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Short Communications

The unc-53 gene negatively regulates rac GTPases to inhibit unc-5 activity during Distal tip cell migrations in C. elegans

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Pages 195-203 | Received 28 Mar 2017, Accepted 19 Jun 2017, Published online: 26 Oct 2017

References

  • Bashaw GJ, Klein R. Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2010; 2:a001941; PMID:20452961; https://doi.org/10.1101/cshperspect.a001941
  • Reddien PW, Horvitz HR. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol 2000; 2:131-6; PMID:10707082; https://doi.org/10.1038/35004000
  • Dickson BJ. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 2001; 11(1):103-10; PMID:11179879; https://doi.org/10.1016/S0959-4388(00)00180-X
  • Lundquist EA. Rac proteins and control of axon development. Curr Opin Neurobiol 2003; 13:384-90; PMID:12850224; https://doi.org/10.1016/S0959-4388(03)00071-0
  • Bouquet C, Nothias F. Molecular mechanisms of axonal growth. Adv Exp Med Biol 2007; 621:1-16; PMID:18269207
  • Hall A, Lalli G. Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2010; 2:a001818; PMID:20182621; https://doi.org/10.1101/cshperspect.a001818
  • Stringham E, Schmidt KL. Navigating the cell UNC-53 and the navigators, a family of cytoskeletal regulators with multiple roles in cell migration, outgrowth and trafficking. Cell Adhes Migr 2009; 3(4):342-6; https://doi.org/10.4161/cam.3.4.9451
  • Pandey A, Pandey GK. The UNC-53 mediated interactome: Analysis of its role in generation of C. elegans connectome. SpringerBriefs Neuroscience 2014
  • Stringham E, Pujol N, Vanderchove J, Bogaert T. unc-53 controls longitudinal migration in C. elegans. Development 2002; 129:3367-79; PMID:12091307
  • Schmidt KL, Marcus-Gueret N, Adeleye A, Webber J, Baillie D, Stringham EG. The cell migration molecule UNC-53/NAV2 is linked to the ARP2/3 complex by ABI-1. Development 2009; 136:563-74; PMID:19168673; https://doi.org/10.1242/dev.016816
  • Marcus-Gueret N, Schmidt KL, Stringham EG. Distinct cell guidance pathways controlled by the Rac and Rho GEF domains of UNC-73/TRIO in Caenorhabditis elegans. Genetics 2012; 190:129-42; PMID:21996675; https://doi.org/10.1534/genetics.111.134429
  • McShea MA, Schmidt KL, Dubuke ML, Baldiga CE, Sullender ME, Reis AL, Zhang S, O'Toole SM, Jeffers MC, Warden RM, et al. Abelson interactor-1 (ABI-1) interacts with MRL adaptor protein MIG-10 and is required in guided cell migrations and process outgrowth in C. elegans. Dev Biol 2013; 373(1):1-13; PMID:23022657; https://doi.org/10.1016/j.ydbio.2012.09.017
  • Marzinke MA, Mavencamp T, Duratinsky J, Clagett-Dame M. 14-3-3ϵ and NAV2 interact to regulate neurite outgrowth and axon elongation. Arch Biochem Biophys 2013; 540(1-2):94-100; PMID:24161943; https://doi.org/10.1016/j.abb.2013.10.012
  • Abe T, Yamazaki D, Murakami S, Hiroi M, Yohei Nitta, Yuko Maeyama, Tabata T. The NAV2 homolog Sickie regulates F-actin-mediated axonal growth in Drosophila mushroom body neurons via the noncanonical Rac-Cofilin pathway. Development 2014; 141:4716-28; PMID:25411210; https://doi.org/10.1242/dev.113308
  • Kligys K, Yao J, Yu D, Jones JCR. 14-3-3zeta/tau heterodimers regulate Slingshot activity in migrating keratinocytes. Biochem Biophys Res Commun 2009; 383:450-4; PMID:19371722; https://doi.org/10.1016/j.bbrc.2009.04.031
  • Cram EJ, Shang H, Schwarzbauer JE. A systematic RNA interference screen reveals a cell migration gene network in C. elegans. J Cell Sci 2006; 119:4811-8; PMID:17090602; https://doi.org/10.1242/jcs.03274
  • Nishiwaki K. Mutations affecting symmetrical migration of Distal tip cells in Caenorhabditis elegans. Genetics 1999; 152:985-97; PMID:10388818
  • Wong M, Schwarzbauer JE. Gonad morphogenesis and Distal tip cell migration in the Caenorhabditis elegans hermaphrodite. Wiley Interdiscip Rev Dev Biol 2012; 1:519-31
  • Lundquist EA, Reddien PW, Hartweig E, Horvitz HR, Bargmann CI. Three C. elegans Rac proteins and several Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 2001; 128:4475-88; PMID:23559979; https://doi.org/10.1002/wdev.45
  • Wu YC, Horvitz HR. C. elegans phagocytosis and cell migration protein CED-5 is similar to human DOCK180. Nature 1998; 392:501-4; PMID:9548255; https://doi.org/10.1038/32195
  • Gumienny TL, Brugnera E, Tosello-Trampnt AC, Kinchen JM, Haney LB, Nishiwaki K, Walk SF, Nemergut ME, Macara IG, Francis R, et al. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, required for phagocytosis and cell migration. Cell 2001; 107:27-41; PMID:11595183; https://doi.org/10.1016/S0092-8674(01)00520-7
  • Cabello J, Neukomm LJ, Gunesdogan U, Burkart K, Charetle SJ, Lochnit G, Hengartner MO, Schnabel R. The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. Plos Biol 2010; 8(2):e1000297; PMID:20126385; https://doi.org/10.1371/journal.pbio.1000297
  • Hurwitz ME, Vanderzalm PJ, Bloom L, Goldman J, Garriga G, Horvitz HR. Abl kinase inhibits the engulfment of apoptotic [corrected] cells in Caenorhabditis elegans. PLoS Biol 2009; 7:e99; PMID:19402756; https://doi.org/10.1371/annotation/2259f958-a68e-4e57-92b5-2ef003070cf1
  • Levy-Strumpf N, Meghan K, Zheng H, Brown L, Culotti JG. The Wnt frizzled receptor MOM-5 regulates the UNC-5 Netrin receptor through small GTPase-dependent signaling to determine the polarity of migrating cells. PloS Genet 2015; 11(8):e1005446; PMID:26292279; https://doi.org/10.1371/journal.pgen.1005446
  • Zipkin ID, Kindt RM, Kenyon CJ. Role of new Rho family member in cell migration and axon guidance in C. elegans. Cell 1997; 90:883-94; PMID:9298900; https://doi.org/10.1016/S0092-8674(00)80353-0
  • Deng X, Hofmann ER, Villanueva A, Hobert O, Capodieci P, Veach DR, Yin X, Campodonico L, Glekas A, Cordon-Cardo C, et al. Caenorhabditis elegans ABL-1 antagonizes p53-mediated germline apoptosis after ionizing irradiation. Nat Genet 2004; 36:906-12; PMID:15273685; https://doi.org/10.1038/ng1396
  • Hedgecock EM, Culotti JG, Hall DH. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis of C. elegans. Neuron 1990; 4(1):61-85; PMID:2310575; https://doi.org/10.1016/0896-6273(90)90444-K
  • Su M, Merz DC, Killeen MT, Zhou Y, Zheng H, Kramer JM, Hedgecock EM, Culotti JG. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating Distal tip cells in Caenorhabditis elegans. Development 2000; 127:585-94; PMID:10631179
  • Spencer AG, Orita S, Malone CJ, Han M. A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans. Proc Natl Acad Sci USA 2001; 98:13132-7; PMID:11687661; https://doi.org/10.1073/pnas.241504098
  • Steven R, Kubiseski TJ, Zheng H, Kulkarni S, Mancillas J, Ruiz Morales A, Hogue CW, Pawson T, Culotti J. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 1998; 92:785-95; PMID:9529254; https://doi.org/10.1016/S0092-8674(00)81406-3
  • Kulkarni G, Xu Z, Mohamed AM, Li H, Tang X, Limerick G, Wadsworth WG. Experimental evidence for UNC-6 (Netrin) axon outgrowth by stochastic fluctuation of intracellular UNC-40 (DCC) outgrowth activity. Biol Open 2013; 2(12):1300-12; PMID:24337114; https://doi.org/10.1242/bio.20136346
  • Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Krischner MW. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 2002; 418:790-3; PMID:12181570; https://doi.org/10.1038/nature00859
  • Tani K, Sato S, Sukezane T, Kojima H, Hirose H, Hanafusa H, Shishido T. Abl interactor 1 promotes tyrosine 296 phosphorylation of mammalian enabled (Mena) by c-Abl kinase. J Biol Chem 2003; 278:21685-92; PMID:12672821; https://doi.org/10.1074/jbc.M301447200
  • Innocenti M, Gerboth S, Rottner K, Lai F, Hertzog M, Stradal TE, Frittoli E, Didry D, Polo S, Disanza A, et al. Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 2005; 7:969-76; PMID:16155590; https://doi.org/10.1038/ncb1304
  • Levy-Strumpf N, Culotti JG. VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions of UNC-40 in C. elegans. Nat Neurosci 2007; 10:161-8; PMID:17237777; https://doi.org/10.1038/nn1835
  • Watari-Goshima N, Ogura K, Wolf FW, Goshima Y, Garriga G. C. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations. Nat Neurosci 2007; 10:169-76; PMID:17237778; https://doi.org/10.1038/nn1834
  • Vanderzalm PJ, Pandey A, Hurwitz ME, Bloom L, Horvitz HR, Garriga G. C. elegans CARMIL negatively regulates UNC-73/Trio function during neuronal development. Development 2009; 136:1201-10; PMID:19244282; https://doi.org/10.1242/dev.026666
  • Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77(1):71-94; PMID:4366476
  • Ahmadian A, Gharizadeh B, O'Meara D, Odeberg J, Lundeberg J. Genotyping by apyrase-mediated allele-specific extension. Nucl Acids Res 2001; 29:e12; https://doi.org/10.1093/nar/29.24.e121

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