A role for Rab10 in von Willebrand factor release discovered by an AP-1 interactor screen in C. elegans

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 2, 2011, Pages 392-401

  Michaux, G ^a,b   Dyer, C E F ^c   Nightingale, T D ^c   Gallaud, E ^a   Nurrish, S ^c   Cutler, D F ^c  

^a INSERM   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Adaptor complex AP 1; Caenorhabditis elegans; Genomewide RNAi screen; Rab10; Rab8; Von Willebrand factor; Weibel Palade bodies

Indexed keywords

CLATHRIN; RAB PROTEIN; RAB10 PROTIEN; RAB8A PROTEIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; GOLGI COMPLEX; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; RNA INTERFERENCE; THROMBOCYTE ADHESION; TRANS GOLGI NETWORK; UMBILICAL VEIN; UMBILICAL VEIN ENDOTHELIAL CELL; WEIBEL PALADE BODY;

EID: 79251588754     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2010.04138.x     Document Type: Article

References (48)

1. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 1998; 67: 395-424.
2. Bowie EJ, Solberg Jr., LA, Fass DN, Johnson CM, Knutson GJ, Stewart ML, Zoecklein LJ. Transplantation of normal bone marrow into a pig with severe von Willebrand's disease. J Clin Invest 1986; 78: 26-30.
3. Wagner DD. Cell biology of von Willebrand factor. Annu Rev Cell Biol 1990; 6: 217-46.
4. Weibel ER, Palade GE. New cytoplasmic components in arterial endothelia. J Cell Biol 1964; 23: 101-12.
5. Metcalf DJ, Nightingale TD, Zenner HL, Lui-Roberts WW, Cutler DF. Formation and function of Weibel-Palade bodies. J Cell Sci 2008; 121: 19-27.
6. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004; 14: 167-74.
7. Lui-Roberts WW, Collinson LM, Hewlett LJ, Michaux G, Cutler DF. An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells. J Cell Biol 2005; 170: 627-36.
8. Lui-Roberts WW, Ferraro F, Nightingale TD, Cutler DF. Aftiphilin and gamma-synergin are required for secretagogue sensitivity of Weibel-Palade bodies in endothelial cells. Mol Biol Cell 2008; 19: 5072-81.
9. Baust T, Czupalla C, Krause E, Bourel-Bonnet L, Hoflack B. Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc Natl Acad Sci U S A 2006; 103: 3159-64.
10. Lui WW, Collins BM, Hirst J, Motley A, Millar C, Schu P, Owen DJ, Robinson MS. Binding partners for the COOH-terminal appendage domains of the GGAs and gamma-adaptin. Mol Biol Cell 2003; 14: 2385-98.
11. Praefcke GJ, Ford MG, Schmid EM, Olesen LE, Gallop JL, Peak-Chew SY, Vallis Y, Babu MM, Mills IG, McMahon HT. Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis. EMBO J 2004; 23: 4371-83.
12. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, Benmerah A, McMahon HT. Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 2006; 4: e262.
13. Schmid EM, McMahon HT. Integrating molecular and network biology to decode endocytosis. Nature 2007; 448: 883-8.
14. Shim J, Sternberg PW, Lee J. Distinct and redundant functions of mu1 medium chains of the AP-1 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol Biol Cell 2000; 11: 2743-56.
15. Lee J, Jongeward GD, Sternberg PW. Unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes Dev 1994; 8: 60-73.
16. Chen YT, Holcomb C, Moore HP. Expression and localization of two low molecular weight GTP-binding proteins, Rab8 and Rab10, by epitope tag. Proc Natl Acad Sci U S A 1993; 90: 6508-12.
17. Salminen A, Novick PJ. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 1987; 49: 527-38.
18. Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, Mellman I, Simons K. Rab 10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 2007; 8: 47-60.
19. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW. Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 2006; 17: 3156-75.
20. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, Grant BD. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 2006; 17: 1286-97.
21. Ang AL, Folsch H, Koivisto UM, Pypaert M, Mellman I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 2003; 163: 339-50.
22. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 1993; 123: 35-45.
23. Peranen J, Auvinen P, Virta H, Wepf R, Simons K. Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J Cell Biol 1996; 135: 153-67.
24. Chabrillat ML, Wilhelm C, Wasmeier C, Sviderskaya EV, Louvard D, Coudrier E. Rab8 regulates the actin-based movement of melanosomes. Mol Biol Cell 2005; 16: 1640-50.
25. Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 2007; 18: 2828-37.
26. Hannah MJ, Hume AN, Arribas M, Williams R, Hewlett LJ, Seabra MC, Cutler DF. Weibel-Palade bodies recruit Rab27 by a content-driven, maturation-dependent mechanism that is independent of cell type. J Cell Sci 2003; 116: 3939-48.
27. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77: 71-94.
28. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000; 408: 325-30.
29. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003; 30: 313-21.
30. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, Fire A, Ahringer J, Plasterk RH. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 2002; 12: 1317-19.
31. Michelet X, Alberti A, Benkemoun L, Roudier N, Lefebvre C, Legouis R. The ESCRT-III protein CeVPS-32 is enriched in domains distinct from CeVPS-27 and CeVPS-23 at the endosomal membrane of epithelial cells. Biol Cell 2009; 101: 599-615.
32. Michaux G, Hewlett LJ, Messenger SL, Goodeve AC, Peake IR, Daly ME, Cutler DF. Analysis of intracellular storage and regulated secretion of 3 von Willebrand disease-causing variants of von Willebrand factor. Blood 2003; 102: 2452-8.
33. Blagoveshchenskaya AD, Hannah MJ, Allen S, Cutler DF. Selective and signal-dependent recruitment of membrane proteins to secretory granules formed by heterologously expressed von Willebrand factor. Mol Biol Cell 2002; 13: 1582-93.
34. Lopes VS, Ramalho JS, Owen DM, Karl MO, Strauss O, Futter CE, Seabra MC. The ternary Rab27a-Myrip-Myosin VIIa complex regulates melanosome motility in the retinal pigment epithelium. Traffic 2007; 8: 486-99.
35. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-8.
36. Hanson PI, Shim S, Merrill SA. Cell biology of the ESCRT machinery. Curr Opin Cell Biol. 2009; 21: 568-74.
37. Holmes A, Flett A, Coudreuse D, Korswagen HC, Pettitt J. C. elegans disabled is required for cell-type specific endocytosis and is essential in animals lacking the AP-3 adaptor complex. J Cell Sci 2007; 120: 2741-51.
38. Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood 2008; 112: 957-64.
39. Knipe L, Meli A, Hewlett L, Bierings R, Dempster J, Skehel P, Hannah MJ, Carter T. A revised model for the secretion of tPA and cytokines from cultured endothelial cells. Blood 2010; 116: 2183-91.
40. Harrison-Lavoie KJ, Michaux G, Hewlett L, Kaur J, Hannah MJ, Lui-Roberts WW, Norman KE, Cutler DF. P-selectin and CD63 use different mechanisms for delivery to Weibel-Palade bodies. Traffic. 2006; 7: 647-62.
41. Nightingale TD, Pattni K, Hume AN, Seabra MC, Cutler DF. Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 2009; 113: 5010-18.
42. Raposo G, Marks MS. Melanosomes-dark organelles enlighten endosomal membrane transport. Nat Rev Mol Cell Biol 2007; 8: 786-97.
43. Le N, Simon MA. Disabled is a putative adaptor protein that functions during signaling by the sevenless receptor tyrosine kinase. Mol Cell Biol 1998; 18: 4844-54.
44. Mishra SK, Keyel PA, Hawryluk MJ, Agostinelli NR, Watkins SC, Traub LM. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J 2002; 21: 4915-26.
45. Morris SM, Cooper JA. Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2001; 2: 111-23.
46. Babst M, Wendland B, Estepa EJ, Emr SD. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 1998; 17: 2982-93.
47. Folsch H, Ohno H, Bonifacino JS, Mellman I. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 1999; 99: 189-98.
48. Shavit JA, Manichaikul A, Lemmerhirt HL, Broman KW, Ginsburg D. Modifiers of von Willebrand factor identified by natural variation in inbred strains of mice. Blood 2009; 114: 5368-74.