Binding of galectin-1 to αIIbβ3 integrin triggers "outside-in" signals, stimulates platelet activation, and controls primary hemostasis

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 2788-2798

  Romaniuk, Maria A ^a   Croci, Diego O ^a   Lapponi, Maria J ^a   Tribulatti, Maria V ^b   Negrotto, Soledad ^a   Poirier, Francoise ^c   Campetella, Oscar ^b   Rabinovich, Gabriel A ^a   Schattner, Mirta ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

Glycobiology; Inflammation

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AGGLUTININ; ALPHA2 INTEGRIN; ARACHIDONIC ACID; BETA GALACTOSIDE; BETA3 INTEGRIN; BINDING PROTEIN; BLOCKING ANTIBODY; FIBRINOGEN; GALECTIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE SYK; THROMBOXANE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING TIME; BLOOD CLOT RETRACTION; CALCIUM MOBILIZATION; CONTROLLED STUDY; GLANZMANN DISEASE; HEMOSTASIS; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT;

ANIMALS; BLEEDING TIME; GALECTIN 1; HEMOSTASIS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLATELET ACTIVATION; PLATELET ADHESIVENESS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; SIGNAL TRANSDUCTION; THROMBASTHENIA;

MUS;

EID: 84863219389     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-197541     Document Type: Article

References (48)

1. Paulson, J. C., Blixt, O., and Collins, B. E. (2006) Sweet spots in functional glycomics. Nat. Chem. Biol. 2, 238-248
2. Van Kooyk, Y., and Rabinovich, G. A. (2008) Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9, 593-601
3. Yang, R. Y., Rabinovich, G. A., and Liu, F. T. (2008) Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 10, e17
4. Thijssen, V. L., Hulsmans, S., and Griffioen, A. W. (2008) The galectin profile of the endothelium: altered expression and localization in activated and tumor endothelial cells. Am. J. Pathol. 172, 545-553 (Pubitemid 351282039)
5. Al-Ansari, S., Zeebregts, C. J., Slart, R. H., Peppelenbosch, M., and Tio, R. A. (2009) Galectins in atherosclerotic disease. Trends Cardiovasc. Med. 19, 164-169
6. Danguy, A., Camby, I., and Kiss, R. (2002) Galectins and cancer. Biochim. Biophys. Acta 1572, 285-293 (Pubitemid 35246351)
7. Jurk, K., and Kehrel, B. E. (2005) Platelets: physiology and biochemistry. Semin. Thromb. Hemost. 31, 381-392 (Pubitemid 41362342)
8. Wagner, D. D. (2005) New links between inflammation and thrombosis. Arterioscler. Thromb. Vasc. Biol. 25, 1321-1324
9. Li, Z., Delaney, M. K., O'Brien, K. A., and Du, X. (2010) Signaling during platelet adhesion and activation. Arterioscler. Thromb. Vasc. Biol. 30, 2341-2349
10. Ma, Y. Q., Qin, J., and Plow, E. F. (2007) Platelet integrin alpha(IIb)beta(3): activation mechanisms. J. Thromb. Haemost. 5, 1345-1352 (Pubitemid 46965357)
11. Pacienza, N., Pozner, R. G., Bianco, G. A., D'Atri, L. P., Croci, D. O., Negrotto, S., Malaver, E., Gomez, R. M., Rabinovich, G. A., and Schattner, M. (2008) The immunoregulatory glycanbinding protein galectin-1 triggers human platelet activation. FASEB J. 22, 1113-1123 (Pubitemid 351519966)
12. Romaniuk, M. A., Tribulatti, M. V., Cattaneo, V., Lapponi, M. J., Molinas, F. C., Campetella, O., and Schattner, M. Human platelets express and are activated by galectin-8. Biochem. J. 432, 535-547
13. Malik, R. K., Ghurye, R. R., Lawrence-Watt, D. J., and Stewart, H. J. (2009) Galectin-1 stimulates monocyte chemotaxis via the p44/42 MAP kinase pathway and a pertussis toxin-sensitive pathway. Glycobiology 19, 1402-1407
14. Chellan, B., Narayani, J., and Appukuttan, P. S. (2007) Galectin- 1, an endogenous lectin produced by arterial cells, binds lipoprotein(a) [Lp(a)] in situ: relevance to atherogenesis. Exp. Mol. Pathol. 83, 399-404 (Pubitemid 350087018)
15. Moiseeva, E. P., Javed, Q., Spring, E. L., and de Bono, D. P. (2000) Galectin 1 is involved in vascular smooth muscle cell proliferation. Cardiovasc. Res. 45, 493-502 (Pubitemid 30069516)
16. Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Urashima, T., Oka, T., Futai, M., Muller, W. E., Yagi, F., and Kasai, K. (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572, 232-254 (Pubitemid 35246347)
17. Rabinovich, G. A., Daly, G., Dreja, H., Tailor, H., Riera, C. M., Hirabayashi, J., and Chernajovsky, Y. (1999) Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J. Exp. Med. 190, 385-398
18. Malaver, E., Romaniuk, M. A., D'Atri, L. P., Pozner, R. G., Negrotto, S., Benzadon, R., and Schattner, M. (2009) NFkappaB inhibitors impair platelet activation responses. J. Thromb. Haemost. 7, 1333-1343
19. Jones, C. I., Garner, S. F., Moraes, L. A., Kaiser, W. J., Rankin, A., Ouwehand, W. H., Goodall, A. H., and Gibbins, J. M. (2009) PECAM-1 expression and activity negatively regulate multiple platelet signaling pathways. FEBS Lett. 583, 3618-3624
20. Coller, B. S., and Shattil, S. J. (2008) The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood 112, 3011-3025
21. Charo, I. F., Feinman, R. D., and Detwiler, T. C. (1977) Interrelations of platelet aggregation and secretion. J. Clin. Invest. 60, 866-873 (Pubitemid 8208479)
22. Levy-Toledano, S., Maclouf, J., Bryon, P., Savariau, E., Hardisty, R. M., and Caen, J. P. (1982) Human platelet activation in the absence of aggregation: a calcium-dependent phenomenon independent of thromboxane formation. Blood 59, 1078-1085 (Pubitemid 12125603)
23. Abrams, C. S. (2005) Intracellular signaling in platelets. Curr. Opin. Hematol. 12, 401-405
24. Varga-Szabo, D., Braun, A., and Nieswandt, B. (2009) Calcium signaling in platelets. J. Thromb. Haemost. 7, 1057-1066
25. Brass, L. F., Laposata, M., Banga, H. S., and Rittenhouse, S. E. (1986) Regulation of the phosphoinositide hydrolysis pathway in thrombin-stimulated platelets by a pertussis toxin-sensitive guanine nucleotide-binding protein. Evaluation of its contribution to platelet activation and comparisons with the adenylate cyclase inhibitory protein, Gi. J. Biol. Chem. 261, 16838-16847 (Pubitemid 17210323)
26. Harker, L. A., and Slichter, S. J. (1972) The bleeding time as a screening test for evaluation of platelet function. N. Engl. J. Med. 287, 155-159
27. Goschnick, M. W., Lau, L. M., Wee, J. L., Liu, Y. S., Hogarth, P. M., Robb, L. M., Hickey, M. J., Wright, M. D., and Jackson, D. E. (2006) Impaired "outside-in" integrin alphaIIbbeta3 signaling and thrombus stability in TSSC6-deficient mice. Blood 108, 1911-1918 (Pubitemid 44395000)
28. Law, D. A., DeGuzman, F. R., Heiser, P., Ministri-Madrid, K., Killeen, N., and Phillips, D. R. (1999) Integrin cytoplasmic tyrosine motif is required for outside-in alphaIIbbeta3 signalling and platelet function. Nature 401, 808-811
29. Camby, I., Le Mercier, M., Lefranc, F., and Kiss, R. (2006) Galectin-1: a small protein with major functions. Glycobiology 16, 137R-157R (Pubitemid 44530693)
30. Elola, M. T., Chiesa, M. E., Alberti, A. F., Mordoh, J., and Fink, N. E. (2005) Galectin-1 receptors in different cell types. J. Biomed. Sci. 12, 13-29 (Pubitemid 40584806)
31. Huang, E. M., and Detwiler, T. C. (1981) Characteristics of the synergistic actions of platelet agonists. Blood 57, 685-691
32. Shattil, S. J., Hoxie, J. A., Cunningham, M., and Brass, L. F. (1985) Changes in the platelet membrane glycoprotein IIb.IIIa complex during platelet activation. J. Biol. Chem. 260, 11107-11114 (Pubitemid 16253272)
33. Phillips, D. R., Nannizzi-Alaimo, L., and Prasad, K. S. (2001) Beta3 tyrosine phosphorylation in alphaIIbbeta3 (platelet membrane GP IIb-IIIa) outside-in integrin signaling. Thromb. Haemost. 86, 246-258 (Pubitemid 32663955)
34. Payrastre, B., Missy, K., Trumel, C., Bodin, S., Plantavid, M., and Chap, H. (2000) The integrin alpha IIb/beta 3 in human platelet signal transduction. Biochem. Pharmacol. 60, 1069-1074
35. Liao, D. I., Kapadia, G., Ahmed, H., Vasta, G. R., and Herzberg, O. (1994) Structure of S-lectin, a developmentally regulated vertebrate beta-galactoside-binding protein. Proc. Natl. Acad. Sci. U. S. A. 91, 1428-1432
36. Torti, M., Festetics, E. T., Bertoni, A., Sinigaglia, F., and Balduini, C. (1999) Clustering of integrin alphaIIb-beta3 differently regulates tyrosine phosphorylation of pp72syk, PLCgamma2 and pp125FAK in concanavalin A-stimulated platelets. Thromb. Haemost. 81, 124-130 (Pubitemid 29041661)
37. Obergfell, A., Eto, K., Mocsai, A., Buensuceso, C., Moores, S. L., Brugge, J. S., Lowell, C. A., and Shattil, S. J. (2002) Coordinate interactions of Csk, Src, and Syk kinases with αIIbß3 initiate integrin signaling to the cytoskeleton. J. Cell Biol. 157, 265-275 (Pubitemid 34839823)
38. Prasad, K. S., Andre, P., He, M., Bao, M., Manganello, J., and Phillips, D. R. (2003) Soluble CD40 ligand induces beta3 integrin tyrosine phosphorylation and triggers platelet activation by outside-in signaling. Proc. Natl. Acad. Sci. U. S. A. 100, 12367-12371 (Pubitemid 37271566)
39. Andre, P., Prasad, K. S., Denis, C. V., He, M., Papalia, J. M., Hynes, R. O., Phillips, D. R., and Wagner, D. D. (2002) CD40L stabilizes arterial thrombi by a beta3 integrin-dependent mechanism. Nat. Med. 8, 247-252 (Pubitemid 34250102)
40. Watanabe, M., Takemasa, I., Kaneko, N., Yokoyama, Y., Matsuo, E., Iwasa, S., Mori, M., Matsuura, N., Monden, M., and Nishimura, O. (2011) Clinical significance of circulating galectins as colorectal cancer markers. Oncol. Rep. 25, 1217-1226
41. Liu, X., Feng, Q., Chen, Y., Zuo, J., Gupta, N., Chang, Y., and Fang, F. (2009) Proteomics-based identification of differentiallyexpressed proteins including galectin-1 in the blood plasma of type 2 diabetic patients. J. Proteome. Res. 8, 1255-1262
42. ten Cate, H., and Falanga, A. (2008) Overview of the postulated mechanisms linking cancer and thrombosis. Pathophysiol. Haemost. Thromb. 36, 122-130
43. Lemkes, B. A., Hermanides, J., Devries, J. H., Holleman, F., Meijers, J. C., and Hoekstra, J. B. (2010) Hyperglycemia: a prothrombotic factor? J. Thromb. Haemost. 8, 1663-1669
44. Libby, P. (2002) Inflammation in atherosclerosis. Nature 420, 868-874
45. Dhirapong, A., Lleo, A., Leung, P., Gershwin, M. E., and Liu, F. T. (2009) The immunological potential of galectin-1 and -3. Autoimmun. Rev. 8, 360-363
46. Rabinovich, G. A., Baum, L. G., Tinari, N., Paganelli, R., Natoli, C., Liu, F. T., and Iacobelli, S. (2002) Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol. 23, 313-320 (Pubitemid 34628775)
47. Ilarregui, J. M., Croci, D. O., Bianco, G. A., Toscano, M. A., Salatino, M., Vermeulen, M. E., Geffner, J. R., and Rabinovich, G. A. (2009) Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 10, 981-991
48. Toscano, M. A., Bianco, G. A., Ilarregui, J. M., Croci, D. O., Correale, J., Hernandez, J. D., Zwirner, N. W., Poirier, F., Riley, E. M., Baum, L. G., and Rabinovich, G. A. (2007) Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol. 8, 825-834 (Pubitemid 47099035)