Skip to main content
Log in

Are cellular adhesion molecules involved in the metastasis of breast cancer?

  • Review article
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  1. Auerbach R: Patterns of tumor metastasis: organ selectivity in the spread of cancer cells. Lab Invest 58: 361–364, 1988

    Google Scholar 

  2. Nicolson GL: Cancer metastasis: tumor cell and host organ properties important in metastasis to specific secondary sites. Biochim Biophys Acta 948: 175–224, 1988

    Google Scholar 

  3. Blood CH, Zetter BR: Tumor interactions with the vasculature: angiogenesis and tumor metastasis. Biochim Biophys Acta 1032: 89–118, 1990

    Google Scholar 

  4. McCormick BA, Zetter BR: Adhesive interactions in angiogenesis and metastasis. Pharmac Ther 53: 239–260, 1992

    Google Scholar 

  5. Liotta LA: Tumor invasion and metastases - role of the extracellular matrix: Rhoads memorial award lecture. Cancer Res 46: 1–7, 1986

    Google Scholar 

  6. Liotta LA, Steeg PS, Stetler-Stevenson WG: Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64: 327–336, 1991

    Google Scholar 

  7. Kaminski M, Auerbach R: Tumor cells are protected from NK-cell-mediated lysis by adhesion to endothelial cells. Int J Cancer 41: 847–849, 1988

    Google Scholar 

  8. Behrens J: The role of cell adhesion molecules in cancer invasion and metastasis. Breast Cancer Res Treat 24: 175–184, 1993

    Google Scholar 

  9. Coman DR: Mechanism of the invasiveness of cancer. Science 105: 347–348, 1947

    Google Scholar 

  10. Weinstein RS, Merk FB, Alroy J: The structure and function of intercellular junctions in cancer. Adv Cancer Res 23: 23–89, 1976

    Google Scholar 

  11. Bastida E: The metastatic cascade: potential approaches for the inhibition of metastasis. Semin Thromb Hemost 14: 66–72, 1988

    Google Scholar 

  12. De Bruyn PPH, Cho Y: Vascular endothelial invasion via transcellular passage by malignant cells in the primary stage of metastases formation. J Ultrastruct Res 81: 189–201, 1982

    Google Scholar 

  13. Takeichi M: Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251: 1451–1455, 1991

    Google Scholar 

  14. Yoshida CN, Suzuki N, Takeichi M: Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cell studied with a monoclonal antibody. Dev Biol 101: 19–27, 1984

    Google Scholar 

  15. Nose A, Takeichi M: A novel cadherin cell adhesion molecule: its expression petterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 103: 2649–2658, 1986

    Google Scholar 

  16. Hatta K, Okada TS, Takeichi M: A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. Proc Natl Acad Sci USA 82: 2789–2793, 1985

    Google Scholar 

  17. Gallin WJ, Edelman GM, Cunningham BA: Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc Natl Acad Sci USA 80: 1038–1042, 1983

    Google Scholar 

  18. Behrens J, Mareel MM, Roy FMV, Birchmeier W: Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol 108: 2435–2447, 1989

    Google Scholar 

  19. Vleminckx K, Vakaet Jr L, Mareel M, Fiers W, Roy FV: Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66: 107–119, 1991

    Google Scholar 

  20. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Löchner D, Birchmeier W: E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113: 173–185, 1991

    Google Scholar 

  21. Sommers CL, Thompson EW, Torri JA, Kemler R, Gelmann EP, Byers SW: Cell adhesion molecule uvomorulin expression in human breast cancer cell lines: relationship to morphology and invasive capacities. Cell Growth Diff 2: 365–372, 1991

    Google Scholar 

  22. Doki Y, Schiozaki H, Tahara H, Inoue M, Oka H, Iihara K, Kadowaki T, Takeichi M, Mori T: Correlation between Ecadherin expression and invasivenessin vitro in a human esophageal cancer cell line. Cancer Res 53: 3421–3426, 1993

    Google Scholar 

  23. Shiozaki H, Tahara H, Oka H, Miyata M, Kobayashi K, Tamura S, Iihara K, Doki Y, Hirano S, Takeichi M, Mori T: Expression of immunoreactive E-cadherin adhesion molecules in human cancers. Am J Pathol 139: 17–23, 1991

    Google Scholar 

  24. Mayer B, Johnson JP, Leitl F, Jauch KW, Heiss MM, Schildberg FW, Birchmeier W, Funke I: E-cadherin expression in primary and metastatic gastric cancer: down-regulation correlates with cellular dedifferentiation and glandular disintegration. Cancer Res 53: 1690–1695, 1993

    Google Scholar 

  25. Oka H, Shiozaki H, Kobayashi K, Inoue M, Tahara H, Kobayashi T, Takatsuka Y, Matsuyoshi N, Hirano S, Takeichi M, Mori T: Expression of E-cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis. Cancer Res 53: 1696–1701, 1993

    Google Scholar 

  26. Hashimoto M, Niwa O, Nitta Y, Takeichi M, Yokoro K: Unstable expression of E-cadherin adhesion molecules in metastatic ovarian tumor cells. Jpn J Cancer Res 80: 459–463, 1989

    Google Scholar 

  27. Umbas R, Schalken JA, Aalders TW, Carter BS, Karthaus HFM, Schaafsma HE, Debruyne FMJ, Isaacs WB: Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer. Cancer Res 52: 5104–5109, 1992

    Google Scholar 

  28. Tohma Y, Yamashita Y, Yamashita J: Immunohistochemical localization of cell adhesion molecule epithelial cadherin in human arachnoid villi and meningiomas. Cancer Res 52: 1981–1987, 1992

    Google Scholar 

  29. Shimoyama Y, Hirohashi S: Cadherin intercellular adhesion molecule in hepatocellular carcinomas: loss of E-cadherin expression in an undifferentiated carcinoma. Cancer Lett 57: 131–135, 1991

    Google Scholar 

  30. Schipper JH, Frixen UH, Behrens J, Unger A, Jahnke K, Birchmeier W: E-cadherin expression in squamous cell carcinomas of head and neck: inverse correlation with tumor dedifferentiation and lymph node metastasis. Cancer Res 51: 6328–6337, 1991

    Google Scholar 

  31. Morton RA, Ewing CM, Nagafuchi A, Tsukita S, Isaacs WB: Reduction of E-cadherin levels and deletion of the α-catenin gene in human prostate cancer cells. Cancer Res 53: 3585–3590, 1993

    Google Scholar 

  32. Rutishauser U, Hoffman S, Edelman GM: Binding properties of a cell adhesion molecule from neural tissue. Proc Natl Acad Sci USA 79: 685–689, 1982

    Google Scholar 

  33. Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM: Neural cell adhesion molecule: Structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236: 799–806, 1987

    Google Scholar 

  34. Andersson AM, Moran N, Linneman D, Bjerkvig R, Laerum OD, Bock E: Characterization of NCAM expression and function in BT4C and BT4Cn glioma cells. Int J Cancer 47: 124–129, 1991

    Google Scholar 

  35. Linnemann D, Raz A, Bock E: Differential expression of cell adhesion molecules in variants of K1735 melanoma cells differing in metastatic capacity. Int J Cancer 43: 709–712, 1989

    Google Scholar 

  36. Faeron ER, Cho KR, Nigro JM, Kern SE, Simons JW, Ruppert JM, Hamilton SR, Preisinger AC, Thomas G, Kinzler KW, Vogelstein B: Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 247: 49–56, 1990

    Google Scholar 

  37. Narayanan R, Lawlor KG, Schaapveld RQJ, Cho KR, Vogelstein B, Tran PB-V, Osborne MP, Telang NT: Antisense RNA to the putative tumor-suppressor gene DCC transforms Rat-1 fibroblasts. Oncogene 7: 553–561, 1992

    Google Scholar 

  38. Yanoshita RK, Konishi M, Fukunari H, Tanaka K, Miyaki M: Loss of expression of the DCC gene during progression of colorectal carcinomas in familial adenomatous polyposis and non-familial adenomatous polyposis patients. Cancer Res 52: 3801–3803, 1992

    Google Scholar 

  39. Höhne MW, Halatsch M-E, Kahl GF, Weinel RJ: Frequent loss of expression of the potential tumor suppressor gene DCC in ductal pancreatic adenocarcinoma. Cancer Res 52: 2616–2619, 1992

    Google Scholar 

  40. Devilee P, van Vliet M, Kuipers-Dijkshoorn N, Pearson PL, Cornelisse CJ: Somatic genetic changes on chromosome 18 in breast carcinomas: is the DCC gene involved? Oncogene 6: 311–315, 1991

    Google Scholar 

  41. Adamson IYR, Young L, Orr FW: Tumor metastasis after hyperoxic injury and repair of the pulmonary endothelium. Lab Invest 57: 71–77, 1987

    Google Scholar 

  42. Morris VL, MacDonald IC, Koop S, Schmidt EE, Chambers AF, Groom AC: Early interactions of cancer cells with the microvasculature in mouse liver and muscle during hematogenous metastasis: videomicroscopic analysis. Clin Exp Metastasis 11: (in press), 1993

  43. Rusciano D, Burger MM: Why do cancer cells metastasize into particular organs? BioEssays 14: 185–194, 1992

    Google Scholar 

  44. Auerbach R, Lu WC, Pardon E, Gumkowski F, Kaminska G, Kaminska M: Specificity of adhesion between murine tumor cells and capillary endothelium: anin vitro correlate of preferential metastasisin vivo. Cancer Res 47: 1492–1496, 1987

    Google Scholar 

  45. Johnson RC, Augustin-Voss HG, Zhu D, Pauli BU: Endothelial cell membrane vesicles in the study of organ preference of metastasis. Cancer Res 51: 394–399, 1991

    Google Scholar 

  46. McCarthy SA, Kuzu I, Gatter KC, Bicknell R: Heterogeneity of the endothelial cell and its role in organ preference of tumour metastasis. TiPS 12: 462–467, 1991

    Google Scholar 

  47. Cummings RD, Smith DF: The selectin family of carbohydrate-binding proteins: structure and importance of carbohydrate ligands for cell adhesion. BioEssay 14: 849–856, 1992

    Google Scholar 

  48. Bevilacqua MP, Stengelin S, Gimbrone Jr MA, Seed B: Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243: 1160–1165, 1989

    Google Scholar 

  49. Phillips ML, Nudelman E, Gaeta FCA, Perez M, Singhal AK, Hakomori S, Paulson JC: ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science 250: 1130–1132, 1990

    Google Scholar 

  50. Berg EL, Robinson MK, Mansson O, Butcher EC, Magnani JL: A carbohydrate domain common to both sialyl Lea and sialyl Lex is recognized by the endothelial cell leukocyte adhesion molecule ELAM-1. J Biol Chem 266: 14869–14872, 1991

    Google Scholar 

  51. Hoff SD, Matsushita Y, Ota DM, Cleary KR, Yamori T, Hakomori S, Irimura T: Increased expression of sialyl-dimeric Lex antigen in liver metastases of human colorectal carcinoma. Cancer Res 49: 6883–6888, 1989

    Google Scholar 

  52. Nakamori S, Kameyama M, Imaoka S, Furukawa H, Ishikawa O, Sasaki Y, Kabuto T, Iwanaga T, Matsushita Y, Irimura T: Increased expression of sialyl Lewisx antigen correlates with poor survival in patients with colorectal carcinoma: clinicopathological and immunohistochemical study. Cancer Res 53: 3632–3637, 1993

    Google Scholar 

  53. Fukushima K, Hirota M, Terasaki PI, Wakisaka A, Togashi H, Chia D, Suyama N, Fukushi Y, Nudelman E, Hakomori S: Characterization of sialosylated Lewisx as a new tumorassociated antigen. Cancer Res 44: 5279–5285, 1984

    Google Scholar 

  54. Sakamoto J, Watanabe T, Tokumaru T, Takagi H, Nakazato H, Lloyd KO: Expression of Lewisa, Lewisb, Lewisx, Lewisy, sialyl-Lewisa, and sialyl-Lewisx blood group antigens in human gastric carcinoma and in normal gastric tissue. Cancer Res 49: 745–752, 1989

    Google Scholar 

  55. Rice GE, Bevilacqua MP: An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science 246: 1303–1306, 1989

    Google Scholar 

  56. Matsushita Y, Nakamori S, Seftor EA, Hendrix MJC, Irimura T: Human colon carcinoma cells with increased invasive capacity obtained by selection for sialyl-dimeric Lex antigen. Exp Cell Res 196: 20–25, 1991

    Google Scholar 

  57. Osborn L, Hession C, Tizard R, Vassallo C, Luhowskyj S, Chi-Rosso G, Lobb R: Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 59: 1203–1211, 1989

    Google Scholar 

  58. Elices MJ, Osborn L, Takada Y, Crouse C, Luhowskyj S, Hemler ME, Lobb RR: VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60: 577–584, 1990

    Google Scholar 

  59. Taichman DB, Cybulsky MI, Djaffar I, Longenecker BM, Teixidó J, Rice E, Aruffo A, Bevilacqua MB: Tumor cell surface α4β1 integrin mediates adhesion to vascular endothelium: demonstration of an interaction with the N-terminal domains of INCAM-110/VCAM-1. Cell Regul 2: 347–355, 1991

    Google Scholar 

  60. Mattila P, Majuri M-L, Renkonen R: VLA-4 integrin on sarcoma cell lines recognizes endothelial VCAM-1 differential regulation of the VLA-4 avidity on various sarcoma cell lines. Int J Cancer 52: 918–923, 1992

    Google Scholar 

  61. Orr FW, Adamson IYR, Young L: Pulmonary inflammation generates chemotactic activity for tumor cells and promotes lung metastasis. Am Rev Respir Dis 131: 607–611, 1985

    Google Scholar 

  62. Murthy SM, Goldschmidt RA, Rao LN, Ammirati M, Buchmann T, Scanlon EF: The influence of surgical trauma on experimental metastasis. Cancer 64: 2035–2044, 1989

    Google Scholar 

  63. Hart IR, Birch M, Marshall JF: Cell adhesion receptor expression during melanoma progression and metastasis. Cancer Metast Rev 10: 115–128, 1991

    Google Scholar 

  64. Spriggs D, Imamura K, Rodriguez C, Horiguchi J, Kufe DW: Induction of tumor necrosis factor expression and resistance in a human breast tumor cell line. Proc Natl Acad Sci 84: 6563–6566, 1987

    Google Scholar 

  65. Goldstein LA, Zhou DFH, Picker LJ, Minty CN, Bargatze RF, Ding JF, Butcher EC: A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins. Cell 56: 1063–1072, 1989

    Google Scholar 

  66. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B: CD44 is the principal cell surface receptor for hyaluronate. Cell 61: 1303–1313, 1990

    Google Scholar 

  67. Jalkanen S, Bargatze RF, de los Toyos J, Butcher EC: Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85–95D glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells. J Cell Biol 105: 983–990, 1987

    Google Scholar 

  68. Gallatin M, St John TP, Siegelman M, Reichert R, Butcher EC, Weissman IL: Lymphocyte homing receptors. Cell 44: 673–680, 1986

    Google Scholar 

  69. Stamenkovic I, Amiot M, Pesando JM, Seed B: A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family. Cell 56: 1057–1062, 1989

    Google Scholar 

  70. Sher BT, Bargatze R, Holtzmann B, Gallatin WM, Matthews D, Wu N, Picker L, Butcher EC, Weissman IL: Homing receptors and metastasis. Adv Cancer Res 51: 361–390, 1988

    Google Scholar 

  71. Birch M, Mitchell S, Hart IR: Isolation and characterization of human melanoma cell variants expressing high and low levels of CD44. Cancer Res 51: 6660–6667, 1991

    Google Scholar 

  72. Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, Haussmann I, Matzku S, Wenzel A, Ponta H, Herrlich P: A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65: 13–24, 1991

    Google Scholar 

  73. Seiter S, Arch R, Reber S, Komitowski D, Hofmann M, Ponta H, Herrlich P, Matzku S, Zöller M: Prevention of tumor metastasis formation by anti-variant CD44. J Exp Med 177: 443–455, 1993

    Google Scholar 

  74. Hofmann M, Rudy W, Zöller M, Tölg C, Ponta H, Herrlich P, Günthert U: CD44 splice variants confer metastatic behavior in rats: homologous sequences are expressed in human tumor cell lines. Cancer Res 51: 5292–5297, 1991

    Google Scholar 

  75. Rudy W, Hofmann M, Schwartz-Albiez R, Zöller M, Heider K-H, Ponta H, Herrlich P: The two major CD44 proteins expressed on a metastatic rat tumor cell line are derived from different splice variants: each one individually suffices to confer metastatic behavior. Cancer Res 53: 1262–1268, 1993

    Google Scholar 

  76. Heider K-H, Hofmann M, Hors E, van den Berg F, Ponta H, Herrlich P, Pals ST: A human homologue of the rat metastasis-associated variant of CD44 is expressed in colorectal carcinomas and adenomatous polyps. J Cell Biol 120: 227–233, 1993

    Google Scholar 

  77. Staunton DE, Marlin SD, Stratowa C, Dustin ML, Springer TA: Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 52: 925–933, 1988

    Google Scholar 

  78. Dustin ML, Springer TA: Lymphocyte function-associated antigen-1 (LFA-1) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells. J Cell Biol 107: 321–331, 1988

    Google Scholar 

  79. Rothlein R, Dustin ML, Marlin SD, Springer TA: A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol 137: 1270–1274, 1986

    Google Scholar 

  80. Johnson JP, Stade BG, Holzmann B, Schwäble W, Riethmüller G:De novo expression of intercellular-adhesion molecule 1 in melanoma correlates with increased risk of metastasis. Proc Natl Acad Sci USA 86: 641–644, 1989

    Google Scholar 

  81. Hawley RG, Wang M-H, Fong AZC, Hawley TS: Association between ICAM-1 expression and metastasis capacity of murine B-cell hydridomas. Clin Exp Metastasis 11: 213–226, 1993

    Google Scholar 

  82. Natali P, Nicotra MR, Cavaliere R, Bigotti A, Romano G, Temponi M, Ferrone S: Differential expression of intercellular adhesion molecule 1 in primary and metastatic melanoma lesions. Cancer Res 50: 1271–1278, 1990

    Google Scholar 

  83. Vogetseder W, Feichtinger H, Schulz TF, Schwaeble W, Tabaczewski P, Mitterer M, Böck G, Marth C, Dapunt O, Mikuz G, Dierich MP: Expression of 7F7-antigen, a human adhesion molecule identical to intercellular adhesion molecule-1 (ICAM-1) in human carcinomas and their stromal fibroblasts. Int J Cancer 43: 768–773, 1989

    Google Scholar 

  84. Kelly CP, O'Keane JC, Orellana J, Schroy III PC, Yang S, Lamont JT, Brady HR: Human colon cancer cells express ICAM-1in vivo and support LFA-1-dependent lymphocyte adhesionin vitro. Am J Physiol 263: G864–870, 1992

    Google Scholar 

  85. Schwaeble W, Kerlin M, Meyer zum Büschenfelde K-H, Dippold W:de novo expression of intercellular adhesion molecule 1 (ICAM-1, CD54) in pancreas cancer. Int J Cancer 53: 328–333, 1993

    Google Scholar 

  86. Tomita Y, Nishiyama T, Watanabe H, Fujiwara M, Sato S: Expression of intercellular adhesion molecule-1 (ICAM-1) on renal-cell cancer: possible significance in host immune responses. Int J Cancer 46: 1001–1006, 1990

    Google Scholar 

  87. Kolbeck PC, Kareggia FF, Johansson SL, Grune MT, Taylor RJ: The relationship among tumor-infiltrating lymphocytes, histopathologic findings, and long-term clinical follow-up in renal cell carcinoma. Modern Pathol 5: 420–425, 1992

    Google Scholar 

  88. Gómez-morales M, Aluaro T, Muñoz M, Garcia Del Moral R, Aguilar D, Caballero T, Aneiros J: Diffuse sclerosing papillary carcinoma of the thyroid gland: immunohistochemical analysis of the local host immune response. Histopathol 18: 427–433, 1991

    Google Scholar 

  89. Stewart THM, Tsai S-CJ: The possible role of stromal cell stimulation in worsening the prognosis of a subset of patients with breast cancer. Clin Exp Metastasis 11: 295–305, 1993

    Google Scholar 

  90. Lichtmer RB, Belloni PN, Nicolson GL: Differential adhesion of metastatic rat mammary carcinoma cells to organ-derived microvessel endothelial cells and subendothelial matrix. Exp Cell Biol 57: 146–152, 1989

    Google Scholar 

  91. Doerr P, Zvibel I, Chiuten D, D'Olimpio J, Reid LM: Clonal growth of tumors on tissue-specific biomatrices and correlation with organ site specificity of metastases. Cancer Res 49: 384–392, 1989

    Google Scholar 

  92. Pauli BU, Lee C-L: Organ preference of metastasis the role of organ-specifically modulated endothelial cells. Lab Invest 58: 379–387, 1988

    Google Scholar 

  93. Albelda SM, Buck CA: Integrins and other cell adhesion molecules. FASEB J 4: 2868–2880, 1990

    Google Scholar 

  94. Ruoslahti E: Integrins. J Clin Invest 87: 1–5, 1991

    Google Scholar 

  95. Ruoslahti E, Pierschbacher MD: New perspectives in cell adhesion: RGD and integrins. Science 238: 491–497, 1987

    Google Scholar 

  96. Gehlsen KR, Argraves WS, Pierschbacher MD, Ruoslahti E: Inhibition ofin vitro tumor cell invasion by Arg-Gly-Asp-containing synthetic peptides. J Cell Biol 106: 925–930, 1988

    Google Scholar 

  97. Humphries MJ, Olden K, Yamada KM: A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233: 467–470, 1986

    Google Scholar 

  98. Saiki I, Iida J, Murata J, Ogawa R, Nishi N, Sugimura K, Tokura S, Azuma I: Inhibition of the metastasis of murine malignant melanoma by synthetic polymeric peptides containing core sequences of cell-adhesive molecules. Cancer Res 49: 3815–3822, 1989

    Google Scholar 

  99. McCarthy JB, Skubitz APN, Palm SL, Furcht LT: Metastasis inhibition of different tumor types by purified laminin fragments and a heparin-binding fragment of fibronectin. J Natl Cancer Inst 80: 108–116, 1988

    Google Scholar 

  100. Dedhar S, Saulnier R: Alterations in integrin receptor expression on chemically transformed human cells: specific enhancement of laminin and collagen receptor complexes. J Cell Biol 110: 481–489, 1990

    Google Scholar 

  101. Yamada KM, Kennedy DW, Yamada SS, Gralnick H, Chen W-T, Akiyama SK: Monoclonal antibody and synthetic peptide inhibitors of human tumor cell migration. Cancer Res 50: 4485–4496, 1990

    Google Scholar 

  102. Fujita S, Suzuki H, Kinoshita M, Hirohashi S: Inhibition of cell attachment, invasion and metastasis of human carcinoma cells by anti-integrin β1 subunit antibody. Jpn J Cancer Res 83: 1317–1326, 1992

    Google Scholar 

  103. Chan BMC, Matsuura N, Takada Y, Zetter B, Hemler ME:In vitro andin vivo consequences of VLA-2 expression on rhabdomyosarcoma cells. Science 251: 1600–1602, 1991

    Google Scholar 

  104. Giancotti FG, Ruoslahti E: Elevated levels of the α5β1 fibronectin receptor suppress the transformed phenotype of chinese hamster ovary cells. Cell 60: 849–859, 1990

    Google Scholar 

  105. Schreiner C, Fisher M, Hussein S, Juliano RL: Increased tumorigenicity of fibronectin receptor deficient chinese hamster ovary cell variants. Cancer Res 51: 1738–1740, 1991

    Google Scholar 

  106. Plantefaber LC, Hynes RO: Changes in integrin receptors on oncogenically transformed cells. Cell 56: 281–290, 1989

    Google Scholar 

  107. Peltonen JP, Larjava H, Jaakkola S, Gralnick H, Akiyama SK, Yamada SS, Yamada KM, Uitto J: Localization of integrin receptors for fibronectin, collagen, and laminin in human skin variable expression in basal and squamous cell carcinomas. J Clin Invest 84: 1916–1923, 1989

    Google Scholar 

  108. Koretz K, Schlag P, Boumsell L, Möller P: Expression of VLA-α2, VLA-α6, and VLA-β1 chains in normal musoca and adenomas of the colon, and in colon carcinomas and their liver metastases. Am J Pathol 138: 741–750, 1991

    Google Scholar 

  109. Pignatelli M, Smith MEF, Bodmer WF: Low expression of collagen receptors in moderate and poorly differentiated colorectal adenocarcinomas. Br J Cancer 61: 636–638, 1990

    Google Scholar 

  110. Korhonen M, Laitinen L, Ylänne J, Koukoulis GK, Quaranta V, Juusela H, Gould VE, Virtanen I: Integrin distribution in renal cell carcinomas of various grades of malignancy. Am J Pathol 141: 1161–1171, 1992

    Google Scholar 

  111. Kirchhofer D, Languino LR, Ruoslahti E, Pierschbacher MD: α2β1 integrins from different cell types show different binding specificities. J Biol Chem 265: 615–618, 1990

    Google Scholar 

  112. Lotz MM, Korzelius CA, Mercurio AM: Human colon carcinoma cells use multiple receptors to adhere to laminin: involvement of α6β4 and α2β1 integrins. Cell Regul 1: 249–257, 1990

    Google Scholar 

  113. Elices MJ, Urry LA, Hemler ME: Receptor functions for the integrin VLA-3: fibronectin, collagen, and laminin binding are differentially influenced by ARG-GLY-ASP peptide and by divalent cations. J Cell Biol 112: 169–181, 1991

    Google Scholar 

  114. Shimizu Y, van Seventer GA, Horgan KJ, Shaw S: Regulated expression and binding of three VLA(β1) integrin receptors on T cells. Nature 345: 250–253, 1990

    Google Scholar 

  115. Hemler ME, Crouse C, Sonnenberg A: Association of the VLA α6 subunit with a novel protein a possible alternative to the common VLA β1 subunit on certain cell lines. J Biol Chem 264: 6529–6535, 1989

    Google Scholar 

  116. Pignatelli M, Hanby AM, Stamp WH: Low expression of β1, α2 and α3 subunits of VLA integrins in malignant mammary tumours. J Pathol 165: 25–32, 1991

    Google Scholar 

  117. Zutter MM, Mazoujian G, Santoro SA: Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am J Pathol 137: 863–870, 1990

    Google Scholar 

  118. Pignatelli M, Cardillo MR, Hanby A, Stamp GWH: Integrins and their accessory adhesion molecules in mammary carcinomas: loss of polarization in poorly differentiated tumors. Hum Pathol 23: 1159–1166, 1992

    Google Scholar 

  119. D'Ardenne AJ, Richman PI, Horton MA, McAuly AE, Jordan S: Co-ordinate expression of the alpha-6-integrin laminin receptor sub-unit and laminin in breast cancer. J Pathol 165: 213–220, 1991

    Google Scholar 

  120. Lampugnani MG, Resnati M, Dejana E, Marchisio PC: The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol 112: 479–490, 1991

    Google Scholar 

  121. Roos E, Roossien FF: Involvement of leukocyte functionassociated antigen-1 (LAF-1) in the invasion of hepatocyte cultures by lymphoma and T-cell hybridoma cells. J Cell Biol 105: 553–559, 1987

    Google Scholar 

  122. Roossien FF, de Rijk D, Bikker A, Roos E: Involvement of LAF-1 in lymphoma invasion and metastasis demonstrated with LAF-1-deficient mutants. J Cell Biol 108: 1979–1985, 1989

    Google Scholar 

  123. Harning R, Myers C, Merluzzi VJ: Monoclonal antibodies to lymphocyte function-associated antigen-1 inhibit invasion of human lymphoma and metastasis of murine lymphoma. Clin Exp Metastasis 11: 337–342, 1993

    Google Scholar 

  124. Gasic GJ, Tuszynski GP, Gorelik E: Interaction of the hemostatic and immune systems in the metastatic spread of tumor cells. Int Rev Exp Pathol 29: 173–212, 1986

    Google Scholar 

  125. Gasic GJ, Gasic TB, Stewart CC: Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA 61: 46–52, 1968

    Google Scholar 

  126. Pearlstein E, Ambrogio C, Karpatkin S: Effect of antiplatelet antibody on the development of pulmonary metastases following injection of CT26 colon adenocarcinoma, Lewis lung carcinoma, and B16 amelanotic melanoma tumor cell into mice. Cancer Res 44: 3884–3887, 1984

    Google Scholar 

  127. Ugen KE, Mahalingam M, Klein PA, Kao K-J: Inhibition of tumor cell-induced platelet aggregation and experimental tumor metastasis by the synthetic Gly-Arg-Gly-Asp-Ser peptide. J Natl Cancer Inst 80: 1461–1466, 1988

    Google Scholar 

  128. Menter DG, Sloane BF, Steinert BW, Onoda J, Craig R, Harkins C, Taylor JD, Honn KV: Platelet enhancement of tumor cell adhesion to subendothelial matrix: role of platelet cytoskeleton and platelet membrane. J Natl Cancer Inst 79: 1077–1090, 1987

    Google Scholar 

  129. Schneider MR, Schirner M: Antimetastatic prostacyclin analogs. Drug Fut 18: 29–48, 1993

    Google Scholar 

  130. McCulloch P, George WD: Warfarin inhibits metastasis of Mtln 3 rat mammary carcinoma without affecting primary tumour growth. Br J Cancer 59: 179–183, 1989

    Google Scholar 

  131. Moncada S, Korbut R, Bunting S, Vane JR: Prostacyclin is a circulating hormone. Nature 273: 767–768, 1978

    Google Scholar 

  132. Boukerche H, Berthier-Vergnes O, Tabone E, Doré J-F, Leung LLK, McGregor JL: Platelet-melanoma cell interaction is mediated by the glycoprotein IIb-IIIa complex. Blood 74: 658–663, 1989

    Google Scholar 

  133. McGregor BC, McGregor JL, Weiss LM, Wood GS, Hu C-H, Boukerche H, Warnke RA: Presence of cytoadhesins (IIb-IIIa-like glycoproteins) on human metastatic melanomas but not on benign melanocytes. Am J Clin Pathol 92: 495–499, 1989

    Google Scholar 

  134. Boukerche H, Berthier-Vergnes O, Bailly M, Doré JF, Leung LLK, McGregor JL: A monoclonal antibody (LYP-18) directed against the blood platelet glycoprotein IIb/IIIa complex inhibits human melanoma growthin vivo. Blood 74: 909–912, 1989

    Google Scholar 

  135. Albelda SM, Mette SA, Elder DE, Stewart R, Damjanovich L, Herlyn M, Buck CA: Integrin distribution in malignant melanoma: association of the β3 subunit with tumor progression. Cancer Res 50: 6757–6764, 1990

    Google Scholar 

  136. Nip J, Shibata H, Loskutoff DJ, Cheresh DA, Brodt P: Human melanoma cells derived from lymphatic metastases use integrin αvβ3 to adhere to lymph node vitronectin. J Clin Invest 90: 1406–1413, 1992

    Google Scholar 

  137. Kennel SJ, Foote LJ, Falcioni R, Sonnenberg A, Stringer CD, Crouse C, Hemler ME: Analysis of the tumor-associated antigen TSP-180 identity with α6β4 in the integrin superfamily. J Biol Chem 264: 15515–15521, 1989

    Google Scholar 

  138. Falcioni R, Kennel SJ, Giacomini P, Sacchi A: Expression of tumor antigen correlated with metastatic potential of Lewis lung carcinoma and B16 melanoma clones in mice. Cancer Res 46: 5772–5778, 1986

    Google Scholar 

  139. Falcioni R, Sacchi A, Resau J, Kennel SJ: Monoclonal antibody to human carcinoma-associated protein complex: quantitation in normal and tumor tissue. Cancer Res 48: 816–821, 1988

    Google Scholar 

  140. Kimmel KA, Carey TE: Altered expression in squamous carcinoma cells of an orientation restricted epithelial antigen detected by monoclonal antibody A9. Cancer Res 46: 3614–3623, 1986

    Google Scholar 

  141. Costantini RM, Falcioni R, Battista P, Zupi G, Kennel SJ, Colasante A, Venturo I, Curcio CG, Sacchi A: Integrin (α64) expression in human lung cancer as monitored by specific monoclonal antibodies. Cancer Res 50: 6107–6112, 1990

    Google Scholar 

  142. Wolf GT, Carey TE, Schmaltz SP, McClatchey KD, Poore J, Glaser L, Hayashida DJS, Hsu S: Altered antigen expression predicts outcome in squamous cell carcinoma of the head and neck. J Natl Cancer Inst 82: 1566–1572, 1990

    Google Scholar 

  143. Kemperman H, Wijnands Y, de Rijk D, Roos E: The integrin α6β4 on TA3/Ha mammary carcinoma cells is involved in adhesion to hepatocytes. Cancer Res 53: 3611–3617, 1993

    Google Scholar 

  144. Roos E, Dingemans KP, van de Pavert IV, van den Bergh-Weerman MA: Mammary-carcinoma cells in mouse liver: infiltration of liver tissue and interaction with Kupffer cells. Br J Cancer 38: 88–99, 1978

    Google Scholar 

  145. Natali PG, Nicotra MR, Botti C, Mottolese M, Bigotti A, Segatto O: Changes in expression of α6/β4 integrin heterodimer in primary and metastatic breast cancer. Br J Cancer 318-322, 1992

  146. Sonnenberg A, Calafat J, Janssen H, Daams H, van der Raaij-Helmer LMH, Falconi R, Kennel SJ, Aplin JD, Baker J, Loizidou M, Garrod D: Integrin α64 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 113: 907–917, 1991

    Google Scholar 

  147. Waes CV, Kozarsky KF, Warren AB, Kidd L, Paugh D, Liebert M, Carey TE: The A9 antigen associated with aggressive human squamous carcinoma is structurally and functionally similar to the newly defined integrin α6β4. Cancer Res 51: 2395–2402, 1991

    Google Scholar 

  148. Hunt G: The role of laminin in cancer invasion and metastasis. Exp Cell Biol 57: 165–176, 1989

    Google Scholar 

  149. Timpl R, Rohde H, Robey PG, Rennard SI, Foidart J-M, Martin GR: Laminin - a glycoprotein from basement membrane. J Biol Chem 254: 9933–9937, 1979

    Google Scholar 

  150. Albini A, Aukerman SL, Ogle RC, Noonan DM, Fridman R, Martin GR, Fidler IJ: Thein vitro invasiveness and interactions with laminin of K-1735 melanoma cells evidence for different laminin-binding affinities in high and low metastatic variants. Clin Exp Metastasis 7: 437–451, 1989

    Google Scholar 

  151. Wewer UM, Taraboletti G, Sobel ME, Albrechtsen R, Liotta LA: Role of laminin receptor in tumor cell migration. Cancer Res 47: 5691–5698, 1987

    Google Scholar 

  152. Cioce V, Castronovo V, Shmookler BM, Garbisa S, Grigioni WF, Liotta LA, Sobel ME: Increased expression of the laminin receptor in human colon cancer. J Natl Cancer Inst 83: 29–36, 1991

    Google Scholar 

  153. Satoh S, Narumi K, Isemura M, Sakai T, Abe T, Matsushima K, Okuda K, Motomiya M: Increased expression of the 67 kDa-laminin receptor gene in human small cell lung cancer. Biochem Biophys Res Comm 182: 746–752, 1992

    Google Scholar 

  154. Aliño SF, Unda FJ, Pérez-Yarza G: Laminin surface binding sites and metastatic potential of 3LL tumor cells increased by indomethacin. Biochem Biophys Res Comm 167: 731–738, 1990

    Google Scholar 

  155. Graf J, Iwamoto Y, Sasaki M, Martin GR, Kleinman HK, Robey FA, Yamada Y: Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell 48: 989–996, 1987

    Google Scholar 

  156. Iwamoto Y, Robey FA, Graf J, Sasaki M, Kleinman HK, Yamada Y, Martin GR: YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 238: 1132–1134, 1987

    Google Scholar 

  157. Nomizu M, Yamamura K, Kleinman HK, Yamada Y: Multimeric forms of Tyr-Ile-Gly-Ser-Arg (YIGSR) peptide enhance the inhibition of tumor growth and metastasis. Cancer Res 53: 3459–3461, 1993

    Google Scholar 

  158. Castronovo V, Colin C, Claysmith AP, Chen PHS, Lifrange E, Lambotte R, Krutzsch H, Liotta LA, Sobel ME: Immunodetection of the metastasis-associated laminin receptor in human breast cancer cells obtained by fine-needle aspiration biopsy. Am J Pathol 137: 1373–1381, 1990

    Google Scholar 

  159. Martignone S, Pellegrini R, Villa E, Tandon NN, Mastroianni A, Tagliabue E, Ménard S, Colnaghi MI: Characterization of two monoclonal antibodies directed against the 67 kDa high affinity laminin receptor and application for the study of breast carcinoma progression. Clin Exp Metastasis 10: 379–386, 1992

    Google Scholar 

  160. Liotta LA, Rao CN: Tumor invasion and metastasis. Monogr Pathol 27: 183–192, 1986

    Google Scholar 

  161. Shi YE, Torri J, Yieh L, Sobel ME, Yamada Y, Lippman ME, Dickson RB, Thompson EW: Expression of 67 kDa laminin receptor in human breast cancer cells: regulation by progestins. Clin Exp Metastasis 11: 251–261, 1993

    Google Scholar 

  162. Castronovo V, Taraboletti G, Liotta LA, Sobel ME: Modulation of laminin receptor expression by estrogen and progestins in human breast cancer cell lines. J Natl Cancer Inst 81: 781–788, 1989

    Google Scholar 

  163. Hrushesky WJM: Breast cancer and the menstrual cycle. J Surg Oncol 53: 1–3, 1993

    Google Scholar 

  164. Martignone S, Ménard S, Bufalino R, Cascinelli N, Pellegrini R, Tagliabue E, Andreola S, Rilke F, Colnaghi MI: Prognostic significance of the 67-kilodalton laminin receptor expression in human breast carcinomas. J Natl Cancer Inst 85: 398–402, 1993

    Google Scholar 

  165. Marques LA, Franco ELF, Torloni H, Brentani MM, da Silva-Neto JB, Brentani RR: Independent prognostic values of laminin receptor expression in breast cancer survival. Cancer Res 50: 1479–1483, 1990

    Google Scholar 

  166. Daidone MG, Silvestrini R, D'Errico A, Di Fronzo G, Benini E, Mancini AM, Garbisa S, Liotta LA, Grigioni WF: Laminin receptors, collagenase IV and prognosis in nodenegative breast cancers. Int J Cancer 48: 529–532, 1991

    Google Scholar 

  167. Malinoff HL, McCoy Jr JP, Varani J, Wicha MS: Metastatic potential of murine fibrosarcoma cells is influenced by cell surface laminin. Int J Cancer 33: 651–655, 1984

    Google Scholar 

  168. Terranova VP, Williams JE, Liotta LA, Martin GR: Modulation of the metastatic activity of melanoma cells by laminin and fibronectin. Science 226: 982–985, 1984

    Google Scholar 

  169. Kanemoto T, Reich R, Royce L, Greatorex D, Adler SH, Shiraishi N, Martin GR, Yamada Y, Kleinman HK: Identification of an amino acid sequence from the laminin A chain that stimulates metastasis and collagenase IV production. Proc Natl Acad Sci USA 87: 2279–2283, 1990

    Google Scholar 

  170. Sakamoto N, Iwahana M, Tanaka NG, Osada Y: Inhibition of angiogenesis and tumor growth by a synthetic laminin peptide, CDPGYIGSR-NH2. Cancer Res 51: 903–906, 1991

    Google Scholar 

  171. Kleinman HK, Cannon FB, Laurie GW, Hassell JR, Aumailley M, Terranova VP, Martin GR, DuBois-Dalcq M: Biological activities of laminin. J Cell Biochem 27: 317–325, 1985

    Google Scholar 

  172. Turpeenniemi-Hujanen T, Thorgeirsson UP, Rao CN, Liotta LA: Laminin increases the release of type IV collagenase from malignant cells. J Biol Chem 261: 1883–1889, 1986

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maemura, M., Dickson, R.B. Are cellular adhesion molecules involved in the metastasis of breast cancer?. Breast Cancer Res Tr 32, 239–260 (1994). https://doi.org/10.1007/BF00666002

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00666002

Key words

Navigation