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PLOS ONE  2013 

Protein Phosphatase 1 β Paralogs Encode the Zebrafish Myosin Phosphatase Catalytic Subunit

DOI: 10.1371/journal.pone.0075766

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Abstract:

Background The myosin phosphatase is a highly conserved regulator of actomyosin contractility. Zebrafish has emerged as an ideal model system to study the in vivo role of myosin phosphatase in controlling cell contractility, cell movement and epithelial biology. Most work in zebrafish has focused on the regulatory subunit of the myosin phosphatase called Mypt1. In this work, we examined the critical role of Protein Phosphatase 1, PP1, the catalytic subunit of the myosin phosphatase. Methodology/Principal Findings We observed that in zebrafish two paralogous genes encoding PP1β, called ppp1cba and ppp1cbb, are both broadly expressed during early development. Furthermore, we found that both gene products interact with Mypt1 and assemble an active myosin phosphatase complex. In addition, expression of this complex results in dephosphorylation of the myosin regulatory light chain and large scale rearrangements of the actin cytoskeleton. Morpholino knock-down of ppp1cba and ppp1cbb results in severe defects in morphogenetic cell movements during gastrulation through loss of myosin phosphatase function. Conclusions/Significance Our work demonstrates that zebrafish have two genes encoding PP1β, both of which can interact with Mypt1 and assemble an active myosin phosphatase. In addition, both genes are required for convergence and extension during gastrulation and correct dosage of the protein products is required.

References

[1]  Landsverk ML, Epstein HF (2005) Genetic analysis of myosin II assembly and organization in model organisms. Cell Mol Life Sci 62: 2270-2282. doi:10.1007/s00018-005-5176-2. PubMed: 16142426.
[2]  Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10: 778-790. doi:10.1038/nrm2786. PubMed: 19851336.
[3]  Hirano K, Derkach DN, Hirano M, Nishimura J, Kanaide H (2003) Protein kinase network in the regulation of phosphorylation and dephosphorylation of smooth muscle myosin light chain. Mol Cell Biochem 248: 105-114. doi:10.1023/A:1024180101032. PubMed: 12870661.
[4]  Haystead TA (2005) ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell Signal 17: 1313-1322. doi:10.1016/j.cellsig.2005.05.008. PubMed: 16005610.
[5]  Grassie ME, Moffat LD, Walsh MP, Macdonald JA (2011) The myosin phosphatase targeting protein (MYPT) family: A regulated mechanism for achieving substrate specificity of the catalytic subunit of protein phosphatase type 1delta. Arch Biochem Biophys.
[6]  Matsumura F, Hartshorne DJ (2008) Myosin phosphatase target subunit: Many roles in cell function. Biochem Biophys Res Commun 369: 149-156. doi:10.1016/j.bbrc.2007.12.090. PubMed: 18155661.
[7]  Hagerty L, Weitzel DH, Chambers J, Fortner CN, Brush MH et al. (2007) ROCK1 phosphorylates and activates zipper-interacting protein kinase. J Biol Chem 282: 4884-4893. PubMed: 17158456.
[8]  Eto M (2009) Regulation of cellular protein phosphatase-1 (PP1) by phosphorylation of the CPI-17 family, C-kinase-activated PP1 inhibitors. J Biol Chem 284: 35273-35277. doi:10.1074/jbc.R109.059972. PubMed: 19846560.
[9]  Weiser DC, Row RH, Kimelman D (2009) Rho-regulated myosin phosphatase establishes the level of protrusive activity required for cell movements during zebrafish gastrulation. Development 136: 2375-2384. doi:10.1242/dev.034892. PubMed: 19515695.
[10]  Ihara E, MacDonald JA (2007) The regulation of smooth muscle contractility by zipper-interacting protein kinase. Can J Physiol Pharmacol 85: 79-87. doi:10.1139/y06-103. PubMed: 17487247.
[11]  Butler T, Paul J, Europe-Finner N, Smith R, Chan EC (2013) Role of serine-threonine phosphoprotein phosphatases in smooth muscle contractility. Am J Physiol Cell Physiol 304: C485-C504. doi:10.1152/ajpcell.00161.2012. PubMed: 23325405.
[12]  Mizuno T, Tsutsui K, Nishida Y (2002) Drosophila myosin phosphatase and its role in dorsal closure. Development 129: 1215-1223. PubMed: 11874917.
[13]  Piekny AJ, Johnson JL, Cham GD, Mains PE (2003) The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis. Development 130: 5695-5704. doi:10.1242/dev.00807. PubMed: 14522875.
[14]  Tan C, Stronach B, Perrimon N (2003) Roles of myosin phosphatase during Drosophila development. Development 130: 671-681. doi:10.1242/dev.00298. PubMed: 12505998.
[15]  Vereshchagina N, Bennett D, Sz?or B, Kirchner J, Gross S et al. (2004) The essential role of PP1beta in Drosophila is to regulate nonmuscle myosin. Mol Biol Cell 15: 4395-4405. doi:10.1091/mbc.E04-02-0139. PubMed: 15269282.
[16]  Okamoto R, Ito M, Suzuki N, Kongo M, Moriki N et al. (2005) The targeted disruption of the MYPT1 gene results in embryonic lethality. Transgenic Res 14: 337-340. doi:10.1007/s11248-005-3453-3. PubMed: 16145842.
[17]  He WQ, Qiao YN, Peng YJ, Zha JM, Zhang CH et al. (2013) Altered Contractile Phenotypes of Intestinal Smooth Muscle in Mice Deficient in Myosin Phosphatase Target Subunit 1. Gastroenterology, 144: 1456–65, 1465.e1 PubMed: 23499953.
[18]  Huang H, Ruan H, Aw MY, Hussain A, Guo L et al. (2008) Mypt1-mediated spatial positioning of Bmp2-producing cells is essential for liver organogenesis. Development 135: 3209-3218. doi:10.1242/dev.024406. PubMed: 18776143.
[19]  Gutzman JH, Sive H (2010) Epithelial relaxation mediated by the myosin phosphatase regulator Mypt1 is required for brain ventricle lumen expansion and hindbrain morphogenesis. Development 137: 795-804. doi:10.1242/dev.042705. PubMed: 20147380.
[20]  Diz-Mu?oz A, Krieg M, Bergert M, Ibarlucea-Benitez I, Muller DJ et al. (2010) Control of directed cell migration in vivo by membrane-to-cortex attachment. PLOS Biol 8: e1000544. PubMed: 21151339.
[21]  Cohen PT (2002) Protein phosphatase 1--targeted in many directions. J Cell Sci 115: 241-256. PubMed: 11839776.
[22]  Virshup DM, Shenolikar S (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 33: 537-545. doi:10.1016/j.molcel.2009.02.015. PubMed: 19285938.
[23]  Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298: 1950-1954. doi:10.1126/science.1079478. PubMed: 12471247.
[24]  Solnica-Krezel L (2006) Gastrulation in zebrafish -- all just about adhesion? Curr Opin Genet Dev 16: 433-441. doi:10.1016/j.gde.2006.06.009. PubMed: 16797963.
[25]  Hammerschmidt M, Wedlich D (2008) Regulated adhesion as a driving force of gastrulation movements. Development 135: 3625-3641. doi:10.1242/dev.015701. PubMed: 18952908.
[26]  Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28: 687-717. doi:10.1146/annurev-cellbio-092910-154043. PubMed: 22804578.
[27]  Tada M, Heisenberg CP (2012) Convergent extension: using collective cell migration and cell intercalation to shape embryos. Development 139: 3897-3904. doi:10.1242/dev.073007. PubMed: 23048180.
[28]  Tada M, Kai M (2012) Planar cell polarity in coordinated and directed movements. Curr Top Dev Biol 101: 77-110. doi:10.1016/B978-0-12-394592-1.00004-1. PubMed: 23140626.
[29]  Weiser DC, Pyati UJ, Kimelman D (2007) Gravin regulates mesodermal cell behavior changes required for axis elongation during zebrafish gastrulation. Genes Dev 21: 1559-1571. doi:10.1101/gad.1535007. PubMed: 17575056.
[30]  Marlow F, Topczewski J, Sepich D, Solnica-Krezel L (2002) Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12: 876-884. doi:10.1016/S0960-9822(02)00864-3. PubMed: 12062050.
[31]  Heroes E, Lesage B, G?rnemann J, Beullens M, Van Meervelt L et al. (2013) The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J 280: 584-595. doi:10.1111/j.1742-4658.2012.08547.x. PubMed: 22360570.
[32]  Ceulemans H, Stalmans W, Bollen M (2002) Regulator-driven functional diversification of protein phosphatase-1 in eukaryotic evolution. Bioessays 24: 371-381. doi:10.1002/bies.10069. PubMed: 11948623.
[33]  Kirchner J, Gross S, Bennett D, Alphey L (2007) Essential, overlapping and redundant roles of the Drosophila protein phosphatase 1 alpha and 1 beta genes. Genetics 176: 273-281. doi:10.1534/genetics.106.069914. PubMed: 17513890.
[34]  Varmuza S, Jurisicova A, Okano K, Hudson J, Boekelheide K et al. (1999) Spermiogenesis is impaired in mice bearing a targeted mutation in the protein phosphatase 1cgamma gene. Dev Biol 205: 98-110. doi:10.1006/dbio.1998.9100. PubMed: 9882500.
[35]  Gibbons JA, Kozubowski L, Tatchell K, Shenolikar S (2007) Expression of human protein phosphatase-1 in Saccharomyces cerevisiae highlights the role of phosphatase isoforms in regulating eukaryotic functions. J Biol Chem 282: 21838-21847. doi:10.1074/jbc.M701272200. PubMed: 17545157.
[36]  Scotto-Lavino E, Garcia-Diaz M, Du G, Frohman MA (2010) Basis for the isoform-specific interaction of myosin phosphatase subunits protein phosphatase 1c beta and myosin phosphatase targeting subunit 1. J Biol Chem 285: 6419-6424. doi:10.1074/jbc.M109.074773. PubMed: 20042605.
[37]  Terry-Lorenzo RT, Carmody LC, Voltz JW, Connor JH, Li S et al. (2002) The neuronal actin-binding proteins, neurabin I and neurabin II, recruit specific isoforms of protein phosphatase-1 catalytic subunits. J Biol Chem 277: 27716-27724. doi:10.1074/jbc.M203365200. PubMed: 12016225.
[38]  Carmody LC, Baucum AJ 2nd, Bass MA, Colbran RJ (2008) Selective targeting of the gamma1 isoform of protein phosphatase 1 to F-actin in intact cells requires multiple domains in spinophilin and neurabin. FASEB J 22: 1660-1671. doi:10.1096/fj.07-092841. PubMed: 18216290.
[39]  Pinheiro AS, Marsh JA, Forman-Kay JD, Peti W (2011) Structural signature of the MYPT1-PP1 interaction. J Am Chem Soc 133: 73-80. doi:10.1021/ja107810r. PubMed: 21142030.
[40]  Bollen M, Peti W, Ragusa MJ, Beullens M (2010) The extended PP1 toolkit: designed to create specificity. Trends Biochem Sci 35: 450-458. doi:10.1016/j.tibs.2010.03.002. PubMed: 20399103.
[41]  Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13: 382-390. doi:10.1101/gr.640303. PubMed: 12618368.
[42]  Taylor JS, Van de Peer Y, Braasch I, Meyer A (2001) Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc Lond B Biol Sci 356: 1661-1679. doi:10.1098/rstb.2001.0975. PubMed: 11604130.
[43]  Eto M, Kirkbride JA, Brautigan DL (2005) Assembly of MYPT1 with protein phosphatase-1 in fibroblasts redirects localization and reorganizes the actin cytoskeleton. Cell Motil Cytoskeleton 62: 100-109. doi:10.1002/cm.20088. PubMed: 16106448.
[44]  Xia D, Stull JT, Kamm KE (2005) Myosin phosphatase targeting subunit 1 affects cell migration by regulating myosin phosphorylation and actin assembly. Exp Cell Res 304: 506-517. doi:10.1016/j.yexcr.2004.11.025. PubMed: 15748895.
[45]  Weiser DC, Kimelman D (2012) Analysis of cell shape and polarity during zebrafish gastrulation. Methods Mol Biol 839: 53-68. doi:10.1007/978-1-61779-510-7_5. PubMed: 22218892.
[46]  Landsverk ML, Weiser DC, Hannibal MC, Kimelman D (2010) Alternative splicing of sept9a and sept9b in zebrafish produces multiple mRNA transcripts expressed throughout development. PLOS ONE 5: e10712. doi:10.1371/journal.pone.0010712. PubMed: 20502708.
[47]  Lesage B, Beullens M, Nuytten M, Van Eynde A, Keppens S et al. (2004) Interactor-mediated nuclear translocation and retention of protein phosphatase-1. J Biol Chem 279: 55978-55984. doi:10.1074/jbc.M411911200. PubMed: 15501817.
[48]  Bodkin DK, Knudson DL (1985) Assessment of sequence relatedness of double-stranded RNA genes by RNA-RNA blot hybridization. J Virol Methods 10: 45-52. doi:10.1016/0166-0934(85)90087-4. PubMed: 3972943.
[49]  Thisse C, Thisse B (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3: 59-69. doi:10.1038/nnano.2008.25. PubMed: 18193022.
[50]  Aguilar HN, Tracey CN, Tsang SC, McGinnis JM, Mitchell BF (2011) Phos-tag-based analysis of myosin regulatory light chain phosphorylation in human uterine myocytes. PLOS ONE 6: e20903. doi:10.1371/journal.pone.0020903. PubMed: 21695279.
[51]  Shoval Y, Pietrokovski S, Kimchi A (2007) ZIPK: a unique case of murine-specific divergence of a conserved vertebrate gene. PLOS Genet 3: 1884-1893. PubMed: 17953487.
[52]  Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-469.
[53]  Eisen JS, Smith JC (2008) Controlling morpholino experiments: don’t stop making antisense. Development 135: 1735-1743. doi:10.1242/dev.001115. PubMed: 18403413.
[54]  Yin C, Kiskowski M, Pouille PA, Farge E, Solnica-Krezel L (2008) Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J Cell Biol 180: 221-232. doi:10.1083/jcb.200704150. PubMed: 18195109.
[55]  Meyer A, Schartl M (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11: 699-704. doi:10.1016/S0955-0674(99)00039-3. PubMed: 10600714.
[56]  Myers DC, Sepich DS, Solnica-Krezel L (2002) Bmp activity gradient regulates convergent extension during zebrafish gastrulation. Dev Biol 243: 81-98. doi:10.1006/dbio.2001.0523. PubMed: 11846479.
[57]  von der Hardt S, Bakkers J, Inbal A, Carvalho L, Solnica-Krezel L et al. (2007) The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr Biol 17: 475-487. doi:10.1016/j.cub.2007.02.013. PubMed: 17331724.
[58]  Chan J, Mably JD, Serluca FC, Chen JN, Goldstein NB et al. (2001) Morphogenesis of prechordal plate and notochord requires intact Eph/ephrin B signaling. Dev Biol 234: 470-482. doi:10.1006/dbio.2001.0281. PubMed: 11397014.
[59]  Ataliotis P, Symes K, Chou MM, Ho L, Mercola M (1995) PDGF signalling is required for gastrulation of Xenopus laevis. Development 121: 3099-3110. PubMed: 7555734.
[60]  Symes K, Mercola M (1996) Embryonic mesoderm cells spread in response to platelet-derived growth factor and signaling by phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 93: 9641-9644. doi:10.1073/pnas.93.18.9641. PubMed: 8790383.
[61]  Coyle RC, Latimer A, Jessen JR (2008) Membrane-type 1 matrix metalloproteinase regulates cell migration during zebrafish gastrulation: evidence for an interaction with non-canonical Wnt signaling. Exp Cell Res 314: 2150-2162. doi:10.1016/j.yexcr.2008.03.010. PubMed: 18423448.
[62]  Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S et al. (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329: 1337-1340. doi:10.1126/science.1191184. PubMed: 20671153.
[63]  Yamashita S, Miyagi C, Carmany-Rampey A, Shimizu T, Fujii R et al. (2002) Stat 3 Controls Cell Movements during Zebrafish Gastrulation. Dev Cell 2: 363-375.
[64]  Miyagi C, Yamashita S, Ohba Y, Yoshizaki H, Matsuda M et al. (2004) Stat 3 noncell-autonomously controls planar cell polarity during zebrafish convergence and extension. J Cell Biol 166: 975-981.
[65]  Roszko I, Sawada A, Solnica-Krezel L (2009) Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin Cell Dev Biol 20: 986-997. doi:10.1016/j.semcdb.2009.09.004. PubMed: 19761865.
[66]  Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17: 295-309. doi:10.1101/gad.1022203. PubMed: 12533515.
[67]  Zhu S, Liu L, Korzh V, Gong Z, Low BC (2006) RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and Diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal 18: 359-372. doi:10.1016/j.cellsig.2005.05.019. PubMed: 16019189.
[68]  Quick RE, Dunlap JA, Jessen JR (2012) Expression analysis of zebrafish membrane type-2 matrix metalloproteinases during embryonic development. Gene Expr Patterns 12: 254-260. doi:10.1016/j.gep.2012.05.003. PubMed: 22684036.
[69]  Jessen JR, Topczewski J, Bingham S, Sepich DS, Marlow F et al. (2002) Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol 4: 610-615. PubMed: 12105418.
[70]  Heisenberg CP, Tada M, Rauch GJ, Saúde L, Concha ML et al. (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81. doi:10.1038/35011068. PubMed: 10811221.
[71]  Wallingford JB, Rowning BA, Vogeli KM, Rothb?cher U, Fraser SE et al. (2000) Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405: 81-85. doi:10.1038/35011077. PubMed: 10811222.
[72]  Sepich DS, Usmani M, Pawlicki S, Solnica-Krezel L (2011) Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. Development 138: 543-552. doi:10.1242/dev.053959. PubMed: 21205798.
[73]  Carreira-Barbosa F, Kajita M, Morel V, Wada H, Okamoto H et al. (2009) Flamingo regulates epiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation. Development 136: 383-392. doi:10.1242/dev.026542. PubMed: 19091770.
[74]  Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT (2003) Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 13: 680-685. doi:10.1016/S0960-9822(03)00240-9. PubMed: 12699626.
[75]  Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW et al. (2003) Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130: 4037-4046. doi:10.1242/dev.00567. PubMed: 12874125.
[76]  Jopling C, den Hertog J (2005) Fyn/Yes and non-canonical Wnt signalling converge on RhoA in vertebrate gastrulation cell movements. EMBO Rep 6: 426-431. doi:10.1038/sj.embor.7400386. PubMed: 15815683.
[77]  Jopling C, Hertog J (2007) Essential role for Csk upstream of Fyn and Yes in zebrafish gastrulation. Mech Dev 124: 129-136. doi:10.1016/j.mod.2006.10.003. PubMed: 17157484.
[78]  Jopling C, van Geemen D, den Hertog J (2007) Shp2 knockdown and Noonan/LEOPARD mutant Shp2-induced gastrulation defects. PLOS Genet 3: e225. doi:10.1371/journal.pgen.0030225. PubMed: 18159945.
[79]  van Eekelen M, Runtuwene V, Masselink W, den Hertog J (2012) Pair-wise regulation of convergence and extension cell movements by four phosphatases via RhoA. PLOS ONE 7: e35913. doi:10.1371/journal.pone.0035913. PubMed: 22545146.
[80]  van Eekelen M, Runtuwene V, Overvoorde J, den Hertog J (2010) RPTPalpha and PTPepsilon signaling via Fyn/Yes and RhoA is essential for zebrafish convergence and extension cell movements during gastrulation. Dev Biol 340: 626-639. doi:10.1016/j.ydbio.2010.02.026. PubMed: 20188722.
[81]  Lin F, Sepich DS, Chen S, Topczewski J, Yin C et al. (2005) Essential roles of G{alpha}12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements. J Cell Biol 169: 777-787. doi:10.1083/jcb.200501104. PubMed: 15928205.
[82]  Weiser DC, St Julien KR, Lang JS, Kimelman D (2008) Cell shape regulation by Gravin requires N-terminal membrane effector domains. Biochem Biophys Res Commun 375: 512-516. doi:10.1016/j.bbrc.2008.08.063. PubMed: 18725198.
[83]  Yu JA, Foley FC, Amack JD, Turner CE (2011) The cell adhesion-associated protein Git2 regulates morphogenetic movements during zebrafish embryonic development. Dev Biol 349: 225-237. doi:10.1016/j.ydbio.2010.10.027. PubMed: 21034731.
[84]  Tanegashima K, Zhao H, Dawid IB (2008) WGEF activates Rho in the Wnt-PCP pathway and controls convergent extension in Xenopus gastrulation. EMBO J 27: 606-617. doi:10.1038/emboj.2008.9. PubMed: 18256687.
[85]  Goudevenou K, Martin P, Yeh YJ, Jones P, Sablitzky F (2011) Def6 is required for convergent extension movements during zebrafish gastrulation downstream of Wnt5b signaling. PLOS ONE 6: e26548. doi:10.1371/journal.pone.0026548. PubMed: 22039507.
[86]  Miyakoshi A, Ueno N, Kinoshita N (2004) Rho guanine nucleotide exchange factor xNET1 implicated in gastrulation movements during Xenopus development. Differentiation 72: 48-55. doi:10.1111/j.1432-0436.2004.07201004.x. PubMed: 15008826.
[87]  Kwan KM, Kirschner MW (2005) A microtubule-binding Rho-GEF controls cell morphology during convergent extension of Xenopus laevis. Development 132: 4599-4610. doi:10.1242/dev.02041. PubMed: 16176947.
[88]  Lai SL, Chan TH, Lin MJ, Huang WP, Lou SW et al. (2008) Diaphanous-related formin 2 and profilin I are required for gastrulation cell movements. PLOS ONE 3: e3439. doi:10.1371/journal.pone.0003439. PubMed: 18941507.
[89]  Lai SL, Chang CN, Wang PJ, Lee SJ (2005) Rho mediates cytokinesis and epiboly via ROCK in zebrafish. Mol Reprod Dev 71: 186-196. doi:10.1002/mrd.20290. PubMed: 15791595.

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