Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability

Golebiewska EM, Harper MT, Williams CM, Savage JS, Goggs R, Fischer von Mollard G, Poole AW (2015)
The Journal of biological chemistry 290(3): 1536-1545.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Golebiewska, Ewelina M; Harper, Matthew T; Williams, Christopher M; Savage, Joshua S; Goggs, Robert; Fischer von Mollard, GabrieleUniBi ; Poole, Alastair W
Abstract / Bemerkung
Platelet secretion not only drives thrombosis and hemostasis, but also mediates a variety of other physiological and pathological processes. The ubiquitous SNARE machinery and a number of accessory proteins have been implicated in regulating secretion in platelet. Although several platelet SNAREs have been identified, further members of the SNARE family may be needed to fine-tune platelet secretion. In this study we identified expression of the t-SNARE syntaxin 8 (STX8) (Qc SNARE) in mouse and human platelets. In mouse studies, whereas STX8 was not essential for α-granule or lysosome secretion, Stx8(-/-) platelets showed a significant defect in dense granule secretion in response to thrombin and CRP. This was most pronounced at intermediate concentrations of agonists. They also showed an aggregation defect that could be rescued with exogenous ADP and increased embolization in Stx8(-/-) mice in vivo consistent with an important autocrine and paracrine role for ADP in aggregation and thrombus stabilization. STX8 therefore specifically contributes to dense granule secretion and represents another member of a growing family of genes that play distinct roles in regulating granule release from platelets and thus platelet function in thrombosis and hemostasis.
Erscheinungsjahr
2015
Zeitschriftentitel
The Journal of biological chemistry
Band
290
Ausgabe
3
Seite(n)
1536-1545
ISSN
1083-351X
Page URI
https://pub.uni-bielefeld.de/record/2730596

Zitieren

Golebiewska EM, Harper MT, Williams CM, et al. Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. The Journal of biological chemistry. 2015;290(3):1536-1545.
Golebiewska, E. M., Harper, M. T., Williams, C. M., Savage, J. S., Goggs, R., Fischer von Mollard, G., & Poole, A. W. (2015). Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. The Journal of biological chemistry, 290(3), 1536-1545. doi:10.1074/jbc.M114.602615
Golebiewska, E. M., Harper, M. T., Williams, C. M., Savage, J. S., Goggs, R., Fischer von Mollard, G., and Poole, A. W. (2015). Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. The Journal of biological chemistry 290, 1536-1545.
Golebiewska, E.M., et al., 2015. Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. The Journal of biological chemistry, 290(3), p 1536-1545.
E.M. Golebiewska, et al., “Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability”, The Journal of biological chemistry, vol. 290, 2015, pp. 1536-1545.
Golebiewska, E.M., Harper, M.T., Williams, C.M., Savage, J.S., Goggs, R., Fischer von Mollard, G., Poole, A.W.: Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. The Journal of biological chemistry. 290, 1536-1545 (2015).
Golebiewska, Ewelina M, Harper, Matthew T, Williams, Christopher M, Savage, Joshua S, Goggs, Robert, Fischer von Mollard, Gabriele, and Poole, Alastair W. “Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability”. The Journal of biological chemistry 290.3 (2015): 1536-1545.

13 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Dynamic cycling of t-SNARE acylation regulates platelet exocytosis.
Zhang J, Huang Y, Chen J, Zhu H, Whiteheart SW., J Biol Chem 293(10), 2018
PMID: 29352103
The life cycle of platelet granules.
Sharda A, Flaumenhaft R., F1000Res 7(), 2018
PMID: 29560259
Kinesin-1 Is a New Actor Involved in Platelet Secretion and Thrombus Stability.
Adam F, Kauskot A, Kurowska M, Goudin N, Munoz I, Bordet JC, Huang JD, Bryckaert M, Fischer A, Borgel D, de Saint Basile G, Christophe OD, Ménasché G., Arterioscler Thromb Vasc Biol 38(5), 2018
PMID: 29519941
Alterations in platelet secretion differentially affect thrombosis and hemostasis.
Joshi S, Banerjee M, Zhang J, Kesaraju A, Pokrovskaya ID, Storrie B, Whiteheart SW., Blood Adv 2(17), 2018
PMID: 30185436
Functional links between Disabled-2 Ser723 phosphorylation and thrombin signaling in human platelets.
Tsai HJ, Chien KY, Liao HR, Shih MS, Lin YC, Chang YW, Cheng JC, Tseng CP., J Thromb Haemost 15(10), 2017
PMID: 28876503
Role of Munc13-4 as a Ca2+-dependent tether during platelet secretion.
Chicka MC, Ren Q, Richards D, Hellman LM, Zhang J, Fried MG, Whiteheart SW., Biochem J 473(5), 2016
PMID: 26637270
Respective contributions of single and compound granule fusion to secretion by activated platelets.
Eckly A, Rinckel JY, Proamer F, Ulas N, Joshi S, Whiteheart SW, Gachet C., Blood 128(21), 2016
PMID: 27625359
VAMP-7 links granule exocytosis to actin reorganization during platelet activation.
Koseoglu S, Peters CG, Fitch-Tewfik JL, Aisiku O, Danglot L, Galli T, Flaumenhaft R., Blood 126(5), 2015
PMID: 25999457
Impact of the serum- and glucocorticoid-inducible kinase 1 on platelet dense granule biogenesis and secretion.
Walker B, Schmid E, Russo A, Schmidt EM, Burk O, Münzer P, Velic A, Macek B, Schaller M, Schwab M, Seabra MC, Gawaz M, Lang F, Borst O., J Thromb Haemost 13(7), 2015
PMID: 25944668

50 References

Daten bereitgestellt von Europe PubMed Central.

Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11.
zur Stadt U, Rohr J, Seifert W, Koch F, Grieve S, Pagel J, Strauss J, Kasper B, Nurnberg G, Becker C, Maul-Pavicic A, Beutel K, Janka G, Griffiths G, Ehl S, Hennies HC., Am. J. Hum. Genet. 85(4), 2009
PMID: 19804848
Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8.
Atlashkin V, Kreykenbohm V, Eskelinen EL, Wenzel D, Fayyazi A, Fischer von Mollard G., Mol. Cell. Biol. 23(15), 2003
PMID: 12861006
Functional divergence of platelet protein kinase C (PKC) isoforms in thrombus formation on collagen.
Gilio K, Harper MT, Cosemans JM, Konopatskaya O, Munnix IC, Prinzen L, Leitges M, Liu Q, Molkentin JD, Heemskerk JW, Poole AW., J. Biol. Chem. 285(30), 2010
PMID: 20479008
Molecular mechanisms of platelet exocytosis: requirements for alpha-granule release.
Lemons PP, Chen D, Whiteheart SW., Biochem. Biophys. Res. Commun. 267(3), 2000
PMID: 10673384
SNAP receptors implicated in vesicle targeting and fusion.
Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE., Nature 362(6418), 1993
PMID: 8455717
Munc13-4 is a limiting factor in the pathway required for platelet granule release and hemostasis.
Ren Q, Wimmer C, Chicka MC, Ye S, Ren Y, Hughson FM, Whiteheart SW., Blood 116(6), 2010
PMID: 20435885
Platelet secretion is kinetically heterogeneous in an agonist-responsive manner.
Jonnalagadda D, Izu LT, Whiteheart SW., Blood 120(26), 2012
PMID: 23086755
The effects of arterial flow on platelet activation, thrombus growth, and stabilization.
Cosemans JM, Angelillo-Scherrer A, Mattheij NJ, Heemskerk JW., Cardiovasc. Res. 99(2), 2013
PMID: 23667186
Platelet dense-granule secretion plays a critical role in thrombosis and subsequent vascular remodeling in atherosclerotic mice.
King SM, McNamee RA, Houng AK, Patel R, Brands M, Reed GL., Circulation 120(9), 2009
PMID: 19687360
SNARE protein expression and localization in human cytotoxic T lymphocytes.
Pattu V, Qu B, Schwarz EC, Strauss B, Weins L, Bhat SS, Halimani M, Marshall M, Rettig J, Hoth M., Eur. J. Immunol. 42(2), 2012
PMID: 22120889
Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs.
Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR., Nat. Struct. Biol. 9(2), 2002
PMID: 11786915
Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network.
Stalker TJ, Traxler EA, Wu J, Wannemacher KM, Cermignano SL, Voronov R, Diamond SL, Brass LF., Blood 121(10), 2013
PMID: 23303817
Syntaxin 11: a member of the syntaxin family without a carboxyl terminal transmembrane domain.
Tang BL, Low DY, Hong W., Biochem. Biophys. Res. Commun. 245(2), 1998
PMID: 9571206
Platelet membrane proteomics: a novel repository for functional research.
Lewandrowski U, Wortelkamp S, Lohrig K, Zahedi RP, Wolters DA, Walter U, Sickmann A., Blood 114(1), 2009
PMID: 19436052
Platelets and primary haemostasis.
Clemetson KJ., Thromb. Res. 129(3), 2011
PMID: 22178577
The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways.
Burkhart JM, Vaudel M, Gambaryan S, Radau S, Walter U, Martens L, Geiger J, Sickmann A, Zahedi RP., Blood 120(15), 2012
PMID: 22869793
The small GTPase Rif is dispensable for platelet filopodia generation in mice.
Goggs R, Savage JS, Mellor H, Poole AW., PLoS ONE 8(1), 2013
PMID: 23359340
Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 in dense core granule release.
Chen D, Bernstein AM, Lemons PP, Whiteheart SW., Blood 95(3), 2000
PMID: 10648404
Syntaxin-11, but not syntaxin-2 or syntaxin-4, is required for platelet secretion.
Ye S, Karim ZA, Al Hawas R, Pessin JE, Filipovich AH, Whiteheart SW., Blood 120(12), 2012
PMID: 22767500
Rab27b regulates number and secretion of platelet dense granules.
Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC., Proc. Natl. Acad. Sci. U.S.A. 104(14), 2007
PMID: 17384153
Endosomal SNARE proteins regulate CFTR activity and trafficking in epithelial cells.
Bilan F, Nacfer M, Fresquet F, Norez C, Melin P, Martin-Berge A, Costa de Beauregard MA, Becq F, Kitzis A, Thoreau V., Exp. Cell Res. 314(11-12), 2008
PMID: 18570918
IκB kinase phosphorylation of SNAP-23 controls platelet secretion.
Karim ZA, Zhang J, Banerjee M, Chicka MC, Al Hawas R, Hamilton TR, Roche PA, Whiteheart SW., Blood 121(22), 2013
PMID: 23613522
CalDAG-GEFI is at the nexus of calcium-dependent platelet activation.
Stefanini L, Roden RC, Bergmeier W., Blood 114(12), 2009
PMID: 19628710
Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery.
Lemons PP, Chen D, Bernstein AM, Bennett MK, Whiteheart SW., Blood 90(4), 1997
PMID: 9269766
Munc18b/STXBP2 is required for platelet secretion.
Al Hawas R, Ren Q, Ye S, Karim ZA, Filipovich AH, Whiteheart SW., Blood 120(12), 2012
PMID: 22791290
Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23.
Sorensen JB, Nagy G, Varoqueaux F, Nehring RB, Brose N, Wilson MC, Neher E., Cell 114(1), 2003
PMID: 12859899
Multiple alterations of platelet functions dominated by increased secretion in mice lacking Cdc42 in platelets.
Pleines I, Eckly A, Elvers M, Hagedorn I, Eliautou S, Bender M, Wu X, Lanza F, Gachet C, Brakebusch C, Nieswandt B., Blood 115(16), 2010
PMID: 20139097
Syntaxin 8 impairs trafficking of cystic fibrosis transmembrane conductance regulator (CFTR) and inhibits its channel activity.
Bilan F, Thoreau V, Nacfer M, Derand R, Norez C, Cantereau A, Garcia M, Becq F, Kitzis A., J. Cell. Sci. 117(Pt 10), 2004
PMID: 15039462
Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages.
Offenhauser C, Lei N, Roy S, Collins BM, Stow JL, Murray RZ., Traffic 12(6), 2011
PMID: 21388490
Endobrevin/VAMP-8 is the primary v-SNARE for the platelet release reaction.
Ren Q, Barber HK, Crawford GL, Karim ZA, Zhao C, Choi W, Wang CC, Hong W, Whiteheart SW., Mol. Biol. Cell 18(1), 2006
PMID: 17065550
PKCalpha regulates platelet granule secretion and thrombus formation in mice.
Konopatskaya O, Gilio K, Harper MT, Zhao Y, Cosemans JM, Karim ZA, Whiteheart SW, Molkentin JD, Verkade P, Watson SP, Heemskerk JW, Poole AW., J. Clin. Invest. 119(2), 2009
PMID: 19147982
Regulation of platelet dense granule secretion by the Ral GTPase-exocyst pathway.
Kawato M, Shirakawa R, Kondo H, Higashi T, Ikeda T, Okawa K, Fukai S, Nureki O, Kita T, Horiuchi H., J. Biol. Chem. 283(1), 2007
PMID: 17938170
A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function.
Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R., EMBO J. 19(23), 2000
PMID: 11101518
Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils.
Mollinedo F, Calafat J, Janssen H, Martin-Martin B, Canchado J, Nabokina SM, Gajate C., J. Immunol. 177(5), 2006
PMID: 16920918
Syntaxin 8 modulates the post-synthetic trafficking of the TrkA receptor and inflammatory pain transmission.
Chen B, Zhao L, Li X, Ji YS, Li N, Xu XF, Chen ZY., J. Biol. Chem. 289(28), 2014
PMID: 24872407
Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes.
Rowley JW, Oler AJ, Tolley ND, Hunter BN, Low EN, Nix DA, Yost CC, Zimmerman GA, Weyrich AS., Blood 118(14), 2011
PMID: 21596849
Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released.
Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL., Blood 111(3), 2007
PMID: 17962514
A HaemAtlas: characterizing gene expression in differentiated human blood cells.
Watkins NA, Gusnanto A, de Bono B, De S, Miranda-Saavedra D, Hardie DL, Angenent WG, Attwood AP, Ellis PD, Erber W, Foad NS, Garner SF, Isacke CM, Jolley J, Koch K, Macaulay IC, Morley SL, Rendon A, Rice KM, Taylor N, Thijssen-Timmer DC, Tijssen MR, van der Schoot CE, Wernisch L, Winzer T, Dudbridge F, Buckley CD, Langford CF, Teichmann S, Gottgens B, Ouwehand WH; Bloodomics Consortium., Blood 113(19), 2009
PMID: 19228925
A draft map of the human proteome.
Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, Madugundu AK, Kelkar DS, Isserlin R, Jain S, Thomas JK, Muthusamy B, Leal-Rojas P, Kumar P, Sahasrabuddhe NA, Balakrishnan L, Advani J, George B, Renuse S, Selvan LD, Patil AH, Nanjappa V, Radhakrishnan A, Prasad S, Subbannayya T, Raju R, Kumar M, Sreenivasamurthy SK, Marimuthu A, Sathe GJ, Chavan S, Datta KK, Subbannayya Y, Sahu A, Yelamanchi SD, Jayaram S, Rajagopalan P, Sharma J, Murthy KR, Syed N, Goel R, Khan AA, Ahmad S, Dey G, Mudgal K, Chatterjee A, Huang TC, Zhong J, Wu X, Shaw PG, Freed D, Zahari MS, Mukherjee KK, Shankar S, Mahadevan A, Lam H, Mitchell CJ, Shankar SK, Satishchandra P, Schroeder JT, Sirdeshmukh R, Maitra A, Leach SD, Drake CG, Halushka MK, Prasad TS, Hruban RH, Kerr CL, Bader GD, Iacobuzio-Donahue CA, Gowda H, Pandey A., Nature 509(7502), 2014
PMID: 24870542
SNAREs and traffic.
Hong W., Biochim. Biophys. Acta 1744(3), 2005
PMID: 16038056
The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners.
Kreykenbohm V, Wenzel D, Antonin W, Atlachkine V, von Mollard GF., Eur. J. Cell Biol. 81(5), 2002
PMID: 12067063
Synaptotagmin-like protein 1 interacts with the GTPase-activating protein Rap1GAP2 and regulates dense granule secretion in platelets.
Neumuller O, Hoffmeister M, Babica J, Prelle C, Gegenbauer K, Smolenski AP., Blood 114(7), 2009
PMID: 19528539
Platelet functions beyond hemostasis.
Smyth SS, McEver RP, Weyrich AS, Morrell CN, Hoffman MR, Arepally GM, French PA, Dauerman HL, Becker RC; 2009 Platelet Colloquium Participants, Arepally GM, Becker RC, Bhatt DL, Cho J, Dauerman HL, Gretler DD, Hoffman MR, Horrow J, Kleiman NS, Kocharian R, Lincoff AM, Maya J, McEver RP, Morrell CN, Prats J, Rusconi CP, Smyth SS, Strony J, Sun H, Veltri EP, Weyrich AS, Wiviott SD, Wood JP., J. Thromb. Haemost. 7(11), 2009
PMID: 19691483

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