Skip to main content

Roles of Rab Family Small G Proteins in Formation of the Apical Junctional Complex in Epithelial Cells

  • Chapter
  • First Online:

Abstract

Epithelial tissue formation and function require organization of monolayer sheets, which is mediated through the apical junctional complex (AJC). The AJC comprises a diverse set of key factors: adhesion molecules including E-cadherin, claudins, and occludin; polarity proteins that support organization and function of apical and basolateral membranes; and proteins that support adhesion, vesicle transport, actin cytoskeletal rearrangement, and membrane scaffolds. These proteins form a dynamic cooperative network that is engaged in the highly elaborate regulation of AJC. Several lines of evidence indicate that Rab family small G proteins play important roles in the regulation of epithelial apical junctions and that the assembly and disassembly of these junctions can be driven by Rab proteins localized at either endosomes or apical junctions. In this review, we provide an overview of the influence of Rab proteins on AJC functions, focusing especially on the role of the complex containing Rab13 and JRAB/MICAL-L2 (junctional Rab13-binding protein/molecule interacting with CasL-like 2) in the regulation of epithelial apical junctions.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Akhtar N, Hotchin NA (2001) RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol Biol Cell 12(4):847–862

    PubMed Central  CAS  PubMed  Google Scholar 

  • Allan BB, Moyer BD, Balch WE (2000) Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 289(5478):444–448

    CAS  PubMed  Google Scholar 

  • Ang AL, Folsch H, Koivisto UM, Pypaert M, Mellman I (2003) The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 163(2):339–350. doi:10.1083/jcb.200307046

    PubMed Central  CAS  PubMed  Google Scholar 

  • Apodaca G, Gallo LI, Bryant DM (2012) Role of membrane traffic in the generation of epithelial cell asymmetry. Nat Cell Biol 14(12):1235–1243. doi:10.1038/ncb2635

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ashida S, Furihata M, Katagiri T, Tamura K, Anazawa Y, Yoshioka H, Miki T, Fujioka T, Shuin T, Nakamura Y, Nakagawa H (2006) Expression of novel molecules, MICAL2-PV (MICAL2 prostate cancer variants), increases with high Gleason score and prostate cancer progression. Clin Cancer Res 12(9):2767–2773. doi:10.1158/1078-0432.CCR-05-1995

    CAS  PubMed  Google Scholar 

  • Assemat E, Bazellieres E, Pallesi-Pocachard E, Le Bivic A, Massey-Harroche D (2008) Polarity complex proteins. Biochim Biophys Acta 1778(3):614–630. doi:10.1016/j.bbamem.2007.08.029

    CAS  PubMed  Google Scholar 

  • Au JS, Puri C, Ihrke G, Kendrick-Jones J, Buss F (2007) Myosin VI is required for sorting of AP-1B-dependent cargo to the basolateral domain in polarized MDCK cells. J Cell Biol 177(1):103–114. doi:10.1083/jcb.200608126

    PubMed Central  CAS  PubMed  Google Scholar 

  • Balzac F, Avolio M, Degani S, Kaverina I, Torti M, Silengo L, Small JV, Retta SF (2005) E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function. J Cell Sci 118(Pt 20):4765–4783. doi:10.1242/jcs.02584

    CAS  PubMed  Google Scholar 

  • Bershadsky A (2004) Magic touch: how does cell-cell adhesion trigger actin assembly? Trends Cell Biol 14(11):589–593. doi:10.1016/j.tcb.2004.09.009

    CAS  PubMed  Google Scholar 

  • Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A (2005) Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 19(8):923–933. doi:10.1096/fj.04-3260com

    CAS  PubMed  Google Scholar 

  • Bryant DM, Mostov KE (2008) From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9(11):887–901. doi:10.1038/nrm2523

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bryant DM, Stow JL (2004) The ins and outs of E-cadherin trafficking. Trends Cell Biol 14(8):427–434. doi:10.1016/j.tcb.2004.07.007

    CAS  PubMed  Google Scholar 

  • Bryant DM, Datta A, Rodriguez-Fraticelli AE, Peranen J, Martin-Belmonte F, Mostov KE (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12(11):1035–1045. doi:10.1038/ncb2106

    PubMed Central  CAS  PubMed  Google Scholar 

  • Carmosino M, Valenti G, Caplan M, Svelto M (2010) Polarized traffic towards the cell surface: how to find the route. Biol Cell 102(2):75–91. doi:10.1042/BC20090134

    CAS  Google Scholar 

  • Carroll KS, Hanna J, Simon I, Krise J, Barbero P, Pfeffer SR (2001) Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292(5520):1373–1376. doi:10.1126/science.1056791

    CAS  PubMed  Google Scholar 

  • Chang J, Seo SG, Lee KH, Nagashima K, Bang JK, Kim BY, Erikson RL, Lee KW, Lee HJ, Park JE, Lee KS (2013) Essential role of Cenexin1, but not Odf2, in ciliogenesis. Cell Cycle 12(4):655–662. doi:10.4161/cc.23585

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen VC, Li X, Perreault H, Nagy JI (2006) Interaction of zonula occludens-1 (ZO-1) with alpha-actinin-4: application of functional proteomics for identification of PDZ domain-associated proteins. J Proteome Res 5(9):2123–2134. doi:10.1021/pr060216l

    CAS  PubMed  Google Scholar 

  • Christoforides C, Rainero E, Brown KK, Norman JC, Toker A (2012) PKD controls alphavbeta3 integrin recycling and tumor cell invasive migration through its substrate Rabaptin-5. Dev Cell 23(3):560–572. doi:10.1016/j.devcel.2012.08.008

    PubMed Central  CAS  PubMed  Google Scholar 

  • Colicelli J (2004) Human RAS superfamily proteins and related GTPases. Sci STKE 2004(250):RE13. doi:10.1126/stke.2502004re13

    PubMed Central  PubMed  Google Scholar 

  • Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422(6927):37–44. doi:10.1038/nature01451

    CAS  PubMed  Google Scholar 

  • Coyne CB, Bergelson JM (2005) CAR: a virus receptor within the tight junction. Adv Drug Deliv Rev 57(6):869–882. doi:10.1016/j.addr.2005.01.007

    CAS  PubMed  Google Scholar 

  • Coyne CB, Shen L, Turner JR, Bergelson JM (2007) Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2(3):181–192. doi:10.1016/j.chom.2007.07.003

    PubMed Central  CAS  PubMed  Google Scholar 

  • D’Souza-Schorey C (2005) Disassembling adherens junctions: breaking up is hard to do. Trends Cell Biol 15(1):19–26. doi:10.1016/j.tcb.2004.11.002

    PubMed  Google Scholar 

  • D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7(5):347–358. doi:10.1038/nrm1910

    PubMed  Google Scholar 

  • de Renzis S, Sonnichsen B, Zerial M (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat Cell Biol 4(2):124–133. doi:10.1038/ncb744

    PubMed  Google Scholar 

  • Delva E, Kowalczyk AP (2009) Regulation of cadherin trafficking. Traffic 10(3):259–267. doi:10.1111/j.1600-0854.2008.00862.x

    PubMed Central  CAS  PubMed  Google Scholar 

  • Di Giovanni S, De Biase A, Yakovlev A, Finn T, Beers J, Hoffman EP, Faden AI (2005) In vivo and in vitro characterization of novel neuronal plasticity factors identified following spinal cord injury. J Biol Chem 280(3):2084–2091. doi:10.1074/jbc.M411975200

    PubMed  Google Scholar 

  • Di Giovanni S, Knights CD, Rao M, Yakovlev A, Beers J, Catania J, Avantaggiati ML, Faden AI (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25(17):4084–4096. doi:10.1038/sj.emboj.7601292

    PubMed Central  PubMed  Google Scholar 

  • Donaldson JG, Jackson CL (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12(6):362–375. doi:10.1038/nrm3117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ebnet K, Suzuki A, Ohno S, Vestweber D (2004) Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 117(Pt 1):19–29. doi:10.1242/jcs.00930

    CAS  PubMed  Google Scholar 

  • Echard A, Jollivet F, Martinez O, Lacapere JJ, Rousselet A, Janoueix-Lerosey I, Goud B (1998) Interaction of a Golgi-associated kinesin-like protein with Rab6. Science 279(5350):580–585

    CAS  PubMed  Google Scholar 

  • Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412

    PubMed Central  CAS  PubMed  Google Scholar 

  • Feng Y, Walsh CA (2004) The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 6(11):1034–1038. doi:10.1038/ncb1104-1034

    CAS  PubMed  Google Scholar 

  • Feng Y, Chen MH, Moskowitz IP, Mendonza AM, Vidali L, Nakamura F, Kwiatkowski DJ, Walsh CA (2006) Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc Natl Acad Sci U S A 103(52):19836–19841. doi:10.1073/pnas.0609628104

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fischer J, Weide T, Barnekow A (2005) The MICAL proteins and rab1: a possible link to the cytoskeleton? Biochem Biophys Res Commun 328(2):415–423. doi:10.1016/j.bbrc.2004.12.182

    CAS  PubMed  Google Scholar 

  • Folsch H (2005) The building blocks for basolateral vesicles in polarized epithelial cells. Trends Cell Biol 15(4):222–228. doi:10.1016/j.tcb.2005.02.006

    PubMed  Google Scholar 

  • Fouraux MA, Deneka M, Ivan V, van der Heijden A, Raymackers J, van Suylekom D, van Venrooij WJ, van der Sluijs P, Pruijn GJ (2004) Rabip4′ is an effector of rab5 and rab4 and regulates transport through early endosomes. Mol Biol Cell 15(2):611–624. doi:10.1091/mbc.E03-05-0343

    PubMed Central  CAS  PubMed  Google Scholar 

  • Furuse M (2010) Molecular basis of the core structure of tight junctions. Cold Spring Harb Perspect Biol 2(1):a002907. doi:10.1101/cshperspect.a002907

    PubMed Central  PubMed  Google Scholar 

  • Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123(6 Pt 2):1777–1788

    CAS  PubMed  Google Scholar 

  • Galvez-Santisteban M, Rodriguez-Fraticelli AE, Bryant DM, Vergarajauregui S, Yasuda T, Banon-Rodriguez I, Bernascone I, Datta A, Spivak N, Young K, Slim CL, Brakeman PR, Fukuda M, Mostov KE, Martin-Belmonte F (2012) Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat Cell Biol 14(8):838–849. doi:10.1038/ncb2541

    PubMed Central  CAS  PubMed  Google Scholar 

  • Giridharan SS, Rohn JL, Naslavsky N, Caplan S (2012) Differential regulation of actin microfilaments by human MICAL proteins. J Cell Sci 125(Pt 3):614–624. doi:10.1242/jcs.089367

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gov N (2011) Cell mechanics: moving under peer pressure. Nat Mater 10(6):412–414. doi:10.1038/nmat3036

    CAS  PubMed  Google Scholar 

  • Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, Scheller RH, Nelson WJ (1998) Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93(5):731–740

    CAS  PubMed  Google Scholar 

  • Hammer JA 3rd, Wu XS (2002) Rabs grab motors: defining the connections between Rab GTPases and motor proteins. Curr Opin Cell Biol 14(1):69–75

    CAS  PubMed  Google Scholar 

  • Hara T, Honda K, Shitashige M, Ono M, Matsuyama H, Naito K, Hirohashi S, Yamada T (2007) Mass spectrometry analysis of the native protein complex containing actinin-4 in prostate cancer cells. Mol Cell Proteomics 6(3):479–491. doi:10.1074/mcp.M600129-MCP200

    CAS  PubMed  Google Scholar 

  • Harris TJ, Tepass U (2010) Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11(7):502–514. doi:10.1038/nrm2927

    CAS  PubMed  Google Scholar 

  • Hattula K, Peranen J (2000) FIP-2, a coiled-coil protein, links Huntingtin to Rab8 and modulates cellular morphogenesis. Curr Biol 10(24):1603–1606

    CAS  PubMed  Google Scholar 

  • Hattula K, Furuhjelm J, Arffman A, Peranen J (2002) A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport. Mol Biol Cell 13(9):3268–3280. doi:10.1091/mbc.E02-03-0143

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hayashida Y, Honda K, Idogawa M, Ino Y, Ono M, Tsuchida A, Aoki T, Hirohashi S, Yamada T (2005) E-cadherin regulates the association between beta-catenin and actinin-4. Cancer Res 65(19):8836–8845. doi:10.1158/0008-5472.CAN-05-0718

    CAS  PubMed  Google Scholar 

  • Hazelett CC, Sheff D, Yeaman C (2011) RalA and RalB differentially regulate development of epithelial tight junctions. Mol Biol Cell 22(24):4787–4800. doi:10.1091/mbc.E11-07-0657

    PubMed Central  CAS  PubMed  Google Scholar 

  • He B, Guo W (2009) The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21(4):537–542. doi:10.1016/j.ceb.2009.04.007

    PubMed Central  CAS  PubMed  Google Scholar 

  • Henry L, Sheff DR (2008) Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol Biol Cell 19(5):2059–2068. doi:10.1091/mbc.E07-09-0902

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hickson GR, Matheson J, Riggs B, Maier VH, Fielding AB, Prekeris R, Sullivan W, Barr FA, Gould GW (2003) Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol Biol Cell 14(7):2908–2920. doi:10.1091/mbc.E03-03-0160

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hirvonen MJ, Buki KG, Sun Y, Mulari MT, Harkonen PL, Vaananen KH (2013) Novel interaction of Rab13 and Rab8 with endospanins. FEBS Open Bio 3:83–88. doi:10.1016/j.fob.2013.01.004

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hoekstra D, Tyteca D, van Ijzendoorn SC (2004) The subapical compartment: a traffic center in membrane polarity development. J Cell Sci 117(Pt 11):2183–2192. doi:10.1242/jcs.01217

    CAS  PubMed  Google Scholar 

  • Honda K, Yamada T, Seike M, Hayashida Y, Idogawa M, Kondo T, Ino Y, Hirohashi S (2004) Alternative splice variant of actinin-4 in small cell lung cancer. Oncogene 23(30):5257–5262. doi:10.1038/sj.onc.1207652

    CAS  PubMed  Google Scholar 

  • Honda K, Yamada T, Hayashida Y, Idogawa M, Sato S, Hasegawa F, Ino Y, Ono M, Hirohashi S (2005) Actinin-4 increases cell motility and promotes lymph node metastasis of colorectal cancer. Gastroenterology 128(1):51–62

    CAS  PubMed  Google Scholar 

  • Hopkins AM, Walsh SV, Verkade P, Boquet P, Nusrat A (2003) Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J Cell Sci 116(Pt 4):725–742

    CAS  PubMed  Google Scholar 

  • Horiuchi H, Lippe R, McBride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, Zerial M (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90(6):1149–1159

    CAS  PubMed  Google Scholar 

  • Huber LA, de Hoop MJ, Dupree P, Zerial M, Simons K, Dotti C (1993a) Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol 123(1):47–55

    CAS  PubMed  Google Scholar 

  • Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K (1993b) Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 123(1):35–45

    CAS  PubMed  Google Scholar 

  • Hulpiau P, van Roy F (2009) Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41(2):349–369. doi:10.1016/j.biocel.2008.09.027

    CAS  PubMed  Google Scholar 

  • Hung RJ, Yazdani U, Yoon J, Wu H, Yang T, Gupta N, Huang Z, van Berkel WJ, Terman JR (2010) Mical links semaphorins to F-actin disassembly. Nature 463(7282):823–827. doi:10.1038/nature08724

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hung RJ, Pak CW, Terman JR (2011) Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334(6063):1710–1713. doi:10.1126/science.1211956

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91(1):119–149. doi:10.1152/physrev.00059.2009

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S (2005) Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171(6):939–945. doi:10.1083/jcb.200510043

    PubMed Central  CAS  PubMed  Google Scholar 

  • Imamura H, Takaishi K, Nakano K, Kodama A, Oishi H, Shiozaki H, Monden M, Sasaki T, Takai Y (1998) Rho and Rab small G proteins coordinately reorganize stress fibers and focal adhesions in MDCK cells. Mol Biol Cell 9(9):2561–2575

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ivanov AI, Nusrat A, Parkos CA (2004) Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 15(1):176–188. doi:10.1091/mbc.E03-05-0319

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ivanov AI, Nusrat A, Parkos CA (2005) Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays 27(4):356–365. doi:10.1002/bies.20203

    CAS  PubMed  Google Scholar 

  • Izumi G, Sakisaka T, Baba T, Tanaka S, Morimoto K, Takai Y (2004) Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. J Cell Biol 166(2):237–248. doi:10.1083/jcb.200401078

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jahn R, Scheller RH (2006) SNAREs—engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631–643. doi:10.1038/nrm2002

    CAS  PubMed  Google Scholar 

  • Jean S, Kiger AA (2012) Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat Rev Mol Cell Biol 13(7):463–470. doi:10.1038/nrm3379

    CAS  PubMed  Google Scholar 

  • Kachhap SK, Faith D, Qian DZ, Shabbeer S, Galloway NL, Pili R, Denmeade SR, DeMarzo AM, Carducci MA (2007) The N-Myc down regulated Gene1 (NDRG1) is a Rab4a effector involved in vesicular recycling of E-cadherin. PLoS One 2(9):e844. doi:10.1371/journal.pone.0000844

    PubMed Central  PubMed  Google Scholar 

  • Kamei T, Matozaki T, Sakisaka T, Kodama A, Yokoyama S, Peng YF, Nakano K, Takaishi K, Takai Y (1999) Coendocytosis of cadherin and c-Met coupled to disruption of cell-cell adhesion in MDCK cells—regulation by Rho, Rac and Rab small G proteins. Oncogene 18(48):6776–6784. doi:10.1038/sj.onc.1203114

    CAS  PubMed  Google Scholar 

  • Kanda I, Nishimura N, Nakatsuji H, Yamamura R, Nakanishi H, Sasaki T (2008) Involvement of Rab13 and JRAB/MICAL-L2 in epithelial cell scattering. Oncogene 27(12):1687–1695. doi:10.1038/sj.onc.1210812

    CAS  PubMed  Google Scholar 

  • Kim M, Gans JD, Nogueira C, Wang A, Paik JH, Feng B, Brennan C, Hahn WC, Cordon-Cardo C, Wagner SN, Flotte TJ, Duncan LM, Granter SR, Chin L (2006) Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125(7):1269–1281. doi:10.1016/j.cell.2006.06.008

    CAS  PubMed  Google Scholar 

  • Kimura T, Sakisaka T, Baba T, Yamada T, Takai Y (2006) Involvement of the Ras-Ras-activated Rab5 guanine nucleotide exchange factor RIN2-Rab5 pathway in the hepatocyte growth factor-induced endocytosis of E-cadherin. J Biol Chem 281(15):10598–10609. doi:10.1074/jbc.M510531200

    CAS  PubMed  Google Scholar 

  • Kinchen JM, Ravichandran KS (2010) Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464(7289):778–782. doi:10.1038/nature08853

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kohler K, Louvard D, Zahraoui A (2004) Rab13 regulates PKA signaling during tight junction assembly. J Cell Biol 165(2):175–180. doi:10.1083/jcb.200312118

    PubMed Central  PubMed  Google Scholar 

  • Langevin J, Morgan MJ, Sibarita JB, Aresta S, Murthy M, Schwarz T, Camonis J, Bellaiche Y (2005) Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev Cell 9(3):365–376

    CAS  PubMed  Google Scholar 

  • Lau AS, Mruk DD (2003) Rab8B GTPase and junction dynamics in the testis. Endocrinology 144(4):1549–1563. doi:10.1210/en.2002-220893

    CAS  PubMed  Google Scholar 

  • Le TL, Yap AS, Stow JL (1999) Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J Cell Biol 146(1):219–232

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li R, Gundersen GG (2008) Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat Rev Mol Cell Biol 9(11):860–873. doi:10.1038/nrm2522

    CAS  PubMed  Google Scholar 

  • Ling K, Bairstow SF, Carbonara C, Turbin DA, Huntsman DG, Anderson RA (2007) Type I gamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J Cell Biol 176(3):343–353. doi:10.1083/jcb.200606023

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lock JG, Stow JL (2005) Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin. Mol Biol Cell 16(4):1744–1755. doi:10.1091/mbc.E04-10-0867

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lu H, Bilder D (2005) Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7(12):1232–1239. doi:10.1038/ncb1324

    PubMed  Google Scholar 

  • Marzesco AM, Galli T, Louvard D, Zahraoui A (1998) The rod cGMP phosphodiesterase delta subunit dissociates the small GTPase Rab13 from membranes. J Biol Chem 273(35):22340–22345

    CAS  PubMed  Google Scholar 

  • Marzesco AM, Dunia I, Pandjaitan R, Recouvreur M, Dauzonne D, Benedetti EL, Louvard D, Zahraoui A (2002) The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells. Mol Biol Cell 13(6):1819–1831, doi:02-02-0029

    PubMed Central  CAS  PubMed  Google Scholar 

  • Matsuda M, Kubo A, Furuse M, Tsukita S (2004) A peculiar internalization of claudins, tight junction-specific adhesion molecules, during the intercellular movement of epithelial cells. J Cell Sci 117(Pt 7):1247–1257. doi:10.1242/jcs.00972

    CAS  PubMed  Google Scholar 

  • McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, Zerial M (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98(3):377–386

    CAS  PubMed  Google Scholar 

  • Mege RM, Gavard J, Lambert M (2006) Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol 18(5):541–548. doi:10.1016/j.ceb.2006.08.004

    CAS  PubMed  Google Scholar 

  • Mellman I, Nelson WJ (2008) Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 9(11):833–845. doi:10.1038/nrm2525

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miranda KC, Khromykh T, Christy P, Le TL, Gottardi CJ, Yap AS, Stow JL, Teasdale RD (2001) A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells. J Biol Chem 276(25):22565–22572. doi:10.1074/jbc.M101907200

    CAS  PubMed  Google Scholar 

  • Mizuno-Yamasaki E, Rivera-Molina F, Novick P (2012) GTPase networks in membrane traffic. Annu Rev Biochem 81:637–659. doi:10.1146/annurev-biochem-052810-093700

    PubMed Central  CAS  PubMed  Google Scholar 

  • Monteiro AC, Parkos CA (2012) Intracellular mediators of JAM-A-dependent epithelial barrier function. Ann N Y Acad Sci 1257:115–124. doi:10.1111/j.1749-6632.2012.06521.x

    PubMed Central  CAS  PubMed  Google Scholar 

  • Morimoto S, Nishimura N, Terai T, Manabe S, Yamamoto Y, Shinahara W, Miyake H, Tashiro S, Shimada M, Sasaki T (2005) Rab13 mediates the continuous endocytic recycling of occludin to the cell surface. J Biol Chem 280(3):2220–2228

    CAS  PubMed  Google Scholar 

  • Mruk DD, Lau AS, Sarkar O, Xia W (2007) Rab4A GTPase catenin interactions are involved in cell junction dynamics in the testis. J Androl 28(5):742–754. doi:10.2164/jandrol.106.002204

    CAS  PubMed  Google Scholar 

  • Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129(6):1201–1213. doi:10.1016/j.cell.2007.03.053

    CAS  PubMed  Google Scholar 

  • Nakamura F, Stossel TP, Hartwig JH (2011) The filamins: organizers of cell structure and function. Cell Adh Migr 5(2):160–169

    PubMed Central  PubMed  Google Scholar 

  • Nakatsuji H, Nishimura N, Yamamura R, Kanayama HO, Sasaki T (2008) Involvement of actinin-4 in the recruitment of JRAB/MICAL-L2 to cell-cell junctions and the formation of functional tight junctions. Mol Cell Biol 28(10):3324–3335

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nikolopoulos SN, Spengler BA, Kisselbach K, Evans AE, Biedler JL, Ross RA (2000) The human non-muscle alpha-actinin protein encoded by the ACTN4 gene suppresses tumorigenicity of human neuroblastoma cells. Oncogene 19(3):380–386. doi:10.1038/sj.onc.1203310

    CAS  PubMed  Google Scholar 

  • Nokes RL, Fields IC, Collins RN, Folsch H (2008) Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells. J Cell Biol 182(5):845–853. doi:10.1083/jcb.200802176

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nottingham RM, Ganley IG, Barr FA, Lambright DG, Pfeffer SR (2011) RUTBC1 protein, a Rab9A effector that activates GTP hydrolysis by Rab32 and Rab33B proteins. J Biol Chem 286(38):33213–33222. doi:10.1074/jbc.M111.261115

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oda H, Takeichi M (2011) Evolution: structural and functional diversity of cadherin at the adherens junction. J Cell Biol 193(7):1137–1146. doi:10.1083/jcb.201008173

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oikonomou KG, Zachou K, Dalekos GN (2011) Alpha-actinin: a multidisciplinary protein with important role in B-cell driven autoimmunity. Autoimmun Rev 10(7):389–396. doi:10.1016/j.autrev.2010.12.009

    CAS  PubMed  Google Scholar 

  • Otey CA, Carpen O (2004) Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskeleton 58(2):104–111. doi:10.1002/cm.20007

    CAS  PubMed  Google Scholar 

  • Oztan A, Silvis M, Weisz OA, Bradbury NA, Hsu SC, Goldenring JR, Yeaman C, Apodaca G (2007) Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol Biol Cell 18(10):3978–3992. doi:10.1091/mbc.E07-02-0097

    PubMed Central  CAS  PubMed  Google Scholar 

  • Palacios F, Price L, Schweitzer J, Collard JG, D’Souza-Schorey C (2001) An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 20(17):4973–4986. doi:10.1093/emboj/20.17.4973

    PubMed Central  CAS  PubMed  Google Scholar 

  • Palacios F, Tushir JS, Fujita Y, D’Souza-Schorey C (2005) Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol 25(1):389–402. doi:10.1128/MCB.25.1.389-402.2005

    PubMed Central  CAS  PubMed  Google Scholar 

  • Paterson AD, Parton RG, Ferguson C, Stow JL, Yap AS (2003) Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J Biol Chem 278(23):21050–21057. doi:10.1074/jbc.M300082200

    CAS  PubMed  Google Scholar 

  • Patrie KM, Drescher AJ, Welihinda A, Mundel P, Margolis B (2002) Interaction of two actin-binding proteins, synaptopodin and alpha-actinin-4, with the tight junction protein MAGI-1. J Biol Chem 277(33):30183–30190. doi:10.1074/jbc.M203072200

    CAS  PubMed  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2000) The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J Mol Biol 301(4):1077–1087. doi:10.1006/jmbi.2000.4010

    CAS  PubMed  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313(4):889–901. doi:10.1006/jmbi.2001.5072

    CAS  PubMed  Google Scholar 

  • Pfeffer S (2003) Membrane domains in the secretory and endocytic pathways. Cell 112(4):507–517

    CAS  PubMed  Google Scholar 

  • Pfeffer SR (2013) Rab GTPase regulation of membrane identity. Curr Opin Cell Biol 25(4):414–419. doi:10.1016/j.ceb.2013.04.002

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pirraglia C, Walters J, Myat MM (2010) Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development 137(24):4177–4189. doi:10.1242/dev.048827

    PubMed Central  CAS  PubMed  Google Scholar 

  • Popowicz GM, Schleicher M, Noegel AA, Holak TA (2006) Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem Sci 31(7):411–419. doi:10.1016/j.tibs.2006.05.006

    CAS  PubMed  Google Scholar 

  • Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141(3):497–508. doi:10.1016/j.cell.2010.03.011

    CAS  PubMed  Google Scholar 

  • Powell RR, Temesvari LA (2004) Involvement of a Rab8-like protein of Dictyostelium discoideum, Sas1, in the formation of membrane extensions, secretion and adhesion during development. Microbiology 150(Pt 8):2513–2525. doi:10.1099/mic.0.27073-0

    CAS  PubMed  Google Scholar 

  • Roberts M, Barry S, Woods A, van der Sluijs P, Norman J (2001) PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 11(18):1392–1402

    CAS  PubMed  Google Scholar 

  • Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR (2007) Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 18(8):2828–2837. doi:10.1091/mbc.E07-02-0169

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F (2005) Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 169(2):285–295. doi:10.1083/jcb.200501162

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sakane A, Honda K, Sasaki T (2010) Rab13 regulates neurite outgrowth in PC12 cells through its effector protein, JRAB/MICAL-L2. Mol Cell Biol 30(4):1077–1087, doi:MCB.01067-09 [pii]10.1128/MCB.01067-09

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sakane A, Abdallah AAM, Nakano K, Honda K, Ikeda W, Nishikawa Y, Matsumoto M, Matsushita N, Kitamura T, Sasaki T (2012) Rab13 small G protein and junctional Rab13-binding protein (JRAB) orchestrate actin cytoskeletal organization during epithelial junctional development. J Biol Chem 287(51):42455–42468. doi:10.1074/jbc.M112.383653

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sakane A, Abdallah AAM, Nakano K, Honda K, Kitamura T, Imoto I, Matsushita N, Sasaki T (2013) Junctional Rab13-binding protein (JRAB) regulates cell spreading via filamins. Genes Cells 18(9):810–822. doi:10.1111/gtc.12078

    CAS  PubMed  Google Scholar 

  • Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, Harada R, Harada A (2007) The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448(7151):366–369. doi:10.1038/nature05929

    CAS  PubMed  Google Scholar 

  • Schweitzer JK, Sedgwick AE, D’Souza-Schorey C (2011) ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin Cell Dev Biol 22(1):39–47. doi:10.1016/j.semcdb.2010.09.002

    PubMed Central  CAS  PubMed  Google Scholar 

  • Seabra MC, Coudrier E (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5(6):393–399. doi:10.1111/j.1398-9219.2004.00190.x

    CAS  PubMed  Google Scholar 

  • Seabra MC, Wasmeier C (2004) Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 16(4):451–457. doi:10.1016/j.ceb.2004.06.014

    CAS  PubMed  Google Scholar 

  • Shen L, Turner JR (2005) Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16(9):3919–3936. doi:10.1091/mbc.E04-12-1089

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sheth B, Fontaine JJ, Ponza E, McCallum A, Page A, Citi S, Louvard D, Zahraoui A, Fleming TP (2000) Differentiation of the epithelial apical junctional complex during mouse preimplantation development: a role for rab13 in the early maturation of the tight junction. Mech Dev 97(1–2):93–104

    CAS  PubMed  Google Scholar 

  • Shin OH, Couvillon AD, Exton JH (2001) Arfophilin is a common target of both class II and class III ADP-ribosylation factors. Biochemistry 40(36):10846–10852

    CAS  PubMed  Google Scholar 

  • Shin K, Fogg VC, Margolis B (2006) Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207–235. doi:10.1146/annurev.cellbio.22.010305.104219

    CAS  PubMed  Google Scholar 

  • Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525. doi:10.1038/nrm2728

    CAS  PubMed  Google Scholar 

  • Su T, Bryant DM, Luton F, Verges M, Ulrich SM, Hansen KC, Datta A, Eastburn DJ, Burlingame AL, Shokat KM, Mostov KE (2010) A kinase cascade leading to Rab11-FIP5 controls transcytosis of the polymeric immunoglobulin receptor. Nat Cell Biol 12(12):1143–1153. doi:10.1038/ncb2118

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sun Y, Bilan PJ, Liu Z, Klip A (2010) Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc Natl Acad Sci U S A 107(46):19909–19914. doi:10.1073/pnas.1009523107

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sunshine C, Francis S, Kirk KL (2000) Rab3B regulates ZO-1 targeting and actin organization in PC12 neuroendocrine cells. Exp Cell Res 257(1):1–10. doi:10.1006/excr.2000.4855

    CAS  PubMed  Google Scholar 

  • Suzuki T, Nakamoto T, Ogawa S, Seo S, Matsumura T, Tachibana K, Morimoto C, Hirai H (2002) MICAL, a novel CasL interacting molecule, associates with vimentin. J Biol Chem 277(17):14933–14941. doi:10.1074/jbc.M111842200

    CAS  PubMed  Google Scholar 

  • Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81(1):153–208

    CAS  PubMed  Google Scholar 

  • Takai Y, Ikeda W, Ogita H, Rikitake Y (2008a) The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu Rev Cell Dev Biol 24:309–342. doi:10.1146/annurev.cellbio.24.110707.175339

    CAS  PubMed  Google Scholar 

  • Takai Y, Miyoshi J, Ikeda W, Ogita H (2008b) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 9(8):603–615. doi:10.1038/nrm2457

    CAS  PubMed  Google Scholar 

  • Takeichi M (2007) The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 8(1):11–20. doi:10.1038/nrn2043

    CAS  PubMed  Google Scholar 

  • Tang VW, Brieher WM (2012) alpha-Actinin-4/FSGS1 is required for Arp2/3-dependent actin assembly at the adherens junction. J Cell Biol 196(1):115–130. doi:10.1083/jcb.201103116

    PubMed Central  CAS  PubMed  Google Scholar 

  • Terai T, Nishimura N, Kanda I, Yasui N, Sasaki T (2006) JRAB/MICAL-L2 is a junctional Rab13-binding protein mediating the endocytic recycling of occludin. Mol Biol Cell 17(5):2465–2475

    PubMed Central  CAS  PubMed  Google Scholar 

  • Terman JR, Mao T, Pasterkamp RJ, Yu HH, Kolodkin AL (2002) MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109(7):887–900

    CAS  PubMed  Google Scholar 

  • Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2(4):285–293. doi:10.1038/35067088

    CAS  PubMed  Google Scholar 

  • Ulrich F, Krieg M, Schotz EM, Link V, Castanon I, Schnabel V, Taubenberger A, Mueller D, Puech PH, Heisenberg CP (2005) Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev Cell 9(4):555–564. doi:10.1016/j.devcel.2005.08.011

    CAS  PubMed  Google Scholar 

  • Utech M, Ivanov AI, Samarin SN, Bruewer M, Turner JR, Mrsny RJ, Parkos CA, Nusrat A (2005) Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 16(10):5040–5052. doi:10.1091/mbc.E05-03-0193

    PubMed Central  CAS  PubMed  Google Scholar 

  • van Ijzendoorn SC, Tuvim MJ, Weimbs T, Dickey BF, Mostov KE (2002) Direct interaction between Rab3b and the polymeric immunoglobulin receptor controls ligand-stimulated transcytosis in epithelial cells. Dev Cell 2(2):219–228

    PubMed  Google Scholar 

  • Vasioukhin V, Bauer C, Yin M, Fuchs E (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100(2):209–219, doi:S0092-8674(00)81559-7 [pii]

    CAS  PubMed  Google Scholar 

  • Wakamatsu Y, Sakai D, Suzuki T, Osumi N (2011) FilaminB is required for the directed localization of cell-cell adhesion molecules in embryonic epithelial development. Dev Dyn 240(1):149–161. doi:10.1002/dvdy.22518

    CAS  PubMed  Google Scholar 

  • Weber E, Berta G, Tousson A, St John P, Green MW, Gopalokrishnan U, Jilling T, Sorscher EJ, Elton TS, Abrahamson DR et al (1994) Expression and polarized targeting of a rab3 isoform in epithelial cells. J Cell Biol 125(3):583–594

    CAS  PubMed  Google Scholar 

  • Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123(5):889–901. doi:10.1016/j.cell.2005.09.020

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yamamura R, Nishimura N, Nakatsuji H, Arase S, Sasaki T (2008) The interaction of JRAB/MICAL-L2 with Rab8 and Rab13 coordinates the assembly of tight junctions and adherens junctions. Mol Biol Cell 19(3):971–983

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yonemura S, Itoh M, Nagafuchi A, Tsukita S (1995) Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J Cell Sci 108:127–142

    CAS  PubMed  Google Scholar 

  • Yoshimura S, Egerer J, Fuchs E, Haas AK, Barr FA (2007) Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol 178(3):363–369. doi:10.1083/jcb.200703047

    PubMed Central  CAS  PubMed  Google Scholar 

  • Youssef G, Gerner L, Naeem AS, Ralph O, Ono M, O’Neill CA, O’Shaughnessy RF (2013) Rab3Gap1 mediates exocytosis of Claudin-1 and tight junction formation during epidermal barrier acquisition. Dev Biol 380(2):274–285. doi:10.1016/j.ydbio.2013.04.034

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yu IM, Hughson FM (2010) Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 26:137–156. doi:10.1146/annurev.cellbio.042308.113327

    CAS  PubMed  Google Scholar 

  • Zahraoui A, Joberty G, Arpin M, Fontaine JJ, Hellio R, Tavitian A, Louvard D (1994) A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J Cell Biol 124(1–2):101–115

    CAS  PubMed  Google Scholar 

  • Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2(2):107–117. doi:10.1038/35052055

    CAS  PubMed  Google Scholar 

  • Zhang XM, Ellis S, Sriratana A, Mitchell CA, Rowe T (2004) Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem 279(41):43027–43034. doi:10.1074/jbc.M402264200

    CAS  PubMed  Google Scholar 

  • Zhang J, Betson M, Erasmus J, Zeikos K, Bailly M, Cramer LP, Braga VM (2005) Actin at cell-cell junctions is composed of two dynamic and functional populations. J Cell Sci 118(Pt 23):5549–5562, doi:jcs.02639 [pii]10.1242/jcs.02639

    CAS  PubMed  Google Scholar 

  • Zhou X, Tian F, Sandzen J, Cao R, Flaberg E, Szekely L, Cao Y, Ohlsson C, Bergo MO, Boren J, Akyurek LM (2007) Filamin B deficiency in mice results in skeletal malformations and impaired microvascular development. Proc Natl Acad Sci U S A 104(10):3919–3924. doi:10.1073/pnas.0608360104

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takuya Sasaki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sakane, A., Sasaki, T. (2015). Roles of Rab Family Small G Proteins in Formation of the Apical Junctional Complex in Epithelial Cells. In: Ebnet, K. (eds) Cell Polarity 1. Springer, Cham. https://doi.org/10.1007/978-3-319-14463-4_15

Download citation

Publish with us

Policies and ethics