Myosin Va acts in concert with Rab27a and MyRIP to regulate acute von-Willebrand factor release from endothelial cells

Traffic

Volumn 12, Issue 10, 2011, Pages 1371-1382

  Rojo Pulido, Inés ^a   Nightingale, Thomas D ^b   Darchen, François ^c   Seabra, Miguel C ^d   Cutler, Daniel F ^b   Gerke, Volker ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c CNRS   (France)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Actin cytoskeleton; Calcium; Histamine; Rab27a; Weibel Palade bodies

Indexed keywords

ACTIN; MYOSIN VA; PROTEIN; PROTEIN MYRIP; RAB27A PROTEIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ACTIN FILAMENT; ARTICLE; CELL ANCHORAGE; CELL STIMULATION; CYTOSKELETON; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; REGULATORY MECHANISM; WEIBEL PALADE BODY;

CELL CULTURE TECHNIQUES; CELL LINE; ENDOTHELIAL CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PLASMIDS; RAB GTP-BINDING PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; VESICULAR TRANSPORT PROTEINS; VON WILLEBRAND FACTOR;

EID: 80052630604     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01248.x     Document Type: Article

References (43)

1. Wagner DD, Frenette PS. The vessel wall and its interactions. Blood 2008;111:5271-5281.
2. Sadler JE. von Willebrand factor assembly and secretion. J Thromb Haemost 2009;7(Suppl. 1):24-27.
3. 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.
4. Michaux G, Abbitt KB, Collinson LM, Haberichter SL, Norman KE, Cutler DF. The physiological function of von Willebrand's factor depends on its tubular storage in endothelial Weibel-Palade bodies. Dev Cell 2006;10:223-232.
5. Dong JF, Moake JL, Nolasco L, Bernardo A, Arceneaux W, Shrimpton CN, Schade AJ, McIntire LV, Fujikawa K, Lopez JA. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 2002;100:4033-4039.
6. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 1998;67:395-424.
7. Sadler JE. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood 2008;112:11-18.
8. Knop M, Aareskjold E, Bode G, Gerke V. Rab3D and annexin A2 play a role in regulated secretion of vWF, but not tPA, from endothelial cells. EMBO J 2004;23:2982-2992.
9. 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;116:3939-3948.
10. 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;113:5010-5018.
11. El-Amraoui A, Schonn JS, Kussel-Andermann P, Blanchard S, Desnos C, Henry JP, Wolfrum U, Darchen F, Petit C. MyRIP, a novel Rab effector, enables myosin VIIa recruitment to retinal melanosomes. EMBO Rep 2002;3:463-470.
12. 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;8:486-499.
13. Desnos C, Schonn JS, Huet S, Tran VS, El-Amraoui A, Raposo G, Fanget I, Chapuis C, Menasche G, de Saint Basile G, Petit C, Cribier S, Henry JP, Darchen F. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 2003;163:559-570.
14. Ivarsson R, Jing X, Waselle L, Regazzi R, Renstrom E. Myosin 5a controls insulin granule recruitment during late-phase secretion. Traffic 2005;6:1027-1035.
15. Espreafico EM, Cheney RE, Matteoli M, Nascimento AA, De Camilli PV, Larson RE, Mooseker MS. Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J Cell Biol 1992;119:1541-1557.
16. Desnos C, Huet S, Darchen F. 'Should I stay or should I go?': myosin V function in organelle trafficking. Biol Cell 2007;99:411-423.
17. Eichler TW, Kogel T, Bukoreshtliev NV, Gerdes HH. The role of myosin Va in secretory granule trafficking and exocytosis. Biochem Soc Trans 2006;34:671-674.
18. Kogel T, Bittins CM, Rudolf R, Gerdes HH. Versatile roles for myosin Va in dense core vesicle biogenesis and function. Biochem Soc Trans 2010;38:199-204.
19. Woolner S, Bement WM. Unconventional myosins acting unconventionally. Trends Cell Biol 2009;19:245-252.
20. Seabra MC, Coudrier E. Rab GTPases and myosin motors in organelle motility. Traffic 2004;5:393-399.
21. Fukuda M, Kuroda TS. Slac2-c (synaptotagmin-like protein homologue lacking C2 domains-c), a novel linker protein that interacts with Rab27, myosin Va/VIIa, and actin. J Biol Chem 2002;277:43096-43103.
22. Manneville JB, Etienne-Manneville S, Skehel P, Carter T, Ogden D, Ferenczi M. Interaction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells. J Cell Sci 2003;116:3927-3938.
23. Rondaij MG, Bierings R, Kragt A, Gijzen KA, Sellink E, van Mourik JA, Fernandez-Borja M, Voorberg J. Dynein-dynactin complex mediates protein kinase A-dependent clustering of Weibel-Palade bodies in endothelial cells. Arterioscler Thromb Vasc Biol 2006;26:49-55.
24. Vischer UM, Barth H, Wollheim CB. Regulated von Willebrand factor secretion is associated with agonist-specific patterns of cytoskeletal remodeling in cultured endothelial cells. Arterioscler Thromb Vasc Biol 2000;20:883-891.
25. Wagner DD, Marder VJ. Biosynthesis of von Willebrand protein by human endothelial cells: processing steps and their intracellular localization. J Cell Biol 1984;99:2123-2130.
26. Kuroda TS, Fukuda M, Ariga H, Mikoshiba K. The Slp homology domain of synaptotagmin-like proteins 1-4 and Slac2 functions as a novel Rab27A binding domain. J Biol Chem 2002;277:9212-9218.
27. Wu X, Bowers B, Rao K, Wei Q, Hammer JA 3rd. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J Cell Biol 1998;143:1899-1918.
28. Desnos C, Huet S, Fanget I, Chapuis C, Bottiger C, Racine V, Sibarita JB, Henry JP, Darchen F. Myosin va mediates docking of secretory granules at the plasma membrane. J Neurosci 2007;27:10636-10645.
29. Ruggeri ZM. Von Willebrand factor: looking back and looking forward. Thromb Haemost 2007;98:55-62.
30. Sadler JE. Low von Willebrand factor: sometimes a risk factor and sometimes a disease. Hematology Am Soc Hematol Educ Program 2009;2009:106-112.
31. Kuroda TS, Itoh T, Fukuda M. Functional analysis of slac2-a/melanophilin as a linker protein between Rab27A and myosin Va in melanosome transport. Methods Enzymol 2005;403:419-431.
32. Watanabe M, Nomura K, Ohyama A, Ishikawa R, Komiya Y, Hosaka K, Yamauchi E, Taniguchi H, Sasakawa N, Kumakura K, Ushiki T, Sato O, Ikebe M, Igarashi M. Myosin-Va regulates exocytosis through the submicromolar Ca2+-dependent binding of syntaxin-1A. Mol Biol Cell 2005;16:4519-4530.
33. Correia SS, Bassani S, Brown TC, Lise MF, Backos DS, El-Husseini A, Passafaro M, Esteban JA. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 2008;11:457-466.
34. Bittins CM, Eichler TW, Gerdes HH. Expression of the dominant-negative tail of myosin Va enhances exocytosis of large dense core vesicles in neurons. Cell Mol Neurobiol 2009;29:597-608.
35. Kogel T, Rudolf R, Hodneland E, Hellwig A, Kuznetsov SA, Seiler F, Sollner TH, Barroso J, Gerdes HH. Distinct roles of myosin Va in membrane remodeling and exocytosis of secretory granules. Traffic 2010;11:637-650.
36. Kondo H, Shirakawa R, Higashi T, Kawato M, Fukuda M, Kita T, Horiuchi H. Constitutive GDP/GTP exchange and secretion-dependent GTP hydrolysis activity for Rab27 in platelets. J Biol Chem 2006;281:28657-28665.
37. Handley MT, Haynes LP, Burgoyne RD. Differential dynamics of Rab3A and Rab27A on secretory granules. J Cell Sci 2007;120:973-984.
38. Hannah MJ, Skehel P, Erent M, Knipe L, Ogden D, Carter T. Differential kinetics of cell surface loss of von Willebrand factor and its propolypeptide after secretion from Weibel-Palade bodies in living human endothelial cells. J Biol Chem 2005;280:22827-22830.
39. Babich V, Meli A, Knipe L, Dempster JE, Skehel P, Hannah MJ, Carter T. Selective release of molecules from Weibel-Palade bodies during a lingering kiss. Blood 2008;111:5282-5290.
40. Swiatecka-Urban A, Talebian L, Kanno E, Moreau-Marquis S, Coutermarsh B, Hansen K, Karlson KH, Barnaby R, Cheney RE, Langford GM, Fukuda M, Stanton BA. Myosin Vb is required for trafficking of the cystic fibrosis transmembrane conductance regulator in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells. J Biol Chem 2007;282:23725-23736.
41. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 1973;52:2745-2756.
42. 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;170:627-636.
43. Disse J, Vitale N, Bader MF, Gerke V. Phospholipase D1 is specifically required for regulated secretion of von Willebrand factor from endothelial cells. Blood 2009;113:973-980.