Advertisement

Clinical & Experimental Metastasis

, Volume 25, Issue 2, pp 171–181 | Cite as

The tumor cell–host organ interface in the early onset of metastatic organ colonisation

  • Peter Gassmann
  • Joerg Haier
Review

Abstract

Metastatic lesions are the leading cause of death among cancer patients. These lesions usually originate from clonal proliferation of single tumor cells dispersed from the primary tumor into the circulation which finally arrest in the capillary bed of distant organs. The microenvironment within the circulation of potential metastatic target organs provides a variety of pro- and anti- metastatic stimuli regulating the onset of organ colonisation by metastatic tumor cells. Mechanical shear stress, anoikis and cell mediated cytotoxicity within the microcirculation probably clear most circulating tumor cells. Adhesion, and eventually extravasation, are essential initial interactions of circulating tumor cells with distant organs and can provide escape from the cytotoxic environment within the circulation. Adhesion to the capillary wall is mostly controlled by the organ-specific availability of adhesion molecules on tumor cells, the endothelium, and the composition of the underlying extracellular matrix. The availability of pro-adhesive and pro-migratory paracrine signals provided by the organ specific microenvironment can further initiate the onset of metastatic organ colonisation. Tumor cell and microenvironment factors regulating survival within the microcirculation, adhesion and extravasation of tumor cells are highlighted in the review.

Keywords

Metastasis Organ selectivity Microenvironment Tumor cell adhesion Extravasation 

References

  1. 1.
    Morris M, Iacopetta B, Platell C (2007) Comparing survival outcomes for patients with colorectal cancer treated in public and private hospitals. Med J Aust 186:296–300PubMedGoogle Scholar
  2. 2.
    Garcia-Closas M, Brinton LA, Lissowska J et al (2006) Established breast cancer risk factors by clinically important tumour characteristics. Br J Cancer 95:123–129PubMedGoogle Scholar
  3. 3.
    Wolfle U, Muller V, Pantel K (2006) Disseminated tumor cells in breast cancer: detection, characterization and clinical relevance. Future Oncol 2:553–561PubMedGoogle Scholar
  4. 4.
    Nicolson GL (1988) Cancer metastasis: TC and host organ properties important in metastasis to specific secondary sites. Biochem Biophys Acta 948:175–224PubMedGoogle Scholar
  5. 5.
    Weiss L (1992) Comments on hematogenous metastatic patterns in humans as revealed by autopsy. Clin Exp Metastasis 10:191–199PubMedGoogle Scholar
  6. 6.
    Fidler IJ (2003) The pathogenesis of cancer metastasis: the seed and soil hypothesis revisited. Nat Rev Cancer 3:1–6Google Scholar
  7. 7.
    Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70PubMedGoogle Scholar
  8. 8.
    Thompson EW, Newgreen DF (2005) Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer Res 65:5991–5995PubMedGoogle Scholar
  9. 9.
    Guarino M, Rubino B, Ballabio G (2007) The role of epithelial-mesenchymal transition in cancer pathology. Pathology 39:305–318PubMedGoogle Scholar
  10. 10.
    Tse JC, Kalluri R (2007) Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment. J Cell Biochem. 101:816–829PubMedGoogle Scholar
  11. 11.
    Grünert S, Jechlinger M, Beug H (2003) Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nature Rev/Mol Cell Biol 4:657–665Google Scholar
  12. 12.
    Timmers M, Vekemans K, Vermijlen D et al (2004) Interactions between rat colon carcinoma cells and Kupffer cells during the onset of hepatic metastasis. Int J Cancer 112:793–802PubMedGoogle Scholar
  13. 13.
    Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2:563–572PubMedGoogle Scholar
  14. 14.
    Ewing J (1928) Neoplastic diseases, 6th edn. W. B. Sanders, PhiladelphiaGoogle Scholar
  15. 15.
    Paget S (1889) The distribution of secondary growth in cancer of the breast. Lancet 1:571–573Google Scholar
  16. 16.
    Weiss L, Voit A, Lane WW (1984) Metastatic patterns in patients with carcinoma of the lower esophagus and upper rectum. Invasion Metastasis 4:47–60PubMedGoogle Scholar
  17. 17.
    Tarin D, Price JE, Kettlewell MG et al (1984) Clinicopathological observations on metastasis in man studied in patients treated with peritoneovenous shunts. Br Med J (Clin Res Ed) 288:749–751CrossRefGoogle Scholar
  18. 18.
    Tarin D, Price JE, Kettlewell MG et al (1984) Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunts. Cancer Res 44:3584–3592PubMedGoogle Scholar
  19. 19.
    Muller A, Homey B, Soto H et al (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410:50–56PubMedGoogle Scholar
  20. 20.
    Glaves D, Huben RP, Weiss L (1988) Haematogeneous dissemination of cells from human renal adenocarcinomas. Br J Cancer 57:32–35PubMedGoogle Scholar
  21. 21.
    Glaves D, Ketch DA, Asch BB (1993) Conservation of epithelial cell phenotypes during hematogeneous metastasis from mammary carcinomas. J Natl Cancer Inst 76:933–938Google Scholar
  22. 22.
    Barbera-Guillem E, Weiss L (1993) Cancer-cell traffic in the liver. III Lethal deformation of B16 melanoma cells in liver sinusoids. Int J Cancer 54:880–884PubMedGoogle Scholar
  23. 23.
    Weiss L, Nannmark U, Johansson BR et al (1992) Lethal deformation of cancer cells in the microcirculation: a potential rate regulator of hematogenous metastasis. Int J Cancer 50:103–107PubMedGoogle Scholar
  24. 24.
    Weiss L (1991) Deformation-driven, lethal damage to cancer cells. Its contribution to metastatic inefficiency. Cell Biophys 18:73–79PubMedGoogle Scholar
  25. 25.
    Weiss L, Harlos JP, Elkin G (1990) Mechanisms for the biomechanical destruction of L1210 leukemia cells: a rate regulator for metastasis. Cell Biophys 16:149–159PubMedGoogle Scholar
  26. 26.
    Weiss L (1988) Biomechanical destruction of cancer cells in the heart: a rate regulator for hematogenous metastasis. Invasion Metastasis 8:228–237PubMedGoogle Scholar
  27. 27.
    Weiss L (1989) Biomechanical destruction of cancer cells in skeletal muscle: a rate-regulator for hematogenous metastasis. Clin Exp Metastasis 7:483–491PubMedGoogle Scholar
  28. 28.
    Haier J, Nicolson GL (2001) Tumor cell adhesion under hydrodynamic conditions of fluid flow. APMIS 109:241–262PubMedGoogle Scholar
  29. 29.
    Kucik DF, Dustin ML, Miller JM (1996) Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. J Clin Invest 97:2139–2144PubMedGoogle Scholar
  30. 30.
    Ni N, Kevil CG, Bullard DC et al (2003) Avidity modulation activates adhesion under flow and requires cooperativity among adhesion receptors. Biophys J 85:4122–4133Google Scholar
  31. 31.
    Korb T, Schlüter K, Enns A et al (2004) Integrity of actin fibres and microtubules influences metastatic tumor cell adhesion. Exp Cell Res 299:236–247PubMedGoogle Scholar
  32. 32.
    McIntire LV (1994) 1992 ALZA distinguished lecture: bioengineering and vascular biology. Ann Biomed Eng 22:2–13PubMedGoogle Scholar
  33. 33.
    Galbraith CG, Sheetz MP (1998) Forces on adhesive contacts affect cell function. Curr Opin Cell Biol 10:566–571PubMedGoogle Scholar
  34. 34.
    von Sengbusch A, Gassmann P, Fisch K et al (2005) Focal Adhesion Kinase regulates dynamic adhesion of carcinoma cells to collagens. Am J Pathol 166:585–593Google Scholar
  35. 35.
    Okuyama M, Ohta Y, Kambayashi J et al (1996) Fluid shear stress induces actin polymerization in human neutrophils. J Cell Biochem 63:432–441PubMedGoogle Scholar
  36. 36.
    Haier J, Nicolson GL (2000) Tumor cell adhesion of human colon carcinoma cells with different metastatic properties to extracellular matrix under dynamic conditions of laminar flow. J Cancer Res Clin Oncol 126:699–706PubMedGoogle Scholar
  37. 37.
    Glinskii OV, Huxley VH, Glinsky GV et al (2005) Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia 7:522–527PubMedGoogle Scholar
  38. 38.
    Mook OR, Van Marle J, Vreeling-Sindelarova H et al (2003) Visualization of early events in tumor formation of eGFP-transfected rat colon cancer cells in liver. Hepatology 38:295–304PubMedGoogle Scholar
  39. 39.
    Steinbauer M, Guba M, Cernaianu G et al (2003) GFP-transfected tumor cells are useful in examining early metastasis in vivo, but immune reaction precludes long-term tumor development studies in immunocompetent mice. Clin Exp Metastasis 20:135–141PubMedGoogle Scholar
  40. 40.
    Ding L, Sunamura M, Kodama T et al (2001) In vivo evaluation of the early events associated with liver metastasis of circulating cancer cells. Br J Cancer 85:431–438PubMedGoogle Scholar
  41. 41.
    Enns A, Gassmann P, Schluter K et al (2004) Integrins can directly mediate metastatic tumor cell adhesion within the liver sinusoids. J Gastrointest Surg 8:1049–1059PubMedGoogle Scholar
  42. 42.
    Enns A, Korb T, Schluter K et al (2005) Alphavbeta5-integrins mediate early steps of metastasis formation. Eur J Cancer 41:1065–1072PubMedGoogle Scholar
  43. 43.
    Haier J, Korb T, Hotz B et al (2003) An intravital model to monitor steps of metastatic tumor cell adhesion within the hepatic microcirculation. J Gastrointest Surg 7:507–514PubMedGoogle Scholar
  44. 44.
    Wang H, Fu W, Im JH et al (2004) Tumor cell alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol 164:935–941PubMedGoogle Scholar
  45. 45.
    Al-Mehdi AB, Tozawa K, Fisher AB et al (2000) Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 6:100–102PubMedGoogle Scholar
  46. 46.
    MacDonald IC, Schmidt EE, Morris VL et al (1992) Intravital videomicroscopy of the chorioallantoic microcirculation: a model system for studying metastasis. Microvasc Res 44:185–199PubMedGoogle Scholar
  47. 47.
    Naumov GN, Wilson SM, MacDonald IC et al (1992) Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J Cell Sci 112:1835–1842Google Scholar
  48. 48.
    Karpatkin S, Pearlstein E (1981) Role of platelets in tumor cell metastases. Ann Intern Med 95:636–641PubMedGoogle Scholar
  49. 49.
    Palumbo JS, Talmage KE, Massari JV et al (2005) Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 105:178–185PubMedGoogle Scholar
  50. 50.
    Nakamori S, Kameyama M, Imaoka S et al (1993) Increased expression of sialyl Lewisx antigen correlates with poor survival in patients with colorectal carcinoma: clinicopathological and immunohistochemical study. Cancer Res 53:3632–3637PubMedGoogle Scholar
  51. 51.
    Amado M, Carneiro F, Seixas M et al (1998) Dimeric sialyl-Le(x) expression in gastric carcinoma correlates with venous invasion and poor outcome. Gastroenterology 114:462–470PubMedGoogle Scholar
  52. 52.
    Steinert BW, Tang DG, Grossi IM et al (1993) Studies on the role of platelet eicosanoid metabolism and integrin alpha IIb beta 3 in tumor-cell-induced platelet aggregation. Int J Cancer 54:92–101PubMedGoogle Scholar
  53. 53.
    Borsig L, Wong R, Hynes RO et al (2002) Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 99:2193–2198PubMedGoogle Scholar
  54. 54.
    Camerer E, Qazi AA, Duong DN et al (2004) Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 104:397–401PubMedGoogle Scholar
  55. 55.
    Amirkhosravi A, Mousa SA, Amaya M et al (2003) Inhibition of tumor cell-induced platelet aggregation and lung metastasis by the oral GpIIb/IIIa antagonist XV454. Thromb Haemost 90:549–554PubMedGoogle Scholar
  56. 56.
    Klepfish A, Greco MA, Karpatkin S (1993) Thrombin stimulates melanoma tumor-cell binding to endothelial cells and subendothelial matrix. Int J Cancer 53:978–982PubMedGoogle Scholar
  57. 57.
    Dardik R, Savion N, Kaufmann Y et al (1998) Thrombin promotes platelet-mediated melanoma cell adhesion to endothelial cells under flow conditions: role of platelet glycoproteins P-selectin and GPIIb-IIIA. Br J Cancer 77:2069–2075PubMedGoogle Scholar
  58. 58.
    Honn KV, Tang DG, Grossi IM et al (1994) Enhanced endothelial cell retraction mediated by 12(S)-HETE: a proposed mechanism for the role of platelets in tumor cell metastasis. Exp Cell Res 210:1–9PubMedGoogle Scholar
  59. 59.
    Liotta LA (1992) Cancer cell invasion and metastasis. Sci Am 266:54–59, 62–63Google Scholar
  60. 60.
    Dong C, Slattery MJ, Rank BM (2002) In vitro characterization and micromechanics of tumor cell chemotactic protrusion, locomotion, and extravasation. Ann Biomed Eng 30:344–355PubMedGoogle Scholar
  61. 61.
    Slattery MJ, Dong C (2003) Neutrophils influence melanoma adhesion and migration under flow conditions. Int J Cancer 106:713–722PubMedGoogle Scholar
  62. 62.
    Slattery MJ, Liang S, Dong C (2005) Distinct role of hydrodynamic shear in leukocyte-facilitated tumor cell extravasation. Am J Physiol Cell Physiol 288:C831–C839PubMedGoogle Scholar
  63. 63.
    Wu QD, Wang JH, Condron C et al (2001) Human neutrophils facilitate tumor cell transendothelial migration. Am J Physiol Cell Physiol 280:C814–C822PubMedGoogle Scholar
  64. 64.
    Khatib AM, Fallavollita L, Wancewicz EV et al (2002) Inhibition of hepatic endothelial E-selectin expression by C-raf antisense oligonucleotides blocks colorectal carcinoma liver metastasis. Cancer Res 62:5393–5398PubMedGoogle Scholar
  65. 65.
    Kim YJ, Borsig L, Han HL et al (1999) Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am J Pathol 155:461–472PubMedGoogle Scholar
  66. 66.
    Wisse E, van’t Noordende JM, van der Meulen J et al (1976) The pit cell: description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res 173:423–435PubMedGoogle Scholar
  67. 67.
    Grundy MA, Zhang T, Sentmann CL (2007) NK cells remove B16F10 tumor cells in a perforin and interferon-gamma independent manner in vivo. Cancer Immunol Immunother 56:1153–1161PubMedGoogle Scholar
  68. 68.
    Wiltrout RH (2000) Regulation and antimetastatic functions of liver-associated natural killer cells. Immunol Rev 174:63–76PubMedGoogle Scholar
  69. 69.
    Vermijlen D, Luo D, Robaye B et al (1999) Pit cells (Hepatic natural killer cells) of the rat induce apoptosis in colon carcinoma cells by the perforin/granzyme pathway. Hepatology 29:51–56PubMedGoogle Scholar
  70. 70.
    Shresta S, MacIvor DM, Heusel JW et al (1995) Natural killer and lymphokine-activated killer cells require granzyme B for the rapid induction of apoptosis in susceptible target cells. Proc Natl Acad Sci USA 92:5679–5683PubMedGoogle Scholar
  71. 71.
    Oshimi Y, Oda S, Honda Y et al (1996) Involvement of Fas ligand and Fas-mediated pathway in the cytotoxicity of human natural killer cells. J Immunol 157:2909–2915PubMedGoogle Scholar
  72. 72.
    Wiltrout RH, Herberman RB, Zhang SR et al (1985) Role of organ-associated NK cells in decreased formation of experimental metastases in lung and liver. J Immunol 134:4267–4275PubMedGoogle Scholar
  73. 73.
    Smyth MJ, Thia KY, Street SE et al (2000) Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med 191:661–668PubMedGoogle Scholar
  74. 74.
    Smyth MJ, Taniguchi M, Street SE (2000) The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol 165:2665–2670PubMedGoogle Scholar
  75. 75.
    Gardner CR, Wasserman AJ, Laskin DL (1987) Differential sensitivity of tumor targets to liver macrophage-mediated cytotoxicity. Cancer Res 47:6686–6691PubMedGoogle Scholar
  76. 76.
    Decker T, Kiderlen AF, Lohmann-Matthes ML (1985) Liver macrophages (Kupffer cells) as cytotoxic effector cells in extracellular and intracellular cytotoxicity. Infect Immun 50:358–364PubMedGoogle Scholar
  77. 77.
    Sturm JW, Magdeburg R, Berger K (2003) Influence of TNFA on the formation of liver metastases in a syngenic mouse model. Int J Cancer 107:11–21PubMedGoogle Scholar
  78. 78.
    Fingar VH, Taber SW, Buschemeyer WC (1997) Constitutive and stimulated expression of ICAM-1 protein on pulmonary endothelial cells in vivo. Microvasc Res 54:135–144PubMedGoogle Scholar
  79. 79.
    Heimburg J, Yan J, Morey S et al (2006) Inhibition of spontaneous breast cancer metastasis by anti-Thomsen-Friedenreich antigen monoclonal antibody JAA-F11. Neoplasia 8:939–948PubMedGoogle Scholar
  80. 80.
    Ito S, Nakanishi H, Ikehara Y (2001) Real-time observation of micrometastasis formation in the living mouse liver using a green fluorescent protein gene-tagged rat tongue carcinoma cell line. Int J Cancer 93:212–217PubMedGoogle Scholar
  81. 81.
    Shimizu S, Yamada N, Sawada T et al (2001) Ultrastructure of early phase hepatic metastasis of human colon carcinoma cells with special reference to desmosomal junctions with hepatocytes. Pathol Int 50:953–959Google Scholar
  82. 82.
    Khatib AM, Kontogiannea M, Fallavollita L et al. (1999). Rapid induction of cytokine and E-selectin expression in the liver in response to metastatic tumor cells. Cancer Res 59:1356–1361PubMedGoogle Scholar
  83. 83.
    Wang HH, McIntosh AR, Hasinoff BB et al (2002) Regulation of B16F1 melanoma cell metastasis by inducible functions of the hepatic microvasculature. Eur J Cancer 38:1261–1270PubMedGoogle Scholar
  84. 84.
    Orr FW, Wang HH, Lafrenie RM et al (2000) Interactions between cancer cells and the endothelium in metastasis. J Pathol 190:310–329PubMedGoogle Scholar
  85. 85.
    Eble JA, Haier J (2006) Integrins in cancer treatment. Curr Cancer Drug Targets 6:89–105PubMedGoogle Scholar
  86. 86.
    Meyer T, Hart IR (1998) Mechanisms of tumour metastasis. Eur J Cancer 34:214–221PubMedGoogle Scholar
  87. 87.
    Gooding JM, Yap KL, Ikura M (2004) The cadherin–catenin complex as a focal point of cell adhesion and signalling: new insights from three-dimensional structures. Bioessays 26:497–511PubMedGoogle Scholar
  88. 88.
    Silbert JE, Sugumaran G (2003) A starting place for the road to function. Glycoconj 19:227–237Google Scholar
  89. 89.
    Haier J, Nasralla M, Nicolson GL (2000) Cell surface molecules and their prognostic values in assessing colorectal carcinomas. Ann Surg 231:11–24PubMedGoogle Scholar
  90. 90.
    Juliano RL, Varner JA (1993) Adhesion molecules in cancer: the role of integrins. Curr Opin Cell Biol 5:812–818PubMedGoogle Scholar
  91. 91.
    Hulleman E, Boonstra J (2001) Regulation of G1 phase progression by growth factors and the extracellular matrix. Cell Mol Life Sci 58:80–93PubMedGoogle Scholar
  92. 92.
    Juliano RL, Varner JA (1993) Adhesion molecules in cancer: the role of integrins. Curr Opin Cell Biol 5:812–818PubMedGoogle Scholar
  93. 93.
    Varner JA, Emerson DA, Juliano RL (1995) Integrin alpha5beta1 expression negatively regulate cell growth: reversal by attachment to fibronectin. Mol Biol Cell 6:725–740PubMedGoogle Scholar
  94. 94.
    Derksen PW, Liu X, Saridin F et al (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437–449PubMedGoogle Scholar
  95. 95.
    Owens DM, Watt FM (2001) Influence of beta1 integrins on epidermal squamous cell carcinoma formation in a transgenic mouse model: alpha3beta1, but not alpha2beta1, suppresses malignant conversion. Cancer Res 61:5248–5254PubMedGoogle Scholar
  96. 96.
    Zutter MM, Santoro SA, Staatz WD (1995) Re-expression of the alpha2beta1 integrin abrogates the malignant phenotype of breast carcinoma cells. Proc Natl Acad Sci USA 92:7411–7415PubMedGoogle Scholar
  97. 97.
    Bogenrieder T, Herlyn M (2003) Axis of evil: molecular mechanisms of cancer metastasis. Oncogene 22:6524–6536PubMedGoogle Scholar
  98. 98.
    Woodhouse EC, Chuaqui RF, Liotta LA (1997) General mechanisms of metastasis. Cancer 80:1529–1537PubMedGoogle Scholar
  99. 99.
    Hood JD, Cheresh DA (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2:91–100PubMedGoogle Scholar
  100. 100.
    Byers SW, Sommers CL, Hoxter B, Mercurio AM, Tozeren A (1995) Role of E-cadherin in the response of tumor cell aggregates to lymphatic, venous and arterial flow: measurement of cell–cell adhesion strength. J Cell Sci 108:2053–2064PubMedGoogle Scholar
  101. 101.
    Wolf K, Mazo I, Leung H (2003) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160:267–277PubMedGoogle Scholar
  102. 102.
    Friedl P, Wolf K (2003) Tumour–cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374PubMedGoogle Scholar
  103. 103.
    Sahai E, Marschall CJ (2003) Differing modes of tumor cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5:711–719PubMedGoogle Scholar
  104. 104.
    Fukumura D, Yuan F, Monsky WL (1997) Effect of host microenvironment on the microcirculation of human colon adenocarcinoma. Am J Pathol 151:679–688PubMedGoogle Scholar
  105. 105.
    Kikkawa H, Kaihou M, Horaguchi N (2002) Role of integrin alphavbeta3 in the early phase of liver metastasis: PET and IVM analyses. Clin Exp Metastasis 19:717–725PubMedGoogle Scholar
  106. 106.
    Nip J, Shibata H, Loskutoff DJ et al (1992) Human melanoma cells derived from lymphatic metastasis use the integrin alpha(V)beta(3) to adhere to lymph node vitronectin. J Clin Invest 90:1406–1413PubMedGoogle Scholar
  107. 107.
    Byzova TV, Kim W, Midura RJ et al (2000) Activation of integrin alpha(V)beta(3) regulates cell adhesion and migration to bone sialoprotein. Exp Cell Res 254:299–308PubMedGoogle Scholar
  108. 108.
    Liapsi H, Flath H, Kitazawa S (1996) Integrin alpha V beta 3 expression by bone-residing breast cancer metastasis. Diagn Mol Pathol 5:127–135Google Scholar
  109. 109.
    Sloan EK, Pouliot N, Stanley KL et al (2006) Tumor-specific expression of alphavbeta3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res 8:R20PubMedGoogle Scholar
  110. 110.
    Bosman FT, Stamenkovic I (2003) Functional structure and composition of the extracellular matrix. J Pathol 200:423–428PubMedGoogle Scholar
  111. 111.
    Hayashi C, Rittling S, Hayata T et al (2007) Serum osteopontin, an enhancer of tumor metastasis to bone, promotes B16 melanoma cell migration. J Cell Biochem 27 [Epub ahead of print]Google Scholar
  112. 112.
    Desai B, Rogers MJ, Chellaiah MA (2007) Mechanisms of osteopontin and CD44 as metastatic principles in prostate cancer cells. Mol Cancer 6:18PubMedGoogle Scholar
  113. 113.
    Paris S, Sesboue R, Chauzy C et al (2006) Hyaluronectin modulation of lung metastasis in nude mice. Eur J Cancer 42:3253–3259PubMedGoogle Scholar
  114. 114.
    Bauerle T, Peterschmitt J, Hilbig H et al (2006) Treatment of bone metastasis induced by MDA-MB-231 breast cancer cells with an antibody against bone sialoprotein. Int J Oncol 28:573–583PubMedGoogle Scholar
  115. 115.
    Jacob K, Webber M, Benayahu D et al (1999) Osteonectin promotes prostate cancer cell migration and invasion: a positive mechanism for metastasis to bone. Cancer Res 59:4453–4457PubMedGoogle Scholar
  116. 116.
    Wang H, Fu W, Im JH et al (2004) Tumor cell alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol 164:935–941PubMedGoogle Scholar
  117. 117.
    Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161–174PubMedGoogle Scholar
  118. 118.
    McCawley LJ, Matrisian LM (2001) Matrix metalloproteinases: they´re not just for matrix anymore. Curr Opin Cell Biol 13:534–540PubMedGoogle Scholar
  119. 119.
    Mackay CR (2001) Chemokines: immunology’s high impact factors. Nat Immunol 2:95–101PubMedGoogle Scholar
  120. 120.
    Schier AF (2003) Chemokine signaling: rules of attraction. Curr Biol 13:R192–R194PubMedGoogle Scholar
  121. 121.
    Youngs SJ, Ali SA, Taub DD et al (1997) Chemokines induce migrational responses in human breast carcinoma cell lines. Int J Cancer 71:257–266PubMedGoogle Scholar
  122. 122.
    Zipin-Roitman A, Meshel T, Sagi-Assif O et al (2007) CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res 67:3396–3405PubMedGoogle Scholar
  123. 123.
    Burger JA, Burger M, Kipps TJ (1999) Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 94:3658–3667PubMedGoogle Scholar
  124. 124.
    Burger M, Glodek A, Hartmann T et al (2003) Functional expression of CXCR4 (CD184) on small-cell lung cancer cells mediates migration, integrin activation, and adhesion to stromal cells. Oncogene 22:8093–8101PubMedGoogle Scholar
  125. 125.
    Zeelenberg IS, Ruuls-Van Stalle L, Roos E (2003) The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 63:3833–3839PubMedGoogle Scholar
  126. 126.
    Cardones AR, Murakami T, Hwang ST (2003) CXCR4 enhances adhesion of B16 tumor cells to endothelial cells In vitro and in vivo via beta(1) integrin. Cancer Res 63:6751–6757PubMedGoogle Scholar
  127. 127.
    Dellacasagrande J, Schreurs OJ, Hofgaard PO et al (2003) Liver metastasis of cancer facilitated by chemokine receptor CCR6. Scand J Immunol 57:534–544PubMedGoogle Scholar
  128. 128.
    Kucia M, Jankowski K, Reca R et al (2004) CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. J Mol Histol 35:233–245PubMedGoogle Scholar
  129. 129.
    Fernandis AZ, Prasad A, Band H et al (2004) Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 23:157–167PubMedGoogle Scholar
  130. 130.
    Wang J, Loberg R, Taichman RS (2006) The pivotal role of CXCL12 (SDF-1)/CXCR4 axis in bone metastasis. Cancer Metastasis Rev 25:573–587PubMedGoogle Scholar
  131. 131.
    Wiley HE, Gonzalez EB, Maki W et al (2001) Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Natl Cancer Inst 93:1638–1643PubMedCrossRefGoogle Scholar
  132. 132.
    Pelletier AJ, van der Laan LJ, Hildbrand P et al (2000) Presentation of chemokine SDF-1 alpha by fibronectin mediates directed migration of T cells. Blood 96:2682–2690PubMedGoogle Scholar
  133. 133.
    McNeel DG, Eickhoff J, Lee FT et al (2005) Phase I trial of a monoclonal antibody specific for alphavbeta3 integrin (MEDI-522) in patients with advanced malignancies, including an assessment of effect on tumor perfusion. Clin Cancer Res 11:7851–7860PubMedGoogle Scholar
  134. 134.
    Ishida T, Ueda R (2006) CCR4 as a novel molecular target for immunotherapy of cancer. Cancer Sci 97:1139–1146PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Molecular Biology Laboratory, Department of General SurgeryUniversity Hospital MuensterMuensterGermany

Personalised recommendations