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VANG-1 and PRKL-1 Cooperate to Negatively Regulate Neurite Formation in


Neuritogenesis is a critical early step in the development and maturation of neurons and neuronal circuits. While extracellular directional cues are known to specify the site and orientation of nascent neurite formation in vivo, little is known about the genetic pathways that block inappropriate neurite emergence in order to maintain proper neuronal polarity. Here we report that the Caenorhabditis elegans orthologues of Van Gogh (vang-1), Prickle (prkl-1), and Dishevelled (dsh-1), core components of planar cell polarity (PCP) signaling, are required in a subset of peripheral motor neurons to restrict neurite emergence to a specific organ axis. In loss-of-function mutants, neurons display supernumerary neurites that extend inappropriately along the orthogonal anteroposterior (A/P) body axis. We show that autonomous and non-autonomous gene activities are required early and persistently to inhibit the formation or consolidation of growth cone protrusions directed away from organ precursor cells. Furthermore, prkl-1 overexpression is sufficient to suppress neurite formation and reorient neuronal polarity in a vang-1– and dsh-1–dependent manner. Our findings suggest a novel role for a PCP–like pathway in maintaining polarized neuronal morphology by inhibiting neuronal responses to extrinsic or intrinsic cues that would otherwise promote extraneous neurite formation.


Vyšlo v časopise: VANG-1 and PRKL-1 Cooperate to Negatively Regulate Neurite Formation in. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002257
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002257

Souhrn

Neuritogenesis is a critical early step in the development and maturation of neurons and neuronal circuits. While extracellular directional cues are known to specify the site and orientation of nascent neurite formation in vivo, little is known about the genetic pathways that block inappropriate neurite emergence in order to maintain proper neuronal polarity. Here we report that the Caenorhabditis elegans orthologues of Van Gogh (vang-1), Prickle (prkl-1), and Dishevelled (dsh-1), core components of planar cell polarity (PCP) signaling, are required in a subset of peripheral motor neurons to restrict neurite emergence to a specific organ axis. In loss-of-function mutants, neurons display supernumerary neurites that extend inappropriately along the orthogonal anteroposterior (A/P) body axis. We show that autonomous and non-autonomous gene activities are required early and persistently to inhibit the formation or consolidation of growth cone protrusions directed away from organ precursor cells. Furthermore, prkl-1 overexpression is sufficient to suppress neurite formation and reorient neuronal polarity in a vang-1– and dsh-1–dependent manner. Our findings suggest a novel role for a PCP–like pathway in maintaining polarized neuronal morphology by inhibiting neuronal responses to extrinsic or intrinsic cues that would otherwise promote extraneous neurite formation.


Zdroje

1. PolleuxFSniderW 2010 Initiating and growing an axon. Cold Spring Harb Perspect Biol 2 a001925

2. TahirovicSBradkeF 2009 Neuronal polarity. Cold Spring Harb Perspect Biol 1 a001644

3. AdlerCEFetterRDBargmannCI 2006 UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci 9 511 518

4. QuinnCCPfeilDSChenEStovallELHardenMV 2006 UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr Biol 16 845 853

5. SalinasPCZouY 2008 Wnt signaling in neural circuit assembly. Annu Rev Neurosci 31 339 358

6. PanCLHowellJEClarkSGHilliardMCordesS 2006 Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell 10 367 377

7. SongSZhangBSunHLiXXiangY 2010 A Wnt-Frz/Ror-Dsh pathway regulates neurite outgrowth in Caenorhabditis elegans. PLoS Genet 6 e1001056 doi:10.1371/journal.pgen.1001056

8. HilliardMABargmannCI 2006 Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev Cell 10 379 390

9. KlassenMPShenK 2007 Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell 130 704 716

10. BejsovecA 2005 Wnt pathway activation: new relations and locations. Cell 120 11 14

11. VladarEKAnticDAxelrodJD 2009 Planar Cell Polarity Signaling: The Developing Cell's Compass. Cold Spring Harb Perspect Biol 1 a002964

12. WuJMlodzikM 2009 A quest for the mechanism regulating global planar cell polarity of tissues. Trends Cell Biol 19 295 305

13. ZallenJA 2007 Planar polarity and tissue morphogenesis. Cell 129 1051 1063

14. MontcouquiolMRachelRALanfordPJCopelandNGJenkinsNA 2003 Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423 173 177

15. GongYMoCFraserSE 2004 Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430 689 693

16. DarkenRSScolaAMRakemanASDasGMlodzikM 2002 The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J 21 976 985

17. JessenJRTopczewskiJBinghamSSepichDSMarlowF 2002 Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol 4 610 615

18. ParkMMoonRT 2002 The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat Cell Biol 4 20 25

19. FenstermakerAGPrasadAABecharaAAdolfsYTissirF 2010 Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J Neurosci 30 16053 16064

20. ShaferBOnishiKLoCColakogluGZouY 2011 Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Dev Cell 20 177 191

21. WaggonerLEZhouGTSchaferRWSchaferWR 1998 Control of alternative behavioral states by serotonin in Caenorhabditis elegans. Neuron 21 203 214

22. WhiteJGSouthgateEThomsonJNBrennerS 1976 The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275 327 348

23. LiCChalfieM 1990 Organogenesis in C. elegans: positioning of neurons and muscles in the egg-laying system. Neuron 4 681 695

24. FeinbergEHVanhovenMKBendeskyAWangGFetterRD 2008 GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57 353 363

25. ColavitaATessier-LavigneM 2003 A Neurexin-related protein, BAM-2, terminates axonal branches in C. elegans. Science 302 293 296

26. Habibi-BabadiNSuAde CarvalhoCEColavitaA 2010 The N-glycanase png-1 acts to limit axon branching during organ formation in Caenorhabditis elegans. J Neurosci 30 1766 1776

27. HoffmannMSegbertCHelbigGBossingerO 2010 Intestinal tube formation in Caenorhabditis elegans requires vang-1 and egl-15 signaling. Dev Biol 339 268 279

28. EisenmannDM 2005 Wnt signaling. WormBook 1 17

29. GreenJLInoueTSternbergPW 2008 Opposing Wnt pathways orient cell polarity during organogenesis. Cell 134 646 656

30. GleasonJESzyleykoEAEisenmannDM 2006 Multiple redundant Wnt signaling components function in two processes during C. elegans vulval development. Dev Biol 298 442 457

31. DuerrJSFrisbyDLGaskinJDukeAAsermelyK 1999 The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 19 72 84

32. GuptaBPSternbergPW 2002 Tissue-specific regulation of the LIM homeobox gene lin-11 during development of the Caenorhabditis elegans egg-laying system. Dev Biol 247 102 115

33. LickteigKMDuerrJSFrisbyDLHallDHRandJB 2001 Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/groucho in Caenorhabditis elegans cholinergic motor neurons. J Neurosci 21 2001 2014

34. KoppenMSimskeJSSimsPAFiresteinBLHallDH 2001 Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 3 983 991

35. LiuZKirchSAmbrosV 1995 The Caenorhabditis elegans heterochronic gene pathway controls stage-specific transcription of collagen genes. Development 121 2471 2478

36. StruttHStruttD 2009 Asymmetric localisation of planar polarity proteins: Mechanisms and consequences. Semin Cell Dev Biol 20 957 963

37. Sharma-KishoreRWhiteJGSouthgateEPodbilewiczB 1999 Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. Development 126 691 699

38. TreeDRShulmanJMRoussetRScottMPGubbD 2002 Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109 371 381

39. BastockRStruttHStruttD 2003 Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130 3007 3014

40. JennyADarkenRSWilsonPAMlodzikM 2003 Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22 4409 4420

41. SweedeMAnkemGChutvirasakulBAzurmendiHFChbeirS 2008 Structural and membrane binding properties of the prickle PET domain. Biochemistry 47 13524 13536

42. GrosJSerralboOMarcelleC 2009 WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 457 589 593

43. TavernarakisNWangSLDorovkovMRyazanovADriscollM 2000 Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nat Genet 24 180 183

44. WallingfordJBRowningBAVogeliKMRothbacherUFraserSE 2000 Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405 81 85

45. Ybot-GonzalezPSaveryDGerrelliDSignoreMMitchellCE 2007 Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134 789 799

46. SeifertJRMlodzikM 2007 Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8 126 138

47. ChenWSAnticDMatisMLoganCYPovelonesM 2008 Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133 1093 1105

48. WuJMlodzikM 2008 The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev Cell 15 462 469

49. ParraLMZouY 2010 Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat Neurosci 13 29 35

50. SteinETessier-LavigneM 2001 Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291 1928 1938

51. KishidaSYamamotoHKikuchiA 2004 Wnt-3a and Dvl induce neurite retraction by activating Rho-associated kinase. Mol Cell Biol 24 4487 4501

52. BitoHFuruyashikiTIshiharaHShibasakiYOhashiK 2000 A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26 431 441

53. SassiHERenihanSSpenceAMCooperstockRL 2005 Gene CATCHR–gene cloning and tagging for Caenorhabditis elegans using yeast homologous recombination: a novel approach for the analysis of gene expression. Nucleic Acids Res 33 e163

54. TabaraHSarkissianMKellyWGFleenorJGrishokA 1999 The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99 123 132

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