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Cancer and Metastasis Reviews

, Volume 36, Issue 2, pp 199–213 | Cite as

Platelet “first responders” in wound response, cancer, and metastasis

  • David G. MenterEmail author
  • Scott Kopetz
  • Ernest Hawk
  • Anil K. Sood
  • Jonathan M. Loree
  • Paolo Gresele
  • Kenneth V. Honn
Article

Abstract

Platelets serve as “first responders” during normal wounding and homeostasis. Arising from bone marrow stem cell lineage megakaryocytes, anucleate platelets can influence inflammation and immune regulation. Biophysically, platelets are optimized due to size and discoid morphology to distribute near vessel walls, monitor vascular integrity, and initiate quick responses to vascular lesions. Adhesion receptors linked to a highly reactive filopodia-generating cytoskeleton maximizes their vascular surface contact allowing rapid response capabilities. Functionally, platelets normally initiate rapid clotting, vasoconstriction, inflammation, and wound biology that leads to sterilization, tissue repair, and resolution. Platelets also are among the first to sense, phagocytize, decorate, or react to pathogens in the circulation. These platelet first responder properties are commandeered during chronic inflammation, cancer progression, and metastasis. Leaky or inflammatory reaction blood vessel genesis during carcinogenesis provides opportunities for platelet invasion into tumors. Cancer is thought of as a non-healing or chronic wound that can be actively aided by platelet mitogenic properties to stimulate tumor growth. This growth ultimately outstrips circulatory support leads to angiogenesis and intravasation of tumor cells into the blood stream. Circulating tumor cells reengage additional platelets, which facilitates tumor cell adhesion, arrest and extravasation, and metastasis. This process, along with the hypercoagulable states associated with malignancy, is amplified by IL6 production in tumors that stimulate liver thrombopoietin production and elevates circulating platelet numbers by thrombopoiesis in the bone marrow. These complex interactions and the “first responder” role of platelets during diverse physiologic stresses provide a useful therapeutic target that deserves further exploration.

Keywords

Platelet TCIPA Metastasis Thrombosis Extravasation CTC 

Notes

Acknowledgements

Grant and other support

Boone Pickens Distinguished Chair for Early Prevention of Cancer, Duncan Family Institute, Colorectal Cancer Moon Shot, P30CA016672-41, 1R01CA187238-01, 5R01CA172670-03, and 1R01CA184843-01A1, CA177909, and the American Cancer Society Research Professor Award.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflicts of interest.

References

  1. 1.
    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 Reviews, 33(1), 231–269.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Menter, D., Davis, J., Tucker, S., Hawk, E., Crissman, J., Sood, A., et al. (2017). Platelets “First Responders” in cancer progression and metastasis. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 1111–1132). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  3. 3.
    Leunissen, T. C., Wisman, P. P., van Holten, T. C., de Groot, P. G., Korporaal, S. J., Koekman, A. C., et al. (2016). The effect of P2Y12 inhibition on platelet activation assessed with aggregation- and flow cytometry-based assays. Platelets, 1–9.Google Scholar
  4. 4.
    Liu, X., Li, Y., Zhu, H., Zhao, Z., Zhou, Y., Zaske, A. M., et al. (2015). Use of non-contact hopping probe ion conductance microscopy to investigate dynamic morphology of live platelets. Platelets, 26(5), 480–485.PubMedCrossRefGoogle Scholar
  5. 5.
    Lof, A., Muller, J. P., Benoit, M., & Brehm, M. A. (2017). Biophysical approaches promote advances in the understanding of von Willebrand factor processing and function. Advances in Biological Regulation, 63, 81–91.PubMedCrossRefGoogle Scholar
  6. 6.
    Heijnen, H., & Korporaal, S. (2017). Platelet morphology and ultrastructure. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 21–37). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  7. 7.
    O'Brien, S., Kent, N. J., Lucitt, M., Ricco, A. J., McAtamney, C., Kenny, D., et al. (2012). Effective hydrodynamic shaping of sample streams in a microfluidic parallel-plate flow-assay device: matching whole blood dynamic viscosity. IEEE Transactions on Biomedical Engineering, 59(2), 374–382.PubMedCrossRefGoogle Scholar
  8. 8.
    Jen, C. J., & Tai, Y. W. (1992). Morphological study of platelet adhesion dynamics under whole blood flow conditions. Platelets, 3(3), 145–153.PubMedCrossRefGoogle Scholar
  9. 9.
    Folie, B. J., & McIntire, L. V. (1989). Mathematical analysis of mural thrombogenesis. Concentration profiles of platelet-activating agents and effects of viscous shear flow. Biophysical Journal, 56(6), 1121–1141.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Fedosov, D. A., Noguchi, H., & Gompper, G. (2014). Multiscale modeling of blood flow: from single cells to blood rheology. Biomechanics and Modeling in Mechanobiology, 13(2), 239–258.PubMedCrossRefGoogle Scholar
  11. 11.
    Kumar, A., & Graham, M. D. (2012). Mechanism of margination in confined flows of blood and other multicomponent suspensions. Physical Review Letters, 109(10), 108102.PubMedCrossRefGoogle Scholar
  12. 12.
    Tokarev, A. A., Butylin, A. A., & Ataullakhanov, F. I. (2011). Platelet adhesion from shear blood flow is controlled by near-wall rebounding collisions with erythrocytes. Biophysical Journal, 100(4), 799–808.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Tokarev, A. A., Butylin, A. A., Ermakova, E. A., Shnol, E. E., Panasenko, G. P., & Ataullakhanov, F. I. (2011). Finite platelet size could be responsible for platelet margination effect. Biophysical Journal, 101(8), 1835–1843.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Lee, S. Y., Ferrari, M., & Decuzzi, P. (2009). Design of bio-mimetic particles with enhanced vascular interaction. Journal of Biomechanics, 42(12), 1885–1890.PubMedCrossRefGoogle Scholar
  15. 15.
    Stukelj, R., Schara, K., Bedina-Zavec, A., Sustar, V., Pajnic, M., Paden, L., et al. (2017). Effect of shear stress in the flow through the sampling needle on concentration of nanovesicles isolated from blood. European Journal of Pharmaceutical Sciences, 98, 17–29.PubMedCrossRefGoogle Scholar
  16. 16.
    De Gruttola, S., Boomsma, K., & Poulikakos, D. (2005). Computational simulation of a non-newtonian model of the blood separation process. Artificial Organs, 29(12), 949–959.PubMedCrossRefGoogle Scholar
  17. 17.
    Nesbitt, W. S., Westein, E., Tovar-Lopez, F. J., Tolouei, E., Mitchell, A., Fu, J., et al. (2009). A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nature Medicine, 15(6), 665–673.PubMedCrossRefGoogle Scholar
  18. 18.
    Menter, D. G., Steinert, B. W., Sloane, B. F., Gundlach, N., O'Gara, C. Y., Marnett, L. J., et al. (1987). Role of platelet membrane in enhancement of tumor cell adhesion to endothelial cell extracellular matrix. Cancer Research, 47(24 Pt 1), 6751–6762.PubMedGoogle Scholar
  19. 19.
    Crissman, J. D., Hatfield, J. S., Menter, D. G., Sloane, B., & Honn, K. V. (1988). Morphological study of the interaction of intravascular tumor cells with endothelial cells and subendothelial matrix. Cancer Research, 48(14), 4065–4072.PubMedGoogle Scholar
  20. 20.
    Walsh, T. G., Metharom, P., & Berndt, M. C. (2015). The functional role of platelets in the regulation of angiogenesis. Platelets, 26(3), 199–211.PubMedCrossRefGoogle Scholar
  21. 21.
    Kim, K. H., Barazia, A., & Cho, J. (2013). Real-time imaging of heterotypic platelet-neutrophil interactions on the activated endothelium during vascular inflammation and thrombus formation in live mice. Journal of Visualized Experiments, 74.Google Scholar
  22. 22.
    Spectre, G., Zhu, L., Ersoy, M., Hjemdahl, P., Savion, N., Varon, D., et al. (2012). Platelets selectively enhance lymphocyte adhesion on subendothelial matrix under arterial flow conditions. Thrombosis and Haemostasis, 108(2), 328–337.PubMedCrossRefGoogle Scholar
  23. 23.
    Gardiner, E., & Andrews, R. (2017). Platelet adhesion. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 309–319). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  24. 24.
    Pothapragada, S., Zhang, P., Sheriff, J., Livelli, M., Slepian, M. J., Deng, Y., et al. (2015). A phenomenological particle-based platelet model for simulating filopodia formation during early activation. International Journal of Numerical Methods in Biomedical Engineering, 31(3), e02702.CrossRefGoogle Scholar
  25. 25.
    Kunert, S., Meyer, I., Fleischhauer, S., Wannack, M., Fiedler, J., Shivdasani, R. A., et al. (2009). The microtubule modulator RanBP10 plays a critical role in regulation of platelet discoid shape and degranulation. Blood, 114(27), 5532–5540.PubMedCrossRefGoogle Scholar
  26. 26.
    Jackson, S. P., Nesbitt, W. S., & Westein, E. (2009). Dynamics of platelet thrombus formation. Journal of Thrombosis and Haemostasis, 7(Suppl 1), 17–20.PubMedCrossRefGoogle Scholar
  27. 27.
    Italiano Jr., J. E., Bergmeier, W., Tiwari, S., Falet, H., Hartwig, J. H., Hoffmeister, K. M., et al. (2003). Mechanisms and implications of platelet discoid shape. Blood, 101(12), 4789–4796.PubMedCrossRefGoogle Scholar
  28. 28.
    Hartwig, J. H., Barkalow, K., Azim, A., & Italiano, J. (1999). The elegant platelet: signals controlling actin assembly. Thrombosis and Haemostasis, 82(2), 392–398.PubMedGoogle Scholar
  29. 29.
    White, J. G., & Rao, G. H. (1998). Microtubule coils versus the surface membrane cytoskeleton in maintenance and restoration of platelet discoid shape. The American Journal of Pathology, 152(2), 597–609.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Polanowska-Grabowska, R., Geanacopoulos, M., & Gear, A. R. (1993). Platelet adhesion to collagen via the alpha 2 beta 1 integrin under arterial flow conditions causes rapid tyrosine phosphorylation of pp125FAK. Biochemical Journal, 296(Pt 3), 543–547.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Falet, H. (2017). Anatomy of the platelet cytoskeleton. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 139–156). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  32. 32.
    Nurden, A. T., & Nurden, P. (2014). Congenital platelet disorders and understanding of platelet function. British Journal of Haematology, 165(2), 165–178.PubMedCrossRefGoogle Scholar
  33. 33.
    Coburn, L. A., Damaraju, V. S., Dozic, S., Eskin, S. G., Cruz, M. A., & McIntire, L. V. (2011). GPIbalpha-vWF rolling under shear stress shows differences between type 2B and 2M von Willebrand disease. Biophysical Journal, 100(2), 304–312.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Colace, T. V., & Diamond, S. L. (2013). Direct observation of von Willebrand factor elongation and fiber formation on collagen during acute whole blood exposure to pathological flow. Arteriosclerosis, Thrombosis, and Vascular Biology, 33(1), 105–113.PubMedCrossRefGoogle Scholar
  35. 35.
    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(10), 3684–3693.PubMedGoogle Scholar
  36. 36.
    Jackson, S. P., Mistry, N., & Yuan, Y. (2000). Platelets and the injured vessel wall—“rolling into action”: focus on glycoprotein Ib/V/IX and the platelet cytoskeleton. Trends in Cardiovascular Medicine, 10(5), 192–197.PubMedCrossRefGoogle Scholar
  37. 37.
    Yago, T., Lou, J., Wu, T., Yang, J., Miner, J. J., Coburn, L., et al. (2008). Platelet glycoprotein Ibalpha forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. The Journal of Clinical Investigation, 118(9), 3195–3207.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Clemetson, K. J. (2007). A short history of platelet glycoprotein Ib complex. Thrombosis and Haemostasis, 98(1), 63–68.PubMedGoogle Scholar
  39. 39.
    Li, R., & Emsley, J. (2013). The organizing principle of the platelet glycoprotein Ib-IX-V complex. Journal of Thrombosis and Haemostasis, 11(4), 605–614.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bernard, J., & Soulier, J. (1948). Sur une nouvelle variété de dystrophie thrombocytaire-hémorragipare congénitale. Semin Hôp Paris, 24, 3217–3223.Google Scholar
  41. 41.
    Ozaki, Y., Suzuki-Inoue, K., & Inoue, O. (2013). Platelet receptors activated via mulitmerization: glycoprotein VI, GPIb-IX-V, and CLEC-2. Journal of Thrombosis and Haemostasis, 11(Suppl 1), 330–339.PubMedCrossRefGoogle Scholar
  42. 42.
    Bernardo, A., Ball, C., Nolasco, L., Choi, H., Moake, J. L., & Dong, J. F. (2005). Platelets adhered to endothelial cell-bound ultra-large von Willebrand factor strings support leukocyte tethering and rolling under high shear stress. Journal of Thrombosis and Haemostasis, 3(3), 562–570.PubMedCrossRefGoogle Scholar
  43. 43.
    De Ceunynck, K., De Meyer, S. F., & Vanhoorelbeke, K. (2013). Unwinding the von Willebrand factor strings puzzle. Blood, 121(2), 270–277.PubMedCrossRefGoogle Scholar
  44. 44.
    Desch, A., Strozyk, E. A., Bauer, A. T., Huck, V., Niemeyer, V., Wieland, T., et al. (2012). Highly invasive melanoma cells activate the vascular endothelium via an MMP-2/integrin alphavbeta5-induced secretion of VEGF-A. The American Journal of Pathology, 181(2), 693–705.PubMedCrossRefGoogle Scholar
  45. 45.
    Coller, B. S., & 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(8), 3011–3025.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kim, C., & Kim, M. C. (2013). Differences in alpha-beta transmembrane domain interactions among integrins enable diverging integrin signaling. Biochemical and Biophysical Research Communications, 436(3), 406–412.PubMedCrossRefGoogle Scholar
  47. 47.
    Kim, C., Lau, T. L., Ulmer, T. S., & Ginsberg, M. H. (2009). Interactions of platelet integrin alphaIIb and beta3 transmembrane domains in mammalian cell membranes and their role in integrin activation. Blood, 113(19), 4747–4753.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Shattil, S. J. (2009). The beta3 integrin cytoplasmic tail: protein scaffold and control freak. Journal of Thrombosis and Haemostasis, 7(Suppl 1), 210–213.PubMedCrossRefGoogle Scholar
  49. 49.
    Nurden, A. T., & Caen, J. P. (1974). An abnormal platelet glycoprotein pattern in three cases of Glanzmann's thrombasthenia. British Journal of Haematology, 28(2), 253–260.PubMedCrossRefGoogle Scholar
  50. 50.
    Phillips, D. R., Jenkins, C. S., Luscher, E. F., & Larrieu, M. (1975). Molecular differences of exposed surface proteins on thrombasthenic platelet plasma membranes. Nature, 257(5527), 599–600.PubMedCrossRefGoogle Scholar
  51. 51.
    Glanzmann, E. (1918). Hereditare hammorhagische thrombastehnie. Beitr Pathologie Bluplatchen J Kinderkt, 88, 113–141.Google Scholar
  52. 52.
    Zhang, C., Zhang, L., Zhang, Y., Sun, N., Jiang, S., Fujihara, T. J., et al. (2016). Development of antithrombotic nanoconjugate blocking integrin alpha2beta1-collagen interactions. Scientific Reports, 6, 26292.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Szanto, T., Joutsi-Korhonen, L., Deckmyn, H., & Lassila, R. (2012). New insights into von Willebrand disease and platelet function. Seminars in Thrombosis and Hemostasis, 38(1), 55–63.PubMedCrossRefGoogle Scholar
  54. 54.
    Maurer, E., Schaff, M., Receveur, N., Bourdon, C., Mercier, L., Nieswandt, B., et al. (2015). Fibrillar cellular fibronectin supports efficient platelet aggregation and procoagulant activity. Thrombosis and Haemostasis, 114(6), 1175–1188.PubMedCrossRefGoogle Scholar
  55. 55.
    McCarty, O. J., Zhao, Y., Andrew, N., Machesky, L. M., Staunton, D., Frampton, J., et al. (2004). Evaluation of the role of platelet integrins in fibronectin-dependent spreading and adhesion. Journal of Thrombosis and Haemostasis, 2(10), 1823–1833.PubMedCrossRefGoogle Scholar
  56. 56.
    Schaff, M., Tang, C., Maurer, E., Bourdon, C., Receveur, N., Eckly, A., et al. (2013). Integrin alpha6beta1 is the main receptor for vascular laminins and plays a role in platelet adhesion, activation, and arterial thrombosis. Circulation, 128(5), 541–552.PubMedCrossRefGoogle Scholar
  57. 57.
    Inoue, O., Suzuki-Inoue, K., McCarty, O. J., Moroi, M., Ruggeri, Z. M., Kunicki, T. J., et al. (2006). Laminin stimulates spreading of platelets through integrin alpha6beta1-dependent activation of GPVI. Blood, 107(4), 1405–1412.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Clemetson, K. J. (1995). Platelet activation: signal transduction via membrane receptors. Thrombosis and Haemostasis, 74(1), 111–116.PubMedGoogle Scholar
  59. 59.
    Moroi, M., Jung, S. M., Okuma, M., & Shinmyozu, K. (1989). A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. The Journal of Clinical Investigation, 84(5), 1440–1445.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Asselin, J., Knight, C. G., Farndale, R. W., Barnes, M. J., & Watson, S. P. (1999). Monomeric (glycine-proline-hydroxyproline)10 repeat sequence is a partial agonist of the platelet collagen receptor glycoprotein VI. Biochemical Journal, 339(Pt 2), 413–418.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Kehrel, B., Wierwille, S., Clemetson, K. J., Anders, O., Steiner, M., Knight, C. G., et al. (1998). Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood, 91(2), 491–499.PubMedGoogle Scholar
  62. 62.
    Zahid, M., Mangin, P., Loyau, S., Hechler, B., Billiald, P., Gachet, C., et al. (2012). The future of glycoprotein VI as an antithrombotic target. Journal of Thrombosis and Haemostasis, 10(12), 2418–2427.PubMedCrossRefGoogle Scholar
  63. 63.
    Li, P., Qiao, J. L., & Xu, K. L. (2017). Advances of studies on platelet GPVI as antithrombotic target—review. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 25(1), 264–269.PubMedGoogle Scholar
  64. 64.
    Poulter, N. S., Pollitt, A. Y., Owen, D. M., Gardiner, E. E., Andrews, R. K., Shimizu, H., et al. (2017). Clustering of glycoprotein VI (GPVI) dimers upon adhesion to collagen as a mechanism to regulate GPVI signaling in platelets. Journal of Thrombosis and Haemostasis, 15(3), 549–564.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Pierre, S., Linke, B., Suo, J., Tarighi, N., Del Turco, D., Thomas, D., et al. (2017). GPVI and thromboxane receptor on platelets promote proinflammatory macrophage phenotypes during cutaneous inflammation. The Journal of Investigative Dermatology, 137(3), 686–695.PubMedCrossRefGoogle Scholar
  66. 66.
    Bergmeier, W., & Stefanini, L. (2013). Platelet ITAM signaling. Current Opinion in Hematology, 20(5), 445–450.PubMedCrossRefGoogle Scholar
  67. 67.
    Takemoto, A., Okitaka, M., Takagi, S., Takami, M., Sato, S., Nishio, M., et al. (2017). A critical role of platelet TGF-beta release in podoplanin-mediated tumour invasion and metastasis. Scientific Reports, 7, 42186.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Nakazawa, Y., Sato, S., Naito, M., Kato, Y., Mishima, K., Arai, H., et al. (2008). Tetraspanin family member CD9 inhibits aggrus/podoplanin-induced platelet aggregation and suppresses pulmonary metastasis. Blood, 112(5), 1730–1739.PubMedCrossRefGoogle Scholar
  69. 69.
    Navarro-Nunez, L., Langan, S. A., Nash, G. B., & Watson, S. P. (2013). The physiological and pathophysiological roles of platelet CLEC-2. Thrombosis and Haemostasis, 109(6), 991–998.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Suzuki-Inoue, K., Fuller, G. L., Garcia, A., Eble, J. A., Pohlmann, S., Inoue, O., et al. (2006). A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood, 107(2), 542–549.PubMedCrossRefGoogle Scholar
  71. 71.
    Suzuki-Inoue, K., Kato, Y., Inoue, O., Kaneko, M. K., Mishima, K., Yatomi, Y., et al. (2007). Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. The Journal of Biological Chemistry, 282(36), 25993–26001.PubMedCrossRefGoogle Scholar
  72. 72.
    Pula, B., Witkiewicz, W., Dziegiel, P., & Podhorska-Okolow, M. (2013). Significance of podoplanin expression in cancer-associated fibroblasts: a comprehensive review. International Journal of Oncology, 42(6), 1849–1857.PubMedGoogle Scholar
  73. 73.
    Watson, A. A., Brown, J., Harlos, K., Eble, J. A., Walter, T. S., & O'Callaghan, C. A. (2007). The crystal structure and mutational binding analysis of the extracellular domain of the platelet-activating receptor CLEC-2. The Journal of Biological Chemistry, 282(5), 3165–3172.PubMedCrossRefGoogle Scholar
  74. 74.
    Watson, A. A., & O'Callaghan, C. A. (2005). Crystallization and X-ray diffraction analysis of human CLEC-2. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications, 61(Pt 12), 1094–1096.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Suzuki-Inoue, K., Inoue, O., & Ozaki, Y. (2011). Novel platelet activation receptor CLEC-2: from discovery to prospects. Journal of Thrombosis and Haemostasis, 9(Suppl 1), 44–55.PubMedCrossRefGoogle Scholar
  76. 76.
    Johnston, G. I., Cook, R. G., & McEver, R. P. (1989). Cloning of GMP-140, a granule membrane protein of platelets and endothelium: sequence similarity to proteins involved in cell adhesion and inflammation. Cell, 56(6), 1033–1044.PubMedCrossRefGoogle Scholar
  77. 77.
    Stenberg, P. E., McEver, R. P., Shuman, M. A., Jacques, Y. V., & Bainton, D. F. (1985). A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. The Journal of Cell Biology, 101(3), 880–886.PubMedCrossRefGoogle Scholar
  78. 78.
    Zarbock, A., Muller, H., Kuwano, Y., & Ley, K. (2009). PSGL-1-dependent myeloid leukocyte activation. Journal of Leukocyte Biology, 86(5), 1119–1124.PubMedCrossRefGoogle Scholar
  79. 79.
    Picker, L. J., Warnock, R. A., Burns, A. R., Doerschuk, C. M., Berg, E. L., & Butcher, E. C. (1991). The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell, 66(5), 921–933.PubMedCrossRefGoogle Scholar
  80. 80.
    Polley, M. J., Phillips, M. L., Wayner, E., Nudelman, E., Singhal, A. K., Hakomori, S., et al. (1991). CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x. Proceedings of the National Academy of Sciences of the United States of America, 88(14), 6224–6228.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Foxall, C., Watson, S. R., Dowbenko, D., Fennie, C., Lasky, L. A., Kiso, M., et al. (1992). The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. The Journal of Cell Biology, 117(4), 895–902.PubMedCrossRefGoogle Scholar
  82. 82.
    Habets, K. L., Huizinga, T. W., & Toes, R. E. (2013). Platelets and autoimmunity. European Journal of Clinical Investigation, 43(7), 746–757.PubMedCrossRefGoogle Scholar
  83. 83.
    Kazmi, R. S., Cooper, A. J., & Lwaleed, B. A. (2011). Platelet function in pre-eclampsia. Seminars in Thrombosis and Hemostasis, 37(2), 131–136.PubMedCrossRefGoogle Scholar
  84. 84.
    Nurden, A. T. (2011). Platelets, inflammation and tissue regeneration. Thrombosis and Haemostasis, 105(Suppl 1), S13–S33.PubMedCrossRefGoogle Scholar
  85. 85.
    Borsig, L. (2008). The role of platelet activation in tumor metastasis. Expert Review of Anticancer Therapy, 8(8), 1247–1255.PubMedCrossRefGoogle Scholar
  86. 86.
    Dammacco, F., Vacca, A., Procaccio, P., Ria, R., Marech, I., & Racanelli, V. (2013). Cancer-related coagulopathy (Trousseau's syndrome): review of the literature and experience of a single center of internal medicine. Clinical and Experimental Medicine, 13(2), 85–97.PubMedCrossRefGoogle Scholar
  87. 87.
    Erpenbeck, L., & Schon, M. P. (2010). Deadly allies: the fatal interplay between platelets and metastasizing cancer cells. Blood, 115(17), 3427–3436.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Gay, L. J., & Felding-Habermann, B. (2011). Contribution of platelets to tumour metastasis. Nature Reviews. Cancer, 11(2), 123–134.PubMedCrossRefGoogle Scholar
  89. 89.
    Gay, L. J., & Felding-Habermann, B. (2011). Platelets alter tumor cell attributes to propel metastasis: programming in transit. Cancer Cell, 20(5), 553–554.PubMedCrossRefGoogle Scholar
  90. 90.
    Kyriazi, V., & Theodoulou, E. (2013). Assessing the risk and prognosis of thrombotic complications in cancer patients. Archives of Pathology & Laboratory Medicine, 137(9), 1286–1295.CrossRefGoogle Scholar
  91. 91.
    McEver, R. P. (1997). Selectin-carbohydrate interactions during inflammation and metastasis. Glycoconjugate Journal, 14(5), 585–591.PubMedCrossRefGoogle Scholar
  92. 92.
    Dangel, O., Mergia, E., Karlisch, K., Groneberg, D., Koesling, D., & Friebe, A. (2010). Nitric oxide-sensitive guanylyl cyclase is the only nitric oxide receptor mediating platelet inhibition. Journal of Thrombosis and Haemostasis, 8(6), 1343–1352.PubMedCrossRefGoogle Scholar
  93. 93.
    Koziak, K., Sevigny, J., Robson, S. C., Siegel, J. B., & Kaczmarek, E. (1999). Analysis of CD39/ATP diphosphohydrolase (ATPDase) expression in endothelial cells, platelets and leukocytes. Thrombosis and Haemostasis, 82(5), 1538–1544.PubMedGoogle Scholar
  94. 94.
    Moncada, S., Gryglewski, R., Bunting, S., & Vane, J. R. (1976). An enzyme isolated from arteries transforms prostaglandin endoperoxides to an unstable substance that inhibits platelet aggregation. Nature, 263(5579), 663–665.PubMedCrossRefGoogle Scholar
  95. 95.
    Sabetkar, M., Naseem, K. M., Tullett, J. M., Friebe, A., Koesling, D., & Bruckdorfer, K. R. (2001). Synergism between nitric oxide and hydrogen peroxide in the inhibition of platelet function: the roles of soluble guanylyl cyclase and vasodilator-stimulated phosphoprotein. Nitric Oxide, 5(3), 233–242.PubMedCrossRefGoogle Scholar
  96. 96.
    Zimmermann, H. (1999). Nucleotides and cd39: principal modulatory players in hemostasis and thrombosis. Nature Medicine, 5(9), 987–988.PubMedCrossRefGoogle Scholar
  97. 97.
    Aleman, M. M., Gardiner, C., Harrison, P., & Wolberg, A. S. (2011). Differential contributions of monocyte- and platelet-derived microparticles towards thrombin generation and fibrin formation and stability. Journal of Thrombosis and Haemostasis, 9(11), 2251–2261.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Feng, D., Nagy, J. A., Pyne, K., Dvorak, H. F., & Dvorak, A. M. (1998). Platelets exit venules by a transcellular pathway at sites of F-met peptide-induced acute inflammation in guinea pigs. International Archives of Allergy and Immunology, 116(3), 188–195.PubMedCrossRefGoogle Scholar
  99. 99.
    Gawaz, M., & Vogel, S. (2013). Platelets in tissue repair: control of apoptosis and interactions with regenerative cells. Blood, 122(15), 2550–2554.PubMedCrossRefGoogle Scholar
  100. 100.
    Lowenhaupt, R. W., Glueck, H. I., Miller, M. A., & Kline, D. L. (1977). Factors which influence blood platelet migration. The Journal of Laboratory and Clinical Medicine, 90(1), 37–45.PubMedGoogle Scholar
  101. 101.
    Nathan, P. (1973). The migration of human platelets in vitro. Thrombosis et Diathesis Haemorrhagica, 30(1), 173–177.PubMedGoogle Scholar
  102. 102.
    Schmidt, E. M., Munzer, P., Borst, O., Kraemer, B. F., Schmid, E., Urban, B., et al. (2011). Ion channels in the regulation of platelet migration. Biochemical and Biophysical Research Communications, 415(1), 54–60.PubMedCrossRefGoogle Scholar
  103. 103.
    Banerjee, D., Mazumder, S., & Kumar Sinha, A. (2016). Involvement of nitric oxide on calcium mobilization and arachidonic acid pathway activation during platelet aggregation with different aggregating agonists. International Journal of Biomedical Sciences, 12(1), 25–35.Google Scholar
  104. 104.
    Philipose, S., Konya, V., Lazarevic, M., Pasterk, L. M., Marsche, G., Frank, S., et al. (2012). Laropiprant attenuates EP3 and TP prostanoid receptor-mediated thrombus formation. PloS One, 7(8), e40222.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Feletou, M., Huang, Y., & Vanhoutte, P. M. (2010). Vasoconstrictor prostanoids. Pflügers Archiv, 459(6), 941–950.PubMedCrossRefGoogle Scholar
  106. 106.
    Kandhi, S., Zhang, B., Froogh, G., Qin, J., Alruwali, N., Le, Y., et al. (2017). EETs promote hypoxic pulmonary vasoconstriction via constrictor prostanoids. American Journal of Physiology. Lung Cellular and Molecular Physiology ajplung 00038 02017.Google Scholar
  107. 107.
    Bhagwat, S. S., Hamann, P. R., Still, W. C., Bunting, S., & Fitzpatrick, F. A. (1985). Synthesis and structure of the platelet aggregation factor thromboxane A2. Nature, 315(6019), 511–513.CrossRefGoogle Scholar
  108. 108.
    Hamberg, M., Svensson, J., & Samuelsson, B. (1975). Thromboxanes: a new group of biologically active compounds derived from prostaglandin endoperoxides. Proceedings of the National Academy of Sciences of the United States of America, 72(8), 2994–2998.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Fukami, M. H., & Salganicoff, L. (1977). Human platelet storage organelles. A review. Thrombosis and Haemostasis, 38(4), 963–970.PubMedGoogle Scholar
  110. 110.
    Koseoglu, S., & Flaumenhaft, R. (2013). Advances in platelet granule biology. Current Opinion in Hematology, 20(5), 464–471.PubMedCrossRefGoogle Scholar
  111. 111.
    Wihlborg, A. K., Wang, L., Braun, O. O., Eyjolfsson, A., Gustafsson, R., Gudbjartsson, T., et al. (2004). ADP receptor P2Y12 is expressed in vascular smooth muscle cells and stimulates contraction in human blood vessels. Arteriosclerosis, Thrombosis, and Vascular Biology, 24(10), 1810–1815.PubMedCrossRefGoogle Scholar
  112. 112.
    Goschnick, M. W., & Jackson, D. E. (2007). Tetraspanins-structural and signalling scaffolds that regulate platelet function. Mini Reviews in Medicinal Chemistry, 7(12), 1248–1254.PubMedCrossRefGoogle Scholar
  113. 113.
    Haining, E. J., Yang, J., & Tomlinson, M. G. (2011). Tetraspanin microdomains: fine-tuning platelet function. Biochemical Society Transactions, 39(2), 518–523.PubMedCrossRefGoogle Scholar
  114. 114.
    Protty, M. B., Watkins, N. A., Colombo, D., Thomas, S. G., Heath, V. L., Herbert, J. M., et al. (2009). Identification of Tspan9 as a novel platelet tetraspanin and the collagen receptor GPVI as a component of tetraspanin microdomains. Biochemical Journal, 417(1), 391–400.PubMedCrossRefGoogle Scholar
  115. 115.
    Israels, S. J., McMillan, E. M., Robertson, C., Singhory, S., & McNicol, A. (1996). The lysosomal granule membrane protein, LAMP-2, is also present in platelet dense granule membranes. Thrombosis and Haemostasis, 75(4), 623–629.PubMedGoogle Scholar
  116. 116.
    Xu, L., Harada, H., & Taniguchi, A. (2008). The effects of LAMP1 and LAMP3 on M180 amelogenin uptake, localization and amelogenin mRNA induction by amelogenin protein. Journal of Biochemistry, 144(4), 531–537.PubMedCrossRefGoogle Scholar
  117. 117.
    Vanags, D. M., Rodgers, S. E., Duncan, E. M., Lloyd, J. V., & Bochner, F. (1992). Potentiation of ADP-induced aggregation in human platelet-rich plasma by 5-hydroxytryptamine and adrenaline. British Journal of Pharmacology, 106(4), 917–923.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Petito, E., Momi, S., & Gresele, P. (2017). The migration of platelets and their interaction with other migrating cells. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 337–351). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  119. 119.
    Sandri, G., Bonferoni, M. C., Rossi, S., Ferrari, F., Mori, M., Cervio, M., et al. (2015). Platelet lysate embedded scaffolds for skin regeneration. Expert Opinion on Drug Delivery, 12(4), 525–545.PubMedCrossRefGoogle Scholar
  120. 120.
    Kurokawa, T., & Ohkohchi, N. (2017). Platelets in liver disease, cancer and regeneration. World Journal of Gastroenterology, 23(18), 3228–3239.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Mancuso, M. E., & Santagostino, E. (2017). Platelets: much more than bricks in a breached wall. British Journal of Haematology, 4, 1–10.Google Scholar
  122. 122.
    Anitua, E., Troya, M., Zalduendo, M., & Orive, G. (2017). Personalized plasma-based medicine to treat age-related diseases. Materials Science & Engineering. C, Materials for Biological Applications, 74, 459–464.CrossRefGoogle Scholar
  123. 123.
    Meschi, N., Castro, A. B., Vandamme, K., Quirynen, M., & Lambrechts, P. (2016). The impact of autologous platelet concentrates on endodontic healing: a systematic review. Platelets, 27(7), 613–633.PubMedCrossRefGoogle Scholar
  124. 124.
    Mlynarek, R. A., Kuhn, A. W., & Bedi, A. (2016). Platelet-rich plasma (PRP) in orthopedic sports medicine. American Journal of Orthopedics (Belle Mead, N.J.), 45(5), 290–326.Google Scholar
  125. 125.
    Goubran, H. A., Stakiw, J., Radosevic, M., & Burnouf, T. (2014). Platelets effects on tumor growth. Seminars in Oncology, 41(3), 359–369.PubMedCrossRefGoogle Scholar
  126. 126.
    Unwith, S., Zhao, H., Hennah, L., & Ma, D. (2015). The potential role of HIF on tumour progression and dissemination. International Journal of Cancer, 136(11), 2491–2503.PubMedCrossRefGoogle Scholar
  127. 127.
    Schmidt, E. M., Kraemer, B. F., Borst, O., Munzer, P., Schonberger, T., Schmidt, C., et al. (2012). SGK1 sensitivity of platelet migration. Cellular Physiology and Biochemistry, 30(1), 259–268.PubMedCrossRefGoogle Scholar
  128. 128.
    Kraemer, B. F., Borst, O., Gehring, E. M., Schoenberger, T., Urban, B., Ninci, E., et al. (2010). PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). Journal of Molecular Medicine (Berlin), 88(12), 1277–1288.CrossRefGoogle Scholar
  129. 129.
    Brandt, E., Ludwig, A., Petersen, F., & Flad, H. D. (2000). Platelet-derived CXC chemokines: old players in new games. Immunological Reviews, 177, 204–216.PubMedCrossRefGoogle Scholar
  130. 130.
    Stone, R. L., Nick, A. M., McNeish, I. A., Balkwill, F., Han, H. D., Bottsford-Miller, J., et al. (2012). Paraneoplastic thrombocytosis in ovarian cancer. The New England Journal of Medicine, 366(7), 610–618.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Kraemer, B. F., Schmidt, C., Urban, B., Bigalke, B., Schwanitz, L., Koch, M., et al. (2011). High shear flow induces migration of adherent human platelets. Platelets, 22(6), 415–421.PubMedCrossRefGoogle Scholar
  132. 132.
    Chatterjee, M., Huang, Z., Zhang, W., Jiang, L., Hultenby, K., Zhu, L., et al. (2011). Distinct platelet packaging, release, and surface expression of proangiogenic and antiangiogenic factors on different platelet stimuli. Blood, 117(14), 3907–3911.PubMedCrossRefGoogle Scholar
  133. 133.
    Shenkman, B., Brill, A., Brill, G., Lider, O., Savion, N., & Varon, D. (2004). Differential response of platelets to chemokines: RANTES non-competitively inhibits stimulatory effect of SDF-1 alpha. Journal of Thrombosis and Haemostasis, 2(1), 154–160.PubMedCrossRefGoogle Scholar
  134. 134.
    Gleissner, C. A., von Hundelshausen, P., & Ley, K. (2008). Platelet chemokines in vascular disease. Arteriosclerosis, Thrombosis, and Vascular Biology, 28(11), 1920–1927.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Rossaint, J., & Zarbock, A. (2015). Platelets in leucocyte recruitment and function. Cardiovascular Research, 107(3):386–95.Google Scholar
  136. 136.
    Garraud, O., Berthet, J., Hamzeh-Cognasse, H., & Cognasse, F. (2011). Pathogen sensing, subsequent signalling, and signalosome in human platelets. Thrombosis Research, 127(4), 283–286.PubMedCrossRefGoogle Scholar
  137. 137.
    von Hundelshausen, P., & Weber, C. (2007). Platelets as immune cells: bridging inflammation and cardiovascular disease. Circulation Research, 100(1), 27–40.CrossRefGoogle Scholar
  138. 138.
    Rath, D., Chatterjee, M., Borst, O., Muller, K., Langer, H., Mack, A. F., et al. (2015). Platelet surface expression of stromal cell-derived factor-1 receptors CXCR4 and CXCR7 is associated with clinical outcomes in patients with coronary artery disease. Journal of Thrombosis and Haemostasis, 13(5), 719–728.PubMedCrossRefGoogle Scholar
  139. 139.
    Rafii, S., Cao, Z., Lis, R., Siempos, I. I., Chavez, D., Shido, K., et al. (2015). Platelet-derived SDF-1 primes the pulmonary capillary vascular niche to drive lung alveolar regeneration. Nature Cell Biology, 17(2), 123–136.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Chatterjee, M., Seizer, P., Borst, O., Schonberger, T., Mack, A., Geisler, T., et al. (2014). SDF-1alpha induces differential trafficking of CXCR4-CXCR7 involving cyclophilin A, CXCR7 ubiquitination and promotes platelet survival. The FASEB Journal, 28(7), 2864–2878.PubMedCrossRefGoogle Scholar
  141. 141.
    Rath, D., Chatterjee, M., Borst, O., Muller, K., Stellos, K., Mack, A. F., et al. (2014). Expression of stromal cell-derived factor-1 receptors CXCR4 and CXCR7 on circulating platelets of patients with acute coronary syndrome and association with left ventricular functional recovery. European Heart Journal, 35(6), 386–394.PubMedCrossRefGoogle Scholar
  142. 142.
    Iannacone, M. (2016). Platelet-mediated modulation of adaptive immunity. Seminars in Immunology, 28(6), 555–560.PubMedCrossRefGoogle Scholar
  143. 143.
    Danese, S., & Fiocchi, C. (2016). Endothelial cell-immune cell interaction in IBD. Digestive Diseases, 34(1–2), 43–50.PubMedCrossRefGoogle Scholar
  144. 144.
    Chatterjee, M., & Geisler, T. (2016). Inflammatory contribution of platelets revisited: new players in the arena of inflammation. Seminars in Thrombosis and Hemostasis, 42(3), 205–214.PubMedCrossRefGoogle Scholar
  145. 145.
    Carestia, A., Kaufman, T., & Schattner, M. (2016). Platelets: new bricks in the building of neutrophil extracellular traps. Frontiers in Immunology, 7, 271.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Lam, F. W., Vijayan, K. V., & Rumbaut, R. E. (2015). Platelets and their interactions with other immune cells. Comprehensive Physiology, 5(3), 1265–1280.PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Kapur, R., Zufferey, A., Boilard, E., & Semple, J. W. (2015). Nouvelle cuisine: platelets served with inflammation. Journal of Immunology, 194(12), 5579–5587.CrossRefGoogle Scholar
  148. 148.
    Cognasse, F., Nguyen, K. A., Damien, P., McNicol, A., Pozzetto, B., Hamzeh-Cognasse, H., et al. (2015). The inflammatory role of platelets via their TLRs and Siglec receptors. Frontiers in Immunology, 6, 83.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Chatterjee, M., Rath, D., & Gawaz, M. (2015). Role of chemokine receptors CXCR4 and CXCR7 for platelet function. Biochemical Society Transactions, 43(4), 720–726.PubMedCrossRefGoogle Scholar
  150. 150.
    Varki, A. (2011). Since there are PAMPs and DAMPs, there must be SAMPs? Glycan “self-associated molecular patterns” dampen innate immunity, but pathogens can mimic them. Glycobiology, 21(9), 1121–1124.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Menter, D. G., Steinert, B. W., Sloane, B. F., Taylor, J. D., & Honn, K. V. (1987). A new in vitro model for investigation of tumor cell-platelet-endothelial cell interactions and concomitant eicosanoid biosynthesis. Cancer Research, 47(9), 2425–2432.PubMedGoogle Scholar
  152. 152.
    Chopra, H., Timar, J., Rong, X., Grossi, I. M., Hatfield, J. S., Fligiel, S. E., et al. (1992). Is there a role for the tumor cell integrin alpha IIb beta 3 and cytoskeleton in tumor cell-platelet interaction? Clinical & Experimental Metastasis, 10(2), 125–137.CrossRefGoogle Scholar
  153. 153.
    Bennett, J. S., Zigmond, S., Vilaire, G., Cunningham, M. E., & Bednar, B. (1999). The platelet cytoskeleton regulates the affinity of the integrin alpha(IIb)beta(3) for fibrinogen. The Journal of Biological Chemistry, 274(36), 25301–25307.PubMedCrossRefGoogle Scholar
  154. 154.
    Breckenridge, M. T., Egelhoff, T. T., & Baskaran, H. (2010). A microfluidic imaging chamber for the direct observation of chemotactic transmigration. Biomedical Microdevices, 12(3), 543–553.PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Ellingsen, T., Storgaard, M., Moller, B. K., Buus, A., Andersen, P. L., Obel, N., et al. (2000). Migration of mononuclear cells in the modified Boyden chamber as evaluated by DNA quantification and flow cytometry. Scandinavian Journal of Immunology, 52(3), 257–263.PubMedCrossRefGoogle Scholar
  156. 156.
    Friedl, P., Wolf, K., & Lammerding, J. (2011). Nuclear mechanics during cell migration. Current Opinion in Cell Biology, 23(1), 55–64.PubMedCrossRefGoogle Scholar
  157. 157.
    Bdeir, K., Gollomp, K., Stasiak, M., Mei, J., Papiewska-Pajak, I., Zhao, G., et al. (2017). Platelet-specific chemokines contribute to the pathogenesis of acute lung injury. American Journal of Respiratory Cell and Molecular Biology, 56(2), 261–270.PubMedGoogle Scholar
  158. 158.
    Bruce, I. J., & Kerry, R. (1987). The effect of chloramphenicol and cycloheximide on platelet aggregation and protein synthesis. Biochemical Pharmacology, 36(11), 1769–1773.PubMedCrossRefGoogle Scholar
  159. 159.
    Borisova, T. A., & Markosian, R. A. (1977). Age and biosynthesis and breakdown of thrombocyte proteins. Biulleten' Eksperimental'noĭ Biologii i Meditsiny, 83(1), 20–21.PubMedGoogle Scholar
  160. 160.
    Pagel, O., Walter, E., Jurk, K., & Zahedi, R. P. (2017). Taking the stock of granule cargo: platelet releasate proteomics. Platelets, 28(2), 119–128.PubMedCrossRefGoogle Scholar
  161. 161.
    Melki, I., Tessandier, N., Zufferey, A., & Boilard, E. (2017). Platelet microvesicles in health and disease. Platelets, 28(3), 214–221.PubMedCrossRefGoogle Scholar
  162. 162.
    Wang, Z. T., Wang, Z., & Hu, Y. W. (2016). Possible roles of platelet-derived microparticles in atherosclerosis. Atherosclerosis, 248, 10–16.PubMedCrossRefGoogle Scholar
  163. 163.
    Franco, A. T., Corken, A., & Ware, J. (2015). Platelets at the interface of thrombosis, inflammation, and cancer. Blood, 126(5), 582–588.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Cointe, S., Lacroix, R., & Dignat-George, F. (2017). Platelet-derived microparticles. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 379–392). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  165. 165.
    Zilberman-Rudenko, J., Sylman, J. L., Lakshmanan, H. H. S., McCarty, O. J. T., & Maddala, J. (2017). Dynamics of blood flow and thrombus formation in a multi-bypass microfluidic ladder network. Cellular and Molecular Bioengineering, 10(1), 16–29.PubMedCrossRefGoogle Scholar
  166. 166.
    Whyte, C. S., Mitchell, J. L., & Mutch, N. J. (2017). Platelet-mediated modulation of fibrinolysis. Seminars in Thrombosis and Hemostasis, 43(2), 115–128.PubMedCrossRefGoogle Scholar
  167. 167.
    Biolik, G., Kokot, M., Sznapka, M., Swieszek, A., Ziaja, D., Pawlicki, K., et al. (2017). Platelet reactivity in thromboelastometry. Revision of the FIBTEM test: a basic study. Scandinavian Journal of Clinical and Laboratory Investigation, 77(3), 216–222.PubMedCrossRefGoogle Scholar
  168. 168.
    Mammadova-Bach, E., Ollivier, V., Loyau, S., Schaff, M., Dumont, B., Favier, R., et al. (2015). Platelet glycoprotein VI binds to polymerized fibrin and promotes thrombin generation. Blood, 126(5), 683–691.PubMedCrossRefGoogle Scholar
  169. 169.
    Kral, J. B., Schrottmaier, W. C., Salzmann, M., & Assinger, A. (2016). Platelet interaction with innate immune cells. Transfusion Medicine and Hemotherapy, 43(2), 78–88.PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Clark, S. R., Ma, A. C., Tavener, S. A., McDonald, B., Goodarzi, Z., Kelly, M. M., et al. (2007). Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nature Medicine, 13(4), 463–469.PubMedCrossRefGoogle Scholar
  171. 171.
    Joshi, S., & Whiteheart, S. W. (2017). The nuts and bolts of the platelet release reaction. Platelets, 28(2), 129–137.PubMedCrossRefGoogle Scholar
  172. 172.
    Suades, R., Padro, T., & Badimon, L. (2015). The role of blood-borne microparticles in inflammation and hemostasis. Seminars in Thrombosis and Hemostasis, 41(6), 590–606.PubMedCrossRefGoogle Scholar
  173. 173.
    Gill, P., Jindal, N. L., Jagdis, A., & Vadas, P. (2015). Platelets in the immune response: revisiting platelet-activating factor in anaphylaxis. The Journal of Allergy and Clinical Immunology, 135(6), 1424–1432.PubMedCrossRefGoogle Scholar
  174. 174.
    Momi, S., & Wiwanitkit, V. (2017). Phylogeny of blood platelets. In P. Gresele, N. Kleiman, J. Lopez, & C. Page (Eds.), Platelets in thrombotic and non-thrombotic disorders (Vol. 2, pp. 11–19). Switzerland: Springer International Publishing.CrossRefGoogle Scholar
  175. 175.
    Roch, G. J., & Sherwood, N. M. (2014). Glycoprotein hormones and their receptors emerged at the origin of metazoans. Genome Biology and Evolution, 6(6), 1466–1479.PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    He, W., Tang, Y., Qi, B., Lu, C., Qin, C., Wei, Y., et al. (2014). Phylogenetic analysis and positive-selection site detecting of vascular endothelial growth factor family in vertebrates. Gene, 535(2), 345–352.PubMedCrossRefGoogle Scholar
  177. 177.
    Mercer, P. F., & Chambers, R. C. (2013). Coagulation and coagulation signalling in fibrosis. Biochimica et Biophysica Acta, 1832(7), 1018–1027.PubMedCrossRefGoogle Scholar
  178. 178.
    Yamaguchi, Y., & Yoshikawa, K. (2001). Cutaneous wound healing: an update. The Journal of Dermatology, 28(10), 521–534.PubMedCrossRefGoogle Scholar
  179. 179.
    Gerarduzzi, C., & Di Battista, J. A. (2017). Myofibroblast repair mechanisms post-inflammatory response: a fibrotic perspective. Inflammation Research, 66(6), 451–465.PubMedCrossRefGoogle Scholar
  180. 180.
    Greaves, N. S., Ashcroft, K. J., Baguneid, M., & Bayat, A. (2013). Current understanding of molecular and cellular mechanisms in fibroplasia and angiogenesis during acute wound healing. Journal of Dermatological Science, 72(3), 206–217.PubMedCrossRefGoogle Scholar
  181. 181.
    Carthy, J. M. (2017). TGFbeta signaling and the control of myofibroblast differentiation: implications for chronic inflammatory disorders. Journal of Cellular Physiology. doi: 10.1002/jcp.25879.
  182. 182.
    Ghosh, D., McGrail, D. J., & Dawson, M. R. (2017). TGF-beta1 pretreatment improves the function of mesenchymal stem cells in the wound bed. Frontiers in Cell and Development Biology, 5, 28.CrossRefGoogle Scholar
  183. 183.
    Valcourt, U., Carthy, J., Okita, Y., Alcaraz, L., Kato, M., Thuault, S., et al. (2016). Analysis of epithelial-mesenchymal transition induced by transforming growth factor beta. Methods in Molecular Biology, 1344, 147–181.PubMedCrossRefGoogle Scholar
  184. 184.
    Das, U. N. (2016). Inflammatory bowel disease as a disorder of an imbalance between pro- and anti-inflammatory molecules and deficiency of resolution bioactive lipids. Lipids in Health and Disease, 15, 11.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Gensel, J. C., & Zhang, B. (2015). Macrophage activation and its role in repair and pathology after spinal cord injury. Brain Research, 1619, 1–11.PubMedCrossRefGoogle Scholar
  186. 186.
    Shinde, A. V., & Frangogiannis, N. G. (2014). Fibroblasts in myocardial infarction: a role in inflammation and repair. Journal of Molecular and Cellular Cardiology, 70, 74–82.PubMedCrossRefGoogle Scholar
  187. 187.
    Arwert, E. N., Hoste, E., & Watt, F. M. (2012). Epithelial stem cells, wound healing and cancer. Nature Reviews. Cancer, 12(3), 170–180.PubMedCrossRefGoogle Scholar
  188. 188.
    Dovizio, M., Sacco, A., & Patrignani, P. (2017). Curbing tumorigenesis and malignant progression through the pharmacological control of the wound healing process. Vascular Pharmacology, 89, 1–11.PubMedCrossRefGoogle Scholar
  189. 189.
    Dvorak, H. F. (2015). Tumors: wounds that do not heal-redux. Cancer Immunology Research, 3(1), 1–11.PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Lichtenberger, L., Fang, D., Bick, R., Poindexter, B., Phan, T., Bergeron, A., et al. (2017). Unlocking aspirin's chemopreventive activity: role of irreversibly inhibiting platelet cyclooxygenase-1. Cancer Prevention Reseach, 10, 142–152.CrossRefGoogle Scholar
  191. 191.
    Menter, D. G., Hatfield, J. S., Harkins, C., Sloane, B. F., Taylor, J. D., Crissman, J. D., et al. (1987). Tumor cell-platelet interactions in vitro and their relationship to in vivo arrest of hematogenously circulating tumor cells. Clinical & Experimental Metastasis, 5(1), 65–78.CrossRefGoogle Scholar
  192. 192.
    Menter, D. G., Harkins, C., Onoda, J., Riorden, W., Sloane, B. F., Taylor, J. D., et al. (1987). Inhibition of tumor cell induced platelet aggregation by prostacyclin and carbacyclin: an ultrastructural study. Invasion & Metastasis, 7(2), 109–128.Google Scholar
  193. 193.
    Umar, A., Steele, V. E., Menter, D. G., & Hawk, E. T. (2016). Mechanisms of nonsteroidal anti-inflammatory drugs in cancer prevention. Seminars in Oncology, 43(1), 65–77.PubMedCrossRefGoogle Scholar
  194. 194.
    Drew, D. A., Cao, Y., & Chan, A. T. (2016). Aspirin and colorectal cancer: the promise of precision chemoprevention. Nature Reviews. Cancer, 16(3), 173–186.PubMedCrossRefGoogle Scholar
  195. 195.
    Holmes, C. E., Jasielec, J., Levis, J. E., Skelly, J., & Muss, H. B. (2013). Initiation of aspirin therapy modulates angiogenic protein levels in women with breast cancer receiving tamoxifen therapy. Clinical and Translational Science, 6(5), 386–390.PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Bardia, A., Ebbert, J. O., Vierkant, R. A., Limburg, P. J., Anderson, K., Wang, A. H., et al. (2007). Association of aspirin and nonaspirin nonsteroidal anti-inflammatory drugs with cancer incidence and mortality. Journal of the National Cancer Institute, 99(11), 881–889.PubMedCrossRefGoogle Scholar
  197. 197.
    Bosetti, C., Rosato, V., Gallus, S., Cuzick, J., & La Vecchia, C. (2012). Aspirin and cancer risk: a quantitative review to 2011. Annals of Oncology, 23(6), 1403–1415.PubMedCrossRefGoogle Scholar
  198. 198.
    Chan, A. T., Manson, J. E., Feskanich, D., Stampfer, M. J., Colditz, G. A., & Fuchs, C. S. (2007). Long-term aspirin use and mortality in women. Archives of Internal Medicine, 167(6), 562–572.PubMedCrossRefGoogle Scholar
  199. 199.
    Ratnasinghe, L. D., Graubard, B. I., Kahle, L., Tangrea, J. A., Taylor, P. R., & Hawk, E. (2004). Aspirin use and mortality from cancer in a prospective cohort study. Anticancer Research, 24(5B), 3177–3184.PubMedGoogle Scholar
  200. 200.
    Sandler, R. S., Halabi, S., Baron, J. A., Budinger, S., Paskett, E., Keresztes, R., et al. (2003). A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. The New England Journal of Medicine, 348(10), 883–890.PubMedCrossRefGoogle Scholar
  201. 201.
    Baron, J. A., Cole, B. F., Sandler, R. S., Haile, R. W., Ahnen, D., Bresalier, R., et al. (2003). A randomized trial of aspirin to prevent colorectal adenomas. The New England Journal of Medicine, 348(10), 891–899.PubMedCrossRefGoogle Scholar
  202. 202.
    Burn, J., Gerdes, A. M., Macrae, F., Mecklin, J. P., Moeslein, G., Olschwang, S., et al. (2011). Long-term effect of aspirin on cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2 randomised controlled trial. Lancet, 378(9809), 2081–2087.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    Drew, D. A., Chin, S. M., Gilpin, K. K., Parziale, M., Pond, E., Schuck, M. M., et al. (2017). ASPirin intervention for the REDuction of colorectal cancer risk (ASPIRED): a study protocol for a randomized controlled trial. Trials, 18(1), 50.PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    Honn, K. V., Cicone, B., & Skoff, A. (1981). Prostacyclin: a potent antimetastatic agent. Science, 212(4500), 1270–1272.PubMedCrossRefGoogle Scholar
  205. 205.
    Honn, K. V., Menter, D., Cavanaugh, P. G., Neagos, G., Moilanen, D., Taylor, J. D., et al. (1983). A review of prostaglandins and the treatment of tumor metastasis. Acta Clinica Belgica, 38(1), 53–67.PubMedCrossRefGoogle Scholar
  206. 206.
    Gasic, G. J., Gasic, T. B., & Stewart, C. C. (1968). Antimetastatic effects associated with platelet reduction. Proceedings of the National Academy of Sciences of the United States of America, 61(1), 46–52.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Woods, J. R. (1964). Experimental studies of the intravascular dissemination of Ascitic V2 carcinoma cells in the rabbit, with special reference to fibrinogen and fibrinolytic agents. Bulletin der Schweizerischen Akademie der Medizinischen Wissenschaften, 20, 92–121.PubMedGoogle Scholar
  208. 208.
    Horejsova, M., Pavlickova, V., Koukolik, F., & Strritesky, J. (1995). Morphologic verification of neoplastic portal vein obstruction. Casopís Lékar̆ů C̆eských, 134(20), 655–657.PubMedGoogle Scholar
  209. 209.
    Benazzi, C., Al-Dissi, A., Chau, C. H., Figg, W. D., Sarli, G., de Oliveira, J. T., et al. (2014). Angiogenesis in spontaneous tumors and implications for comparative tumor biology. ScientificWorldJournal, 2014, 919570.PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    Fein, M. R., & Egeblad, M. (2013). Caught in the act: revealing the metastatic process by live imaging. Disease Models & Mechanisms, 6(3), 580–593.CrossRefGoogle Scholar
  211. 211.
    Starke, J., Wehrle-Haller, B., & Friedl, P. (2014). Plasticity of the actin cytoskeleton in response to extracellular matrix nanostructure and dimensionality. Biochemical Society Transactions, 42(5), 1356–1366.PubMedCrossRefGoogle Scholar
  212. 212.
    Gritsenko, P. G., Ilina, O., & Friedl, P. (2012). Interstitial guidance of cancer invasion. The Journal of Pathology, 226(2), 185–199.PubMedCrossRefGoogle Scholar
  213. 213.
    Friedl, P., Sahai, E., Weiss, S., & Yamada, K. M. (2012). New dimensions in cell migration. Nature Reviews. Molecular Cell Biology, 13(11), 743–747.PubMedCrossRefGoogle Scholar
  214. 214.
    Friedl, P., Wolf, K., & Zegers, M. M. (2014). Rho-directed forces in collective migration. Nature Cell Biology, 16(3), 208–210.PubMedCrossRefGoogle Scholar
  215. 215.
    Haeger, A., Krause, M., Wolf, K., & Friedl, P. (2014). Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. Biochimica et Biophysica Acta, 1840(8), 2386–2395.PubMedCrossRefGoogle Scholar
  216. 216.
    Deng, G., Krishnakumar, S., Powell, A. A., Zhang, H., Mindrinos, M. N., Telli, M. L., et al. (2014). Single cell mutational analysis of PIK3CA in circulating tumor cells and metastases in breast cancer reveals heterogeneity, discordance, and mutation persistence in cultured disseminated tumor cells from bone marrow. BMC Cancer, 14, 456.PubMedPubMedCentralCrossRefGoogle Scholar
  217. 217.
    Powell, A. A., Talasaz, A. H., Zhang, H., Coram, M. A., Reddy, A., Deng, G., et al. (2012). Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PloS One, 7(5), e33788.PubMedPubMedCentralCrossRefGoogle Scholar
  218. 218.
    Tang, J., Gao, X., Zhi, M., Zhou, H. M., Zhang, M., Chen, H. W., et al. (2015). Plateletcrit: a sensitive biomarker for evaluating disease activity in Crohn's disease with low hs-CRP. Journal of Digestive Diseases, 16(3), 118–124.PubMedCrossRefGoogle Scholar
  219. 219.
    Pasula, S., Cai, X., Dong, Y., Messa, M., McManus, J., Chang, B., et al. (2012). Endothelial epsin deficiency decreases tumor growth by enhancing VEGF signaling. The Journal of Clinical Investigation, 122(12), 4424–4438.PubMedPubMedCentralCrossRefGoogle Scholar
  220. 220.
    Hellberg, C., Ostman, A., & Heldin, C. H. (2010). PDGF and vessel maturation. Recent Results in Cancer Research, 180, 103–114.PubMedCrossRefGoogle Scholar
  221. 221.
    Carmeliet, P. (2005). VEGF as a key mediator of angiogenesis in cancer. Oncology, 69(Suppl 3), 4–10.PubMedCrossRefGoogle Scholar
  222. 222.
    Keskin, D., Kim, J., Cooke, V. G., Wu, C. C., Sugimoto, H., Gu, C., et al. (2015). Targeting vascular pericytes in hypoxic tumors increases lung metastasis via angiopoietin-2. Cell Reports, 10(7), 1066–1081.PubMedPubMedCentralCrossRefGoogle Scholar
  223. 223.
    Nagy, J. A., Dvorak, A. M., & Dvorak, H. F. (2012). Vascular hyperpermeability, angiogenesis, and stroma generation. Cold Spring Harbor Perspectives in Medicine, 2(2), a006544.PubMedPubMedCentralCrossRefGoogle Scholar
  224. 224.
    Fukumura, D., & Jain, R. K. (2008). Imaging angiogenesis and the microenvironment. APMIS, 116(7–8), 695–715.PubMedPubMedCentralCrossRefGoogle Scholar
  225. 225.
    Kisucka, J., Butterfield, C. E., Duda, D. G., Eichenberger, S. C., Saffaripour, S., Ware, J., et al. (2006). Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proceedings of the National Academy of Sciences of the United States of America, 103(4), 855–860.PubMedPubMedCentralCrossRefGoogle Scholar
  226. 226.
    Schumacher, D., Strilic, B., Sivaraj, K. K., Wettschureck, N., & Offermanns, S. (2013). Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell, 24(1), 130–137.PubMedCrossRefGoogle Scholar
  227. 227.
    O'Byrne, K. J., & Steward, W. P. (2001). Tumour angiogenesis: a novel therapeutic target in patients with malignant disease. Expert Opinion on Emerging Drugs, 6(1), 155–174.PubMedGoogle Scholar
  228. 228.
    Satelli, A., Mitra, A., Brownlee, Z., Xia, X., Bellister, S., Overman, M. J., et al. (2015). Epithelial-mesenchymal transitioned circulating tumor cells capture for detecting tumor progression. Clinical Cancer Research, 21(4), 899–906.PubMedCrossRefGoogle Scholar
  229. 229.
    Labelle, M., & Hynes, R. O. (2012). The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discovery, 2(12), 1091–1099.PubMedPubMedCentralCrossRefGoogle Scholar
  230. 230.
    Labelle, M., Begum, S., & Hynes, R. O. (2011). Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell, 20(5), 576–590.PubMedPubMedCentralCrossRefGoogle Scholar
  231. 231.
    van Es, N., Sturk, A., Middeldorp, S., & Nieuwland, R. (2014). Effects of cancer on platelets. Seminars in Oncology, 41(3), 311–318.PubMedCrossRefGoogle Scholar
  232. 232.
    Nistico, P., Bissell, M. J., & Radisky, D. C. (2012). Epithelial-mesenchymal transition: general principles and pathological relevance with special emphasis on the role of matrix metalloproteinases. Cold Spring Harbor Perspectives in Biology, 4(2), 1–10.Google Scholar
  233. 233.
    Gresele, P., Falcinelli, E., Sebastiano, M., & Momi, S. (2017). Matrix metalloproteinases and platelet function. Progress in Molecular Biology and Translational Science, 147, 133–165.PubMedCrossRefGoogle Scholar
  234. 234.
    Fidler, I. J. (1978). Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Research, 38(9), 2651–2660.PubMedGoogle Scholar
  235. 235.
    Billroth, T. (1878). Lectures on surgical pathology and therapeutics, a handbook for students and practitioners (Vol. II). London: The New Sydenham Society.Google Scholar
  236. 236.
    Johnson, J. H., & Woods, J. R. (1963). An in vitro study of fibrinolytic agents on V2 carcinoma cells and intravascular thrombi in rabbits. Bulletin of the Johns Hopkins Hospital, 113, 335–346.PubMedGoogle Scholar
  237. 237.
    Baserga, R., & Saffiotti, U. (1955). Experimental studies on histogenesis of blood-borne metastases. A.M.A. Archives of Pathology, 59(1), 26–34.PubMedGoogle Scholar
  238. 238.
    Jones, D. S., Wallace, A. C., & Fraser, E. E. (1971). Sequence of events in experimental metastases of Walker 256 tumor: light, immunofluorescent, and electron microscopic observations. Journal of the National Cancer Institute, 46(3), 493–504.PubMedGoogle Scholar
  239. 239.
    Chew, E. C., & Wallace, A. C. (1976). Demonstration of fibrin in early stages of experimental metastases. Cancer Research, 36(6), 1904–1909.PubMedGoogle Scholar
  240. 240.
    Warren, B. A., & Vales, O. (1972). The adhesion of thromboplastic tumour emboli to vessel walls in vivo. British Journal of Experimental Pathology, 53(3), 301–313.PubMedPubMedCentralGoogle Scholar
  241. 241.
    Warren, B. A., & Vales, O. (1972). The release of vesicles from platelets following adhesion to vessel walls in vitro. British Journal of Experimental Pathology, 53(2), 206–215.PubMedPubMedCentralGoogle Scholar
  242. 242.
    Warren, B. A. (1976). Some aspects of blood borne tumour emboli associated with thrombosis. Zeitschrift für Krebsforschung und Klinische Onkologie. Cancer Research and Clinical Oncology, 87(1), 1–15.PubMedGoogle Scholar
  243. 243.
    Kinjo, M. (1978). Lodgement and extravasation of tumour cells in blood-borne metastasis: an electron microscope study. British Journal of Cancer, 38(2), 293–301.PubMedPubMedCentralCrossRefGoogle Scholar
  244. 244.
    Gastpar, H. (1978). Inhibition of cancer cell stickiness, a model for the testing of in vivo thrombocyte aggregation inhibitors. IV. Effect of sulfinpyrazone. Fortschritte der Medizin, 96(36), 1823–1827.PubMedGoogle Scholar
  245. 245.
    Paul, C. D., Mistriotis, P., & Konstantopoulos, K. (2017). Cancer cell motility: lessons from migration in confined spaces. Nature Reviews. Cancer, 17(2), 131–140.PubMedCrossRefGoogle Scholar
  246. 246.
    Tonisen, F., Perrin, L., Bayarmagnai, B., van den Dries, K., Cambi, A., & Gligorijevic, B. (2017). EP4 receptor promotes invadopodia and invasion in human breast cancer. European Journal of Cell Biology, 96(2), 218–226.PubMedCrossRefGoogle Scholar
  247. 247.
    Lonsdorf, A. S., Kramer, B. F., Fahrleitner, M., Schonberger, T., Gnerlich, S., Ring, S., et al. (2012). Engagement of alphaIIbbeta3 (GPIIb/IIIa) with alphanubeta3 integrin mediates interaction of melanoma cells with platelets: a connection to hematogenous metastasis. The Journal of Biological Chemistry, 287(3), 2168–2178.PubMedCrossRefGoogle Scholar
  248. 248.
    Lichtenberger, L. M., Fang, D., Bick, R. J., Poindexter, B. J., Phan, T., Bergeron, A. L., et al. (2017). Unlocking aspirin’s chemopreventive activity: role of irreversibly inhibiting platelet cyclooxygenase-1. Cancer Prevention Research (Philadelphia, Pa.), 10(2), 142–152.CrossRefGoogle Scholar
  249. 249.
    Hu, Q., Wang, M., Cho, M. S., Wang, C., Nick, A. M., Thiagarajan, P., et al. (2016). Lipid profile of platelets and platelet-derived microparticles in ovarian cancer. BBA Clin, 6, 76–81.PubMedPubMedCentralCrossRefGoogle Scholar
  250. 250.
    Haemmerle, M., Bottsford-Miller, J., Pradeep, S., Taylor, M. L., Choi, H. J., Hansen, J. M., et al. (2016). FAK regulates platelet extravasation and tumor growth after antiangiogenic therapy withdrawal. The Journal of Clinical Investigation, 126(5), 1885–1896.PubMedPubMedCentralCrossRefGoogle Scholar
  251. 251.
    Qi, C., Li, B., Guo, S., Wei, B., Shao, C., Li, J., et al. (2015). P-selectin-mediated adhesion between platelets and tumor cells promotes intestinal tumorigenesis in Apc(min/+) mice. International Journal of Biological Sciences, 11(6), 679–687.PubMedPubMedCentralCrossRefGoogle Scholar
  252. 252.
    Crissman, J. D., Hatfield, J., Schaldenbrand, M., Sloane, B. F., & Honn, K. V. (1985). Arrest and extravasation of B16 amelanotic melanoma in murine lungs. A light and electron microscopic study. Laboratory Investigation, 53(4), 470–478.PubMedGoogle Scholar
  253. 253.
    Oleksowicz, L., Mrowiec, Z., Schwartz, E., Khorshidi, M., Dutcher, J. P., & Puszkin, E. (1995). Characterization of tumor-induced platelet aggregation: the role of immunorelated GPIb and GPIIb/IIIa expression by MCF-7 breast cancer cells. Thrombosis Research, 79(3), 261–274.PubMedCrossRefGoogle Scholar
  254. 254.
    Bouvenot, G., Escande, M., Xeridat, B., Simonin, G., Boucoiran, J., & Delboy, C. (1977). Thrombocytosis and cancer. Apropos of a chronological series of 100 patients. La Semaine des Hôpitaux, 53(36), 1921–1925.PubMedGoogle Scholar
  255. 255.
    Honn, K. V., Tang, D. G., & Crissman, J. D. (1992). Platelets and cancer metastasis: a causal relationship? Cancer Metastasis Reviews, 11(3–4), 325–351.PubMedCrossRefGoogle Scholar
  256. 256.
    Levin, J., & Conley, C. L. (1964). Thrombocytosis associated with malignant disease. Archives of Internal Medicine, 114, 497–500.PubMedCrossRefGoogle Scholar
  257. 257.
    Rank, A., Liebhardt, S., Zwirner, J., Burges, A., Nieuwland, R., & Toth, B. (2012). Circulating microparticles in patients with benign and malignant ovarian tumors. Anticancer Research, 32(5), 2009–2014.PubMedGoogle Scholar
  258. 258.
    Nieuwland, R., Berckmans, R. J., Rotteveel-Eijkman, R. C., Maquelin, K. N., Roozendaal, K. J., Jansen, P. G., et al. (1997). Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation, 96(10), 3534–3541.PubMedCrossRefGoogle Scholar
  259. 259.
    van Doormaal, F., Kleinjan, A., Berckmans, R. J., Mackman, N., Manly, D., Kamphuisen, P. W., et al. (2012). Coagulation activation and microparticle-associated coagulant activity in cancer patients. An exploratory prospective study. Thrombosis and Haemostasis, 108(1), 160–165.PubMedCrossRefGoogle Scholar
  260. 260.
    Cokic, V. P., Mitrovic-Ajtic, O., Beleslin-Cokic, B. B., Markovic, D., Buac, M., Diklic, M., et al. (2015). Proinflammatory cytokine IL-6 and JAK-STAT signaling pathway in myeloproliferative neoplasms. Mediators of Inflammation, 2015, 453020.PubMedPubMedCentralCrossRefGoogle Scholar
  261. 261.
    Matsuo, K., Hasegawa, K., Yoshino, K., Murakami, R., Hisamatsu, T., Stone, R. L., et al. (2015). Venous thromboembolism, interleukin-6 and survival outcomes in patients with advanced ovarian clear cell carcinoma. European Journal of Cancer, 51(14), 1978–1988.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • David G. Menter
    • 1
    Email author
  • Scott Kopetz
    • 1
  • Ernest Hawk
    • 2
  • Anil K. Sood
    • 3
    • 4
    • 5
  • Jonathan M. Loree
    • 1
  • Paolo Gresele
    • 6
  • Kenneth V. Honn
    • 7
    • 8
    • 9
  1. 1.Department of Gastrointestinal Medical OncologyM. D. Anderson Cancer CenterHoustonUSA
  2. 2.Office of the Vice President Cancer Prevention & Population ScienceM. D. Anderson Cancer CenterHoustonUSA
  3. 3.Gynocologic Oncology & Reproductive Medicine M. D. Anderson Cancer CenterHoustonUSA
  4. 4.Department of Cancer BiologyM. D. Anderson Cancer CenterHoustonUSA
  5. 5.Center for RNA Interference and Non-Coding RNA The University of Texas MD Anderson Cancer CenterHoustonUSA
  6. 6.Department of Medicine, Section of Internal and Cardiovascular MedicineUniversity of PerugiaPerugiaItaly
  7. 7.Bioactive Lipids Research Program, Department of PathologyWayne State UniversityDetroitUSA
  8. 8.Department of PathologyWayne State UniversityDetroitUSA
  9. 9.Cancer Biology DivisionWayne State University School of MedicineDetroitUSA

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