Rab35 regulates cadherin-mediated adherens junction formation and myoblast fusion

Molecular Biology of the Cell

Volumn 24, Issue 3, 2013, Pages 234-245

  Charrasse, Sophie ^a   Comunale, Franck ^a   De Rossi, Sylvain ^b   Echard, Arnaud ^c   Gauthier Rouvière, Ćcile ^a  

^a Centre National de la Recherche Scientifique   (France)

^b University of Montpellier   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CATENIN; CLATHRIN; GUANOSINE TRIPHOSPHATASE; M CADHERIN; NERVE CELL ADHESION MOLECULE; PHOSPHATIDYL INOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL; PROTEIN P120; RAB35 ENZYME; TRANSFERRIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CELL FUSION; CELL JUNCTION; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MYOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL DIFFERENTIATION; CELL FUSION; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MICE; MYOBLASTS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN STABILITY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84873365417     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-02-0167     Document Type: Article

References (54)

1. Akiyama C, Shinozaki-Narikawa N, Kitazawa T, Hamakubo T, Kodama T, Shibasaki Y (2005). Phosphatidylinositol-4-phosphate 5-kinase gamma is associated with cell-cell junction in A431 epithelial cells. Cell Biol Int 29, 514-520.
2. Allaire PD, Marat AL, Dall'Armi C, Di Paolo G, McPherson PS, Ritter B (2010). The Connecdenn DENN domain: a GEF for Rab35 mediating cargo-specific exit from early endosomes. Mol Cell 37, 370-382.
3. Bach AS, Enjalbert S, Comunale F, Bodin S, Vitale N, Charrasse S, Gauthier-Rouviere C (2010). ADP-ribosylation factor 6 regulates mammalian myoblast fusion through phospholipase D1 and phosphatidylinositol 4,5-bisphosphate signaling pathways. Mol Biol Cell 21, 2412-2424.
4. Baum B, Georgiou M (2011). Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192, 907-917.
5. Bhuin T, Roy JK (2009). Rab11 is required for myoblast fusion in Drosophila. Cell Tissue Res 336, 489-499.
6. Braga VM, Betson M, Li X, Lamarche-Vane N (2000). Activation of the small GTPase Rac is sufficient to disrupt cadherin-dependent cell-cell adhesion in normal human keratinocytes. Mol Biol Cell 11, 3703-3721.
7. Charrasse S, Comunale F, Grumbach Y, Poulat F, Blangy A, Gauthier-Rouviere C (2006). RhoA GTPase regulates M-cadherin activity and myoblast fusion. Mol Biol Cell 17, 749-759.
8. Charrasse S, Meriane M, Comunale F, Blangy A, Gauthier-Rouviere C (2002). N-cadherin-dependent cell-cell contact regulates Rho GTPases and beta-catenin localization in mouse C2C12 myoblasts. J Cell Biol 158, 953-965.
9. Chesneau L, Dambournet D, Machicoane M, Kouranti I, Fukuda M, Goud B, Echard A (2012). An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol 22, 147-152.
10. Chevallier J, Koop C, Srivastava A, Petrie RJ, Lamarche-Vane N, Presley JF (2009). Rab35 regulates neurite outgrowth and cell shape. FEBS Lett 583, 1096-1101.
11. Christofori G (2003). Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression. EMBO J 22, 2318-2322.
12. Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, El Marjou A, Formstecher E, Salomon R, Goud B, Echard A (2011). Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13, 981-988.
13. Davis MA, Ireton RC, Reynolds AB (2003). A core function for p120-catenin in cadherin turnover. J Cell Biol 163, 525-534.
14. Delva E, Kowalczyk AP (2009). Regulation of cadherin trafficking. Traffic 10, 259-267.
15. Desclozeaux M, Venturato J, Wylie FG, Kay JG, Joseph SR, Le HT, Stow JL (2008). Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am J Physiol Cell Physiol 295, C545-556.
16. Egami Y, Fukuda M, Araki N (2011). Rab35 regulates phagosome formation through recruitment of ACAP2 in macrophages during FcgammaR-mediated phagocytosis. J Cell Sci 124, 3557-3567.
17. El Sayegh TY, Arora PD, Ling K, Laschinger C, Janmey PA, Anderson RA, McCulloch CA (2007). Phosphatidylinositol-4,5 bisphosphate produced by PIP5KIgamma regulates gelsolin, actin assembly, and adhesion strength of N-cadherin junctions. Mol Biol Cell 18, 3026-3038.
18. Fortier M, Comunale F, Kucharczak J, Blangy A, Charrasse S, Gauthier-Rouviere C (2008). RhoE controls myoblast alignment prior fusion through RhoA and ROCK. Cell Death Differ 15, 1221-1231.
19. Fukata M, Kaibuchi K (2001). Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat Rev Mol Cell Biol 2, 887-897.
20. Gabev E, Kasianowicz J, Abbott T, McLaughlin S (1989). Binding of neomycin to phosphatidylinositol 4,5-bisphosphate (PIP2). Biochim Biophys Acta 979, 105-112.
21. Gao Y, Balut CM, Bailey MA, Patino-Lopez G, Shaw S, Devor DC (2010). Recycling of the Ca2+-activated K+ channel, KCa2.3, is dependent upon RME-1, Rab35/EPI64C, and an N-terminal domain. J Biol Chem 285, 17938-17952.
22. Griffin HD, Hawthorne JN (1978). Calcium-activated hydrolysis of phosphatidyl-myo-inositol 4-phosphate and phosphatidyl-myo-inositol 4,5-bisphosphate in guinea-pig synaptosomes. Biochem J 176, 541-552.
23. Halbleib JM, Nelson WJ (2006). Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20, 3199-3214.
24. Hallcher LM, Sherman WR (1980). The effects of lithium ion and other agents on the activity of myo-inositol-1-phosphatase from bovine brain. J Biol Chem 255, 10896-10901.
25. Hammond GR, Schiavo G, Irvine RF (2009). Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P(2). Biochem J 422, 23-35.
26. Harris TJ, Tepass U (2011). Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11, 502-514.
27. Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, Nakajima K, Nabeshima Y, Hoshino M (2010). Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67, 588-602.
28. Kemler R (1993). From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 9, 317-321.
29. Kobayashi H, Fukuda M (2012). Rab35 regulates Arf6 activity through centaurin-B2 (ACAP2) during neurite outgrowth. J Cell Sci 125, 2235-2242.
30. Kouranti I, Sachse M, Arouche N, Goud B, Echard A (2006). Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16, 1719-1725.
31. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P (2000). GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149, 1455-1472.
32. Ling K, Bairstow SF, Carbonara C, Turbin DA, Huntsman DG, Anderson RA (2007). Type Igamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J Cell Biol 176, 343-352.
33. Lozano E, Betson M, Braga VM (2003). Tumor progression: small GTPases and loss of cell-cell adhesion. Bioessays 25, 452-462.
34. Macia E, Partisani M, Favard C, Mortier E, Zimmermann P, Carlier MF, Gounon P, Luton F, Franco M (2008). The pleckstrin homology domain of the Arf6-specific exchange factor EFA6 localizes to the plasma membrane by interacting with phosphatidylinositol 4,5-bisphosphate and F-actin. J Biol Chem 283, 19836-19844.
35. Naslavsky N, Caplan S (2011). EHD proteins: key conductors of endocytic transport. Trends Cell Biol 21, 122-131.
36. 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, 4973-4986.
37. 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, 389-402.
38. Patino-Lopez G, Dong X, Ben-Aissa K, Bernot KM, Itoh T, Fukuda M, Kruhlak MJ, Samelson LE, Shaw S (2008). Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J Biol Chem 283, 18323-18330.
39. Perez-Moreno M, Jamora C, Fuchs E (2003). Sticky business: orchestrating cellular signals at adherens junctions. Cell 112, 535-548.
40. Ponti A, Schward P, Gulati A, Bäcker V (2007). Huygens Remote Manager. Imaging Microsc 9, 57-58.
41. Posey ADJr., Pytel P, Gardikiotes K, Demonbreun AR, Rainey M, George M, Band H, McNally EM (2011). Endocytic recycling proteins EHD1 and EHD2 interact with fer-1-like-5 (Fer1L5) and mediate myoblast fusion. J Biol Chem 286, 7379-7388.
42. Rahajeng J, Panapakkam Giridharan SS, Cai B, Naslavsky N, Caplan S (2012). MICAL-L1 is a tubular endosomal membrane hub that connects Rab35 and Arf6 with Rab8a. Traffic 13, 82-92.
43. Roeth JF, Sawyer JK, Wilner DA, Peifer M (2009). Rab11 helps maintain apical crumbs and adherens junctions in the Drosophila embryonic ectoderm. PLoS One 4, e7634.
44. Schill NJ, Anderson RA (2009). Out, in and back again: PtdIns(4,5)P(2) regulates cadherin trafficking in epithelial morphogenesis. Biochem J 418, 247-260.
45. Shim J, Lee SM, Lee MS, Yoon J, Kweon HS, Kim YJ (2010). Rab35 mediates transport of Cdc42 and Rac1 to the plasma membrane during phagocytosis. Mol Cell Biol 30, 1421-1432.
46. Stenmark H (2009). Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10, 513-525.
47. Takeichi M (1995). Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7, 619-627.
48. Taulet N, Comunale F, Favard C, Charrasse S, Bodin S, Gauthier-Rouviere C (2009). N-cadherin/p120 catenin association at cell-cell contacts occurs in cholesterol-rich membrane domains and is required for RhoA activation and myogenesis. J Biol Chem 284, 23137-23145.
49. Troyanovsky S (2005). Cadherin dimers in cell-cell adhesion. Eur J Cell Biol 84, 225-232.
50. Varnai P, Balla T (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium-and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143, 501-510.
51. Xiao K, Allison DF, Buckley KM, Kottke MD, Vincent PA, Faundez V, Kowalczyk AP (2003). Cellular levels of p120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells. J Cell Biol 163, 535-545.
52. Yap AS, Crampton MS, Hardin J (2007). Making and breaking contacts: the cellular biology of cadherin regulation. Curr Opin Cell Biol 19, 508-514.
53. Zerial M, McBride H (2001). Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2, 107-117.
54. Zhang J, Fonovic M, Suyama K, Bogyo M, Scott MP (2009). Rab35 controls actin bundling by recruiting fascin as an effector protein. Science 325, 1250-1254.