A human platelet receptor protein microarray identifies the high affinity immunoglobulin e receptor subunit α (FcεR1α) as an activating platelet endothelium aggregation receptor 1 (PEAR1) ligand

Molecular and Cellular Proteomics

Volumn 14, Issue 5, 2015, Pages 1265-1274

  Sun, Yi ^a   Vandenbriele, Christophe ^b   Kauskot, Alexandre ^b,c   Verhamme, Peter ^b   Hoylaerts, Marc F ^b   Wright, Gavin J ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c Dept Environ Med Natl Inst Publ HIth   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E RECEPTOR; IMMUNOGLOBULIN E RECEPTOR SUBUNIT ALPHA; OMALIZUMAB; PLATELET ENDOTHELIUM AGGREGATION RECEPTOR 1; THROMBOCYTE RECEPTOR; UNCLASSIFIED DRUG; FCEPSILONRI ALPHA-CHAIN, HUMAN; LIGAND; PEAR1 PROTEIN, HUMAN; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INVESTIGATIVE PROCEDURES; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; THROMBOCYTE AGGREGATION; BINDING SITE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; KINETICS; METABOLISM; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; THROMBOCYTE;

BINDING SITES; BLOOD PLATELETS; GENE EXPRESSION; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN E; KINETICS; LIGANDS; OMALIZUMAB; PHOSPHORYLATION; PLATELET AGGREGATION; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, CELL SURFACE; RECEPTORS, IGE; RECOMBINANT PROTEINS;

EID: 84929659585     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.046946     Document Type: Article

References (42)

1. Yusuf, S., Reddy, S., Ounpuu, S., and Anand, S. (2001) Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 104, 2746-2753
2. CARDIoGRAMplusC4D Consortium, Deloukas, P., Kanoni, S., Willenborg, C., Farrall, M., Assimes, T. L., Thompson, J. R., Ingelsson, E., Saleheen, D., Erdmann, J., Goldstein, B. A., Stirrups, K., König, I. R., Cazier, J. B., Johansson, A., Hall, A. S., Lee, J. Y., Willer, C. J., Chambers, J. C., Esko, T., Folkersen, L., Goel, A., Grundberg, E., Havulinna, A. S., Ho, W. K., Hopewell, J. C., Eriksson, N., Kleber, M. E., Kristiansson, K., Lundmark, P., Lyytikäinen, L. P., Rafelt, S., Shungin, D., Strawbridge, R. J., Thorleifsson, G., Tikkanen, E., Van Zuydam, N., Voight, B. F., Waite, L. L., Zhang, W., Ziegler, A., Absher, D., Altshuler, D., Balmforth, A. J., Barroso, I., Braund, P. S., Burgdorf, C., Claudi-Boehm, S., Cox, D., Dimitriou, M., Do, R.; DIAGRAM Consortium; CARDIOGENICS Consortium, Doney, A. S., El Mokhtari, N., Eriksson, P., Fischer, K., Fontanillas, P., Franco-Cereceda, A., Gigante, B., Groop, L., Gustafsson, S., Hager, J., Hallmans, G., Han, B. G., Hunt, S. E., Kang, H. M., Illig, T., Kessler, T., Knowles, J. W., Kolovou, G., Kuusisto, J., Langenberg, C., Langford, C., Leander, K., Lokki, M. L., Lundmark, A., McCarthy, M. I., Meisinger, C., Melander, O., Mihailov, E., Maouche, S., Morris, A. D., Müller-Nurasyid, M.; MuTHER Consortium, Nikus, K., Peden, J. F., Rayner, N. W., Rasheed, A., Rosinger, S., Rubin, D., Rumpf, M. P., Schäfer, A., Sivananthan, M., Song, C., Stewart, A. F., Tan, S. T., Thorgeirsson, G., van der Schoot, C. E., Wagner, P. J.; Wellcome Trust Case Control Consortium, Wells, G. A., Wild, P. S., Yang, T. P., Amouyel, P., Arveiler, D., Basart, H., Boehnke, M., Boerwinkle, E., Brambilla, P., Cambien, F., Cupples, A. L., de Faire, U., Dehghan, A., Diemert, P., Epstein, S. E., Evans, A., Ferrario, M. M., Ferrières, J., Gauguier, D., Go, A. S., Goodall, A. H., Gudnason, V., Hazen, S. L., Holm, H., Iribarren, C., Jang, Y., Kähönen, M., Kee, F., Kim, H. S., Klopp, N., Koenig, W., Kratzer, W., Kuulasmaa, K., Laakso, M., Laaksonen, R., Lee, J. Y., Lind, L., Ouwehand, W. H., Parish, S., Park, J. E., Pedersen, N. L., Peters, A., Quertermous, T., Rader, D. J., Salomaa, V., Schadt, E., Shah, S. H., Sinisalo, J., Stark, K., Stefansson, K., Trégouët, D. A., Virtamo, J., Wallentin, L., Wareham, N., Zimmermann, M. E., Nieminen, M. S., Hengstenberg, C., Sandhu, M. S., Pastinen, T., Syvänen, A. C., Hovingh, G. K., Dedoussis, G., Franks, P. W., Lehtimäki, T., Metspalu, A., Zalloua, P. A., Siegbahn, A., Schreiber, S., Ripatti, S., Blankenberg, S. S., Perola, M., Clarke, R., Boehm, B. O., O'Donnell, C., Reilly, M. P., März, W., Collins, R., Kathiresan, S., Hamsten, A., Kooner, J. S., Thorsteinsdottir, U., Danesh, J., Palmer, C. N., Roberts, R., Watkins, H., Schunkert, H., and Samani, N. J. (2013) Large-scale association analysis identifies new risk loci for coronary artery disease. Nat. Genet. 45, 25-33
3. Johnson, A. D., Yanek, L. R., Chen, M. H., Faraday, N., Larson, M. G., Tofler, G., Lin, S. J., Kraja, A. T., Province, M. A., Yang, Q., Becker, D. M., O'Donnell, C. J., and Becker, L. C. (2010) Genome-wide meta-analyses identifies seven loci associated with platelet aggregation in response to agonists. Nat. Genet. 42, 608-613
4. Faraday, N., Yanek, L. R., Yang, X. P., Mathias, R., Herrera-Galeano, J. E., Suktitipat, B., Qayyum, R., Johnson, A. D., Chen, M. H., Tofler, G. H., Ruczinski, I., Friedman, A. D., Gylfason, A., Thorsteinsdottir, U., Bray, P. F., O'Donnell, C. J., Becker, D. M., and Becker, L. C. (2011) Identification of a specific intronic PEAR1 gene variant associated with greater platelet aggregability and protein expression. Blood 118, 3367-3375
5. Herrera-Galeano, J. E., Becker, D. M., Wilson, A. F., Yanek, L. R., Bray, P., Vaidya, D., Faraday, N., and Becker, L. C. (2008) A novel variant in the platelet endothelial aggregation receptor-1 gene is associated with increased platelet aggregability. Arterioscler. Thromb. Vasc. Biol. 28, 1484-1490
6. Jones, C. I., Bray, S., Garner, S. F., Stephens, J., de Bono, B., Angenent, W. G., Bentley, D., Burns, P., Coffey, A., Deloukas, P., Earthrowl, M., Farndale, R. W., Hoylaerts, M. F., Koch, K., Rankin, A., Rice, C. M., Rogers, J., Samani, N. J., Steward, M., Walker, A., Watkins, N. A., Akkerman, J. W., Dudbridge, F., Goodall, A. H., and Ouwehand, W. H. (2009) A functional genomics approach reveals novel quantitative trait loci associated with platelet signaling pathways. Blood 114, 1405-1416
7. Lewis, J. P., Ryan, K., O'Connell, J. R., Horenstein, R. B., Damcott, C. M., Gibson, Q., Pollin, T. I., Mitchell, B. D., Beitelshees, A. L., Pakzy, R., Tanner, K., Parsa, A., Tantry, U. S., Bliden, K. P., Post, W. S., Faraday, N., Herzog, W., Gong, Y., Pepine, C. J., Johnson, J. A., Gurbel, P. A., and Shuldiner, A. R. (2013) Genetic variation in PEAR1 is associated with platelet aggregation and cardiovascular outcomes. Circ. Cardiovasc. Genet. 6, 184-192
8. Kauskot, A., Di Michele, M., Loyen, S., Freson, K., Verhamme, P., and Hoylaerts, M. F. (2012) A novel mechanism of sustained platelet αIIbß3 activation via PEAR1. Blood 119, 4056-4065
9. Nanda, N., Bao, M., Lin, H., Clauser, K., Komuves, L., Quertermous, T., Conley, P. B., Phillips, D. R., and Hart, M. J. (2005) Platelet endothelial aggregation receptor 1 (PEAR1), a novel epidermal growth factor repeat-containing transmembrane receptor, participates in platelet contact-induced activation. J. Biol. Chem. 280, 24680-24689
10. Wright, G. J. (2009) Signal initiation in biological systems: the properties and detection of transient extracellular protein interactions. Mol. Biosyst. 5, 1405-1412
11. Bushell, K. M., Söllner, C., Schuster-Boeckler, B., Bateman, A., and Wright, G. J. (2008) Large-scale screening for novel low-affinity extracellular protein interactions. Genome Res. 18, 622-630
12. Özkan, E., Carrillo, R. A., Eastman, C. L., Weiszmann, R., Waghray, D., Johnson, K. G., Zinn, K., Celniker, S. E., and Garcia, K. C. (2013) An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks. Cell 154, 228-239
13. Ramani, S. R., Tom, I., Lewin-Koh, N., Wranik, B., Depalatis, L., Zhang, J., Eaton, D., and Gonzalez, L. C. (2012) A secreted protein microarray platform for extracellular protein interaction discovery. Anal. Biochem. 420, 127-138
14. Wojtowicz, W. M., Wu, W., Andre, I., Qian, B., Baker, D., and Zipursky, S. L. (2007) A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130, 1134-1145
15. Sun, Y., Gallagher-Jones, M., Barker, C., and Wright, G. J. (2012) A benchmarked protein microarray-based platform for the identification of novel low-affinity extracellular protein interactions. Anal. Biochem. 424, 45-53
16. Bianchi, E., Doe, B., Goulding, D., and Wright, G. J. (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508, 483-487
17. Crosnier, C., Bustamante, L. Y., Bartholdson, S. J., Bei, A. K., Theron, M., Uchikawa, M., Mboup, S., Ndir, O., Kwiatkowski, D. P., Duraisingh, M. T., Rayner, J. C., and Wright, G. J. (2011) Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480, 534-537
18. Powell, G. T., and Wright, G. J. (2011) Jamb and jamc are essential for vertebrate myocyte fusion. PLoS Biol. 9, e1001216
19. Crosnier, C., Wanaguru, M., McDade, B., Osier, F. H., Marsh, K., Rayner, J. C., and Wright, G. J. (2013) A library of functional recombinant cellsurface and secreted P. falciparum merozoite proteins. Mol. Cell. Proteomics 12, 3976-3986
20. Kerr, J. S., and Wright, G. J. (2012) Avidity-based extracellular interaction screening (AVEXIS) for the scalable detection of low-affinity extracellular receptor-ligand interactions. J. Vis. Exp. 20, e3881
21. Briesewitz, R., Epstein, M. R., and Marcantonio, E. E. (1993) Expression of native and truncated forms of the human integrin α1 subunit. J. Biol. Chem. 268, 2989-2996
22. Lane-Serff, H., Sun, Y., Metcalfe, P., and Wright, G. J. (2013) Expression of recombinant ITGA2 and CD109 for the detection of human platelet antigen (HPA)-5 and -15 alloantibodies. Br. J. Haematol. 161, 453-455
23. Martin, S., Söllner, C., Charoensawan, V., Adryan, B., Thisse, B., Thisse, C., Teichmann, S., and Wright, G. J. (2010) Construction of a large extracellular protein interaction network and its resolution by spatiotemporal expression profiling. Mol. Cell. Proteomics 9, 2654-2665
24. Söllner, C., and Wright, G. J. (2009) A cell surface interaction network of neural leucine-rich repeat receptors. Genome Biol. 10, R99
25. Battle, T., Antonsson, B., Feger, G., and Besson, D. (2006) A high-throughput mammalian protein expression, purification, aliquoting and storage pipeline to assemble a library of the human secretome. Comb. Chem. High Throughput Screen. 9, 639-649
26. Gonzalez, R., Jennings, L. L., Knuth, M., Orth, A. P., Klock, H. E., Ou, W., Feuerhelm, J., Hull, M. V., Koesema, E., Wang, Y., Zhang, J., Wu, C., Cho, C. Y., Su, A. I., Batalov, S., Chen, H., Johnson, K., Laffitte, B., Nguyen, D. G., Snyder, E. Y., Schultz, P. G., Harris, J. L., and Lesley, S. A. (2010) Screening the mammalian extracellular proteome for regulators of embryonic human stem cell pluripotency. Proc. Natl. Acad. Sci. U.S.A. 107, 3552-3557
27. Garman, S. C., Wurzburg, B. A., Tarchevskaya, S. S., Kinet, J. P., and Jardetzky, T. S. (2000) Structure of the Fc fragment of human IgE bound to its high-affinity receptor FcεRIα. Nature 406, 259-266
28. Hasegawa, S., Pawankar, R., Suzuki, K., Nakahata, T., Furukawa, S., Okumura, K., and Ra, C. (1999) Functional expression of the high affinity receptor for IgE (FcεRI) in human platelets and its' intracellular expression in human megakaryocytes. Blood 93, 2543-2551
29. Joseph, M., Gounni, A. S., Kusnierz, J. P., Vorng, H., Sarfati, M., Kinet, J. P., Tonnel, A. B., Capron, A., and Capron, M. (1997) Expression and functions of the high-affinity IgE receptor on human platelets and megakaryocyte precursors. Eur. J. Immunol. 27, 2212-2218
30. Herscovitch, M., Perkins, E., Baltus, A., and Fan, M. (2012) Addgene provides an open forum for plasmid sharing. Nat. Biotechnol. 30, 316-317
31. Gould, H. J., and Sutton, B. J. (2008) IgE in allergy and asthma today. Nat. Rev. Immunol. 8, 205-217
32. McDonnell, J. M., Calvert, R., Beavil, R. L., Beavil, A. J., Henry, A. J., Sutton, B. J., Gould, H. J., and Cowburn, D. (2001) The structure of the IgE Cε2 domain and its role in stabilizing the complex with its high-affinity receptor FcεRIα. Nat. Struct. Biol. 8, 437-441
33. Gallagher, J. S., Bernstein, I. L., Maccia, C. A., Splansky, G. L., and Glueck, H. I. (1978) Cyclic platelet dysfunction in IgE-mediated allergy. J. Allergy Clin. Immunol. 62, 229-235
34. Maccia, C. A., Gallagher, J. S., Ataman, G., Glueck, H. I., Brooks, S. M., and Bernstein, I. L. (1977) Platelet thrombopathy in asthmatic patients with elevated immunoglobulin E. J. Allergy Clin. Immunol. 59, 101-108
35. Palma-Carlos, A. G., Palma-Carlos, M. L., Santos, M. C., and de Sousa, J. R. (1991) Platelet aggregation in allergic reactions. Int. Arch. Allergy Appl. Immunol. 94, 251-253
36. Ind, P. W. (1991) Platelet and clotting abnormalities in asthma. Clin. Exp. Allergy 21, 395-398
37. Harwell, W. B., Patterson, J. T., Lieberman, P., and Beachey, E. (1973) Platelet aggregation in atopic and normal patients. J. Allergy Clin. Immunol. 51, 274-284
38. McDonald, J. R., Tan, E. M., Stevenson, D. D., and Vaughan, J. H. (1974) Platelet aggregation in asthmatic and normal subjects. J. Allergy Clin. Immunol. 54, 200-208
39. Lieberman, J. A., and Chehade, M. (2013) Use of omalizumab in the treatment of food allergy and anaphylaxis. Curr. Allergy Asthma Rep. 13, 78-84
40. Holgate, S., Casale, T., Wenzel, S., Bousquet, J., Deniz, Y., and Reisner, C. (2005) The anti-inflammatory effects of omalizumab confirm the central role of IgE in allergic inflammation. J. Allergy Clin. Immunol. 115, 459-465
41. MacGlashan, D. W., Jr., Bochner, B. S., Adelman, D. C., Jardieu, P. M., Togias, A., McKenzie-White, J., Sterbinsky, S. A., Hamilton, R. G., and Lichtenstein, L. M. (1997) Down-regulation of FcεRI expression on human basophils during in vivo treatment of atopic patients with anti-IgE antibody. J. Immunol. 158, 1438-1445
42. Ali, A. K., and Hartzema, A. G. (2012) Assessing the association between omalizumab and arteriothrombotic events through spontaneous adverse event reporting. J. Asthma Allergy 5, 1-9