RPM-1 Uses Both Ubiquitin Ligase and Phosphatase-Based Mechanisms to Regulate DLK-1 during Neuronal Development

1. JinY, GarnerCC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24 : 237–262.

2. O'DonnellM, ChanceRK, BashawGJ (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32 : 383–412.

3. Kolodkin AL, Tessier-Lavigne M (2011) Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol 3 . doi:10.1101/cshperspect.a001727

4. AlsinaB, VuT, Cohen-CoryS (2001) Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat Neurosci 4 : 1093–1101.

5. Ben FredjN, HammondS, OtsunaH, ChienCB, BurroneJ, et al. (2010) Synaptic activity and activity-dependent competition regulates axon arbor maturation, growth arrest, and territory in the retinotectal projection. J Neurosci 30 : 10939–10951.

6. MeyerMP, SmithSJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26 : 3604–3614.

7. RuthazerES, LiJ, ClineHT (2006) Stabilization of axon branch dynamics by synaptic maturation. J Neurosci 26 : 3594–3603.

8. AhmariSE, BuchananJ, SmithSJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3 : 445–451.

9. FriedmanHV, BreslerT, GarnerCC, ZivNE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27 : 57–69.

10. YoshiharaM, RheubenMB, KidokoroY (1997) Transition from growth cone to functional motor nerve terminal in Drosophila embryos. J Neurosci 17 : 8408–8426.

11. ZitoK, ParnasD, FetterRD, IsacoffEY, GoodmanCS (1999) Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22 : 719–729.

12. ZhaoH, NonetML (2000) A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction. Development 127 : 1253–1266.

13. BudnikV, ZhongY, WuCF (1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci 10 : 3754–3768.

14. HuaJY, SmearMC, BaierH, SmithSJ (2005) Regulation of axon growth in vivo by activity-based competition. Nature 434 : 1022–1026.

15. ShenK, CowanCW (2010) Guidance molecules in synapse formation and plasticity. Cold Spring Harb Perspect Biol 2: a001842.

16. Colon-RamosDA, MargetaMA, ShenK (2007) Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318 : 103–106.

17. KlassenMP, ShenK (2007) Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell 130 : 704–716.

18. PoonVY, KlassenMP, ShenK (2008) UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature 455 : 669–673.

19. HedgecockEM, CulottiJG, HallDH (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4 : 61–85.

20. LiH, KulkarniG, WadsworthWG (2008) RPM-1, a Caenorhabditis elegans protein that functions in presynaptic differentiation, negatively regulates axon outgrowth by controlling SAX-3/robo and UNC-5/UNC5 activity. J Neurosci 28 : 3595–3603.

21. PoMD, HwangC, ZhenM (2010) PHRs: bridging axon guidance, outgrowth and synapse development. Curr Opin Neurobiol 20 : 100–107.

22. LewcockJW, GenoudN, LettieriK, PfaffSL (2007) The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56 : 604–620.

23. BloomAJ, MillerBR, SanesJR, DiAntonioA (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.

24. BurgessRW, PetersonKA, JohnsonMJ, RoixJJ, WelshIC, et al. (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 : 1096–1105.

25. D'SouzaJ, HendricksM, Le GuyaderS, SubburajuS, GrunewaldB, et al. (2005) Formation of the retinotectal projection requires Esrom, an ortholog of PAM (protein associated with Myc). Development 132 : 247–256.

26. HendricksM, JesuthasanS (2009) PHR regulates growth cone pausing at intermediate targets through microtubule disassembly. J Neurosci 29 : 6593–6598.

27. ShinJE, DiAntonioA (2011) Highwire regulates guidance of sister axons in the Drosophila mushroom body. J Neurosci 31 : 17689–17700.

28. CulicanSM, BloomAJ, WeinerJA, DiAntonioA (2009) Phr1 regulates retinogeniculate targeting independent of activity and ephrin-A signalling. Mol Cell Neurosci 41 : 304–312.

29. SchaeferAM, HadwigerGD, NonetML (2000) rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26 : 345–356.

30. KimJH, WangX, CoolonR, YeB (2013) Dscam expression levels determine presynaptic arbor sizes in Drosophila sensory neurons. Neuron 78 : 827–838.

31. ZhenM, HuangX, BamberB, JinY (2000) Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26 : 331–343.

32. WanHI, DiAntonioA, FetterRD, BergstromK, StraussR, et al. (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26 : 313–329.

33. HammarlundM, NixP, HauthL, JorgensenEM, BastianiM (2009) Axon regeneration requires a conserved MAP kinase pathway. Science 323 : 802–806.

34. XiongX, WangX, EwanekR, BhatP, DiantonioA, et al. (2010) Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J Cell Biol 191 : 211–223.

35. XiongX, HaoY, SunK, LiJ, LiX, et al. (2012) The Highwire ubiquitin ligase promotes axonal degeneration by tuning levels of Nmnat protein. PLoS Biol 10: e1001440.

36. BabettoE, BeirowskiB, RusslerEV, MilbrandtJ, DiAntonioA (2013) The Phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell Rep 3 : 1422–1429.

37. HuangC, ZhengX, ZhaoH, LiM, WangP, et al. (2012) A permissive role of mushroom body alpha/beta core neurons in long-term memory consolidation in Drosophila. Curr Biol 22 : 1981–1989.

38. NakataK, AbramsB, GrillB, GoncharovA, HuangX, 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 : 407–420.

39. GrillB, BienvenutWV, BrownHM, AckleyBD, QuadroniM, et al. (2007) C. elegans RPM-1 Regulates Axon Termination and Synaptogenesis through the Rab GEF GLO-4 and the Rab GTPase GLO-1. Neuron 55 : 587–601.

40. YanD, WuZ, ChisholmAD, JinY (2009) The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138 : 1005–1018.

41. CollinsCA, WairkarYP, JohnsonSL, DiantonioA (2006) Highwire Restrains Synaptic Growth by Attenuating a MAP Kinase Signal. Neuron 51 : 57–69.

42. ScholichK, PierreS, PatelTB (2001) Protein associated with Myc (PAM) is a potent inhibitor of adenylyl cyclases. J Biol Chem 276 : 47583–47589.

43. PierreSC, HauslerJ, BirodK, GeisslingerG, ScholichK (2004) PAM mediates sustained inhibition of cAMP signaling by sphingosine-1-phosphate. EMBO J 23 : 3031–3040.

44. TianX, LiJ, ValakhV, DiAntonioA, WuC (2011) Drosophila Rae1 controls the abundance of the ubiquitin ligase Highwire in post-mitotic neurons. Nat Neurosci 14 : 1267–1275.

45. GrillB, ChenL, TulgrenED, BakerST, BienvenutW, et al. (2012) RAE-1, a Novel PHR Binding Protein, Is Required for Axon Termination and Synapse Formation in Caenorhabditis elegans. J Neurosci 32 : 2628–2636.

46. MurthyV, HanS, BeauchampRL, SmithN, HaddadLA, et al. (2004) Pam and its ortholog highwire interact with and may negatively regulate the TSC1.TSC2 complex. J Biol Chem 279 : 1351–1358.

47. HollandS, CosteO, ZhangDD, PierreSC, GeisslingerG, et al. (2011) The ubiquitin ligase MYCBP2 regulates transient receptor potential vanilloid receptor 1 (TRPV1) internalization through inhibition of p38 MAPK signaling. J Biol Chem 286 : 3671–3680.

48. ParkEC, GlodowskiDR, RongoC (2009) The ubiquitin ligase RPM-1 and the p38 MAPK PMK-3 regulate AMPA receptor trafficking. PLoS One 4: e4284.

49. HanS, WittRM, SantosTM, PolizzanoC, SabatiniBL, et al. (2008) Pam (Protein associated with Myc) functions as an E3 ubiquitin ligase and regulates TSC/mTOR signaling. Cell Signal 20 : 1084–1091.

50. PierreS, MaeurerC, CosteO, BeckerW, SchmidtkoA, et al. (2008) Toponomics analysis of functional interactions of the ubiquitin ligase PAM (Protein Associated with Myc) during spinal nociceptive processing. Mol Cell Proteomics 7 : 2475–2485.

51. LiaoEH, HungW, AbramsB, ZhenM (2004) An SCF-like ubiquitin ligase complex that controls presynaptic differentiation. Nature 430 : 345–350.

52. WuC, DanielsRW, DiAntonioA (2007) DFsn collaborates with Highwire to down-regulate the Wallenda/DLK kinase and restrain synaptic terminal growth. Neural Dev 2 : 16.

53. SaigaT, FukudaT, MatsumotoM, TadaH, OkanoHJ, et al. (2009) Fbxo45 forms a novel ubiquitin ligase complex and is required for neuronal development. Mol Cell Biol 29 : 3529–3543.

54. Huntwork-RodriguezS, WangB, WatkinsT, GhoshAS, PozniakCD, et al. (2013) JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J Cell Biol 202 : 747–763.

55. HiraiS, Cui deF, MiyataT, OgawaM, KiyonariH, 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 : 11992–12002.

56. WangX, KimJH, BazziM, RobinsonS, CollinsCA, et al. (2013) Bimodal control of dendritic and axonal growth by the dual leucine zipper kinase pathway. PLoS Biol 11: e1001572.

57. EtoK, KawauchiT, OsawaM, TabataH, NakajimaK (2010) Role of dual leucine zipper-bearing kinase (DLK/MUK/ZPK) in axonal growth. Neurosci Res 66 : 37–45.

58. ItohA, HoriuchiM, BannermanP, PleasureD, ItohT (2009) Impaired regenerative response of primary sensory neurons in ZPK/DLK gene-trap mice. Biochem Biophys Res Commun 383 : 258–262.

59. ShinJE, ChoY, BeirowskiB, MilbrandtJ, CavalliV, et al. (2012) Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74 : 1015–1022.

60. WatkinsTA, WangB, Huntwork-RodriguezS, YangJ, JiangZ, et al. (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.

61. MillerBR, PressC, DanielsRW, SasakiY, MilbrandtJ, et al. (2009) A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat Neurosci 12 : 387–389.

62. GhoshAS, WangB, PozniakCD, ChenM, WattsRJ, et al. (2011) DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J Cell Biol 194 : 751–764.

63. MataM, MerrittSE, FanG, YuGG, HolzmanLB (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 : 16888–16896.

64. DaviauA, Di FruscioM, BlouinR (2009) The mixed-lineage kinase DLK undergoes Src-dependent tyrosine phosphorylation and activation in cells exposed to vanadate or platelet-derived growth factor (PDGF). Cell Signal 21 : 577–587.

65. NihalaniD, MeyerD, PajniS, HolzmanLB (2001) Mixed lineage kinase-dependent JNK activation is governed by interactions of scaffold protein JIP with MAPK module components. EMBO J 20 : 3447–3458.

66. ValakhV, WalkerLJ, SkeathJB, DiantonioA (2013) Loss of the Spectraplakin Short Stop Activates the DLK Injury Response Pathway in Drosophila. J Neurosci 33 : 17863–17873.

67. Ghosh-RoyA, WuZ, GoncharovA, JinY, ChisholmAD (2010) Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J Neurosci 30 : 3175–3183.

68. YanD, JinY (2012) Regulation of DLK-1 Kinase Activity by Calcium-Mediated Dissociation from an Inhibitory Isoform. Neuron 76 : 534–548.

69. SternA, PrivmanE, RasisM, LaviS, PupkoT (2007) Evolution of the metazoan protein phosphatase 2C superfamily. J Mol Evol 64 : 61–70.

70. JacksonMD, FjeldCC, DenuJM (2003) Probing the function of conserved residues in the serine/threonine phosphatase PP2Calpha. Biochemistry 42 : 8513–8521.

71. TakekawaM, MaedaT, SaitoH (1998) Protein phosphatase 2Calpha inhibits the human stress-responsive p38 and JNK MAPK pathways. EMBO J 17 : 4744–4752.

72. DuH, ChalfieM (2001) Genes regulating touch cell development in Caenorhabditis elegans. Genetics 158 : 197–207.

73. ChalfieM, ThomsonJN (1979) Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J Cell Biol 82 : 278–289.

74. Ch'ngQ, WilliamsL, LieYS, SymM, WhangboJ, et al. (2003) Identification of genes that regulate a left-right asymmetric neuronal migration in Caenorhabditis elegans. Genetics 164 : 1355–1367.

75. TulgrenED, BakerST, RappL, GurneyAM, GrillB (2011) PPM-1, a PP2Calpha/beta phosphatase, regulates axon termination and synapse formation in Caenorhabditis elegans. Genetics 189 : 1297–1307.

76. HanadaM, Ninomiya-TsujiJ, KomakiK, OhnishiM, KatsuraK, et al. (2001) Regulation of the TAK1 signaling pathway by protein phosphatase 2C. J Biol Chem 276 : 5753–5759.

77. MeskieneI, BogreL, GlaserW, BalogJ, BrandstotterM, et al. (1998) MP2C, a plant protein phosphatase 2C, functions as a negative regulator of mitogen-activated protein kinase pathways in yeast and plants. Proc Natl Acad Sci U S A 95 : 1938–1943.

78. BarilC, SahmiM, Ashton-BeaucageD, StronachB, TherrienM (2009) The PP2C Alphabet is a negative regulator of stress-activated protein kinase signaling in Drosophila. Genetics 181 : 567–579.

79. NguyenAN, ShiozakiK (1999) Heat-shock-induced activation of stress MAP kinase is regulated by threonine -⁠ and tyrosine-specific phosphatases. Genes Dev 13 : 1653–1663.

80. AbramsB, GrillB, HuangX, JinY (2008) Cellular and molecular determinants targeting the Caenorhabditis elegans PHR protein RPM-1 to perisynaptic regions. Dev Dyn 237 : 630–639.

81. SunH, CharlesCH, LauLF, TonksNK (1993) MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75 : 487–493.

82. FurukawaT, ItohM, KruegerNX, StreuliM, SaitoH (1994) Specific interaction of the CD45 protein-tyrosine phosphatase with tyrosine-phosphorylated CD3 zeta chain. Proc Natl Acad Sci U S A 91 : 10928–10932.

83. HallamSJ, JinY (1998) lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans. Nature 395 : 78–82.

84. GuoQ, XieJ, DangCV, LiuET, BishopJM (1998) Identification of a large Myc-binding protein that contains RCC1-like repeats. Proc Natl Acad Sci U S A 95 : 9172–9177.

85. NixP, HisamotoN, MatsumotoK, BastianiM (2011) Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. Proc Natl Acad Sci U S A 108 : 10738–10743.

86. SakumaH, IkedaA, OkaS, KozutsumiY, ZanettaJP, et al. (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 : 28622–28629.

87. HolzmanLB, MerrittSE, FanG (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 : 30808–30817.

88. AitkenA, CohenP, SantikarnS, WilliamsDH, CalderAG, et al. (1982) Identification of the NH2-terminal blocking group of calcineurin B as myristic acid. FEBS Lett 150 : 314–318.

89. AlonsoA, NarisawaS, BogetzJ, TautzL, HadzicR, et al. (2004) VHY, a novel myristoylated testis-restricted dual specificity protein phosphatase related to VHX. J Biol Chem 279 : 32586–32591.

90. SchwertassekU, BuckleyDA, XuCF, LindsayAJ, McCaffreyMW, et al. (2010) Myristoylation of the dual-specificity phosphatase c-JUN N-terminal kinase (JNK) stimulatory phosphatase 1 is necessary for its activation of JNK signaling and apoptosis. FEBS J 277 : 2463–2473.

91. ChidaT, AndoM, MatsukiT, MasuY, NagauraY, et al. (2013) N-myristoylation is essential for protein phosphatases PPM1A and PPM1B to dephosphorylate their physiological substrates in cells. Biochem J 449 : 741–749.

92. FengJ, ZhaoJ, LiJ, ZhangL, JiangL (2010) Functional characterization of the PP2C phosphatase CaPtc2p in the human fungal pathogen Candida albicans. Yeast 27 : 753–764.

93. SahaS, WolozinB (2011) A simple, quantitative immunoblot protocol using equal numbers of nematodes. Worm Breeder's Gazette 19 : 6–7.