A novel and essential role for FcγRIIa in cancer cell-induced platelet activation

Blood

Volumn 123, Issue 2, 2014, Pages 249-260

  Mitrugno, Annachiara ^a   Williams, David ^a   Kerrigan, Steven W ^a   Moran, Niamh ^a  

^a BEAUMONT HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; FC RECEPTOR IIA; PHOSPHOLIPASE C; PROTEIN KINASE C; PROTEIN KINASE SYK; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN RECEPTOR; THROMBOXANE RECEPTOR; ADHESION RECEPTOR; FC RECEPTOR; FIBRINOGEN RECEPTOR; FOCAL ADHESION KINASE 1; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; PURINERGIC P2Y RECEPTOR;

ANIMAL CELL; ARTICLE; CACO 2 CELL LINE; CANCER CELL; CELL ADHESION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RELEASE REACTION; ANIMAL; BIOLOGICAL MODEL; METABOLISM; NEOPLASM; SECRETION (PROCESS); SIGNAL TRANSDUCTION; THROMBOCYTE; TUMOR CELL LINE;

ANIMALS; BLOOD PLATELETS; CELL LINE, TUMOR; FOCAL ADHESION KINASE 1; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MODELS, BIOLOGICAL; NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PLATELET ACTIVATION; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; RECEPTOR, PAR-1; RECEPTORS, IGG; RECEPTORS, PURINERGIC P2Y; RECEPTORS, THROMBOXANE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84897018797     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-03-492447     Document Type: Article

References (54)

1. Ho-Tin-Noé B, Goerge T, Cifuni SM, Duerschmied D, Wagner DD. Platelet granule secretion continuously prevents intratumor hemorrhage. Cancer Res. 2008; 68(16): 6851-6858.
2. Kopp HG, Placke T, Salih HR Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res. 2009; 69(19): 7775-7783.
3. Labelle M, Begum S, Hynes RO Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011; 20(5): 576-590.
4. Battinelli EM, Markens BA, Italiano JE Jr. Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood. 2011; 118(5): 1359-1369.
5. Tranum BL, Haut A. Thrombocytosis: platelet kinetics in neoplasia. J Lab Clin Med. 1974; 84(5): 615-619.
6. Levin J, Conley CL Thrombocytosis associated with malignant disease. Arch Intern Med. 1964; 114: 497-500.
7. Boneu B, Bugat R, Boneu A., Eche N, Sie P, Combes PF Exhausted platelets in patients with malignant solid tumors without evidence of active consumption coagulopathy. Eur J Cancer Clin Oncol. 1984; 20(7): 899-903. (Pubitemid 14086913)
8. Gasic GJ, Gasic TB, Stewart CC Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci U S A. 1968; 61(1): 46-52.
9. Karpatkin S, Pearlstein E. Role of platelets in tumor cell metastases. Ann Intern Med. 1981; 95(5): 636-641. (Pubitemid 12231807)
10. Peterson JE, Zurakowski D, Italiano JE Jr, et al Normal ranges of angiogenesis regulatory proteins in human platelets. Am J Hematol. 2010; 85(7): 487-493.
11. Assoian RK, Komoriya A, Meyers C.A., Miller DM, Sporn MB Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem. 1983; 258(11): 7155-7160. (Pubitemid 13059967)
12. Italiano JE J.r., Battinelli EM Selective sorting of alpha-granule proteins. J Thromb Haemost. 2009; 7(SUPPL. 1): 173-176.
13. Kerr BA, Miocinovic R, Smith A.K., Klein EA, Byzova TV Comparison of tumor and microenvironment secretomes in plasma and in platelets during prostate cancer growth in a xenograft model. Neoplasia. 2010; 12(5): 388-396.
14. Radomski MW, Jenkins DC, Holmes L, Moncada S. Human colorectal adenocarcinoma cells: differential nitric oxide synthesis determines their ability to aggregate platelets. Cancer Res. 1991; 51(22): 6073-6078.
15. Medina C, Jurasz P, Santos-Martinez MJ, et al Platelet aggregation-induced by caco-2 cells: regulation by matrix metalloproteinase-2 and adenosine diphosphate. J Pharmacol Exp Ther. 2006; 317(2): 739-745.
16. Radomski M, Moncada S. An improved method for washing of human platelets with prostacyclin. Thromb Res. 1983; 30(4): 383-389. (Pubitemid 13053477)
17. Poole A, Gibbins JM, Turner M, et al The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J. 1997; 16(9): 2333-2341. (Pubitemid 27258634)
18. Konopatskaya O, Gilio K, Harper M.T., et al PKCalpha regulates platelet granule secretion and thrombus formation in mice. J Clin Invest. 2009; 119(2): 399-407.
19. Sun B, Tandon NN, Yamamoto N, Yoshitake M., Kambayashi J. Luminometric assay of platelet activation in 96-well microplate. Biotechniques. 2001; 31(5): 1174, 1176, 1178 passim.
20. Edwards RJ, Moran N, Devocelle M., et al Bioinformatic discovery of novel bioactive peptides. Nat Chem Biol. 2007; 3(2): 108-112. (Pubitemid 46134997)
21. Law DA, Nannizzi-Alaimo L, Phillips DR Outside-in integrin signal transduction. Alpha IIb beta 3-(GP IIb IIIa) tyrosine phosphorylation induced by platelet aggregation. J Biol Chem. 1996; 271(18): 10811-10815.
22. Kozlowski JM, Fidler IJ, Campbell D, Xu Z.L., Kaighn ME, Hart IR Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res. 1984; 44(8): 3522-3529. (Pubitemid 14098607)
23. Lombardi F, de Chaumont C, Shields DC, Moran N. Platelet signalling networks: pathway perturbation demonstrates differential sensitivity of ADP secretion and fibrinogen binding. Platelets. 2012; 23(1): 17-25.
24. Kerrigan SW, Douglas I, Wray A., et al A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation. Blood. 2002; 100(2): 509-516. (Pubitemid 34761113)
25. Pula G, Crosby D, Baker J., Poole AW Functional interaction of protein kinase Calpha with the tyrosine kinases Syk and Src in human platelets. J Biol Chem. 2005; 280(8): 7194-7205. (Pubitemid 40341277)
26. de Leval X., Benoit V, Delarge J., et al Pharmacological evaluation of the novel thromboxane modulator BM-567 (II/II). Effects of BM-567 on osteogenic sarcoma-cell-induced platelet aggregation. Prostaglandins Leukot Essent Fatty Acids. 2003; 68(1): 55-59. (Pubitemid 36197487)
27. Mehta P, Lawson D, Ward M.B., Lee-Ambrose L, Kimura A. Effects of thromboxane A2 inhibition on osteogenic sarcoma cell-induced platelet aggregation. Cancer Res. 1986; 46(10): 5061-5063. (Pubitemid 16008266)
28. Alonso-Escolano D., Strongin AY, Chung A.W., Deryugina EI, Radomski MW Membrane type-1 matrix metalloproteinase stimulates tumour cell-induced platelet aggregation: role of receptor glycoproteins. Br J Pharmacol. 2004; 141(2): 241-252. (Pubitemid 38250894)
29. Egan K, Crowley D, Smyth P., et al Platelet adhesion and degranulation induce pro-survival and pro-angiogenic signalling in ovarian cancer cells. PLoS ONE. 2011; 6(10):e26125.
30. Oleksowicz L, Mrowiec Z, Schwartz E., Khorshidi M, Dutcher JP, Puszkin E. Characterization of tumor-induced platelet aggregation: the role of immunorelated GPIb and GPIIb/IIIa expression by MCF-7 breast cancer cells. Thromb Res. 1995; 79(3): 261-274.
31. Jurasz P, Alonso-Escolano D, Radomski MW Platelet-cancer interactions: mechanisms and pharmacology of tumour cell-induced platelet aggregation. Br J Pharmacol. 2004; 143(7): 819-826. (Pubitemid 39664840)
32. Erpenbeck L, Schön MP. Deadly allies: the fatal interplay between platelets and metastasizing cancer cells. Blood. 2010; 115(17): 3427-3436.
33. Amirkhosravi A, Amaya M, Siddiqui F., Biggerstaff JP, Meyer TV, Francis JL Blockade of GpIIb/IIIa inhibits the release of vascular endothelial growth factor (VEGF) from tumor cell-activated platelets and experimental metastasis. Platelets. 1999; 10(5): 285-292. (Pubitemid 29490854)
34. Jackson SP, Schoenwaelder SM, Goncalves I, et al PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med. 2005; 11(5): 507-514. (Pubitemid 40685973)
35. Pestina TI, Stenberg PE, Druker B.J., et al Identification of the Src family kinases, Lck and Fgr in platelets. Their tyrosine phosphorylation status and subcellular distribution compared with other Src family members. Arterioscler Thromb Vasc Biol. 1997; 17(11): 3278-3285. (Pubitemid 28016089)
36. Wang LE, Ma H, Hale K.S., et al Roles of genetic variants in the PI3K and RAS/RAF pathways in susceptibility to endometrial cancer and clinical outcomes. J Cancer Res Clin Oncol. 2012; 138(3): 377-385.
37. Hitchcock IS, Fox NE, Prévost N, Sear K., Shattil SJ, Kaushansky K. Roles of focal adhesion kinase (FAK) in megakaryopoiesis and platelet function: studies using a megakaryocyte lineage specific FAK knockout. Blood. 2008; 111(2): 596-604.
38. Weyrich AS, Zimmerman GA Platelets: signaling cells in the immune continuum. Trends Immunol. 2004; 25(9): 489-495. (Pubitemid 39490256)
39. Chacko GW, Duchemin AM, Coggeshall K.M., Osborne JM, Brandt JT, Anderson CL Clustering of the platelet Fc gamma receptor induces noncovalent association with the tyrosine kinase p72syk. J Biol Chem. 1994; 269(51): 32435-32440.
40. Canobbio I, Bertoni A, Lova P., et al Platelet activation by von Willebrand factor requires coordinated signaling through thromboxane A2 and Fc gamma IIA receptor. J Biol Chem. 2001; 276(28): 26022-26029.
41. Harper MT, Poole AW Diverse functions of protein kinase C isoforms in platelet activation and thrombus formation. J Thromb Haemost. 2010; 8(3): 454-462.
42. Karpatkin S, Pearlstein E, Salk P.L., Yogeeswaran G. Role of platelets in tumor cell metastases. Ann N Y Acad Sci. 1981; 370: 101-118. (Pubitemid 11049623)
43. Karpatkin S, Pearlstein E, Ambrogio C., Coller BS Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest. 1988; 81(4): 1012-1019.
44. Bambace NM, Holmes CE The platelet contribution to cancer progression. J Thromb Haemost. 2011; 9(2): 237-249.
45. Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011; 11(2): 123-134.
46. Buergy D, Wenz F, Groden C., Brockmann MA Tumor-platelet interaction in solid tumors. Int J Cancer. 2012; 130(12): 2747-2760.
47. Huang ZY, Chien P, Indik Z.K., Schreiber AD Human platelet FcγRIIA and phagocytes in immune-complex clearance. Mol Immunol. 2011; 48(4): 691-696.
48. Lowe KL, Navarro-Nunez L, Watson SP Platelet CLEC-2 and podoplanin in cancer metastasis. Thromb Res. 2012; 129(SUPPL. 1): S30-S37.
49. Keely PJ, Parise LV The alpha2beta1 integrin is a necessary co-receptor for collagen-induced activation of Syk and the subsequent phosphorylation of phospholipase Cgamma2 in platelets. J Biol Chem. 1996; 271(43): 26668-26676. (Pubitemid 26359072)
50. Tabuchi A, Yoshioka A, Higashi T., et al Direct demonstration of involvement of protein kinase Calpha in the Ca21-induced platelet aggregation. J Biol Chem. 2003; 278(29): 26374-26379. (Pubitemid 36876776)
51. Zhi H, Rauova L, Hayes V., et al Cooperative integrin/ITAM signaling in platelets enhances thrombus formation in vitro and in vivo. Blood. 2013; 121(10): 1858-1867.
52. Rothwell PM, Wilson M, Price J.F., Belch JF, Meade TW, Mehta Z. Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet. 2012; 379(9826): 1591-1601.
53. Miller MC, Doyle GV, Terstappen LW Significance of circulating tumor cells detected by the CellSearch system in patients with metastatic breast colorectal and prostate cancer. J Oncol. 2010; 2010: 617421.
54. Molloy TJ, Bosma AJ, Baumbusch L.O., et al The prognostic significance of tumour cell detection in the peripheral blood versus the bone marrow in 733 early-stage breast cancer patients. Breast Cancer Res. 2011; 13(3):R61.