Platelets and cancer angiogenesis nexus

Cancer and Metastasis Reviews

Volumn 36, Issue 2, 2017, Pages 249-262

  Wojtukiewicz, Marek Z ^a,b   Sierko, Ewa ^a,b   Hempel, Dominika ^a,b   Tucker, Stephanie C ^c   Honn, Kenneth V ^c,d,e  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^b Regional Comprehensive Cancer Center in Bialystok   (Poland)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WAYNE STATE UNIVERSITY   (United States)

^e KARMANOS CANCER INSTITUTE   (United States)

Author keywords

Angiogenesis; Cancer; Growth factors; Microparticles; MicroRNA; miRNAs; Platelets

Indexed keywords

LIPID; MICRORNA; RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL STRUCTURE; HUMAN; NONHUMAN; PLATELET MICROPARTICLE; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTOSIS; TUMOR VASCULARIZATION; ANIMAL; BLOOD; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

ANIMALS; BLOOD PLATELETS; HUMANS; MICRORNAS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 85021837749     PISSN: 01677659     EISSN: 15737233     Source Type: Journal    
DOI: 10.1007/s10555-017-9673-1     Document Type: Article

References (180)

1. Bizzozero, J. (1882). Űber einen neunen formbestandteil des blutes und dessen rolle bei der thrombose und blutgerinnung. Virchows Archiv für Pathologische Anatomie und Physiologie und für Klinische Medizin, 90, 262–332.
2. Geatano, G. (2001). Historical overview of the role of platelets in hemostasis and thrombosis. Heamatologica, 86, 349–356.
3. Billroth, T. (1878). Lectures on surgical pathology and therapeutics: a new handbook for students and practitioners (p. 355). London: The New Sydenham Society.
4. Mac Kay, W. (1930). The blood platelet: its clinical significance. Quartely Journal of Medicine, 24, 285–293.
5. Zacharski, L. R., Wojtukiewicz, M. Z., Costantini, V., Ornstein, D. L., & Memoli, V. A. (1992). Pathways of coagulation/fibrinolysis activation in malignancy. Seminars in Thrombosis and Hemostasis, 18, 104–116.
6. Miller, S. P., Sanchez-Avalos, J., Stefanski, T., & Zuckerman, L. (1967). Coagulation disorders in cancer I. Clinical and laboratory studies. Cancer, 20, 1452–1465.
7. Edwards, R. L., Rickles, F. R., Moritz, T. E., Henderson, W. G., Zacharski, L. R., Forman, W. B., et al. (1987). Abnormalities of blood coagulation tests in patients with cancer. American Journal of Clinical Pathology, 88, 596–602.
8. Rickles, F. R., Levine, M., & Edwards, R. L. (1992). Hemostatic alterations in cancer patients. Cancer Metastasis Review, 11, 237–248.
9. Francis, J. L., Biggerstaff, J., & Amirkhosravi, A. (1998). Hemostasis and malignancy. Seminars in Thrombosis and Hemostasis, 24, 93–109.
10. Wojtukiewicz, M. Z., Sierko, E., & Kisiel, W. (2007). The role of hemostatic system inhibitors in malignancy. Seminars in Thrombosis and Hemostasis, 33, 621–641.
11. Costantini, V., Zacharski, L. R., Moritz, T. E., & Edwards, R. L. (1990). The platelet count in carcinoma of the lung and colon. Thrombosis and Haemostasis, 64, 501–505.
12. Moller-Pedresen, L., & Milman, N. (1996). Prognostic significance of thrombocytosis in patients with primary lung cancer. European Respiratory Journal, 9, 1826–1830.
13. Ikeda, M., Furukawa, H., Imamura, H., Shimizu, J., Ishida, H., Masutani, S., et al. (2002). Poor prognosis associated with thrombocytosis in patients with gastric cancer. Annals of Surgical Oncology, 9, 287–291.
14. Symbas, N. P., Townsend, M. F., El, G. R., Keane, T. E., Graham, S. D., & Petros, J. A. (2000). Poor prognosis associated with thrombocytosis in patients with renal cell carcinoma. BJU International, 86, 203–207.
15. Ribeiro, M., Ruff, P., & Falkson, G. (1997). Low serum testosterone and a younger age predict for a poor outcome in metastatic prostate cancer. American Journal of Clinical Oncology, 20, 605–608.
16. Lopez, A., Daras, V., Cross, P. A., Robertson, G., Beynon, G., & Monaghan, J. M. (1994). Thrombocytosis as a prognostic factor in women with cervical cancer. Cancer, 74, 90–92.
17. Gücer, F., Moser, F., Tamussino, K., Reich, O., Haas, J., Arikan, G., et al. (1998). Thrombocytosis as a prognostic factor in endometrial carcinoma. Gynecologic Oncology, 70, 210–214.
18. Zeimet, A. G., Marth, C., Muller Holzner, E., Daxenbichler, G., & Dapunt, O. (1994). Significance of thrombocytosis in patients with epithelial ovarian cancer. American Journal Obstetrics & Gynecology, 170, 549–554.
19. Nakano, T., Fujii, J., Tamura, S., Hada, T., & Higashino, K. (1986). Thrombocytosis in patients with malignant mesothelioma. Cancer, 58, 1699–1701.
20. Gao, L., Zhang, H., Zhang, B., Zhang, L., & Wang, C. (2017). Prognostic value of combination of preoperative platelet count and mean platelet volume in patients with resectable non-small cell lung cancer. Oncotarget. doi:10.18632/oncotarget.14921.
21. Wang, Y. H., Deng, S. J., Yang, Y. D., Yao, N., Zhao, J. M., Min, G. T., et al. (2017). The pretreatment thrombocytosis may predict prognosis of patients with colorectal cancer: a systematic review and meta-analysis. Biomarkers in Medicine, 11(2), 195–210.
22. Schwartz, R. E. (1999). Platelet counts and prognosis of pancreatic cancer. Lancet, 353, 2158–2159.
23. Slichter, S. J., & Harker, L. A. (1974). Hemostasis in malignancy. Annals of the New York Academy of Sciences, 230, 252–262.
24. Tang, D. G., & Honn, K. V. (1994-1995). Adhesion molecules and tumor metastasis: an update. Invasion & Metastasis, 14, 109–122.
25. Honn, K. V., Tang, G. T., & Chen, Y. Q. (1992). Platelets and cancer metastasis: more than an epiphenomenon. Seminars in Thrombosis and Hemostasis, 18, 392–415.
26. Gasic, G. J., Gasic, T. B., & Steward, C. C. (1968). Antimetastatic effects associated with platelet reduction. Proceedings of the National Academy of Sciences USA, 61, 46–52.
27. Nierodzik, M. L., Klepfish, A., & Karpatkin, S. (1995). Role of platelets, thrombin, integrin IIb-IIIa, fibronectin and von Willebrand factor on tumor adhesion in vitro and metastasis in vivo. Thrombosis and Haemostasis, 74, 282–290.
28. Dvorak, H. F. (1986). Tumors: wounds that do not heal. New England Journal of Medicine, 315, 1650–1659.
29. Folkman, J. (1971). Tumor angiogenesis: therapeutic implications. New England Journal Medicine, 285, 1182–1186.
30. Folkman, J. (1995). Angiogenesis in cancer, vascular, rheumatoid and other diseases. Nature Medicine, 1, 27–31.
31. Wojtukiewicz, M. Z., Sierko, E., Klement, P., & Rak, J. (2001). The hemostatic system and angiogenesis in malignancy. Neoplasia, 3, 371–384.
32. Zacharski, L. R., Constantini, V., Wojtukiewicz, M. Z., Memoli, V. A., & Kudryk, B. J. (1990). Anticoagulants as cancer therapy. Seminars in Oncology, 17, 217–227.
33. Sierko, E., & Wojtukiewicz, M. Z. (2004). Platelets and angiogenesis in malignancy. Seminars in Thrombosis and Hemostasis, 30, 95–108.
34. Wojtukiewicz, M. Z., Sierko, E., & Rak, J. (2004). Contribution of hemostatic system to angiogenesis in cancer. Seminars in Thrombosis and Hemostasis, 30, 5–20.
35. Sierko, E., Wojtukiewicz, M. Z., Zimnoch, L., Brekken, R., Thorpe, P., & Kisiel, W. (2011). Co-localization of prothrombin fragment F1+2 and VEGFR-2 bound VEGF in human colon cancer. Anticancer Research, 31, 843–847.
36. D’Asti, E., Huang, A., Kool, M., Meehan, B., Chan, J. A., Jabado, N., et al. (2016). Tissue factor regulation by miR-520g in primitive neuronal brain tumor cells: a possible link between oncomirs and the vascular tumor microenvironment. American Journal of Pathology, 186(2), 446–459.
37. D’Asti, E., Kool, M., Pfister, S. M., & Rak, J. (2014). Coagulation and angiogenic gene expression profiles are defined by molecular subgroups of medulloblastoma: evidence for growth factor-thrombin cross-talk. Journal of Thrombosis and Haemostasis., 2(11), 1838–1849.
38. Verheul, H. M. W., Hoekman, K., Luykx-de Bakkerr, E., Eekm, C. A., Folman, C. C., Broxterman, H. J., & Pinedo, H. M. (1997). Platelet transporter of vascular endothelial growth factor. Clinical Cancer Research, 3, 2187–2190.
39. Wartiovaara, U., Salven, P., & Mikkola Heta, I. (1998). Peripheral blood platelets express VEGF-C and VEGF which are released during platelet activation. Thrombosis Haemostasis, 80, 171–175.
40. Verheul, H. M. W., Hoekman, K., Lupu, F., Broxterman, H. J., van der Valk, P., Kakkar, A. K., & Pinedo, H. M. (2000). Platelet and coagulation activation with vascular endothelial growth factor generation in soft tissue sarcomas. Clinical Cancer Research, 6, 166–171.
41. Möhle, R., Green, D., Moore, R. L., Nachman, R. L., & Raffi, S. (1997). Constitutive production of thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proceedings of the National Academy of Sciences USA, 94, 663–669.
42. Pipli-Synestos, E., Papadimitriou, E., & Maragoudakis, M. E. (1998). Evidence that platelets promote tube formation by endothelial cells on Matrigel. British Journal of Pharmacology, 125, 1252–1257.
43. Kisucka, J., Butterfield, C.E., Duda, D.G., Eichenberger, S.C., Saffaripour, S., & Ware, J. (2006). Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proceedings of the National Academy of Sciences USA, 103, 855-860.
44. Andrews, R. K., Shen, Y., Gardiner, E. E., & Berndt, M. C. (2001). Platelet adhesion receptors and (patho)physiological thrombus formation. Histology and Histopathology, 16, 969–980.
45. Chen, H., Locke, D., Liu, Y., & Kahn, M. L. (2002). The platelet receptor GPVI mediates both adhesion and signaling responses to collagen in a receptor density-dependent fashion. The Journal of Biological Chemistry, 277, 3011–3019.
46. Kamata, T., & Takada, Y. (2001). Platelet integrin alphaIIbbeta3-ligand interactions: what we learn from the structure? International Journal of Hematology, 74, 382–389.
47. Coughlin, S. R. (1999). Protease-activated receptors and platelet function. Thrombosis and Haemostasis, 82, 353–356.
48. Di Virgilio, F., Chiozzi, P., Ferrari, D., Falzoni, S., Sanz, J. M., Morelli, A., et al. (2001). Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood, 97, 587–600.
49. Ruggeri, Z. M., & Mendolicchio, G. L. (2007). Adhesion mechanisms in platelet function. Circulation Research, 100(12), 1673–1685.
50. Farndale, R. W. (2006). Collagen-induced platelet activation. Blood Cells, Molecules and Diseases, 36, 162–165.
51. Fredrickson, B. J., Dong, J. F., McIntire, L. V., & Lopez, J. A. (1998). Shear-dependent rolling on von Willebrand factor of mammalian cells expressing the platelet glycoprotein Ib-IX-V complex. Blood, 92, 449–461.
52. Heemskerk, J. W. M., Bevers, E. M., & Lindhout, T. (2002). Platelet activation and blood coagulation. Thrombosis and Heamostasis, 88, 186–193.
53. Hartwig, J. M., & DeSisto, M. (1991). The cytoskeleton of the resting human blood platelets: structure of the membrane skeleton and its attachment to actin filaments. The Journal of Cell Biology, 112, 407–425.
54. Serrano, K., & Devine, D. V. (2002). Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation. Thrombosis and Haemostasis, 88, 315–320.
55. Thon, J. N., & Italiano, J. E. (2012). Platelets: production, morphology and ultrastructure. Handbook of Experimental Pharmacology, 210, 3–22.
56. Rendu, F., & Brohard-Bohn, B. (2001). The platelet release reaction: granules’ constituents, secretion and functions. Platelets, 12, 261–273.
57. Menter, D. G., Tucker, S. C., Kopetz, S., Sood, A. K., Crissman, J. D., & Honn, K. V. (2014). Platelets and cancer: a casual or causal relationship: revisited. Cancer Metastasis Review, 33(1), 231–269.
58. Kato, N., Yasukawa, K., Onozuka, T., & Kimura, K. (1999). Paraneoplastic syndromes of leukocytosis, thrombocytosis, and hypercalcemia associated with squamous cell carcinoma. Journal of Dermatology, 26, 352–358.
59. Estrov, A., Talpaz, M., Mavlight, G., Pazdur, R., Harris, D., Greenberg, S. M., et al. (1995). Elevated plasma thrombopoietic activity in patients with metastatic cancer-related thrombocytosis. American Journal of Medicine, 98, 551–558.
60. Gastl, G., Plante, M., Finstad, C. L., Wong, G. Y., Federici, M. G., Bander, N. H., et al. (1993). High IL-6 levels in ascitic fluid correlate with reactive thrombocytosis in patients with epithelial ovarian cancer. British Journal of Haematology, 83, 433–441.
61. Suzuki, A., Takahashi, T., Nakamura, K., Tsuyuoka, R., Okuno, Y., Enomoto, T., et al. (1992). Thrombocytosis in patients with tumors producing colony-stimulating factor. Blood, 80, 2052–2059.
62. Rafi, S., Shapiro, F., Pettengeli, R., Ferris, B., Nachman, R. L., Moore, M. A., et al. (1995). Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood, 86, 3353–3363.
63. Higashihara, M., Sunaga, S., Tange, T., Oohashi, H., & Kurokawa, K. (1992). Increased secretion of interleukin-6 in malignant mesothelioma cells from a patient with marked thrombosis. Cancer, 70, 2105–2108.
64. Uppenkamp, M., Makarove, E., Petrasch, S., & Brittinger, G. (1998). Thrombopoietin serum concentration in patients with reactive and myeloproliferative thrombocytosis. Annals of Hematology, 77, 217–223.
65. Stone, R. L., Nick, A. M., McNeish, I. A., Balkwill, F., Dong, H. H., Bottsford-Miller, J., et al. (2013). Paraneoplastic thrombocytosis in ovarian cancer. The New England Journal of Medicine, 366, 610–618.
66. Sasaki, Y., Takahashi, T., Miyazaki, H., Matsumoto, A., Kato, T., Nakamura, K., et al. (1999). Production of thrombopoietin by human carcinomas and its novel isoforms. Blood, 94, 1952–1960.
67. Baj-Krzyworzecka, M., Majka, M., Pratico, D., Ratajczak, J., Vilaire, G., Kijowski, J., et al. (2002). Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Experimental Hematology, 30, 450–459.
68. Rafi, S., Mohle, R., Shapiro, F., Frey, B. M., & Moore, M. A. (1997). Regulation of hematopoiesis by microvascular endothelium. Leukemia & Lymphoma, 27, 375–386.
69. Wickenhauser, C., Lorenzen, J., Thiele, J., Hillienhof, A., Jungheim, K., Schmitz, B., et al. (1995). Secretion of cytokines (interleukines-1 alpha, -3, and granulocyte-macrophage colony stimulating factor) by normal human bone marrow megakaryocytes. Blood, 85, 685–691.
70. Jones, C. L., Witte, D. P., Feller, M. J., Fugman, D. A., Dorn, G. W., Liebermann, M., & A. (1992). Response of human megakaryocytic cell line to thrombin: Increase in intracellular free calcium and mitogen release. Biochimica et Biophysica Acta, 1136, 272–282.
71. Avraham, H., Banu, N., Scadden, D. T., Abraham, J., & Groopman, J. E. (1994). Modulation of megakaryocytopoiesis by human basic fibroblast growth factor. Blood, 83, 2126–2132.
72. Broxmeyer, H. E., Cooper, S., Li, Z. H., Lu, L., Song, H. Y., Kwon, B. S., et al. (1995). Myeloid progenitor cell regulatory effects of vascular endothelial cell growth factor. International Journal of Hematology, 62, 203–215.
73. Tavasolli, M., & Aoki, M. (1989). Localization of megakaryocytes in the bone marrow. Blood Cells, 15, 3–14.
74. Feng, W., Madajka, M., Kerr, B. A., Mahabeleshwar, G. H., Whiteheart, S. W., & Byzova, T. V. (2011). A novel role for platelet secretion in angiogenesis: mediating bone marrow–derived cell mobilization and homing. Blood, 117(14), 3893–3902.
75. Salgado, R., Vermeulen, P. B., Benoy, I., Weytjens, R., Huget, P., Van Marck, E., & Dirix, L. Y. (1999). Platelet number and interleukin-6 correlate with VEGF but not with bFGF serum levels of advanced cancer patients. British Journal of Cancer, 80, 892–897.
76. Yang, M., Li, K., Ng, M. H., Yuen, P. M., Fok, T. F., Li, C. K., et al. (2003). Thrombospondin-1 inhibits in vitro megakaryocytopoiesis via CD36. Thrombosis Research, 109, 47–54.
77. Bikfalvi, A., & Han, Z. C. (1994). Angiogenic factors are hematopoietic growth factors and vice versa. Leukemia, 8, 523–529.
78. Falanga, A., & Rickles, F. R. (1999). Pathophysiology of the thrombophilic state in the cancer patient. Seminars in Thrombosis and Hemostasis, 25, 173–182.
79. Kitagawa, H., Yamamoto, N., Yamamoto, K., Tanoue, K., Kosaki, G., & Yamazaki, H. (1989). Involvement of platelet membrane glycoprotein Ib and glycoprotein IIb/IIIa complex in thrombin-dependent and –independent platelet aggregations induced by tumor cells. Cancer Research, 49, 537–541.
80. Wehmeier, A., Tschope, D., Esser, J., Menzel, C., Nieuwenhuis, H. K., & Schneider, W. (1991). Circulating activated platelets in myeloproliferative disorders. Thrombosis Research, 61(3), 271–278.
81. Blann, A. D., Gurney, M., Wadley, D., Bareford, D., Stonelake, P., & Lip, G. Y. (2001). Increased soluble P-selectin in patients with haematological and breast cancer: a comparison with fibrinogen, plasminogen activator inhibitor and von Willebrand factor. Blood Coagulation and Fibrinolysis, 12(1), 43–50.
82. Caine, G. J., Lip, G. Y., & Blann, A. D. (2004). Platelet-derived VEGF, Flt-1, angiopoietin-1 and P-selectin in breast and prostate cancer: further evidence for a role of platelets in tumour angiogenesis. Annals of Medicine, 36(4), 273–277.
83. Wu, L. Q., Zhang, W. J., Niu, J. X., Ye, L. X., Yang, Z. H., Grau, G. E., & Lou, J. N. (2008). Phenotypic and functional differences between human liver cancer endothelial cells and liver sinusoidal endothelial cells. Journal of Vascular Research, 45, 78–86.
84. Han, X., Guo, B., Li, Y., & Zhu, B. (2014 Aug 1). Tissue factor in tumor microenvironment: a systematic review. Journal of Hematololgy and Oncology., 7, 54. doi:10.1186/s13045-014-0054-8.
85. Jurasz, P., Alonso-Escolano, D., & Radomski, M. W. (2004). Platelet-cancer interactions: mechanisms and pharmacology of tumor-cell-induced platelet aggregation. British Journal of Pharmacology, 143, 819–826.
86. Bastida, E., Ordinas, A., Giardina, S., & Jamieson, G. A. (1982). Differentiation of platelet-aggregating effects of human tumor cell lines based on inhibition studies with apyrase, hirudin, and phospholipase. Cancer Research, 42(11), 4348–4352.
87. Raica, M., Cimpean, A. M., & Ribatti, D. (2008). The role of podoplanin in tumor progression and metastasis. Anticancer Research, 28, 2997–3006.
88. Dang, Q., Liu, J., Li, J., & Sun, Y. (2014). Podoplanin: a novel regulator of tumor invasion and metastasis. Medical Oncology, 31(9), 24–29.
89. Lowe, K. L., Navarro-Nunez, L., & Watson, S. P. (2012). Platelet CLEC-2 and podoplanin in cancer metastasis. Thrombosis Research, 129(suppl 1), S30–S37.
90. Takagi, S., Sato, S., Oh-hara, T., Takami, M., Koike, S., Mishima, Y., et al. (2013). Platelets promote tumor growth and metastasis via direct interaction of between Aggrus/podoplanin and CLEC-2. PloS One, 8, e73609. doi:10.1371/journal.pone.0073609.
91. Demers, M., Krause, D. S., Schatzberg, D., Martinod, K., Voorhees, J. R., Fuchs, T. A., et al. (2012). Cancer predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proceedings of the National Academy of Sciences USA, 109, 13076-13081.
92. Karpatkin, S., Nierodzik, M. L., & Klepfish, A. (1996). A role of platelets, thrombin in cancer. Vessels, 2, 17–23.
93. Pinedo, H. M., Verhaul, H. M. W., D’Amato, R. J., & Folkman, J. (1998). Involvement of platelets in tumor angiogenesis? Lancet, 352(9142), 1775–1777.
94. Verheul, H. M. W., Jorna, A. S., Hoekman, K., Broxterman, H. J., Gebbink, M. F., & Pinedo, H. M. (2000). Vascular endothelial growth factor-stimulated endothelial cells promote adhesion and activation of platelets. Blood, 96(13), 4216–4221.
95. Slupsky, J. R., Kalbas, M., Willuwelt, A., Henn, V., Kroczek, R. A., & Müller-Berghaus, G. (1998). Activated platelets induce tissue factor expression on human umbilical vein endothelial cells by ligation of CD40. Thrombosis and Haemostasis, 80(6), 1008–1014.
96. Karmann, K., Min, W., Fanslow, W.C., & Pober, J. S. (1996), Activation and homologous desensitization of human endothelial cells by CD40 ligand, tumor necrosis factor, and interleukin 1. Journal of Experimental Medicine,184(1), 173-182.
97. Rafii, D. C., Psaila, B., Butler, J., Jin, D. K., & Lyden, D. (2008). Regulation of vasculogenesis by platelet-mediated recruitment of bone marrow–derived cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 28, 217–222.
98. Klement, G. L., Yip, T. T., Cassiola, F., Kikuchi, L., Cervi, D., Podust, V., et al. (2009). Platelets actively sequester angiogenesis regulators. Blood, 113, 2835–2842.
99. Kuznetsov, H. S., Marsh, T., Markens, B. A., Castaño, Z., Greene-Colozzi, A., Hay, S. A., et al. (2012). Identification of luminal breast cancers that establish a tumor-supportive microenvironment defined by proangiogenic platelets and bone marrow-derived cells. Cancer Discovery, 2, 1150–1165.
100. Best, M. G., Sol, N., Kooi, I., Tannous, B. A., Wesseling, P., & Wurdinger, T. (2015). RNA-Seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell, 28, 666–676.
101. Banks, R. E., Forbes, M. A., Kinsey, S. E., Stanley, A., Ingham, E., Walters, C., et al. (1998). Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. British Journal of Cancer, 77, 956–964.
102. Caine, G. J., Lip, G. Y., Stonelake, P. S., Ryan, P., & Blann, A. D. (2004). Platelet activation, coagulation and angiogenesis in breast and prostate carcinoma. Thrombosis and Haemostasis, 92, 185–190.
103. McDowell, G., Temple, I., Li, C., Kirwan, C. C., Bundred, N. J., McCollum, C. N., et al. (2005). Alteration in platelet function in patients with early breast cancer. Anticancer Research, 25, 3963–3966.
104. Werther, K., Christensen, I. J., & Nielsen, H. J. (2002). Determination of vascular endothelial growth factor (VEGF) in circulating blood: significance of various leukocytes and platelets. Scandinavian Journal of Clinical and Laboratory Investigation, 62, 343–350.
105. Jelkman, W. (2001). Pitfalls in the measurement of circulating vascular endothelial growth factor. Clinical Chemistry, 47, 617–623.
106. Kim, S. J., Choi, I. K., Park, K. H., Yoon, S. Y., Oh, S. C., Seo, J. H., et al. (2004). Serum vascular endothelial growth factor per platelet count in hepatocellular carcinoma: correlations with clinical parameters and survival. Journal of Clinical Oncology, 34, 184–190.
107. Brekken, R. A., Huang, X., King, S. W., & Thorpe, P. E. (1998). Vascular endothelial growth factor as a marker of tumor endothelium. Cancer Research, 58, 1952–1959.
108. Chen, F. H., Crist, S. A., Zhang, G. J., Iwamoto, Y., & See, W. A. (2002). Interleukin-6 production by human bladder tumor cell lines is up-regulated by bacillus Calmatte-Guerin through nuclear factor-kappaB and Ap-1 via an early pathway. Journal of Urology, 168, 786–797.
109. 2+ and von Willebrand factor release in human cells. American Journal of Pathology, 138, 213–221.
110. Thurston, G., Rudge, J. S., Ioffe, E., Zhou, H., Ross, L., Croll, S. D., et al. (2000). Angiopoietin-1 protects the adult vasculature against plasma leakage. Nature Medicine, 6, 460–463.
111. Wojtukiewicz, M. Z., Hempel, D., Sierko, E., Tucker, S. C., & Honn, K. V. (2016). Thrombin-unique coagulation system protein with multifaceted impacts on cancer and metastasis. Cancer Metastasis Review, 35(2), 213–233.
112. Wojtukiewicz, M. Z., Hempel, D., Sierko, E., Tucker, S. C., & Honn, K. V. (2015). Protease-activated receptors (PARs)-biology and role in cancer invasion and metastasis. Cancer Metastasis Review, 34(4), 775–796.
113. Clauss, M., Gerlach, M., Gerlach, H., Brett, J., Wang, F., Familletti, P. C., et al. (1990). Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. The Journal of Experimental Medicine, 172(6), 1535–1545.
114. Ma, L., Perini, R., McKnight, W., Klein, A., Hollenberg, M.D., & Wallace, J.L. (2005). Proteinase-activated receptors 1 and 4 counter-regulate endostatin and VEGF release from human platelets. Proceedings of the National Academy of Sciences USA, 102, 216-220.
115. Wijelath, E. S., Murray, J., Rahman, S., Patel, Y., Ishida, A., Strand, K., et al. (2002). Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circulation Research, 91(1), 25–31.
116. Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: back to Virchow? Lancet, 357, 539–545.
117. Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Behrendtsen, O., et al. (1999). Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes & Development, 13(11), 1382–1397.
118. McMahon, G. A., Petitclerc, E., Stefansson, S., Smith, E., Wong, M. K., Westrick, R. J., et al. (2001). Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis. The Journal of Biological Chemistry, 276(36), 33964–33968.
119. Bajou, K., Noel, A., Gerard, R. D., Masson, V., Brunner, N., Holst-Hansen, C., et al. (1998). Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nature Medicine, 4(8), 923–928.
120. Peterson, J. E., Zurakowski, D., Italiano Jr., J. E., Michel, L. V., Connors, S., Oenick, M., D’Amato, R. J., et al. (2012). VEGF, PF4 and PDGF are elevated in platelets of colorectal cancer patients. Angiogenesis, 15(2), 265–273.
121. Browder, T., Folkman, J., & Pirie-Shepherd, S. (2000). The hemostatic system as a regulator of angiogenesis. The Journal of Biological Chemistry, 275(3), 1521–1524.
122. Jurasz, P., Alonso, D., Castro-Blanco, S., Murad, F., & Radomski, M. W. (2003). Generation and role of angiostatin in human platelets. Blood, 102(9), 3217–3223.
123. Jurasz, P., Santos-Martinez, M. J., Radomska, A., & Radomski, M. W. (2006). Generation of platelet angiostatin mediated by urokinase plasminogen activator: effects on angiogenesis. Journal of Thrombosis and Haemostasis, 4(5), 1095–1106.
124. McEver, R. P. (2001). Adhesive interactions of leukocytes, platelets, and the vessel wall during hemostasis and inflammation. Thrombosis and Haemostasis, 86(3), 746–756.
125. Mast, A. E., Stadanlick, J. E., Lockett, M., Dietzen, D. J., Hasty, K. A., & Hall, C. L. (2000). Tissue factor pathway inhibitor binds to platelet thrombospondin-1. The Journal of Biological Chemistry., 275(41), 31715–31721.
126. Selheim, F., Fukami, M. H., Holmsen, H., & Vessbotn, F. S. (2000). Platelet-derived-growth-factor-induced signalling in human platelets: phosphoinositide-3-kinase-dependent inhibition of platelet activation. Biochemical Journal, 350, 469–475.
127. Chui, C. M., Li, K., Yang, M., Chuen, C. K., Fok, T. F., Li, C. K., et al. (2003). Platelet-derived growth factor up-regulates the expression of transcription factors NF-E2, GATA-1 and c-Fos in megakaryocytic cell lines. Cytokine, 21(2), 51–64.
128. Teuscher, E., & Weidlich, V. (1985). Adenosine nucleotides, adenosine and adenine as angiogenesis factors. Biomedica Biochimica Acta, 44, 493–495.
129. English, D., Welch, Z., Kovala, A. T., Harvey, K., Volpert, O. V., Brindley, D. N., et al. (2000). Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB Journal, 14, 2255–2265.
130. Freyssinet, J. M. (2003). Cellular microparticles: what are they bad or good for? Journal of Thrombosis and Haemostasis, 1, 1655–1662.
131. Rhee, J. S., Black, M., Schubert, U., Fischer, S., Morgenstern, E., Hames, H. P., & Preissner, K. T. (2004). The functional role of blood platelet components in angiogenesis. Thrombosis and Hemostasis, 92, 394–402.
132. Italiano, J. E., Mairuhu, A. T. A., & Fleumen Haft, R. (2010). Clinical relevance of microparticles from platelets and megakaryocytes. Current Opinion in Hematology, 17, 578–584.
133. Rak, J. (2010). Microparticles in cancer. Seminars in Thrombosis and Hemostasis, 36, 888–906.
134. Flumenhaft, R. (2006). Formation and fate of platelet microparticles. Blood Cells, Molecules and Diseases, 36, 182–187.
135. Kim, H. K., Sonfg, K. S., Park, Y. S., Kang, Y. H., Lee, Y. J., Lee, K. R., et al. (2003). Elevated levels of circulating platelet microparticles, VEGF, IL-6, and RANTES in patients with gastric cancer: possible role of a metastasis predictor. European Journal of Cancer, 39, 184–191.
136. Ratajczak, J., Wysoczyński-Hajek, F., Janowska-Wieczorek, A., & Ratajczak, M. Z. (2006). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia, 20, 1487–1495.
137. Tan, K. T., & Lip, G. Y. (2005). The potential role of platelet microparticles in atherosclerosis. Thrombosis and Haemostasis, 94, 488–492.
138. Kim, H. K., Song, K. S., Chung, J. H., Lee, K. R., & Lee, S. N. (2004). Platelet microparticles induce angiogenesis in vitro. British Journal of Haematology, 124, 374–384.
139. Brill, A., Dashevsky, O., Rivo, J., Gozal, Y., & Varon, D. (2005). Platelet-derived microparticles induce angiogenesis and stimulate post-ischaemic revascularization. Cardiovascular Research, 67, 30–38.
140. Janowska-Wieczorek, A., Wysoczynski, M., Kijowski, J., Marquez-Crtis, L., Machalinski, B., Ratajczak, J., et al. (2005). Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. International Journal of Cancer, 113, 752–760.
141. Cloutier, N., Pare, A., Farndale, R. W., Schumacher, H. R., Nigrovic, P. A., Lacroix, S., et al. (2012). Platelets can enhance vascular permeability. Blood, 120, 1334–1343.
142. Prokopi, M., Pula, G., Mayr, U., Devue, C., Gallagher, J., Xiao, Q., et al. (2009). Proteome analysis reveals presence of platelet microparticles in endothelial progenitor cell cultures. Blood, 114, 723–732.
143. Li, X., & Cong, H. (2009). Platelet-derived microparticles and the potential of glycoprotein IIb/IIIa antagonists in treating acute coronary syndrome. Texas Heart Institute Journal, 36, 134–139.
144. Martinez, M. C., & Andriantsitohaina, R. (2011). Microparticles in angiogenesis: therapeutic potential. Circulation Research, 109, 110–119.
145. Dashevsky, O., Varon, D., & Brill, A. (2009). Platelet-derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP-2 production. International Journal of Cancer, 124, 1773–1777.
146. Seiki, M. (2003). Membrane-type 1 metalloproteinase: a key enzyme for tumor invasion. Cancer Letters, 194, 1–11.
147. Cocucci, E., Racchetti, G., & Meldolesi, J. (2009). Shedding microvesicles: artefacts no more. Trends in Cell Biology., 19(2), 43–51.
148. Risitano, A., Beaulieu, L. M., Vitseva, O., & Freedman, J. E. (2012). Platelets and platelet-like particles mediate intercellular RNA transfer. Blood, 119(26), 6288–6295.
149. Diehl, P., Fricke, A., Sander, L., Stamm, J., Bassler, N., Htun, N., et al. (2012). Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovascular Research, 93(4), 633–644.
150. Herranz, H., & Cohen, S. M. (2010). MicroRNAs and gene regulatory networks: managing the impact of noise in biological system. Genes & Development, 24, 1339–1344.
151. Czech, B., & Hannon, G. J. (2011). Small RNA sorting: matchmaking for argonuates. Nature Reviews Genetics, 12, 19–31.
152. Denli, A. M., Tops, B. B., Plasterk, R. H., Ketting, R. F., & Hannon, G. J. (2004). Processing of primary microRNA by the microprocessor complex. Nature, 432, 231–235.
153. Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E., & Kutay, U. (2004). Nuclear export of microRNA precursors. Science, 303, 95–98.
154. Diederiche, S., & Haber, D. A. (2007). Dual role for argonuates in microRNA processing and posttranscriptional regulation of micro-RNA expression. Cell, 131, 1097–1108.
155. Ghildiyal, M., Xu, J., Seitz, H., Weng, Z., & Zamore, P. D. (2010). Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA, 16, 43–56.
156. Landry, P., Plante, I., Ouellet, D. L., Perron, M. P., Rousseau, G., & Provost, P. (2009). Existence of a microRNA pathway in anucleate platelets. Nature Structural & Molecular Biology, 16(9), 961–966.
157. Ple’, H., Landry, P., Benham, A., Coarfa, C., Gunaratne, P. H., & Provost, P. (2012). The repertoire and features of human platelet microRNAs. PloS One. doi:10.1371/journal.pone.0050746 Accessed 25 December 2012.
158. Kondkar, A. A., Bray, M. S., Leal, S. M., Nagalla, S., Liu, D. J., & Jin, Y. (2010). VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. Journal of Thrombosis and Haemostasis, 8(2), 369–378.
159. Nagalla, S., Shaw, C., Kong, X., Kondkar, A. A., Edelstein, L. C., Ma, L., et al. (2011). Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood, 117(19), 5189–5197.
160. Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proceedings of the National Academy of Sciences USA, 108(12), 5003–5008.
161. Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., & Remaley, A. T. (2011). MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nature Cell Biology, 13(4), 423–433.
162. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology, 9(6), 654–659.
163. Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., et al. (2009). Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Science Signaling, 2(100), ra81. doi:10.1126/scisignal. 2000610. Dec~8 Accessed 8 December 2009.
164. Boilard, E., Nigrovic, P. A., Larabee, K., Watts, G. F., Coblyn, J. S., Weinblatt, M. E., et al. (2010). Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science, 327, 580–583.
165. Gidlöf, O., van der Brug, M., Ohman, J., Gilje, P., Olde, P., Wahlestedt, C., & Erlinge, D. (2013). Platelets activated during myocardial infarction release functional miRNA, which can be taken up by endothelial cells and regulate ICAM1 expression. Blood, 121, 3908–3917.
166. Laffont, B., Corduan, A., Plé, H., Duchez, A. C., Cloutier, N., Boilard, E., & Provost, P. (2013). Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles. Blood, 122(2), 253–261.
167. Yi, P., Liang, H., Liu, H., Li, D., Chen, X., Li, L., Zhang, C.-Y., & Zen, K. (2014). Platelet-secreted microRNA-223 promotes endothelial cell apoptosis induced by advanced glycation end products via targeting the insulin-like growth factor1 receptor. Journal of Immunology, 192, 437–446.
168. Nicoli, S., Standley, C., Walker, P., Hurlstone, A., Fogarty, K. E., & Lawson, N. D. (2010). MicroRNA-mediated integration of haemodynamics and Vegf signaling during angiogenesis. Nature, 464, 1196–1200.
169. Fish, J. E., Santoro, M. M., Morton, S. U., Yu, S., Yeh, R. F., et al. (2008). miR-126 regulates angiogenic signaling and vascular integrity. Developmental Cell, 15, 272–284.
170. Nicolas, F. E., Pais, H., Schwach, F., Lindow, M., Kauppinen, S., Moulton, V., & Dalmay, T. (2008). Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA, 14, 2513–2520.
171. Poliseno, L., Tuccoli, A., Mariani, L., Evangelista, M., Citti, L., Woods, K., et al. (2006). MicroRNAs modulate the angiogenic properties of HUVECs. Blood, 108, 3068–3071.
172. le Sage, C., Nagel, R., Egan, D. A., Schrier, M., Mesman, E., Mangiola, A., et al. (2007). Regulation of the p27/(Kip1) tumor suppressor by miR-221 and niR-222 promotes cancer cell proliferation. EMBO Journal, 26, 3699–3708.
173. Italiano Jr., J. E., Richardson, J. L., Patel-Hett, S., Battinelli, E., Zaslavsky, A., Short, S., et al. (2008). Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood, 111(3), 1227–1233.
174. Cattaneo, M. (2010). New P2Y(12) inhibitors. Circulation, 121, 171–179.
175. Batinelli, E. M., Markens, B. A., & Italiano Jr., J. E. (2011). Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood, 118, 1359–1369.
176. Bambace, N. M., Levis, J. E., & Holmes, C. E. (2010). The effect of P2Y-mediated platelet activation on the release of VEGF and endostatin from platelets. Platelets, 21, 85–93.
177. Kamykowski, J., Carlton, P., Sehgal, S., & Storie, B. (2011). Quantitative immunofluorescecnce mapping reveales little functional coclustering of proteins within platelets alpha-granules. Blood, 118, 1370–1378.
178. Jonnalagadda, D., Izu, L. T., & Whiteheart, S. W. (2012). Platelet secretion is kinetically heterogeneous in an agonist-responsive manner. Blood, 120, 5209–5216.
179. Sierko, E., & Wojtukiewicz, M. Z. (2007). Inhibition of platelet function: does it offer a chance of better cancer progression control. Seminars in Thrombosis and Hemostasis, 33, 712–721.
180. Wojtukiewicz, M. Z., Sierko, E., & Zacharski, L. R. (2004). Interfering with hemostatic system components: possible new approaches to antiangiogenic therapy. Seminars in Thrombosis and Hemostasis, 30, 145–156.