization of functional domains in a mixed lineage kinase LZK. FEBS Lett 488:190–95
     [Google Scholar]
  48. 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. 383:258–62
     [Google Scholar]
  49. Itoh T, Horiuchi M, Ikeda RH Jr., Xu J, Bannerman P et al. 2014. ZPK/DLK and MKK4 form the critical gateway to axotomy-induced motoneuron death in neonates. J. Neurosci. 34:10729–42
     [Google Scholar]
  50. Joy MT, Ben Assayag E, Shabashov-Stone D, Liraz-Zaltsman S, Mazzitelli J et al. 2019. CCR5 is a therapeutic target for recovery after stroke and traumatic brain injury. Cell 176:1143–57
     [Google Scholar]
  51. Karney-Grobe S, Russo A, Frey E, Milbrandt J, DiAntonio A 2018. HSP90 is a chaperone for DLK and is required for axon injury signaling. PNAS 115:E9899–908
     [Google Scholar]
  52. Klinedinst S, Wang X, Xiong X, Haenfler JM, Collins CA 2013. Independent pathways downstream of the Wnd/DLK MAPKKK regulate synaptic structure, axonal transport, and injury signaling. J. Neurosci. 33:12764–78
     [Google Scholar]
  53. Kurup N, Yan D, Goncharov A, Jin Y 2015. Dynamic microtubules drive circuit rewiring in the absence of neurite remodeling. Curr. Biol. 25:1594–605
     [Google Scholar]
  54. Larhammar M, Huntwork-Rodriguez S, Jiang Z, Solanoy H, Sengupta Ghosh A et al. 2017a. Dual leucine zipper kinase–dependent PERK activation contributes to neuronal degeneration following insult. eLife 6:e20725
     [Google Scholar]
  55. Larhammar M, Huntwork-Rodriguez S, Rudhard Y, Sengupta-Ghosh A, Lewcock JW 2017b. The Ste20 family kinases MAP4K4, MINK1, and TNIK converge to regulate stress-induced JNK signaling in neurons. J. Neurosci. 37:11074–84
     [Google Scholar]
  56. Le Pichon CE, Meilandt WJ, Dominguez S, Solanoy H, Lin H et al. 2017. Loss of dual leucine zipper kinase signaling is protective in animal models of neurodegenerative disease. Sci. Transl. Med. 9:eaag0394
     [Google Scholar]
  57. Lewcock JW, Genoud N, Lettieri K, Pfaff SL 2007. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56:604–20
     [Google Scholar]
  58. Lippi G, Fernandes CC, Ewell LA, John D, Romoli B et al. 2016. MicroRNA-101 regulates multiple developmental programs to constrain excitation in adult neural networks. Neuron 92:1337–51
     [Google Scholar]
  59. Liu K, Lu Y, Lee JK, Samara R, Willenberg R et al. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 13:1075–81
     [Google Scholar]
  60. Ma X, Chen Y, Zhang S, Xu W, Shao Y et al. 2016. Rho1-Wnd signaling regulates loss-of-cell polarity-induced cell invasion in Drosophila. Oncogene 35:846–55
     [Google Scholar]
  61. Marcette JD, Chen JJ, Nonet ML 2014. The Caenorhabditis elegans microtubule minus-end binding homolog PTRN-1 stabilizes synapses and neurites. eLife 3:e01637
     [Google Scholar]
  62. Masaki M, Ikeda A, Shiraki E, Oka S, Kawasaki T 2003. Mixed lineage kinase LZK and antioxidant protein-1 activate NF-κB synergistically. Eur. J. Biochem. 270:76–83
     [Google Scholar]
  63. Massaro CM, Pielage J, Davis GW 2009. Molecular mechanisms that enhance synapse stability despite persistent disruption of the spectrin/ankyrin/microtubule cytoskeleton. J. Cell Biol. 187:101–17
     [Google Scholar]
  64. 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. J. Biol. Chem. 271:16888–96
     [Google Scholar]
  65. McQuarrie IG, Grafstein B. 1973. Axon outgrowth enhanced by a previous nerve injury. Arch. Neurol. 29:53–55
     [Google Scholar]
  66. Miller BR, 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. 12:387–89
     [Google Scholar]
  67. Nadeau A, Grondin G, Blouin R 1997. In situ hybridization analysis of ZPK gene expression during murine embryogenesis. J. Histochem. Cytochem. 45:107–18
     [Google Scholar]
  68. Nakata K, Abrams B, Grill B, Goncharov A, Huang X et al. 2005. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407–20
     [Google Scholar]
  69. 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. J. Biol. Chem. 275:7273–79
     [Google Scholar]
  70. Nihalani D, Meyer D, Pajni S, Holzman LB 2001. Mixed lineage kinase–dependent JNK activation is governed by interactions of scaffold protein JIP with MAPK module components. EMBO J 20:3447–58
     [Google Scholar]
  71. Nix P, Hisamoto N, Matsumoto K, Bastiani M 2011. Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. PNAS 108:10738–43
     [Google Scholar]
  72. Nolan JJ, Ludvik B, Beerdsen P, Joyce M, Olefsky J 1994. Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. N. Engl. J. Med. 331:1188–93
     [Google Scholar]
  73. Oetjen E, Lechleiter A, Blume R, Nihalani D, Holzman L, Knepel W 2006. Inhibition of membrane depolarization–induced transcriptional activity of cyclic AMP response element binding protein (CREB) by the dual-leucine-zipper-bearing kinase in a pancreatic islet beta cell line. Diabetologia 49:332–42
     [Google Scholar]
  74. Park EC, Rongo C. 2018. RPM-1 and DLK-1 regulate pioneer axon outgrowth by controlling Wnt signaling. Development 145:dev164897
     [Google Scholar]
  75. Park KK, Liu K, Hu Y, Smith PD, Wang C et al. 2008. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963–66
     [Google Scholar]
  76. Patel S, Cohen F, Dean BJ, De La Torre K, Deshmukh G et al. 2015a. Discovery of dual leucine zipper kinase (DLK, MAP3K12) inhibitors with activity in neurodegeneration models. J. Med. Chem. 58:401–18
     [Google Scholar]
  77. Patel S, Harris SF, Gibbons P, Deshmukh G, Gustafson A et al. 2015b. Scaffold-hopping and structure-based discovery of potent, selective, and brain penetrant N-(1H-pyrazol-3-yl)pyridin-2-amine inhibitors of dual leucine zipper kinase (DLK, MAP3K12). J. Med. Chem. 58:8182–99
     [Google Scholar]
  78. Patel S, Meilandt WJ, Erickson RI, Chen J, Deshmukh G et al. 2017. Selective inhibitors of dual leucine zipper kinase (DLK, MAP3K12) with activity in a model of Alzheimer's disease. J. Med. Chem. 60:8083–102
     [Google Scholar]
  79. Phu DT, Wallbach M, Depatie C, Fu A, Screaton RA, Oetjen E 2011. Regulation of the CREB coactivator TORC by the dual leucine zipper kinase at different levels. Cell. Signal. 23:344–53
     [Google Scholar]
  80. Pozniak CD, Sengupta Ghosh A, Gogineni A, Hanson JE, Lee SH et al. 2013. Dual leucine zipper kinase is required for excitotoxicity-induced neuronal degeneration. J. Exp. Med. 210:2553–67
     [Google Scholar]
  81. Richardson CE, Spilker KA, Cueva JG, Perrino J, Goodman MB, Shen K 2014. PTRN-1, a microtubule minus end-binding CAMSAP homolog, promotes microtubule function in Caenorhabditis elegans neurons. eLife 3:e01498
     [Google Scholar]
  82. Robitaille H, Proulx R, Robitaille K, Blouin R, Germain L 2005. The mitogen-activated protein kinase kinase kinase dual leucine zipper–bearing kinase (DLK) acts as a key regulator of keratinocyte terminal differentiation. J. Biol. Chem. 280:12732–41
     [Google Scholar]
  83. Robitaille H, Simard-Bisson C, Larouche D, Tanguay RM, Blouin R, Germain L 2010. The small heat-shock protein Hsp27 undergoes ERK-dependent phosphorylation and redistribution to the cytoskeleton in response to dual leucine zipper–bearing kinase expression. J. Investig. Dermatol. 130:74–85
     [Google Scholar]
  84. Sakuma H, Ikeda A, Oka S, Kozutsumi Y, Zanetta JP, Kawasaki T 1997. Molecular cloning and functional expression of a cDNA encoding a new member of mixed lineage protein kinase from human brain. J. Biol. Chem. 272:28622–29
     [Google Scholar]
  85. Schaefer AM, Hadwiger GD, Nonet ML 2000. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26:345–56
     [Google Scholar]
  86. Sheu ML, Chiang CY, Su HL, Chen CJ, Sheehan J, Pan HC 2018. Intrathecal injection of dual zipper kinase shRNA alleviating the neuropathic pain in a chronic constrictive nerve injury model. Int. J. Mol. Sci. 19:E2421
     [Google Scholar]
  87. 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 74:1015–22
     [Google Scholar]
  88. Simard-Bisson C, Bidoggia J, Larouche D, Guerin SL, Blouin R et al. 2017. A role for DLK in microtubule reorganization to the cell periphery and in the maintenance of desmosomal and tight junction integrity. J. Investig. Dermatol. 137:132–41
     [Google Scholar]
  89. Siu M, Sengupta Ghosh A, Lewcock JW 2018. Dual leucine zipper kinase inhibitors for the treatment of neurodegeneration. J. Med. Chem. 61:8078–87
     [Google Scholar]
  90. Smith PD, Sun F, Park KK, Cai B, Wang C et al. 2009. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64:617–23
     [Google Scholar]
  91. Soares L, Parisi M, Bonini NM 2014. Axon injury and regeneration in the adult Drosophila. Sci. Rep 4:6199
     [Google Scholar]
  92. Song Y, Ori-McKenney KM, Zheng Y, Han C, Jan LY, Jan YN 2012. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev 26:1612–25
     [Google Scholar]
  93. Stahnke MJ, Dickel C, Schroder S, Kaiser D, Blume R et al. 2014. Inhibition of human insulin gene transcription and MafA transcriptional activity by the dual leucine zipper kinase. Cell. Signal. 26:1792–99
     [Google Scholar]
  94. Stone MC, Albertson RM, Chen L, Rolls MM 2014. Dendrite injury triggers DLK-independent regeneration. Cell Rep 6:247–53
     [Google Scholar]
  95. Stone MC, Nguyen MM, Tao J, Allender DL, Rolls MM 2010. Global up-regulation of microtubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol. Biol. Cell 21:767–77
     [Google Scholar]
  96. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J et al. 1993. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. PNAS 90:1977–81
     [Google Scholar]
  97. Suenaga J, Cui DF, Yamamoto I, Ohno S, Hirai S 2006. Developmental changes in the expression pattern of the JNK activator kinase MUK/DLK/ZPK and active JNK in the mouse cerebellum. Cell Tissue Res 325:189–95
     [Google Scholar]
  98. Summers DW, Milbrandt J, DiAntonio A 2018. Palmitoylation enables MAPK-dependent proteostasis of axon survival factors. PNAS 115:E8746–54
     [Google Scholar]
  99. Sun F, Park KK, Belin S, Wang D, Lu T et al. 2011. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 480:372–75
     [Google Scholar]
  100. Sun H, Tawa G, Wallqvist A 2012. Classification of scaffold-hopping approaches. Drug Discov. Today 17:310–24
     [Google Scholar]
  101. Suzich JB, Cliffe AR. 2018. Strength in diversity: understanding the pathways to herpes simplex virus reactivation. Virology 522:81–91
     [Google Scholar]
  102. Tedeschi A, Bradke F. 2013. The DLK signalling pathway—a double-edged sword in neural development and regeneration. EMBO Rep 14:605–14
     [Google Scholar]
  103. Valakh V, Frey E, Babetto E, Walker LJ, DiAntonio A 2015. Cytoskeletal disruption activates the DLK/JNK pathway, which promotes axonal regeneration and mimics a preconditioning injury. Neurobiol. Dis. 77:13–25
     [Google Scholar]
  104. Valakh V, Walker LJ, Skeath JB, DiAntonio A 2013. Loss of the spectraplakin short stop activates the DLK injury response pathway in Drosophila. J. Neurosci 33:17863–73
     [Google Scholar]
  105. van der Vaart A, Rademakers S, Jansen G 2015. DLK-1/p38 MAP kinase signaling controls cilium length by regulating RAB-5 mediated endocytosis in Caenorhabditis elegans. PLOS Genet 11:e1005733
     [Google Scholar]
  106. Wallbach M, Duque Escobar J, Babaeikelishomi R, Stahnke MJ, Blume R et al. 2016. Distinct functions of the dual leucine zipper kinase depending on its subcellular localization. Cell. Signal. 28:272–83
     [Google Scholar]
  107. Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS 2000. Highwire regulates synaptic growth in Drosophila. Neuron 26:313–29
     [Google Scholar]
  108. Wang X, Kim JH, Bazzi M, Robinson S, Collins CA, Ye B 2013. Bimodal control of dendritic and axonal growth by the dual leucine zipper kinase pathway. PLOS Biol 11:e1001572
     [Google Scholar]
  109. Watkins TA, Wang B, Huntwork-Rodriguez S, Yang J, Jiang Z et al. 2013. DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. PNAS 110:4039–44
     [Google Scholar]
  110. Welsbie DS, Mitchell KL, Jaskula-Ranga V, Sluch VM, Yang Z et al. 2017. Enhanced functional genomic screening identifies novel mediators of dual leucine zipper kinase–dependent injury signaling in neurons. Neuron 94:1142–54.e6
     [Google Scholar]
  111. Welsbie DS, Yang Z, Ge Y, Mitchell KL, Zhou X et al. 2013. Functional genomic screening identifies dual leucine zipper kinase as a key mediator of retinal ganglion cell death. PNAS 110:4045–50
     [Google Scholar]
  112. Wilcox CL, Johnson EM Jr 1987. Nerve growth factor deprivation results in the reactivation of latent herpes simplex virus in vitro. J. Virol. 61:2311–15
     [Google Scholar]
  113. Wlaschin JJ, Gluski JM, Nguyen E, Silberberg H, Thompson JH et al. 2018. Dual leucine zipper kinase is required for mechanical allodynia and microgliosis after nerve injury. eLife 7:e33910
     [Google Scholar]
  114. Wu CC, Wu HJ, Wang CH, Lin CH, Hsu SC et al. 2015. Akt suppresses DLK for maintaining self-renewal of mouse embryonic stem cells. Cell Cycle 14:1207–17
     [Google Scholar]
  115. Wu Z, Ghosh-Roy A, Yanik MF, Zhang JZ, Jin Y, Chisholm AD 2007. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. PNAS 104:15132–37
     [Google Scholar]
  116. 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. 191:211–23
     [Google Scholar]
  117. Yan D, Jin Y. 2012. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76:534–48
     [Google Scholar]
  118. 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 138:1005–18
     [Google Scholar]
  119. Yang J, Wu Z, Renier N, Simon DJ, Uryu K et al. 2015. Pathological axonal death through a MAPK cascade that triggers a local energy deficit. Cell 160:161–76
     [Google Scholar]
  120. Yanik MF, Cinar H, Cinar HN, Chisholm AD, Jin Y, Ben-Yakar A 2004. Neurosurgery: functional regeneration after laser axotomy. Nature 432:822
     [Google Scholar]
  121. Yin C, Huang GF, Sun XC, Guo Z, Zhang JH 2017. DLK silencing attenuated neuron apoptosis through JIP3/MA2K7/JNK pathway in early brain injury after SAH in rats. Neurobiol. Dis. 103:133–43
     [Google Scholar]
  122. Zhen M, Huang X, Bamber B, Jin Y 2000. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26:331–43
     [Google Scholar]
  123. Chen CH, Sung CS, Huang SY, Feng CW, Hung HCet al 2016. The role of the PI3K/Akt/mTOR pathway in glial scar formation following spinal cord injury. Exp. Neurol 278:27–41
     [Google Scholar]
  124. Herrmann JE, Imura T, Song B, Qi J, Ao Yet al 2008. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J. Neurosci 28:7231–43
     [Google Scholar]
  125. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki Tet al 2006. Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med 12:829–34
     [Google Scholar]
  126. Shin JE, Ha H, Kim YK, Cho Y, DiAntonio A 2019. DLK regulates a distinctive transcriptional regeneration program after peripheral nerve injury. Neurobiol. Dis 127:178–92 This study examines transcriptome changes following periphery nerve injury. They show that DLK is required for inducing expression of pro-regenerative genes, as well as ion transport and immune response genes .
     [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100617-062644
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Multitasking: Dual Leucine Zipper–Bearing Kinases in Neuronal Development and Stress Management
Annual Review of Cell and Developmental Biology 35, 501 (2019); https://doi.org/10.1146/annurev-cellbio-100617-062644
/content/journals/10.1146/annurev-cellbio-100617-062644
/content/journals/10.1146/annurev-cellbio-100617-062644
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  • Article Type: Review Article

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