2,423
Views
34
CrossRef citations to date
0
Altmetric
REVIEW

Rho GTPases in embryonic development

&
Article: e972857 | Received 24 Jun 2014, Accepted 24 Jun 2014, Published online: 12 Dec 2014

References

  • Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005; 21:247-69; PMID:16212495; http://dx.doi.org/10.1146/annurev.cellbio.21.020604.150721
  • Tcherkezian J, Lamarche-Vane N. Current knowledge of the large RhoGAP family of proteins. Biol Cell 2007; 99:67-86; PMID:17222083; http://dx.doi.org/10.1042/BC20060086
  • Cherfils J, Zeghouf M. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 2013; 93:269-309; PMID:23303910; http://dx.doi.org/10.1152/physrev.00003.2012
  • Tapon N, Hall A. Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr Opin Cell Biol 1997; 9:86-92; PMID:9013670; http://dx.doi.org/10.1016/S0955-0674(97)80156-1
  • Kozma R, Ahmed S, Best A, Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 1995; 15:1942-52; PMID:7891688
  • Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995; 81:53-62; PMID:7536630; http://dx.doi.org/10.1016/0092-8674(95)90370-4
  • Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992; 70:401-10; PMID:1643658; http://dx.doi.org/10.1016/0092-8674(92)90164-8
  • Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992; 70:389-99; PMID:1643657; http://dx.doi.org/10.1016/0092-8674(92)90163-7
  • Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-35; PMID:12478284; http://dx.doi.org/10.1038/nature01148
  • Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, Otani H, Sakagami H, Kondo H, Nozawa S, Aiba A, et al. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 1998; 17:3427-33; PMID:10030666; http://dx.doi.org/10.1038/sj.onc.1202595
  • Chen F, Ma L, Parrini MC, Mao X, Lopez M, Wu C, Marks PW, Davidson L, Kwiatkowski DJ, Kirchhausen T, et al. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr Biol 2000; 10:758-65; PMID:10898977; http://dx.doi.org/10.1016/S0960-9822(00)00571-6
  • Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 2008; 9:690-701; PMID:18719708; http://dx.doi.org/10.1038/nrm2476
  • Wang L, Zheng Y. Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol 2007; 17:58-64; PMID:17161947; http://dx.doi.org/10.1016/j.tcb.2006.11.009
  • Arnold SJ, Robertson EJ. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 2009; 10:91-103; PMID:19129791; http://dx.doi.org/10.1038/nrm2618
  • Gilbert SF. Developmental biology, ninth edition. Sunderland, MA: Sinauer Associates, Inc., 2010.
  • He X, Liu J, Qi Y, Brakebusch C, Chrostek-Grashoff A, Edgar D, Yurchenco PD, Corbett SA, Lowry SF, Graham AM, et al. Rac1 is essential for basement membrane-dependent epiblast survival. Mol Cell Biol 2010; 30:3569-81; PMID:20457815; http://dx.doi.org/10.1128/MCB.01366-09
  • Migeotte I, Grego-Bessa J, Anderson KV. Rac1 mediates morphogenetic responses to intercellular signals in the gastrulating mouse embryo. Development 2011; 138:3011-20; PMID:21693517; http://dx.doi.org/10.1242/dev.059766
  • Migeotte I, Omelchenko T, Hall A, Anderson KV. Rac1-dependent collective cell migration is required for specification of the anterior-posterior body axis of the mouse. PLoS Biol 2010; 8:e1000442; PMID:20689803; http://dx.doi.org/10.1371/journal.pbio.1000442
  • Wallingford JB, Niswander LA, Shaw GM, Finnell RH. The continuing challenge of understanding, preventing, and treating neural tube defects. Science 2013; 339:1222002; PMID:23449594; http://dx.doi.org/10.1126/science.1222002
  • Juriloff DM, Harris MJ. Mouse models for neural tube closure defects. Hum Mol Genet 2000; 9:993-1000; PMID:10767323; http://dx.doi.org/10.1093/hmg/9.6.993
  • Camerer E, Barker A, Duong DN, Ganesan R, Kataoka H, Cornelissen I, Darragh MR, Hussain A, Zheng YW, Srinivasan Y, et al. Local protease signaling contributes to neural tube closure in the mouse embryo. Dev Cell 2010; 18:25-38; PMID:20152175; http://dx.doi.org/10.1016/j.devcel.2009.11.014
  • Wu X, Li S, Chrostek-Grashoff A, Czuchra A, Meyer H, Yurchenco PD, Brakebusch C. Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev Dyn 2007; 236:2767-78; PMID:17849438; http://dx.doi.org/10.1002/dvdy.21309
  • Pedersen E, Brakebusch C. Rho GTPase function in development: how in vivo models change our view. Exp Cell Res 2012; 318:1779-87; PMID:22659168; http://dx.doi.org/10.1016/j.yexcr.2012.05.004
  • Marchiando AM, Graham WV, Turner JR. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 2010; 5:119-44; PMID:20078218; http://dx.doi.org/10.1146/annurev.pathol.4.110807.092135
  • Bryant DM, Mostov KE. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 2008; 9:887-901; PMID:18946477; http://dx.doi.org/10.1038/nrm2523
  • Mellman I, Nelson WJ. Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 2008; 9:833-45; PMID:18946473; http://dx.doi.org/10.1038/nrm2525
  • Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, Mostov K. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007; 128:383-97; PMID:17254974; http://dx.doi.org/10.1016/j.cell.2006.11.051
  • Iden S, Collard JG. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 2008; 9:846-59; PMID:18946474; http://dx.doi.org/10.1038/nrm2521
  • Schmidt-Ullrich R, Paus R. Molecular principles of hair follicle induction and morphogenesis. Bioessays 2005; 27:247-61; PMID:15714560; http://dx.doi.org/10.1002/bies.20184
  • Alonso L, Fuchs E. Stem cells in the skin: waste not, Wnt not. Genes Dev 2003; 17:1189-200; PMID:12756224; http://dx.doi.org/10.1101/gad.1086903
  • Wu X, Quondamatteo F, Lefever T, Czuchra A, Meyer H, Chrostek A, Paus R, Langbein L, Brakebusch C. Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes Dev 2006; 20:571-85; PMID:16510873; http://dx.doi.org/10.1101/gad.361406
  • Jackson B, Peyrollier K, Pedersen E, Basse A, Karlsson R, Wang Z, Lefever T, Ochsenbein AM, Schmidt G, Aktories K, et al. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol Biol Cell 2011; 22:593-605; PMID:21209320; http://dx.doi.org/10.1091/mbc.E09-10-0859
  • Iruela-Arispe ML, Beitel GJ. Tubulogenesis. Development 2013; 140:2851-5; PMID:23821032; http://dx.doi.org/10.1242/dev.070680
  • Rodríguez-Fraticelli AE, Gálvez-Santisteban M, Martín-Belmonte F. Divide and polarize: recent advances in the molecular mechanism regulating epithelial tubulogenesis. Curr Opin Cell Biol 2011; 23:638-46; PMID:21807489; http://dx.doi.org/10.1016/j.ceb.2011.07.002
  • Kesavan G, Sand FW, Greiner TU, Johansson JK, Kobberup S, Wu X, Brakebusch C, Semb H. Cdc42-mediated tubulogenesis controls cell specification. Cell 2009; 139:791-801; PMID:19914171; http://dx.doi.org/10.1016/j.cell.2009.08.049
  • Chauhan BK, Lou M, Zheng Y, Lang RA. Balanced Rac1 and RhoA activities regulate cell shape and drive invagination morphogenesis in epithelia. Proc Natl Acad Sci U S A 2011; 108:18289-94; PMID:22021442; http://dx.doi.org/10.1073/pnas.1108993108
  • Wan H, Liu C, Wert SE, Xu W, Liao Y, Zheng Y, Whitsett JA. CDC42 is required for structural patterning of the lung during development. Dev Biol 2013; 374:46-57; PMID:23219958; http://dx.doi.org/10.1016/j.ydbio.2012.11.030
  • Scott RP, Hawley SP, Ruston J, Du J, Brakebusch C, Jones N, Pawson T. Podocyte-specific loss of Cdc42 leads to congenital nephropathy. J Am Soc Nephrol 2012; 23:1149-54; PMID:22518006; http://dx.doi.org/10.1681/ASN.2011121206
  • Reginensi A, Scott RP, Gregorieff A, Bagherie-Lachidan M, Chung C, Lim DS, Pawson T, Wrana J, McNeill H. Yap- and Cdc42-dependent nephrogenesis and morphogenesis during mouse kidney development. PLoS Genet 2013; 9:e1003380; PMID:23555292; http://dx.doi.org/10.1371/journal.pgen.1003380
  • van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009; 71:241-60; PMID:18808327; http://dx.doi.org/10.1146/annurev.physiol.010908.163145
  • Sakamori R, Das S, Yu S, Feng S, Stypulkowski E, Guan Y, Douard V, Tang W, Ferraris RP, Harada A, et al. Cdc42 and Rab8a are critical for intestinal stem cell division, survival, and differentiation in mice. J Clin Invest 2012; 122:1052-65; PMID:22354172; http://dx.doi.org/10.1172/JCI60282
  • Melendez J, Liu M, Sampson L, Akunuru S, Han X, Vallance J, Witte D, Shroyer N, Zheng Y. Cdc42 coordinates proliferation, polarity, migration, and differentiation of small intestinal epithelial cells in mice. Gastroenterology 2013; 145:808-19; PMID:23792201; http://dx.doi.org/10.1053/j.gastro.2013.06.021
  • Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005; 6:777-88; PMID:16314867; http://dx.doi.org/10.1038/nrm1739
  • Nadarajah B, Parnavelas JG. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 2002; 3:423-32; PMID:12042877; http://dx.doi.org/10.1038/nrn845
  • Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Bräuninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB, et al. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 2006; 9:1099-107; PMID:16892058; http://dx.doi.org/10.1038/nn1744
  • Garvalov BK, Flynn KC, Neukirchen D, Meyn L, Teusch N, Wu X, Brakebusch C, Bamburg JR, Bradke F. Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci 2007; 27:13117-29; PMID:18045906; http://dx.doi.org/10.1523/JNEUROSCI.3322-07.2007
  • Chen L, Liao G, Yang L, Campbell K, Nakafuku M, Kuan CY, Zheng Y. Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc Natl Acad Sci U S A 2006; 103:16520-5; PMID:17050694; http://dx.doi.org/10.1073/pnas.0603533103
  • Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2000; 2:540-7; PMID:10934475; http://dx.doi.org/10.1038/35019592
  • Katayama K, Melendez J, Baumann JM, Leslie JR, Chauhan BK, Nemkul N, Lang RA, Kuan CY, Zheng Y, Yoshida Y. Loss of RhoA in neural progenitor cells causes the disruption of adherens junctions and hyperproliferation. Proc Natl Acad Sci U S A 2011; 108:7607-12; PMID:21502507; http://dx.doi.org/10.1073/pnas.1101347108
  • Katayama K, Imai F, Campbell K, Lang RA, Zheng Y, Yoshida Y. RhoA and Cdc42 are required in pre-migratory progenitors of the medial ganglionic eminence ventricular zone for proper cortical interneuron migration. Development 2013; 140:3139-45; PMID:23861058; http://dx.doi.org/10.1242/dev.092585
  • Cappello S, Böhringer CR, Bergami M, Conzelmann KK, Ghanem A, Tomassy GS, Arlotta P, Mainardi M, Allegra M, Caleo M, et al. A radial glia-specific role of RhoA in double cortex formation. Neuron 2012; 73:911-24; PMID:22405202; http://dx.doi.org/10.1016/j.neuron.2011.12.030
  • Herzog D, Loetscher P, van Hengel J, Knüsel S, Brakebusch C, Taylor V, Suter U, Relvas JB. The small GTPase RhoA is required to maintain spinal cord neuroepithelium organization and the neural stem cell pool. J Neurosci 2011; 31:5120-30; PMID:21451048; http://dx.doi.org/10.1523/JNEUROSCI.4807-10.2011
  • Katayama K, Leslie JR, Lang RA, Zheng Y, Yoshida Y. Left-right locomotor circuitry depends on RhoA-driven organization of the neuroepithelium in the developing spinal cord. J Neurosci 2012; 32:10396-407; PMID:22836272; http://dx.doi.org/10.1523/JNEUROSCI.6474-11.2012
  • Leone DP, Srinivasan K, Brakebusch C, McConnell SK. The rho GTPase Rac1 is required for proliferation and survival of progenitors in the developing forebrain. Dev Neurobiol 2010; 70:659-78; PMID:20506362
  • Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan CY. Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci 2007; 27:3884-93; PMID:17409253; http://dx.doi.org/10.1523/JNEUROSCI.3509-06.2007
  • Chen L, Melendez J, Campbell K, Kuan CY, Zheng Y. Rac1 deficiency in the forebrain results in neural progenitor reduction and microcephaly. Dev Biol 2009; 325:162-70; PMID:19007770; http://dx.doi.org/10.1016/j.ydbio.2008.10.023
  • Evans TA, Bashaw GJ. Axon guidance at the midline: of mice and flies. Curr Opin Neurobiol 2010; 20:79-85; PMID:20074930; http://dx.doi.org/10.1016/j.conb.2009.12.006
  • Li X, Saint-Cyr-Proulx E, Aktories K, Lamarche-Vane N. Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in N1E-115 neuroblastoma cells. J Biol Chem 2002; 277:15207-14; PMID:11844789; http://dx.doi.org/10.1074/jbc.M109913200
  • Shekarabi M, Kennedy TE. The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol Cell Neurosci 2002; 19:1-17; PMID:11817894; http://dx.doi.org/10.1006/mcne.2001.1075
  • Briançon-Marjollet A, Ghogha A, Nawabi H, Triki I, Auziol C, Fromont S, Piché C, Enslen H, Chebli K, Cloutier JF, et al. Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol Cell Biol 2008; 28:2314-23; PMID:18212043; http://dx.doi.org/10.1128/MCB.00998-07
  • Kassai H, Terashima T, Fukaya M, Nakao K, Sakahara M, Watanabe M, Aiba A. Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur J Neurosci 2008; 28:257-67; PMID:18702697; http://dx.doi.org/10.1111/j.1460-9568.2008.06343.x
  • Vidaki M, Tivodar S, Doulgeraki K, Tybulewicz V, Kessaris N, Pachnis V, Karagogeos D. Rac1-dependent cell cycle exit of MGE precursors and GABAergic interneuron migration to the cortex. Cereb Cortex 2012; 22:680-92; PMID:21690261; http://dx.doi.org/10.1093/cercor/bhr145
  • Threadgill R, Bobb K, Ghosh A. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 1997; 19:625-34; PMID:9331353; http://dx.doi.org/10.1016/S0896-6273(00)80376-1
  • Vaghi V, Pennucci R, Talpo F, Corbetta S, Montinaro V, Barone C, Croci L, Spaiardi P, Consalez GG, Biella G, et al. Rac1 and rac3 GTPases control synergistically the development of cortical and hippocampal GABAergic interneurons. Cereb Cortex 2014; 24:1247-58; PMID:23258346; http://dx.doi.org/10.1093/cercor/bhs402
  • Corbetta S, Gualdoni S, Ciceri G, Monari M, Zuccaro E, Tybulewicz VL, de Curtis I. Essential role of Rac1 and Rac3 GTPases in neuronal development. FASEB J 2009; 23:1347-57; PMID:19126596; http://dx.doi.org/10.1096/fj.08-121574
  • Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, Flynn KC, Stradal TE, Chrostek-Grashoff A, Brakebusch C, Bradke F. Rac1 regulates neuronal polarization through the WAVE complex. J Neurosci 2010; 30:6930-43; PMID:20484635; http://dx.doi.org/10.1523/JNEUROSCI.5395-09.2010
  • Wang G, Woods A, Agoston H, Ulici V, Glogauer M, Beier F. Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 2007; 306:612-23; PMID:17467682; http://dx.doi.org/10.1016/j.ydbio.2007.03.520
  • Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008; 133:340-53; PMID:18423204; http://dx.doi.org/10.1016/j.cell.2008.01.052
  • Suzuki D, Yamada A, Amano T, Yasuhara R, Kimura A, Sakahara M, Tsumaki N, Takeda S, Tamura M, Nakamura M, et al. Essential mesenchymal role of small GTPase Rac1 in interdigital programmed cell death during limb development. Dev Biol 2009; 335:396-406; PMID:19766620; http://dx.doi.org/10.1016/j.ydbio.2009.09.014
  • Aizawa R, Yamada A, Suzuki D, Iimura T, Kassai H, Harada T, Tsukasaki M, Yamamoto G, Tachikawa T, Nakao K, et al. Cdc42 is required for chondrogenesis and interdigital programmed cell death during limb development. Mech Dev 2012; 129:38-50; PMID:22387309; http://dx.doi.org/10.1016/j.mod.2012.02.002
  • Southgate L, Machado RD, Snape KM, Primeau M, Dafou D, Ruddy DM, Branney PA, Fisher M, Lee GJ, Simpson MA, et al. Gain-of-function mutations of ARHGAP31, a Cdc42/Rac1 GTPase regulator, cause syndromic cutis aplasia and limb anomalies. Am J Hum Genet 2011; 88:574-85; PMID:21565291; http://dx.doi.org/10.1016/j.ajhg.2011.04.013
  • Shaheen R, Faqeih E, Sunker A, Morsy H, Al-Sheddi T, Shamseldin HE, Adly N, Hashem M, Alkuraya FS. Recessive mutations in DOCK6, encoding the guanidine nucleotide exchange factor DOCK6, lead to abnormal actin cytoskeleton organization and Adams-Oliver syndrome. Am J Hum Genet 2011; 89:328-33; PMID:21820096; http://dx.doi.org/10.1016/j.ajhg.2011.07.009

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.