Connecdenn 3/DENND1C binds actin linking Rab35 activation to the actin cytoskeleton

Molecular Biology of the Cell

Volumn 23, Issue 1, 2012, Pages 163-175

  Marat, Andrea L ^a   Ioannou, Maria S ^a   McPherson, Peter S ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CONNECDENN 3; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAB PROTEIN; RAB35 PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SHAPE; CYTOSKELETON; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ACTIN CYTOSKELETON; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL SHAPE; CONSERVED SEQUENCE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS;

EID: 84855393932     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-05-0474     Document Type: Article

References (55)

1. Adams JC, Clelland JD, Collett GD, Matsumura F, Yamashiro S, Zhang L (1999). Cell-matrix adhesions differentially regulate fascin phosphorylation. Mol Biol Cell 10, 4177-4190.
2. Allaire PD, Marat AL, Dall'Armi C, Di PG, 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. Allaire PD, Ritter B, Thomas S, Burman JL, Denisov AY, Legendre-Guillemin V, Harper SQ, Davidson BL, Gehring K, McPherson PS (2006). Connecdenn, a novel DENN domain-containing protein of neuronal clathrin-coated vesicles functioning in synaptic vesicle endocytosis. J Neurosci 26, 13202-13212. (Pubitemid 46011630)
4. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW (2006). Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17, 3156-3175. (Pubitemid 43993517)
5. Carney DS, Davies BA, Horazdovsky BF (2006). Vps9 domain-containing proteins: activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol 16, 27-35. (Pubitemid 43077092)
6. 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, 1373-1376. (Pubitemid 32476223)
7. 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.
8. Chua CE, Lim YS, Tang BL (2010). Rab35-a vesicular traffic-regulating small GTPase with actin modulating roles. FEBS Lett 584, 1-6.
9. Corbett MA et al. (2010). A focal epilepsy and intellectual disability syndrome is due to a mutation in TBC1D24. Am J Hum Genet 87, 371-375.
10. Delprato A, Merithew E, Lambright DG (2004). Structure, exchange determinants, and family-wide Rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 118, 607-617. (Pubitemid 39179713)
11. dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, Berry DA, Nosworthy NJ (2003). Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 83, 433-473. (Pubitemid 36378678)
12. Ducka AM, Joel P, Popowicz GM, Trybus KM, Schleicher M, Noegel AA, Huber R, Holak TA, Sitar T (2010). Structures of actin-bound Wiskott-Aldrich syndrome protein homology 2 (WH2) domains of Spire and the implication for filament nucleation. Proc Natl Acad Sci USA 107, 11757-11762.
13. Falace A et al. (2010). TBC1D24, an ARF6-interacting protein, is mutated in familial infantile myoclonic epilepsy. Am J Hum Genet 87, 365-370.
14. Friederich E, Vancompernolle K, Huet C, Goethals M, Finidori J, Vandekerckhove J, Louvard D (1992). An actin-binding site containing a conserved motif of charged amino acid residues is essential for the morphogenic effect of villin. Cell 70, 81-92.
15. Fukuda M (2011). TBC proteins: GAPs for mammalian small GTPase Rab? Biosci Rep 31, 159-168.
16. 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, 17938-17953.
17. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006). PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461. (Pubitemid 44871952)
18. Heo WD, Meyer T (2003). Switch-of-function mutants based on morphology classification of Ras superfamily small GTPases. Cell 113, 315-328. (Pubitemid 36556114)
19. Hsu C et al. (2010). Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189, 223-232.
20. Hussain NK et al. (2001). Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3, 927-932. (Pubitemid 32952259)
21. Hutagalung AH, Novick PJ (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91, 119-149.
22. Kanno E, Ishibashi K, Kobayashi H, Matsui T, Ohbayashi N, Fukuda M (2010). Comprehensive screening for novel Rab-binding proteins by GST pull-down assay using 60 different mammalian Rabs. Traffic 11, 491-507.
23. Kloer DP, Rojas R, Ivan V, Moriyama K, Ivan V, Murthy N, Ghirlando R, van der Sluijs P, Hurley JH, Bonifacino JS (2010). Assembly of the biogenesis of lysosome-related organelles complex-3 (BLOC-3) and its interaction with Rab9. J Biol Chem 285, 7794-7804.
24. 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. (Pubitemid 44691778)
25. Levivier E, Goud B, Souchet M, Calmels TP, Mornon JP, Callebaut I (2001). uDENN, DENN, and dDENN: indissociable domains in Rab and MAP kinases signaling pathways. Biochem Biophys Res Commun 287, 688-695. (Pubitemid 32912769)
26. Liao Y et al. (1999). RA-GEF, a novel Rap1A guanine nucleotide exchange factor containing a Ras/Rap1A-associating domain, is conserved between nematode and humans. J Biol Chem 274, 37815-37820. (Pubitemid 30026845)
27. Liao Y, Satoh T, Gao X, Jin TG, Hu CD, Kataoka T (2001). RA-GEF-1, a guanine nucleotide exchange factor for Rap1, is activated by translocation induced by association with Rap1*GTP and enhances Rap1-dependent B-Raf activation. J Biol Chem 276, 28478-28483.
28. Marat AL, Dokainish H, McPherson PS (2011). DENN domain proteins: regulators of Rab GTPases. J Biol Chem 286, 13791-13800.
29. Marat AL, McPherson PS (2010). The connecdenn family, Rab35 guanine nucleotide exchange factors interfacing with the clathrin machinery. J Biol Chem 285, 10627-10637.
30. Miki H, Miura K, Takenawa T (1996). N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J 15, 5326-5335. (Pubitemid 26336215)
31. 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, 3324-3335. (Pubitemid 351657096)
32. 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, 845-853.
33. 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.
34. Saito K, Murai J, Kajiho H, Kontani K, Kurosu H, Katada T (2002). A novel binding protein composed of homophilic tetramer exhibits unique properties for the small GTPase Rab5. J Biol Chem 277, 3412-3418. (Pubitemid 34953210)
35. 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, 1077-1087.
36. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, Chavez JA, Lienhard GE, McGraw TE (2007). Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5, 293-303. (Pubitemid 46477855)
37. Sano H, Peck GR, Kettenbach AN, Gerber SA, Lienhard GE (2011). Insulin-stimulated GLUT4 protein translocation in adipocytes requires the Rab10 guanine nucleotide exchange factor Dennd4C. J Biol Chem 286, 16541-16545.
38. Sato M, Sato K, Liou W, Pant S, Harada A, Grant BD (2008). Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J 27, 1183-1196. (Pubitemid 351574749)
39. Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A (2009). RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol Cell 36, 1060-1072.
40. Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, Mellman I, Simons K (2007). Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8, 47-60. (Pubitemid 44921882)
41. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007). Rab GTPases at a glance. J Cell Sci 120, 3905-3910. (Pubitemid 350269396)
42. Shi A, Chen CC, Banerjee R, Glodowski D, Audhya A, Rongo C, Grant BD (2010). EHBP-1 functions with RAB-10 during endocytic recycling in Caenorhabditis elegans. Mol Biol Cell 21, 2930-2943.
43. 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, 1421-1433.
44. Stenmark H (2009). Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10, 513-525.
45. Stringham E, Pujol N, Vandekerckhove J, Bogaert T (2002). unc-53 controls longitudinal migration in C. elegans. Development 129, 3367-3379.
46. Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K, Verstreken P (2011). Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 145, 117-132.
47. Vaduva G, Martin NC, Hopper AK (1997). Actin-binding verprolin is a polarity development protein required for the morphogenesis and function of the yeast actin cytoskeleton. J Cell Biol 139, 1821-1833. (Pubitemid 28079245)
48. Van TM, Dewitte D, Goethals M, Carlier MF, Vandekerckhove J, Ampe C (1996). The actin binding site of thymosin beta 4 mapped by mutational analysis. EMBO J 15, 201-210. (Pubitemid 26029199)
49. Vancompernolle K, Goethals M, Huet C, Louvard D, Vandekerckhove J (1992). G- to F-actin modulation by a single amino acid substitution in the actin binding site of actobindin and thymosin beta 4. EMBO J 11, 4739-4746. (Pubitemid 23023416)
50. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006). Role of fascin in filopodial protrusion. J. Cell Biol 174, 863-875. (Pubitemid 44373735)
51. Walseng E, Bakke O, Roche PA (2008). Major histocompatibility complex class II-peptide complexes internalize using a clathrin- and dynamin-independent endocytosis pathway. J Biol Chem 283, 14717-14727.
52. Wang D, Lou J, Ouyang C, Chen W, Liu Y, Liu X, Cao X, Wang J, Lu L (2010). Ras-related protein Rab10 facilitates TLR4 signaling by promoting replenishment of TLR4 onto the plasma membrane. Proc Natl Acad Sci USA 107, 13806-13811.
53. Yoshimura S, Gerondopoulos A, Linford A, Rigden DJ, Barr FA (2010). Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors. J Cell Biol 191, 367-381.
54. Zerial M, McBride H (2001). Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2, 107-117. (Pubitemid 33674039)
55. 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.