Proteomic profiling of platelet signalling

Expert Review of Proteomics

Volumn 10, Issue 4, 2013, Pages 355-364

  Howes, Joanna Marie ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

phosphorylation; platelets; proteomics; signaling; thrombosis

Indexed keywords

BLOOD PLATELETS; HUMANS; PHOSPHORYLATION; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 84894035151     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/14789450.2013.820534     Document Type: Review

References (76)

1. Herr AB, Farndale RW. Structural insights into the interactions between platelet receptors and fibrillar collagen. J. Biol. Chem. 284(30), 19781-19785 (2009).
2. Luo GP, Ni B, Yang X, Wu YZ. von Willebrand factor: more than a regulator of hemostasis and thrombosis. Acta. Haematol. 128(3), 158-169 (2012).
3. Chen J, Lopez JA. Interactions of platelets with subendothelium and endothelium. Microcirculation 12(3), 235-246 (2005).
4. Cruz MA, Chen J, Whitelock JL, Morales LD, Lopez JA. The platelet glycoprotein Ib-von Willebrand factor interaction activates the collagen receptor alpha2beta1 to bind collagen: activation-dependent conformational change of the alpha2-I domain. Blood 105(5), 1986-1991 (2005).
5. Nieswandt B, Pleines I, Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J. Thromb. Haemost. 9(Suppl. 1), 92-104 (2011).
6. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb. Vasc. Biol. 30(12), 2341-2349 (2010).
7. Coughlin SR, Camerer E. PARticipation in inflammation. J. Clin. Invest. 111(1), 25-27 (2003).
8. Stegner D, Nieswandt B. Platelet receptor signaling in thrombus formation. J. Mol. Med. (Berl.) 89(2), 109-121 (2011).
9. Schweigel H, Geiger J, Beck F et al. Deciphering of ADP-induced, phosphotyrosine-dependent signaling networks in human platelets by Src-homology 2 region (SH2)-profiling. Proteomics 13(6), 1016-1027 (2013).
10. Jennings LK. Role of platelets in atherothrombosis. Am. J. Cardiol. 103(3 Suppl.), 4A-10A (2009).
11. Zufferey A, Fontana P, Reny JL, Nolli S, Sanchez JC. Platelet proteomics. Mass Spectrom Rev. 31(2), 331-351 (2012).
12. Yates JR, Ruse CI, Nakorchevsky A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 11, 49-79 (2009).
13. Ng EW, Wong MY, Poon TC. Advances in MALDI mass spectrometry in clinical diagnostic applications. Top Curr. Chem. doi:10.1007/128-2012-413 (2013) (Epub ahead of print).
14. Switzar L, Giera M, Niessen WM. Protein digestion: an overview of the available techniques and recent developments. J. Proteome Res. 12(3), 1067-1077 (2013).
15. Ali-Khan N, Zuo X, Speicher DW. Overview of proteome analysis. Curr. Protoc. Protein Sci. Chapter 22, Unit 22 21 (2003).
16. Brewis IA, Brennan P. Proteomics technologies for the global identification and quantification of proteins. Adv. Protein Chem. Struct. Biol. 80, 1-44 (2010).
17. Wasinger VC, Zeng M, Yau Y. Current status and advances in quantitative proteomic mass spectrometry. Int. J. Proteomics 2013, 180605 (2013).
18. Marouga R, David S, Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382(3), 669-678 (2005).
19. Weiss W, Gorg A. High-resolution two-dimensional electrophoresis. Methods Mol. Biol. 564, 13-32 (2009).
20. Rogne M, Tasken K. Cell signalling analyses in the functional genomics era. N. Biotechnol. 30(3), 333-338 (2013).
21. Lander ES, Linton LM, Birren B et al. Initial sequencing and analysis of the human genome. Nature 409(6822), 860-921 (2001).
22. Choudhary C, Mann M. Decoding signalling networks by mass spectrometrybased proteomics. Nat. Rev. Mol. Cell Biol. 11(6), 427-439 (2010).
23. Hu J, Rho HS, Newman RH et al. Global analysis of phosphorylation networks in humans. Biochim. Biophys. Acta. doi:10.1016/j.bbapap.2013.03.009 (2013) (Epub ahead of print).
24. Ngounou Wetie AG, Sokolowska I, Woods AG, Roy U, Deinhardt K, Darie CC. Protein-protein interactions: switch from classical methods to proteomics and bioinformatics-based approaches. Cell Mol. Life Sci. doi:10.1007/s00018-013- 1333-1 (2013) (Epub ahead of print).
25. Fila J, Honys D. Enrichment techniques employed in phosphoproteomics. Amino Acids 43(3), 1025-1047 (2012).
26. Engholm-Keller K, Larsen MR. Technologies and challenges in large-scale phosphoproteomics. Proteomics 13(6), 910-931 (2013).
27. Kaneko T, Joshi R, Feller SM, Li SS. Phosphotyrosine recognition domains: the typical, the atypical and the versatile. Cell Commun. Signal 10(1), 32 (2012).
28. Dierck K, Machida K, Voigt A et al. Quantitative multiplexed profiling of cellular signaling networks using phosphotyrosine-specific DNA-tagged SH2 domains. Nat. Methods 3(9), 737-744 (2006).
29. Machida K, Thompson CM, Dierck K et al. High-throughput phosphotyrosine profiling using SH2 domains. Mol. Cell 26(6), 899-915 (2007).
30. Di Michele M, Van Geet C, Freson K. Recent advances in platelet proteomics. Expert Rev. Proteomics 9(4), 451-466 (2012).
31. Schulz C, Leuschen NV, Frohlich T et al. Identification of novel downstream targets of platelet glycoprotein VI activation by differential proteome analysis: implications for thrombus formation. Blood 115(20), 4102-4110 (2010).
32. Kaiser WJ, Holbrook LM, Tucker KL, Stanley RG, Gibbins JM. 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. 8(6), 2903-2914 (2009).
33. Smethurst PA, Onley DJ, Jarvis GE et al. Structural basis for the platelet-collagen interaction: the smallest motif within collagen that recognizes and activates platelet glycoprotein VI contains two glycine-proline-hydroxyproline triplets. J. Biol. Chem. 282(2), 1296-1304 (2007).
34. Garcia A, Senis YA, Antrobus R et al. A global proteomics approach identifies novel phosphorylated signaling proteins in GPVI-activated platelets: involvement of G6f, a novel platelet Grb2-binding membrane adapter. Proteomics 6(19), 5332-5343 (2006).
35. Wright B, Stanley RG, Kaiser WJ, Mills DJ, Gibbins JM. Analysis of protein networks in resting and collagen receptor (GPVI)-stimulated platelet sub-proteomes. Proteomics 11(23), 4588-4592 (2011).
36. Tucker RP, Chiquet-Ehrismann R. Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev. Biol. 290(2), 237-245 (2006).
37. Kalabis J, Rosenberg I, Podolsky DK. Vangl1 protein acts as a downstream effector of intestinal trefoil factor (ITF)/TFF3 signaling and regulates wound healing of intestinal epithelium. J. Biol. Chem. 281(10), 6434-6441 (2006).
38. Shikata Y, Birukov KG, Birukova AA, Verin A, Garcia JG. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate-and thrombininduced focal adhesion remodeling: role of Src and GIT. FASEB J. 17(15), 2240-2249 (2003).
39. Zahradka P, Storie B, Wright B. IGF-1 receptor transactivation mediates Src-dependent cortactin phosphorylation in response to angiotensin II. Can. J. Physiol. Pharmacol. 87(10), 805-812 (2009).
40. Suzuki Inoue K, Inoue O, Ozaki Y. [Identification of the novel platelet activation receptor CLEC-2 and Its pathological and physiological roles]. Rinsho. Byori. 58(12), 1193-1202 (2010).
41. Watson SP, Herbert JM, Pollitt AY. GPVI and CLEC-2 in hemostasis and vascular integrity. J. Thromb. Haemost. 8(7), 1456-1467 (2010).
42. Parguiña AF, Alonso J, Rosa I et al. A detailed proteomic analysis of rhodocytinactivated platelets reveals novel clues on the CLEC-2 signalosome: implications for CLEC-2 signaling regulation. Blood 120(26), e117-e126 (2012).
43. Lee H, Hamilton Jr. Physiology, pharmacology, and therapeutic potential of protease-activated receptors in vascular disease. Pharmacol. Ther. 134(2), 246-259 (2012).
44. De Candia E. Mechanisms of platelet activation by thrombin: a short history. Thromb. Res. 129(3), 250-256 (2012).
45. Murugappan S, Shankar H, Bhamidipati S, Dorsam RT, Jin J, Kunapuli SP. Molecular mechanism and functional implications of thrombin-mediated tyrosine phosphorylation of PKCdelta in platelets. Blood 106(2), 550-557 (2005).
46. Maguire PB, Wynne KJ, Harney DF, O'Donoghue NM, Stephens G, Fitzgerald DJ. Identification of the phosphotyrosine proteome from thrombin activated platelets. Proteomics 2(6), 642-648 (2002).
47. Jones ML, Shawe-Taylor AJ, Williams CM, Poole AW. Characterization of a novel focal adhesion kinase inhibitor in human platelets. Biochem. Biophys. Res. Commun. 389(1), 198-203 (2009).
48. Garcia A, Prabhakar S, Hughan S et al. Differential proteome analysis of TRAPactivated platelets: involvement of DOK-2 and phosphorylation of RGS proteins. Blood 103(6), 2088-2095 (2004).
49. Ma P, Cierniewska A, Signarvic R et al. A newly identified complex of spinophilin and the tyrosine phosphatase, SHP-1, modulates platelet activation by regulating G protein-dependent signaling. Blood 119(8), 1935-1945 (2012).
50. Tucker KL, Kaiser WJ, Bergeron AL et al. Proteomic analysis of resting and thrombin-stimulated platelets reveals the translocation and functional relevance of HIP-55 in platelets. Proteomics 9(18), 4340-4354 (2009).
51. Han J, Shui JW, Zhang X, Zheng B, Han S, Tan TH. HIP-55 is important for T-cell proliferation, cytokine production, and immune responses. Mol. Cell Biol. 25(16), 6869-6878 (2005).
52. Cimmino G, Golino P. Platelet Biology and Receptor Pathways. J. Cardiovasc. Transl. Res. 6(3), 299-309 (2013).
53. Hechler B, Gachet C. P2 receptors and platelet function. Purinergic Signal 7(3), 293-303 (2011).
54. Tello-Montoliu A, Jover E, Rivera J, Valdes M, Angiolillo DJ, Marin F. New perspectives in antiplatelet therapy. Curr. Med. Chem. 19(3), 406-427 (2012).
55. Hattori M, Gouaux E. Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485(7397), 207-212 (2012).
56. Nieswandt B, Varga-Szabo D, Elvers M. Integrins in platelet activation. J. Thromb. Haemost. 7(Suppl. 1), 206-209 (2009).
57. Bennett JS, Berger BW, Billings PC. The structure and function of platelet integrins. J. Thromb. Haemost. 7(Suppl. 1), 200-205 (2009).
58. Takagi J. Structural basis for ligand recognition by RGD (Arg-Gly-Asp)-dependent integrins. Biochem. Soc. Trans. 32(Pt3), 403-406 (2004).
59. Qureshi AH, Chaoji V, Maiguel D et al. Proteomic and phospho-proteomic profile of human platelets in basal, resting state: insights into integrin signaling. PLoS One 4(10), e7627 (2009).
60. Kirk RI, Sanderson MR, Lerea KM. Threonine phosphorylation of the beta 3 integrin cytoplasmic tail, at a site recognized by PDK1 and Akt/PKB in vitro, regulates Shc binding. J. Biol. Chem. 275(40), 30901-30906 (2000).
61. Sato K, Nagao T, Kakumoto M et al. Adaptor protein Shc is an isoform-specific direct activator of the tyrosine kinase c-Src. J. Biol. Chem. 277(33), 29568-29576 (2002).
62. Senis YA, Antrobus R, Severin S et al. Proteomic analysis of integrin alphaIIbbeta3 outside-in signaling reveals Src-kinase-independent phosphorylation of Dok-1 and Dok-3 leading to SHIP-1 interactions. J. Thromb. Haemost. 7(10), 1718-1726 (2009).
63. Rex S, Beaulieu LM, Perlman DH et al. Immune versus thrombotic stimulation of platelets differentially regulates signalling pathways, intracellular protein-protein interactions, and alpha-granule release. Thromb. Haemost. 102(1), 97-110 (2009).
64. Mateos-Caceres PJ, Macaya C, Azcona L et al. Different expression of proteins in platelets from aspirin-resistant and aspirin-sensitive patients. Thromb. Haemost. 103(1), 160-170 (2010).
65. Cheng Z, Sundberg-Smith LJ, Mangiante LE et al. Focal adhesion kinase regulates smooth muscle cell recruitment to the developing vasculature. Arterioscler Thromb. Vasc. Biol. 31(10), 2193-2202 (2011).
66. Nossaman BD, Kadowitz PJ. Stimulators of soluble guanylyl cyclase: future clinical indications. Ochsner. J. 13(1), 147-156 (2013).
67. Pena E, Padro T, Molins B, Vilahur G, Badimon L. Proteomic signature of thrombin-activated platelets after in vivo nitric oxide-donor treatment: coordinated inhibition of signaling (phosphatidylinositol 3-kinase-gamma, 14-3-3zeta, and growth factor receptor-bound protein 2) and cytoskeleton protein translocation. Arterioscler. Thromb. Vasc. Biol. 31(11), 2560-2569 (2011).
68. Parguiña AF, Grigorian-Shamajian L, Agra RM et al. Proteins involved in platelet signaling are differentially regulated in acute coronary syndrome: a proteomic study. PLoS One 5(10), e13404 (2011).
69. Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP. Structural basis of sequence-specific collagen recognition by SPARC. Proc. Natl Acad. Sci. USA 105(47), 18273-18277 (2008).
70. Parguiña AF, Grigorian-Shamagian L, Agra RM et al. Variations in platelet proteins associated with ST-elevation myocardial infarction: novel clues on pathways underlying platelet activation in acute coronary syndromes. Arterioscler Thromb. Vasc. Biol. 31(12), 2957-2964 (2011).
71. Froebel J, Cadeddu RP, Hartwig S et al. Platelet proteome analysis reveals integrindependent aggregation defects in patients with myelodysplastic syndromes. Mol. Cell Proteomics 12(5), 1272-1280(2013).
72. Kanaji T, Ware J, Okamura T, Newman PJ. GPIbalpha regulates platelet size by controlling the subcellular localization of filamin. Blood 119(12), 2906-2913 (2012).
73. Maurer-Spurej E, Devine DV. Platelet aggregation is not initiated by platelet shape change. Lab. Invest. 81(11), 1517-1525 (2001).
74. 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 120(15), e73-e82 (2012).
75. Senis Y, Garcia A. Platelet proteomics: state of the art and future perspective. Methods Mol. Biol. 788, 367-399 (2012).
76. Boyanova D, Nilla S, Birschmann I, Dandekar T, Dittrich M. PlateletWeb: a systems biologic analysis of signaling networks in human platelets. Blood 119(3), e22-e34 (2012).