Characterization of the platelet granule proteome: Evidence of the presence of MHC1 in alpha-granules

Journal of Proteomics

Volumn 101, Issue , 2014, Pages 130-140

  Zufferey, Anne ^a,b   Schvartz, Domitille ^b   Nolli, Séverine ^a,b   Reny, Jean Luc ^a,b   Sanchez, Jean Charles ^b   Fontana, Pierre ^a,b  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Granules; MHC I; Platelet; Proteomics; 2 Microglobulin

Indexed keywords

BETA 2 MICROGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEASOME; PROTEINASE; PROTEOME; VON WILLEBRAND FACTOR; HLA ANTIGEN CLASS 1; PLASMA PROTEIN;

ANTIGEN PRESENTATION; ARTICLE; CELL FRACTIONATION; CELL GRANULE; CELL MEMBRANE; HUMAN; IMMUNE SYSTEM; IMMUNOFLUORESCENCE; IMMUNOMODULATION; MALE; MASS SPECTROMETRY; METABOLISM; NORMAL HUMAN; PLATELET GRANULE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; QUALITATIVE ANALYSIS; THROMBOCYTE ACTIVATION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ADULT; SIGNAL TRANSDUCTION; THROMBOCYTE; ULTRASTRUCTURE;

ADULT; ANTIGEN PRESENTATION; BLOOD PLATELETS; BLOOD PROTEINS; CYTOPLASMIC GRANULES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MALE; MASS SPECTROMETRY; PROTEOME; SIGNAL TRANSDUCTION;

EID: 84896870734     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.02.008     Document Type: Article

References (44)

1. Battinelli E.M., Hartwig J.H., Italiano J.E. Delivering new insight into the biology of megakaryopoiesis and thrombopoiesis. Curr Opin Hematol 2007, 14:419-426.
2. Hansson G.K., Robertson A.K., Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol 2006, 1:297-329.
3. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol 2012, 32:2045-2051.
4. Coppinger J.A., Maguire P.B. Insights into the platelet releasate. Curr Pharm Des 2007, 13:2640-2646.
5. Semple J.W., Italiano J.E., Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011, 11:264-274.
6. Libby P., Lichtman A.H., Hansson G.K. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013, 38:1092-1104.
7. Lahoute C., Herbin O., Mallat Z., Tedgui A. Adaptive immunity in atherosclerosis: mechanisms and future therapeutic targets. Nat Rev Cardiol 2011, 8:348-358.
8. Thon J.N., Peters C.G., Machlus K.R., Aslam R., Rowley J., Macleod H., et al. T granules in human platelets function in TLR9 organization and signaling. J Cell Biol 2012, 198:561-574.
9. Maynard D.M., Heijnen H.F., Horne M.K., White J.G., Gahl W.A. Proteomic analysis of platelet alpha-granules using mass spectrometry. J Thromb Haemost 2007, 5:1945-1955.
10. Raghavachari N., Xu X., Harris A., Villagra J., Logun C., Barb J., et al. Amplified expression profiling of platelet transcriptome reveals changes in arginine metabolic pathways in patients with sickle cell disease. Circulation 2007, 115:1551-1562.
11. Burkhart J.M., Vaudel M., Gambaryan S., Radau S., Walter U., Martens L., 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. O'Neill E.E., Brock C.J., von Kriegsheim A.F., Pearce A.C., Dwek R.A., Watson S.P., et al. Towards complete analysis of the platelet proteome. Proteomics 2002, 2:288-305.
13. Kaiser W.J., Holbrook L.M., Tucker K.L., Stanley R.G., Gibbins J.M. A functional proteomic method for the enrichment of peripheral membrane proteins reveals the collagen binding protein Hsp47 is exposed on the surface of activated human platelets. J Proteome Res 2009, 8:2903-2914.
14. Cazenave J.P., Ohlmann P., Cassel D., Eckly A., Hechler B., Gachet C. Preparation of washed platelet suspensions from human and rodent blood. Methods Mol Biol 2004, 272:13-28.
15. Brunner Y., Coute Y., Iezzi M., Foti M., Fukuda M., Hochstrasser D.F., et al. Proteomics analysis of insulin secretory granules. Mol Cell Proteomics 2007, 6:1007-1017.
16. Scherl A., Shaffer S.A., Taylor G.K., Kulasekara H.D., Miller S.I., Goodlett D.R. Genome-specific gas-phase fractionation strategy for improved shotgun proteomic profiling of proteotypic peptides. Anal Chem 2008, 80:1182-1191.
17. Gluck F., Hoogland C., Antinori P., Robin X., Nikitin F., Zufferey A., et al. EasyProt - an easy-to-use graphical platform for proteomics data analysis. J Proteomics 2013, 79:146-160.
18. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 2007, 4:207-214.
19. Vizcaino J.A., Cote R.G., Csordas A., Dianes J.A., Fabregat A., Foster J.M., et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013, 41:D1063-D1069.
20. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
21. Italiano J.E., Richardson J.L., Patel-Hett S., Battinelli E., Zaslavsky A., Short S., et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008, 111:1227-1233.
22. Weyrich A.S., Schwertz H., Kraiss L.W., Zimmerman G.A. Protein synthesis by platelets: historical and new perspectives. J Thromb Haemost 2009, 7:241-246.
23. Foster L.J., de Hoog C.L., Zhang Y., Xie X., Mootha V.K., Mann M. A mammalian organelle map by protein correlation profiling. Cell 2006, 125:187-199.
24. Schvartz D., Brunner Y., Coute Y., Foti M., Wollheim C.B., Sanchez J.C. Improved characterization of the insulin secretory granule proteomes. J Proteomics 2012, 75:4620-4631.
25. Lubke T., Lobel P., Sleat D.E. Proteomics of the lysosome. Biochim Biophys Acta 2009, 1793:625-635.
26. Broekman M.J., Westmoreland N.P., Cohen P. An improved method for isolating alpha granules and mitochondria from human platelets. J Cell Biol 1974, 60:507-519.
27. Andreyev A.Y., Shen Z., Guan Z., Ryan A., Fahy E., Subramaniam S., et al. Application of proteomic marker ensembles to subcellular organelle identification. Mol Cell Proteomics 2010, 9:388-402.
28. Berger G., Masse J.M., Cramer E.M. Alpha-granule membrane mirrors the platelet plasma membrane and contains the glycoproteins Ib, IX, and V. Blood 1996, 87:1385-1395.
29. Heijnen H.F., Schiel A.E., Fijnheer R., Geuze H.J., Sixma J.J. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999, 94:3791-3799.
30. Blair P., Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev 2009, 23:177-189.
31. Stinchcombe J., Bossi G., Griffiths G.M. Linking albinism and immunity: the secrets of secretory lysosomes. Science 2004, 305:55-59.
32. Hume A.N., Seabra M.C. Melanosomes on the move: a model to understand organelle dynamics. Biochem Soc Trans 2011, 39:1191-1196.
33. Salles I.I., Feys H.B., Iserbyt B.F., De Meyer S.F., Vanhoorelbeke K., Deckmyn H. Inherited traits affecting platelet function. Blood Rev 2008, 22:155-172.
34. Gutwein P., Mechtersheimer S., Riedle S., Stoeck A., Gast D., Joumaa S., et al. ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J 2003, 17:292-294.
35. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
36. Gorbea C., Goellner G.M., Teter K., Holmes R.K., Rechsteiner M. Characterization of mammalian Ecm29, a 26S proteasome-associated protein that localizes to the nucleus and membrane vesicles. J Biol Chem 2004, 279:54849-54861.
37. Gorbea C., Pratt G., Ustrell V., Bell R., Sahasrabudhe S., Hughes R.E., et al. A protein interaction network for Ecm29 links the 26S proteasome to molecular motors and endosomal components. J Biol Chem 2010, 285:31616-31633.
38. Kao K.J., Cook D.J., Scornik J.C. Quantitative analysis of platelet surface HLA by W6/32 anti-HLA monoclonal antibody. Blood 1986, 68:627-632.
39. Ghio M., Contini P., Mazzei C., Brenci S., Barberis G., Filaci G., et al. Soluble HLA class I, HLA class II, and Fas ligand in blood components: a possible key to explain the immunomodulatory effects of allogeneic blood transfusions. Blood 1999, 93:1770-1777.
40. Puppo F., Bignardi D., Contini P., Hamby C.V., Brenci S., Lanza L., et al. Beta2-micro-free HLA class I heavy chain levels in sera of healthy individuals. Lack of association with beta2-micro-associated HLA class I heavy chain levels and HLA phenotype. Tissue Antigens 1999, 53:253-262.
41. Gouttefangeas C., Diehl M., Keilholz W., Hornlein R.F., Stevanovic S., Rammensee H.G. Thrombocyte HLA molecules retain nonrenewable endogenous peptides of megakaryocyte lineage and do not stimulate direct allocytotoxicity in vitro. Blood 2000, 95:3168-3175.
42. Aslam R., Speck E.R., Kim M., Freedman J., Semple J.W. Transfusion-related immunomodulation by platelets is dependent on their expression of MHC Class I molecules and is independent of white cells. Transfusion 2008, 48:1778-1786.
43. Elzey B.D., Tian J., Jensen R.J., Swanson A.K., Lees J.R., Lentz S.R., et al. Platelet-mediated modulation of adaptive immunity. A communication link between innate and adaptive immune compartments. Immunity 2003, 19:9-19.
44. Chapman L.M., Aggrey A.A., Field D.J., Srivastava K., Ture S., Yui K., et al. Platelets present antigen in the context of MHC class I. J Immunol 2012, 189:916-923.