Arf6 controls platelet spreading and clot retraction via integrin αIIbβ3 trafficking

Blood

Volumn 127, Issue 11, 2016, Pages 1459-1467

  Huang, Yunjie ^a   Joshi, Smita ^a   Xiang, Binggang ^a   Kanaho, Yasunori ^b   Li, Zhenyu ^a   Bouchard, Beth A ^c   Moncman, Carole L ^a   Whiteheart, Sidney W ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ALPHA2 INTEGRIN; FLUORESCEIN ISOTHIOCYANATE; INTEGRIN; INTEGRIN ALPHA 2B BETA 3; MYOSIN LIGHT CHAIN; RAB11 PROTEIN; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6; FIBRINOGEN; FIBRINOGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSAY; BLEEDING; BLOOD CLOT RETRACTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; EX VIVO STUDY; EXPERIMENTAL MODEL; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; THROMBOCYTE; ANIMAL; BIOTINYLATION; CELL GRANULE; CELL MEMBRANE; CELL SIZE; DEFICIENCY; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ADP-RIBOSYLATION FACTORS; ANIMALS; BIOTINYLATION; BLOOD PLATELETS; CELL MEMBRANE; CELL SIZE; CLOT RETRACTION; CYTOPLASMIC GRANULES; ENDOCYTOSIS; FIBRINOGEN; HUMANS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84961808101     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-05-648550     Document Type: Article

References (36)

1. Karim ZA, Zhang J, Banerjee M, et al. IkB kinase phosphorylation of SNAP-23 controls platelet secretion. Blood. 2013;121(22):4567-4574.
2. Ye S, Huang Y, Joshi S, et al. Platelet secretion and hemostasis require syntaxin-binding protein STXBP5. J Clin Invest. 2014;124(10):4517-4528.
3. Feng W, Madajka M, Kerr BA, Mahabeleshwar GH, Whiteheart SW, Byzova TV. A novel role for platelet secretion in angiogenesis: mediating bone marrow-derived cell mobilization and homing. Blood. 2011;117(14):3893-3902.
4. Ouseph MM, Huang Y, Banerjee M, et al. Autophagy is induced upon platelet activation and is essential for hemostasis and thrombosis. Blood. 2015;126(10):1224-1233.
5. Handagama P, Scarborough RM, Shuman MA, Bainton DF. Endocytosis of fibrinogen into megakaryocyte and platelet alpha-granules is mediated by alpha IIb beta 3 (glycoprotein IIb-IIIa). Blood. 1993;82(1):135-138.
6. Handagama P, Rappolee DA, Werb Z, Levin J, Bainton DF. Platelet alpha-granule fibrinogen, albumin, and immunoglobulin G are not synthesized by rat and mouse megakaryocytes. J Clin Invest. 1990;86(4):1364-1368.
7. Handagama P, Bainton DF, Jacques Y, Conn MT, Lazarus RA, Shuman MA. Kistrin, an integrin antagonist, blocks endocytosis of fibrinogen into guinea pig megakaryocyte and platelet alphagranules. J Clin Invest. 1993;91(1):193-200.
8. Klement GL, Yip TT, Cassiola F, et al. Platelets actively sequester angiogenesis regulators. Blood. 2009;113(12):2835-2842.
9. Donaldson JG. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem. 2003;278(43):41573-41576.
10. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol. 2006;7(5):347-358.
11. Burkhart JM, Vaudel M, Gambaryan S, et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood. 2012;120(15):e73-e82.
12. Choi W, Karim ZA, Whiteheart SW. Arf6 plays an early role in platelet activation by collagen and convulxin. Blood. 2006;107(8):3145-3152.
13. Karim ZA, Choi W, Whiteheart SW. Primary platelet signaling cascades and integrinmediated signaling control ADP-ribosylation factor (Arf) 6-GTP levels during platelet activation and aggregation. J Biol Chem. 2008;283(18):11995-12003.
14. Kanamarlapudi V, Owens SE, Saha K, Pope RJ, Mundell SJ. ARF6-dependent regulation of P2Y receptor traffic and function in human platelets. PLoS One. 2012;7(8):e43532.
15. Moroi M, Jung SM. Integrin-mediated platelet adhesion. Front Biosci. 1998;3:d719-d728.
16. Grüner S, Prostredna M, Schulte V, et al. Multiple integrin-ligand interactions synergize in shearresistant platelet adhesion at sites of arterial injury in vivo. Blood. 2003;102(12):4021-4027.
17. Handagama PJ, Shuman MA, Bainton DF. Incorporation of intravenously injected albumin, immunoglobulin G, and fibrinogen in guinea pig megakaryocyte granules. J Clin Invest. 1989;84(1):73-82.
18. Harrison P, Wilbourn B, Debili N, et al. Uptake of plasma fibrinogen into the alpha granules of human megakaryocytes and platelets. J Clin Invest. 1989;84(4):1320-1324.
19. Eva R, Crisp S, Marland JR, et al. ARF6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. J Neurosci. 2012;32(30):10352-10364.
20. Dunphy JL, Moravec R, Ly K, Lasell TK, Melancon P, Casanova JE. The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr Biol. 2006;16(3):315-320.
21. Chen PW, Luo R, Jian X, Randazzo PA. The Arf6 GTPase-activating proteins ARAP2 and ACAP1 define distinct endosomal compartments that regulate integrin a5b1 traffic. J Biol Chem. 2014;289(44):30237-30248.
22. Arjonen A, Alanko J, Veltel S, Ivaska J. Distinct recycling of active and inactive b1 integrins. Traffic. 2012;13(4):610-625.
23. Duleh SN, Welch MD. Regulation of integrin trafficking, cell adhesion, and cell migration by WASH and the Arp2/3 complex. Cytoskeleton (Hoboken). 2012;69(12):1047-1058.
24. Powelka AM, Sun J, Li J, et al. Stimulationdependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic. 2004;5(1):20-36.
25. Wencel-Drake JD, Boudignon-Proudhon C, Dieter MG, Criss AB, Parise LV. Internalization of bound fibrinogen modulates platelet aggregation. Blood. 1996;87(2):602-612.
26. Akiyama M, Hasegawa H, Hongu T, et al. Transregulation of oligodendrocyte myelination by neurons through small GTPase Arf6-regulated secretion of fibroblast growth factor-2. Nat Commun. 2014;5:4744.
27. Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood. 2007;109(4):1503-1506.
28. Ye S, Karim ZA, Al Hawas R, Pessin JE, Filipovich AH, Whiteheart SW. Syntaxin-11, but not syntaxin-2 or syntaxin-4, is required for platelet secretion. Blood. 2012;120(12):2484-2492.
29. Busetto S, Trevisan E, Patriarca P, Menegazzi R. A single-step, sensitive flow cytofluorometric assay for the simultaneous assessment of membrane-bound and ingested Candida albicans in phagocytosing neutrophils. Cytometry A. 2004;58A(2):201-206.
30. Heijnen HF, Debili N, Vainchencker W, Breton-Gorius J, Geuze HJ, Sixma JJ. Multivesicular bodies are an intermediate stage in the formation of platelet alpha-granules. Blood. 1998;91(7):2313-2325.
31. Piper RC, Katzmann DJ. Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol. 2007;23:519-547.
32. Song J, Khachikian Z, Radhakrishna H, Donaldson JG. Localization of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J Cell Sci. 1998;111(pt 15):2257-2267.
33. Flevaris P, Li Z, Zhang G, Zheng Y, Liu J, Du X. Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPKdependent integrin outside-in retractile signaling pathway. Blood. 2009;113(4):893-901.
34. Suzuki-Inoue K, Hughes CE, Inoue O, et al. Involvement of Src kinases and PLCgamma2 in clot retraction. Thromb Res. 2007;120(2):251-258.
35. De Franceschi N, Hamidi H, Alanko J, Sahgal P, Ivaska J. Integrin traffic - the update. J Cell Sci. 2015;128(5):839-852.
36. Zucker-Franklin D. Endocytosis by human platelets: metabolic and freeze-fracture studies. J Cell Biol. 1981;91(3):706-715.