Microparticle Dissemination of Biological Activities: Implications for Cancer Biology

Chapter

Abstract

The substantial contribution of the tumor microenvironment to the development of malignancy in cancer is well documented, with tumor progression recognized as the product of an evolving cross talk between genetically abnormal cells within the tumor and the surrounding and interwoven stromal framework. The latter includes the extracellular matrix and cellular components such as fibroblasts, immune and inflammatory cells, blood vessel cells, and soluble factors such as cytokines and growth factors. In response to apoptotic signals or cellular activation that may accompany inflammatory or hypercoagulable states, actively growing tumor cells, activated platelets, and tumor-infiltrating lymphocytes and macrophages resident in the tumor microenvironment shed microparticles or microvesicles. Microparticles (MPs) are circular membrane fragments, ranging in size from 0.1 to 1.0 μm, containing both membrane components and cytoplasmic contents “hijacked” from their parent cells. Originally regarded as irrelevant cell debris, MPs have now been shown to be vectors of various signaling proteins, mRNA, and bioactive lipids with important roles in cancer biology. This chapter will provide an overview of how MPs derived from cancer cells or platelets mediate tumor growth, angiogenesis, and metastasis. Furthermore, the potential role of tissue factor-positive MPs in facilitating cancer-associated thrombosis will also be examined. In addition, the potentially pathogenic effects of MPs in blood products (e.g., platelet concentrates) for cancer patients and of MP release associated with blood product processing will also be highlighted.

Keywords

Migration Dust Lymphoma Leukemia Glutathione 

References

  1. 1.
    Furie, B., and Furie, B. C. 2006 Blood Cells Mol Dis 36, 177PubMedGoogle Scholar
  2. 2.
    Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. 2006 Leukemia 20, 1487PubMedGoogle Scholar
  3. 3.
    Amin, C., Mackman, N., and Key, N. S. 2008 Pathophysiol Haemost Thromb 36, 177PubMedGoogle Scholar
  4. 4.
    Tesselaar, M. E., Romijn, F. P., Van Der Linden, I. K., Prins, F. A., Bertina, R. M., and Osanto, S. 2007 J Thromb Haemost 5, 520PubMedGoogle Scholar
  5. 5.
    Castellana, D., Kunzelmann, C., and Freyssinet, J. M. 2009 Hamostaseologie 29, 51PubMedGoogle Scholar
  6. 6.
    Wolf, P. 1967 Br J Haematol 13, 269PubMedGoogle Scholar
  7. 7.
    Crawford, N. 1971 Br J Haematol 21, 53PubMedGoogle Scholar
  8. 8.
    Hugel, B., Martinez, M. C., Kunzelmann, C., and Freyssinet, J. M. 2005 Physiology (Bethesda) 20, 22Google Scholar
  9. 9.
    Thery, C., Zitvogel, L., and Amigorena, S. 2002 Nat Rev Immunol 2, 569PubMedGoogle Scholar
  10. 10.
    VanWijk, M. J., VanBavel, E., Sturk, A., and Nieuwland, R. 2003 Cardiovasc Res 59, 277PubMedGoogle Scholar
  11. 11.
    Morel, O., Toti, F., Hugel, B., Bakouboula, B., Camoin-Jau, L., Dignat-George, F., and Freyssinet, J.-M. 2006 Arterioscler Thromb Vasc Biol 26, 2594PubMedGoogle Scholar
  12. 12.
    Burnier, L., Fontana, P., Kwak, B., and Angelillo-Scherrer, A. 2009 Thromb Haemost. 101, 439PubMedGoogle Scholar
  13. 13.
    Freyssinet, J. M. 2003 J Thromb Haemost 1, 1655PubMedGoogle Scholar
  14. 14.
    Kim, H. K., Song, K. S., Park, Y. S., Kang, Y. H., Lee, Y. J., Lee, K. R., Kim, H. K., Ryu, K. W., Bae, J. M., and Kim, S. 2003 Eur J Cancer 39, 184PubMedGoogle Scholar
  15. 15.
    Savasan, S., Buyukavci, M., Buck, S., and Ravindranath, Y. 2004 J Clin Pathol 57, 651PubMedGoogle Scholar
  16. 16.
    Kalinkovich, A., Tavor, S., Avigdor, A., Kahn, J., Brill, A., Petit, I., Goichberg, P., Tesio, M., Netzer, N., Naparstek, E., Hardan, I., Nagler, A., Resnick, I., Tsimanis, A., and Lapidot, T. 2006 Cancer Res 66, 11013PubMedGoogle Scholar
  17. 17.
    Del Conde, I., Bharwani, L. D., Dietzen, D. J., Pendurthi, U., Thiagarajan, P., and Lopez, J. A. 2007 Journal of Thrombosis and Haemostasis 5, 70PubMedGoogle Scholar
  18. 18.
    Bergmann, C., Strauss, L., Wieckowski, E., Czystowska, M., Albers, A., Wang, Y., Zeidler, R., Lang, S., and Whiteside, T. L. 2009 Head Neck 31, 371PubMedGoogle Scholar
  19. 19.
    Kim, J. W., Wieckowski, E., Taylor, D. D., Reichert, T. E., Watkins, S., and Whiteside, T. L. 2005 Clin Cancer Res 11, 1010PubMedGoogle Scholar
  20. 20.
    Hron, G., Kollars, M., Weber, H., Sagaster, V., Quehenberger, P., Eichinger, S., Kyrle, P. A., and Weltermann, A. 2007 Thromb Haemost 97, 119PubMedGoogle Scholar
  21. 21.
    Amabile, N., Guerin, A. P., Leroyer, A., Mallat, Z., Nguyen, C., Boddaert, J., London, G. M., Tedgui, A., and Boulanger, C. M. 2005 J. Am. Soc. Nephrol. 16, 3381PubMedGoogle Scholar
  22. 22.
    Haubold, K., Rink, M., Spath, B., Friedrich, M., Chun, F. K., Marx, G., Amirkhosravi, A., Francis, J. L., Bokemeyer, C., Eifrig, B., and Langer, F. 2009 Thromb Haemost 101, 1147PubMedGoogle Scholar
  23. 23.
    Kim, H. K., Song, K. S., Park, Y. S., Kang, Y. H., Lee, Y. J., Lee, K. R., Ryu, K. W., Bae, J. M., and Kim, S. 2003 Eur J Cancer 39, 184PubMedGoogle Scholar
  24. 24.
    Zwaal, R. F. A., and Schroit, A. J. 1997 Blood 89, 1121PubMedGoogle Scholar
  25. 25.
    Bevers, E. M., Comfurius, P., Dekkers, D. W. C., and Zwaal, R. F. A. 1999 Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1439, 317Google Scholar
  26. 26.
    Bevers, E. M., Comfurius, P., and Zwaal, R. F. A. 2003 Membrane phospholipid asymmetry: biochemical and pathophysiological perspectives. in Advances in Molecular and Cell Biology E. E. Bittar (Ed.), Elsevier, 387Google Scholar
  27. 27.
    Jimenez, J., Jy W, Mauro LM, Soderland, C., Horstmann, L., and Ahn, Y. 2003 109, 175Google Scholar
  28. 28.
    Tramontano, A. F., O’Leary, J., Black, A. D., Muniyappa, R., Cutaia, M. V., and El-Sherif, N. 2004 Biochemical and Biophysical Research Communications 320, 34PubMedGoogle Scholar
  29. 29.
    Perez-Pujol, S., Marker, P. P., and Key, N. S. 2007 Cytometry Part A 71A, 38Google Scholar
  30. 30.
    Wiedmer, T., Shattil, S. J., Cunningham, M., and Sims, P. J. 1990 Biochemistry 29, 623PubMedGoogle Scholar
  31. 31.
    Hamilton, K. K., Hattori, R., Esmon, C. T., and Sims, P. J. 1990 J. Biol. Chem. 265, 3809PubMedGoogle Scholar
  32. 32.
    Falanga, A., Panova-Noeva, M., and Russo, L. 2009 Best Practice & Research Clinical Haematology 22, 49Google Scholar
  33. 33.
    Kwaan, H. C., and Keer, H. N. 1990 Semin Thromb Hemost 16, 230PubMedGoogle Scholar
  34. 34.
    Rickles, F. R., and Falanga, A. 2001 Thromb Res 102, V215PubMedGoogle Scholar
  35. 35.
    Brodsky, S. V., Malinowski, K., Golightly, M., Jesty, J., and Goligorsky, M. S. 2002 Circulation 106, 2372PubMedGoogle Scholar
  36. 36.
    Varon, D., and Brill, A. 2001 Haemostasis 31 Suppl 1, 64Google Scholar
  37. 37.
    Prandoni, P., Falanga, A., and Piccioli, A. 2005 The Lancet Oncology 6, 401PubMedGoogle Scholar
  38. 38.
    Vaupel, P., and Mayer, A. 2007 Cancer and Metastasis Reviews 26, 225PubMedGoogle Scholar
  39. 39.
    Harris, A. L. 2002 Nat Rev Cancer 2, 38PubMedGoogle Scholar
  40. 40.
    Wysoczynski, M., and Ratajczak, M. Z. 2009 Int J Cancer 125, 1595PubMedGoogle Scholar
  41. 41.
    Grenader, T., Shavit, L., Ospovat, I., Gutfeld, O., and Peretz, T. 2006 Mt Sinai J Med 73, 810PubMedGoogle Scholar
  42. 42.
    Lechner, D., and Weltermann, A. 2008 Semin Thromb Hemost 34, 199PubMedGoogle Scholar
  43. 43.
    Gelderman, M. P., Carter, L. B., and Simak, J. 2004 ASH Annual Meeting Abstracts 104, 3635Google Scholar
  44. 44.
    Simak, J., and Gelderman, M. P. 2006 Transfus Med Rev 20, 1PubMedGoogle Scholar
  45. 45.
    Jy, W., Horstman, L. L., Jimenez, J. J., Ahn, Y. S., Biro, E., Nieuwland, R., Sturk, A., Dignat-George, F., Sabatier, F., Camoin-Jau, L., Sampol, J., Hugel, B., Zobairi, F., Freyssinet, J. M., Nomura, S., Shet, A. S., Key, N. S., and Hebbel, R. P. 2004 J Thromb Haemost 2, 1842PubMedGoogle Scholar
  46. 46.
    Horstman, L. L., Jy, W., Jimenez, J. J., Bidot, C., and Ahn, Y. S. 2004 Keio J Med 53, 210PubMedGoogle Scholar
  47. 47.
    Pula, G., Perera, S., Prokopi, M., Sidibe, A., Boulanger, C., and Mayr, M. 2008 PROTEOMICS - CLINICAL APPLICATIONS 2, 882PubMedGoogle Scholar
  48. 48.
    Liotta, L. A., and Kohn, E. C. 2001 Nature 411, 375PubMedGoogle Scholar
  49. 49.
    Chambers, A. F., Groom, A. C., and MacDonald, I. C. 2002 Nat Rev Cancer 2, 563PubMedGoogle Scholar
  50. 50.
    Mueller, M. M., and Fusenig, N. E. 2004 Nat Rev Cancer 4, 839PubMedGoogle Scholar
  51. 51.
    Taylor, D., and Black, P. 1986 Shedding of plasma membrane fragments. Neoplastic and developmental importance. in Developmental Biology, M.S.Steinberg (Ed.), Plenum Press, New York, 33Google Scholar
  52. 52.
    Barz, D., Goppelt, M., Szamel, M., Schirrmacher, V., and Resch, K. 1985 Biochim Biophys Acta 814, 77PubMedGoogle Scholar
  53. 53.
    Baj-Krzyworzeka, M., Szatanek, R., Weglarczyk, K., Baran, J., Urbanowicz, B., Branski, P., Ratajczak, M. Z., and Zembala, M. 2006 Cancer Immunol Immunother 55, 808PubMedGoogle Scholar
  54. 54.
    Deryugina, E. I., and Quigley, J. P. 2006 Cancer Metastasis Rev 25, 9PubMedGoogle Scholar
  55. 55.
    Dolo, V., Ginestra, A., Cassara, D., Violini, S., Lucania, G., Torrisi, M. R., Nagase, H., Canevari, S., Pavan, A., and Vittorelli, M. L. 1998 Cancer Res 58, 4468PubMedGoogle Scholar
  56. 56.
    Ginestra, A., Monea, S., Seghezzi, G., Dolo, V., Nagase, H., Mignatti, P., and Vittorelli, M. L. 1997 J Biol Chem 272, 17216PubMedGoogle Scholar
  57. 57.
    Graves, L. E., Ariztia, E. V., Navari, J. R., Matzel, H. J., Stack, M. S., and Fishman, D. A. 2004 Cancer Res 64, 7045PubMedGoogle Scholar
  58. 58.
    Taraboletti, G., D’Ascenzo, S., Borsotti, P., Giavazzi, R., Pavan, A., and Dolo, V. 2002 Am J Pathol 160, 673PubMedGoogle Scholar
  59. 59.
    Taraboletti, G., D’Ascenzo, S., Giusti, I., Marchetti, D., Borsotti, P., Millimaggi, D., Giavazzi, R., Pavan, A., and Dolo, V. 2006 Neoplasia 8, 96PubMedGoogle Scholar
  60. 60.
    Skog, J., Wurdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Sena-Esteves, M., Curry, W. T., Jr., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. 2008 Nat Cell Biol 10, 1470PubMedGoogle Scholar
  61. 61.
    Tarin, D. 1972 Epithelial-Mesenchymal Interactions in Carcinogenesis Academic Press, LondonGoogle Scholar
  62. 62.
    Hood, J. D., and Cheresh, D. A. 2002 Nat Rev Cancer 2, 91PubMedGoogle Scholar
  63. 63.
    Ahmed, N., Riley, C., Rice, G., and Quinn, M. 2005 Clin Exp Metastasis 22, 391PubMedGoogle Scholar
  64. 64.
    Augustin, H. G. 2000 Baillieres Best Pract.Res. Clin. Obstet. Gynaecol. 14, 867Google Scholar
  65. 65.
    Reynolds, L. P., Grazul-Bilska, A. T., and Redmer, D. A. 2002 Intl. J. Exptl. Pathol 83, 151Google Scholar
  66. 66.
    Arnold, F., and West, D. C. 1991 Pharmacology & Therapeutics 52, 407Google Scholar
  67. 67.
    Carmeliet, P. 2003 Nat. Med. 9, 653PubMedGoogle Scholar
  68. 68.
    Folkman, J. 2002 Semin Oncol 29, 15PubMedGoogle Scholar
  69. 69.
    Folkman, J. 1995 Nature Med. 1, 27PubMedGoogle Scholar
  70. 70.
    Folkman, J. 1995 N. Engl. J. Med. 333, 1757PubMedGoogle Scholar
  71. 71.
    Folkman, J. 1971 N Engl J Med 285, 1182PubMedGoogle Scholar
  72. 72.
    Papetti, M., and Herman, I.M. 2002 Am J Physiol Cell Physiol 282, 947PubMedGoogle Scholar
  73. 73.
    Carmeliet, P., and Jain, R. K. 2000 Nature 407, 249PubMedGoogle Scholar
  74. 74.
    Brat, D. J., Bellail, A. C., and Van Meir, E. G. 2005 Neuro-oncology 7, 122PubMedGoogle Scholar
  75. 75.
    Eberle, K., Oberpichler, A., Trantakis, C., Krupp, W., Knupfer, M., Tschesche, H., and Seifert, V. 2000 Anticancer Res 20, 1679PubMedGoogle Scholar
  76. 76.
    Rolhion, C., Penault-Llorca, F., Kemeny, J.-L., Lemaire, J.-J., Jullien, C., Labit-Bouvier, C., Finat-Duclos, F., and Verrelle, P. 2001 Journal of Neurosurgery 94, 97PubMedGoogle Scholar
  77. 77.
    Li, A., Dubey, S., Varney, M. L., Dave, B. J., and Singh, R. K. 2003 J Immunol 170, 3369PubMedGoogle Scholar
  78. 78.
    Goswami, S., and Gupta, A. 1998 Journal of Neurochemistry 71, 1837PubMedGoogle Scholar
  79. 79.
    Bergers, G., Brekken, R., McMahon, G., Vu, T., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Z. &, W., and Hanahan, D. 2000 Nature Cell Biology, 2, 737Google Scholar
  80. 80.
    Folkman, J. 2008 Angiostatin and Endostatin: Angiogenesis Inhibitors in Blood and Stroma. in Angiogenesis: An Integrative Approach from Science to Medicine, W.D. Figg and J. Folkman (Eds.), Springer US., 129Google Scholar
  81. 81.
    Sounni, N. E., Devy, L., Hajitou, A., Frankenne, F., Munaut, C., Gilles, C., Deroanne, C., Thompson, E. W., Foidart, J. M., and Noel, A. 2002 FASEB J. 16, 555PubMedGoogle Scholar
  82. 82.
    Deryugina, E. I., Soroceanu, L., and Strongin, A. Y. 2002 Cancer Res 62, 580PubMedGoogle Scholar
  83. 83.
    Sidhu, S. S., Mengistab, A. T., Tauscher, A. N., LaVail, J., and Basbaum, C. 2004 Oncogene 23, 956PubMedGoogle Scholar
  84. 84.
    Millimaggi, D., Mari, M., D’Ascenzo, S., Carosa, E., Jannini, E. A., Zucker, S., Carta, G., Pavan, A., and Dolo, V. 2007 Neoplasia 9, 349PubMedGoogle Scholar
  85. 85.
    Castellana, D., Zobairi, F., Martinez, M. C., Panaro, M. A., Mitolo, V., Freyssinet, J.-M., and Kunzelmann, C. 2009 Cancer Res 69, 785PubMedGoogle Scholar
  86. 86.
    Biswas, C., Zhang, Y., DeCastro, R., Guo, H., Nakamura, T., Kataoka, H., and Nabeshima, K. 1995 Cancer Res 55, 434–439PubMedGoogle Scholar
  87. 87.
    Toole, B. 2003 Curr Top Dev Biol 54, 371–389PubMedGoogle Scholar
  88. 88.
    Tang, Y., Nakada, M. T., Kesavan, P., McCabe, F., Millar, H., Rafferty, P., Bugelski, P., and Yan, L. 2005 Cancer Res 65, 3193PubMedGoogle Scholar
  89. 89.
    Tang, Y., Kesavan, P., Nakada, M. T., and Yan, L. 2004 Mol Cancer Res 2, 73PubMedGoogle Scholar
  90. 90.
    Sun, J., and ME, H. 2001 Cancer Res 61, 2276–2281Google Scholar
  91. 91.
    Guo, H., Zucker, S., Gordon, M. K., Toole, B. P., and Biswas, C. 1997 J Biol Chem 272, 24PubMedGoogle Scholar
  92. 92.
    Caudroy, S., Polette, M. N.-R., B., Cao, J., Toole, B. P., Zucker, S., and Birembaut, P. 2002 Clin Exp Metastasis 19, 697Google Scholar
  93. 93.
    Kanekura, T., and Chen, X. 2010 J Dermatol Sci 57, 149PubMedGoogle Scholar
  94. 94.
    Stetler-Stevenson, W. G., Aznavoorian, S., and Liotta, L. A. 1993 Annu Rev Cell Biol 9, 541PubMedGoogle Scholar
  95. 95.
    Stetler-Stevenson, W. G. 2001 Surg Oncol Clin N Am 10, 383PubMedGoogle Scholar
  96. 96.
    Yu, J., May, L., Milsom, C., Anderson, G. M., Weitz, J. I., Luyendyk, J. P., Broze, G., Mackman, N., and Rak, J. 2008 Arterioscler Thromb Vasc Biol 28, 1975PubMedGoogle Scholar
  97. 97.
    Forster, Y., Meye, A., Albrecht, S., and Schwenzer, B. 2006 Clin Chim Acta 364, 12PubMedGoogle Scholar
  98. 98.
    Rak, J., Milsom, C., Magnus, N., and Yu, J. 2009 Best Pract Res Clin Haematol 22, 71PubMedGoogle Scholar
  99. 99.
    Schaffner, F., and Ruf, W. 2009 Arterioscler Thromb Vasc Biol, Aug 6. [Epub ahead of print]Google Scholar
  100. 100.
    Al-Nedawi, K., Meehan, B., Kerbel, R. S., Allison, A. C., and Rak, J. 2009 Proc Natl Acad Sci USA 106, 3794PubMedGoogle Scholar
  101. 101.
    Amin, D. N., Hida, K., Bielenberg, D. R., and Klagsbrun, M. 2006 Cancer Res 66, 2173PubMedGoogle Scholar
  102. 102.
    Baker, C. H., Kedar, D., McCarty, M. F., Tsan, R., Weber, K. L., Bucana, C. D., and Fidler, I. J. 2002 Am J Pathol 161, 929PubMedGoogle Scholar
  103. 103.
    Yokoi, K., Thaker, P. H., Yazici, S., Rebhun, R. R., Nam, D. H., He, J., Kim, S. J., Abbruzzese, J. L., Hamilton, S. R., and Fidler, I. J. 2005 Cancer Res 65, 3716PubMedGoogle Scholar
  104. 104.
    Cheng, H., Langley, R. R., Wu, Q., Wu, W., Feng, J., Tsan, R., Fan, D., and Fidler, I. J. 2005 Neoplasia 7, 1065PubMedGoogle Scholar
  105. 105.
    Vosseler, S., Mirancea, N., Bohlen, P., Mueller, M. M., and Fusenig, N. E. 2005 Cancer Res 65, 1294PubMedGoogle Scholar
  106. 106.
    Skobe, M., Rockwell, P., Goldstein, N., Vosseler, S., and Fusenig, N. E. 1997 Nature Med. 3, 1222PubMedGoogle Scholar
  107. 107.
    Hellstrom, K. E., and, and Hellstrom, I. 1991 Principles of tumor immunity: tumor antigens. in Biologic Therapy of Cancer V. T. DeVita, S. Hellman, and Rosenberg, S. A. (Eds.), Lippincott, New York, 35Google Scholar
  108. 108.
    Kim, R., Emi, M., Tanabe, K., Uchida, Y., and Toge, T. 2004 Cancer 100, 2281PubMedGoogle Scholar
  109. 109.
    Maher, S., Toomey, D., Condron, C., and Bouchier-Hayes, D. 2002 Immunol Cell Biol 80, 131PubMedGoogle Scholar
  110. 110.
    Rabinowich, H., Reichert, T. E., Kashii, Y., Gastman, B. R., Bell, M. C., and Whiteside, T. L. 1998 J Clin Invest 101, 2579PubMedGoogle Scholar
  111. 111.
    Mottolese, M., Buglioni, S., Bracalenti, C., Cardarell, M. A., i, Ciabocco, L., Giannarelli, D., Botti, C., Natali, P. G., Concetti, A., and Venanzi, F. M. 2000 International Journal of Cancer 89, 127Google Scholar
  112. 112.
    Chopin, D., Barei-Moniri, R., Maille, P., Le Frere-Belda, M.-A., Muscatelli-Groux, B., Merendino, N., Lecerf, L., Stoppacciaro, A., and Velotti, F. 2003 Am J Pathol 162, 1139PubMedGoogle Scholar
  113. 113.
    Mann, B., Gratchev, A., Bohm, C., Hanski, M. L., Foss, H. D., Demel, G., Trojanek, B., Schmidt-Wolf, I., Stein, H., Riecken, E. O., Buhr, H. J., and Hanski, C. 1999 Br J Cancer 79, 1262PubMedGoogle Scholar
  114. 114.
    Lai, P., Rabinowich, H., Crowley-Nowick, P. A., Bell, M. C., Mantovani, G., and Whiteside, T. L. 1996 Clin Cancer Res 2, 161PubMedGoogle Scholar
  115. 115.
    Huber, V., Fais, S., Iero, M., Lugini, L., Canese, P., Squarcina, P., Zaccheddu, A., Colone, M., Arancia, G., Gentile, M., Seregni, E., Valenti, R., Ballabio, G., Belli, F., Leo, E., Parmiani, G., and Rivoltini, L. 2005 Gastroenterology 128, 1796PubMedGoogle Scholar
  116. 116.
    Andreola, G., Rivoltini, L., Castelli, C., Huber, V., Perego, P., Deho, P., Squarcina, P., Accornero, P., Lozupone, F., Lugini, L., Stringaro, A., Molinari, A., Arancia, G., Gentile, M., Parmiani, G., and Fais, S. 2002 J Exp Med 195, 1303PubMedGoogle Scholar
  117. 117.
    Taylor, D. D., Gercel-Taylor, C., Lyons, K. S., Stanson, J., and Whiteside, T. L. 2003 Clin Cancer Res 9, 5113PubMedGoogle Scholar
  118. 118.
    Dolo, V., Pizzurro, P., Ginestra, A., and Vittorelli, M. L. 1995 J Submicrosc Cytol Pathol 27, 535PubMedGoogle Scholar
  119. 119.
    Becker, C., Fantini, M. C., and Neurath, M. F. 2006 Cytokine & Growth Factor Reviews 17, 97Google Scholar
  120. 120.
    Reiss, M., and Barcellos-Hoff, M. H. 1997 Breast Cancer Research and Treatment 45, 81PubMedGoogle Scholar
  121. 121.
    Friedman, E., Gold, L. I., Klimstra, D., Zeng, Z. S., Winawer, S., and Cohen, A. 1995 Cancer Epidemiol Biomarkers Prev 4, 549PubMedGoogle Scholar
  122. 122.
    Matsuzaki, K., Date, M., Furukawa, F., Tahashi, Y., Matsushita, M., Sakitani, K., Yamashiki, N., Seki, T., Saito, H., Nishizawa, M., Fujisawa, J., and Inoue, K. 2000 Cancer Res 60, 1394PubMedGoogle Scholar
  123. 123.
    Reed, J. A., McNutt, N. S., Prieto, V. G., and Albino, A. P. 1994 Am J Pathol 145, 97PubMedGoogle Scholar
  124. 124.
    Gorelik, L., and Flavell, R. A. 2001 Nat Med 7, 1118PubMedGoogle Scholar
  125. 125.
    Hoefer, M., and Anderer, F. A. 1995 Cancer Immunology, Immunotherapy 41, 302Google Scholar
  126. 126.
    Whiteside, T. L. 2005 Br J Cancer 92, 209PubMedGoogle Scholar
  127. 127.
    Garcia-Lora, A., Algarra, I., and Garrido, F. 2003 Journal of Cellular Physiology 195, 346PubMedGoogle Scholar
  128. 128.
    Nicolson, G. L. 1993 Cancer and Metastasis Reviews 12, 325PubMedGoogle Scholar
  129. 129.
    Baggiolini, M. 1998 Nature 392, 565PubMedGoogle Scholar
  130. 130.
    Balkwill, F. 2004 Nat Rev Cancer 4, 540PubMedGoogle Scholar
  131. 131.
    Muller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M. E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S. N., Barrera, J. L., Mohar, A., Verastegui, E., and Zlotnik, A. 2001 Nature 410, 50PubMedGoogle Scholar
  132. 132.
    Rubie, C., Oliveira-Frick, V., Rau, B., Schilling, M., and Wagner, M. 2006 J Clin Oncol 24, 5173PubMedGoogle Scholar
  133. 133.
    Shulby, S. A., Dolloff, N. G., Stearns, M. E., Meucci, O., and Fatatis, A. 2004 Cancer Res 64, 4693PubMedGoogle Scholar
  134. 134.
    Ghadjar, P., Rubie, C., Aebersold, D. M., and Keilholz, U. 2009 Int J Cancer 125, 741PubMedGoogle Scholar
  135. 135.
    Scotton, C. J., Wilson, J. L., Milliken, D., Stamp, G., and Balkwill, F. R. 2001 Cancer Res 61, 4961PubMedGoogle Scholar
  136. 136.
    Burger, J., A., and Bürkle, A. 2007 British Journal of Haematology 137, 288Google Scholar
  137. 137.
    Baj-Krzyworzeka, M., Szatanek, R., Weglarczyk, K., Baran, J., and Zembala, M. 2007 Immunol Lett 113, 76PubMedGoogle Scholar
  138. 138.
    Levesque, M. C., and Haynes, B. F. 1996 J Immunol 156, 1557PubMedGoogle Scholar
  139. 139.
    Honn, K. V., Tang, D. G., and Crissman, J. D. 1992 Cancer Metastasis Rev 11, 325PubMedGoogle Scholar
  140. 140.
    Honn, K. V., Tang, D. G., and Chen, Y. Q. 1992 Semin Thromb Hemost 18, 392PubMedGoogle Scholar
  141. 141.
    Taucher S, Salat A, G. M., Kwasny W, Mlineritsch B, Menzel R, Schmid M, Smola MG, Stierer M, Tausch C, Galid A, Steger G, e. a., and. 2003 Thromb Haemost 89, 1098 –1106Google Scholar
  142. 142.
    McCarty, O. J. T., Mousa, S. A., Bray, P. F., and Konstantopoulos, K. 2000 Blood 96, 1789PubMedGoogle Scholar
  143. 143.
    Nash, G., Turner, L., Scully, M., and Kakkar, A. 2002 Lancet Oncol. 3, 425PubMedGoogle Scholar
  144. 144.
    Jurasz, P., Alonso-Escolano, D., and Radomski, M. W. 2004 Br J Pharmacol 143, 819PubMedGoogle Scholar
  145. 145.
    Radomski, M. W., Jenkins, D. C., Holmes, L., and Moncada, S. 1991 Cancer Res 51, 6073PubMedGoogle Scholar
  146. 146.
    Philippe, C., Philippe, B., Fouqeray, B., Perez, J., Lebret, M., and Baud, L. 1993 Am. J. Pathol. 143, 1713–1723PubMedGoogle Scholar
  147. 147.
    Konstantopoulos, K., and Thomas, S. N. 2009 Annual Review of Biomedical Engineering 11, 177PubMedGoogle Scholar
  148. 148.
    Janowska-Wieczorek, A., Majka, M., Kijowski, J., Baj-Krzyworzeka, M., Reca, R., Turner, A. R., Ratajczak, J., Kowalska, M. A., and Ratajczak, M. Z. 2001 Blood 98, 3143–3149.PubMedGoogle Scholar
  149. 149.
    Baj-Krzyworzeka M, Majka M, Pratico D, Ratajczak J, Vilaire G, Kijowski J, Reca R, Janowska-Wieczorek A, and MZ., R. 2002 Exp Hematol 30, 450 –459Google Scholar
  150. 150.
    English, D., Garcia, J. G. N., and Brindley, D. N. 2001 Cardiovasc Res 49, 588PubMedGoogle Scholar
  151. 151.
    Janowska-Wieczorek, A., Marcin, W., Jacek, K., Leah, M.-C., Bogdan, M., Janina, R., and Mariusz, Z. R. 2005 International Journal of Cancer 113, 752Google Scholar
  152. 152.
    Janowska-Wieczorek, A., Marquez-Curtis, L., Wysoczynski, M., and Ratajczak, M. 2006 Transfusion. 46, 1199PubMedGoogle Scholar
  153. 153.
    Houldsworth, J., Reuter, V., Bosl, G. J., and Chaganti, R. S. 1997 Cell Growth Differ 8, 293PubMedGoogle Scholar
  154. 154.
    Takano, Y., Kato, Y., Masuda, M., Ohshima, Y., and Okayasu, I. 1999 The Journal of Pathology 189, 194PubMedGoogle Scholar
  155. 155.
    Seiki, M., Koshikawa, N., and Yana, I. 2003 Cancer Metastasis Rev 22, 129PubMedGoogle Scholar
  156. 156.
    Zucker, S., Pei, D., Cao, J., and Lopez-Otin, C. 2003 Membrane type-matrix metalloproteinases (MT-MMP). in Current topics in developmental biology: Cell surface proteases (Zucker S, and WT, C. eds.), Academic Press, New York. pp 1Google Scholar
  157. 157.
    English, D., Welch, Z., Kovala, A. T., Harvey, K., Volpert, O. V., Brindley, D. N., and Garcia, J. G. 2000 Faseb J 14, 2255PubMedGoogle Scholar
  158. 158.
    Barry OP, Pratico D, Lawson JA, and GA., F. 1997 J Clin Invest 99, 2118 –2127Google Scholar
  159. 159.
    Barry, O. P., Pratico, D., Lawson, J. A., and FitzGerald, G. A. 1997 J Clin Invest 99, 2118PubMedGoogle Scholar
  160. 160.
    Barry, O. P., Kazanietz, M. G., Pratico, D., and FitzGerald, G. A. 1999 J Biol Chem 274, 7545PubMedGoogle Scholar
  161. 161.
    Kim, C. W., Lee, H. M., Lee, T. H., Kang, C., Kleinman, H. K., and Gho, Y. S. 2002 Cancer Res 62, 6312PubMedGoogle Scholar
  162. 162.
    Baj-Krzyworzeka, M., Majka, M., Pratico, D., Ratajczak, J., Vilaire, G., Kijowski, J., Reca, R., Janowska-Wieczorek, A., and Ratajczak, M. Z. 2002 Experimental Hematology 30, 450PubMedGoogle Scholar
  163. 163.
    Rozmyslowicz, T., Majka, M., Kijowski, J., Murphy, S. L., Conover, D. O., Poncz, M., Ratajczak, J., Gaulton, G. N., and Ratajczak, M. Z. 2003 AIDS 17, 33PubMedGoogle Scholar
  164. 164.
    Prandoni, P., Falanga, A., and Piccioli, A. 2007 Thrombosis Research 120, S137–S140PubMedGoogle Scholar
  165. 165.
    Rauch, U., and Antoniak, S. 2007 Thromb Haemost 97, 9PubMedGoogle Scholar
  166. 166.
    Falanga, A., Barbui, T., and Rickles, F. R. 2008 Semin Thromb Hemost 34, 204PubMedGoogle Scholar
  167. 167.
    Zangari, M., Anaissie, E., Barlogie, B., Badros, A., Desikan, R., Gopal, A. V., Morris, C., Toor, A., Siegel, E., Fink, L., and Tricot, G. 2001 Blood 98, 1614PubMedGoogle Scholar
  168. 168.
    Zangari, M., Elice, F., Fink, L., and Tricot, G. 2007 Expert Rev Anticancer Ther 7, 307PubMedGoogle Scholar
  169. 169.
    Pritchard, K. I., Paterson, A. H., Paul, N. A., Zee, B., Fine, S., and Pater, J. 1996 J Clin Oncol 14, 2731PubMedGoogle Scholar
  170. 170.
    Haddad, T. C., and Greeno, E. W. 2006 Thromb Res 118, 555PubMedGoogle Scholar
  171. 171.
    Petropoulou, A. D., Gerotziafas, G. T., Samama, M. M., Hatmi, M., Rendu, F., and Elalamy, I. 2008 Thrombosis Research 121, 493PubMedGoogle Scholar
  172. 172.
    Varki, A. 2007 Blood 110, 1723PubMedGoogle Scholar
  173. 173.
    Falanga, A. 2005 Semin Thromb Hemost 31, 104PubMedGoogle Scholar
  174. 174.
    Rickles, F. R., and Brenner, B. 2008 Semin Thromb Hemost 34, 143PubMedGoogle Scholar
  175. 175.
    Lopez-Pedrera, C., Barbarroja, N., Dorado, G., Siendones, E., and Velasco, F. 2006 Leukemia 20, 1331PubMedGoogle Scholar
  176. 176.
    Drake, T. A., Morrissey, J. H., and Edgington, T. S. 1989 Am. J. Pathol. 134, 1087PubMedGoogle Scholar
  177. 177.
    Mackman, N. 2004 Arterioscler. Thromb. Vasc. Biol. 24, 1015PubMedGoogle Scholar
  178. 178.
    Giesen, P. L., Rauch, U., Bohrmann, B., Kling, D., Roque, M., Fallon, J. T., Badimon, J. J., Himber, J., Riederer, M. A., and Nemerson, Y. 1999 Proc Natl Acad Sci USA 96, 2311PubMedGoogle Scholar
  179. 179.
    Furie, B., Zwicker, J., LaRocca, T., Kos, C., Bauer, B., and Furie, B. C. 2005 Haematologica reports 1, 5Google Scholar
  180. 180.
    Zwicker, J. I. 2008 Semin Thromb Hemost 34, 195PubMedGoogle Scholar
  181. 181.
    Tilley, R. E., Holscher, T., Belani, R., Nieva, J., and Mackman, N. 2008 Thromb Res 122, 604PubMedGoogle Scholar
  182. 182.
    Davila, M., Amirkhosravi, A., Coll, E., Desai, H., Robles, L., Colon, J., Baker, C. H., and Francis, J. L. 2008 J Thromb Haemost 6, 1517PubMedGoogle Scholar
  183. 183.
    Lechner, D., and Weltermann, A. 2008 Thrombosis Research 122, S47–S54PubMedGoogle Scholar
  184. 184.
    Khorana, A. A., Francis, C. W., Menzies, K. E., Wang, J. G., Hyrien, O., Hathcock, J., Mackman, N., and Taubman, M. B. 2008 J Thromb Haemost 6, 1983PubMedGoogle Scholar
  185. 185.
    Langer, F., Spath, B., Haubold, K., Holstein, K., Marx, G., Wierecky, J., Brummendorf, T. H., Dierlamm, J., Bokemeyer, C., and Eifrig, B. 2008 Ann Hematol 87, 451PubMedGoogle Scholar
  186. 186.
    Falati, S., Liu, Q., Gross, P., Merrill-Skoloff, G., Chou, J., Vandendries, E., Celi, A., Croce, K., Furie, B. C., and Furie, B. 2003 J Exp Med 197, 1585PubMedGoogle Scholar
  187. 187.
    Rauch, U., Bonderman, D., Bohrmann, B., Badimon, J. J., Himber, J., Riederer, M. A., and Nemerson, Y. 2000 Blood 96, 170PubMedGoogle Scholar
  188. 188.
    del Conde, I., Shrimpton, C. N., Thiagarajan, P., and Lopez, J. A. 2005 Blood 106, 1604PubMedGoogle Scholar
  189. 189.
    Muller, I., Klocke, A., Alex, M., Kotzsch, M., Luther, T., Morgenstern, E., Zieseniss, S., Zahler, S., Preissner, K., and Engelmann, B. 2003 Faseb J 17, 476PubMedGoogle Scholar
  190. 190.
    Carr, J. M., Dvorak, A. M., and Dvorak, H. F. 1985 Cancer Res 45, 5944PubMedGoogle Scholar
  191. 191.
    Yu, J. L., and Rak, J. W. 2004 Journal of Thrombosis and Haemostasis 2, 2065PubMedGoogle Scholar
  192. 192.
    Bastida, E., Ordinas, A., Escolar, G., and Jamieson, G. A. 1984 Blood 64, 177PubMedGoogle Scholar
  193. 193.
    Osterud, B. 2003 Dis Mon 49, 7PubMedGoogle Scholar
  194. 194.
    Furie, B., and Furie, B. C. 2004 Trends in Molecular Medicine 10, 171PubMedGoogle Scholar
  195. 195.
    Bach, R. R. 2006 Arterioscler. Thromb. Vasc. Biol. 26, 456PubMedGoogle Scholar
  196. 196.
    Ahamed, J., Versteeg, H. H., Kerver, M., Chen, V. M., Mueller, B. M., Hogg, P. J., and Ruf, W. 2006 Proc Natl Acad Sci USA 103, 13932PubMedGoogle Scholar
  197. 197.
    Graven, K. K., Molvar, C., Roncarati, J. S., Klahn, B. D., Lowrey, S., and Farber, H. W. 2002 Am J Physiol Lung Cell Mol Physiol 282, L996PubMedGoogle Scholar
  198. 198.
    Essex, D. W., Chen, K., and Swiatkowska, M. 1995 Blood 86, 2168PubMedGoogle Scholar
  199. 199.
    Sullivan, D. C., Huminiecki, L., Moore, J. W., Boyle, J. J., Poulsom, R., Creamer, D., Barker, J., and Bicknell, R. 2003 J. Biol. Chem. 278, 47079PubMedGoogle Scholar
  200. 200.
    Chen, K., Detwiler, T. C., and Essex, D. W. 1995 Br J Haematol 90, 425PubMedGoogle Scholar
  201. 201.
    Claudio, J. O., Masih-Khan, E., Tang, H., Goncalves, J., Voralia, M., Li, Z. H., Nadeem, V., Cukerman, E., Francisco-Pabalan, O., Liew, C. C., Woodgett, J. R., and Stewart, A. K. 2002 Blood 100, 2175PubMedGoogle Scholar
  202. 202.
    Raturi, A., Miersch, S., Hudson, J. W., and Mutus, B. 2008 Biochim Biophys Acta 1778, 2790PubMedGoogle Scholar
  203. 203.
    Sinauridze, E. I., Kireev, D. A., Popenko, N. Y., Pichugin, A. V., Panteleev, M. A., Krymskaya, O. V., and Ataullakhanov, F. I. 2007 Thromb Haemost 97, 425PubMedGoogle Scholar
  204. 204.
    Banfi, C., Brioschi, M., Wait, R., Begum, S., Gianazza, E., Pirillo, A., Mussoni, L., and Tremoli, E. 2005 PROTEOMICS 5, 4443PubMedGoogle Scholar
  205. 205.
    Versteeg, H. H., and Ruf, W. 2007 J. Biol. Chem. 282, 25416PubMedGoogle Scholar
  206. 206.
    Cho, J., Furie, B. C., Coughlin, S. R., and Furie, B. 2008 J Clin Invest 118, 1123PubMedGoogle Scholar
  207. 207.
    Reinhardt, C., von Bruhl, M. L., Manukyan, D., Grahl, L., Lorenz, M., Altmann, B., Dlugai, S., Hess, S., Konrad, I., Orschiedt, L., Mackman, N., Ruddock, L., Massberg, S., and Engelmann, B. 2008 J Clin Invest 118, 1110PubMedGoogle Scholar
  208. 208.
    Wilkinson, B., and Gilbert, H. F. 2004 Biochimica et Biophysica Acta (BBA) - Proteins & Proteomics 1699, 35Google Scholar
  209. 209.
    Stone, J. P., and Wagner, D. D. 1993 J Clin Invest 92, 804PubMedGoogle Scholar
  210. 210.
    Brossart, P., Schneider, A., Dill, P., Schammann, T., Grunebach, F., Wirths, S., Kanz, L., Buhring, H.-J., and Brugger, W. 2001 Cancer Res 61, 6846PubMedGoogle Scholar
  211. 211.
    Navarro, J., Obrador, E., Carretero, J., Petschen, I., Avino, J., Perez, P., and Estrela, J. M. 1999 Free Radic Biol Med 26, 410PubMedGoogle Scholar
  212. 212.
    Yu, J. L., May, L., Lhotak, V., Shahrzad, S., Shirasawa, S., Weitz, J. I., Coomber, B. L., Mackman, N., and Rak, J. W. 2005 Blood 105, 1734PubMedGoogle Scholar
  213. 213.
    Rak, J., Milsom, C., and Yu, J. 2008 Curr Opin Hematol 15, 522PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Vascular Immunology Unit, Department of Pathology, Sydney Medical SchoolUniversity of SydneySydneyAustralia

Personalised recommendations