Skip to main content
SpringerLink
Log in

Review: Biologic heterogeneity of cancer metastases

  • 9th San Antonio Breast Cancer Symposium-Plenary Lecture
  • 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

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Fidler IJ: The evolution of biological heterogeneity in metastatic neoplasms. In: Nicolson GL, Milas L (eds): Cancer Invasion and Metastasis: Biologic and Therapeutic Aspects. Raven Press, New York, 1984, pp 5–30

    Google Scholar 

  2. Sugarbaker EV: Cancer metastasis: A product of tumorhost interactions. Curr Probl Cancer 3: 1–59, 1979

    Google Scholar 

  3. Fidler IJ, Poste G: The cellular heterogeneity of malignant neoplasms: Implications for adjuvant chemotherapy. Semin Oncol 12: 207–221, 1985

    PubMed  Google Scholar 

  4. Fidler IJ, Hart IR: Biological diversity in metastatic neoplasms: Origins and implications. Scence 217: 998–1003, 1982

    Google Scholar 

  5. Heppner G: Tumor heterogeneity. Cancer 214: 2259, 1984

    Google Scholar 

  6. Poste G, Fidler IJ: The pathogenesis of cancer metastasis. Nature 283: 139–146, 1979

    Google Scholar 

  7. Nicolson GL, Poste G: Tumor cell diversity and host responses in cancer metastasis. Curr Probl Cancer 7: 4–83, 1982

    PubMed  Google Scholar 

  8. Dexter D, Calabresi P: Intraneoplastic diversity. Biochem Biophys Acta 695:97–112, 1982

    PubMed  Google Scholar 

  9. Paget S: The distribution of secondary growths in cancer of the breast. Lancet 1:571–573, 1889

    Google Scholar 

  10. Hart IR: ‘Seed and Soil’ revisited: Mechanisms of sitespecific metastasis. Cancer Met Rev 1: 5–17, 1982

    Google Scholar 

  11. Nicolson GL: Organ colonization and the cell surface properties of malignant cells. Biochim Biophys Acta 695: 113–176, 1982

    PubMed  Google Scholar 

  12. Nicolson GL, Custead SE: Tumor metastasis is not due to adaption of cells to a new organ environment. Science 215: 176–178, 1982

    PubMed  Google Scholar 

  13. Poste G: Experimental systems for analysis of the malignant phenotype. Cancer Met Rev 1: 141–199, 1982

    Google Scholar 

  14. Tarin D, Price JE, Kettlewell MGW, Souter RG, Vass ACR, Crossley B: Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunt. Cancer Res 44: 3584–3592, 1984

    PubMed  Google Scholar 

  15. Fidler IJ: Metastasis: Quantitative analysis of distribution and fate of tumor emboli labeled with125I-5-iodo-2′-deox-yuridine. JNCI 45: 773–782, 1970

    PubMed  Google Scholar 

  16. Hart IR, Fidler IJ: Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res 40: 2281–2287, 1980

    PubMed  Google Scholar 

  17. Folkman J: Angiogenesis: Initiation and modulation. In Nicolson GL, Milas L (eds): Cancer Invasion and Metastasis: Biologic and Therapeutic Aspects. Raven Press, New York, 1984, pp 201–209

    Google Scholar 

  18. Gabbert H: Mechanisms of tumor invasion: Evidence fromin vivo observations. Cancer Met Rev 4: 293–319, 1985

    Google Scholar 

  19. Jones PA, DeClerck YA: Extracellular matrix destruction by invasive tumor cells. Cancer Met Rev 1: 289–319, 1982

    Google Scholar 

  20. Liotta LA: Tumor invasion and metastases — Role of the extracellular matrix: Rhoads Memorial Award Lecture. Cancer Res 46: 1–7, 1986

    PubMed  Google Scholar 

  21. Liotta LA, Thorgeirsson UP, Gabrisa S: Role of collagenases in tumor cell invasion. Cancer Met Rev 1: 277–288, 1982

    Google Scholar 

  22. Tarin D: Investigations of the mechanisms of metastatic spread of naturally occurring neoplasms. Cancer Met Rev 1: 215–226, 1982

    Google Scholar 

  23. Fisher B, Fisher ER: The interrelationship of hematogenous and lymphatic tumor cell dissemination. Surg Gynecol Obstet 122: 791–798, 1966

    PubMed  Google Scholar 

  24. Fidler IJ, Gersten DM, Kripke ML: Influence of immune status on the metastasis of three murine fibrosarcomas of different immunogenicities. Cancer Res 39: 3816–3821, 1979

    PubMed  Google Scholar 

  25. Hanna N, Fidler IJ: The role of natural killer cells in the destruction of circulating tumor emboli. J Natl Cancer Inst 65: 801–809, 1980

    PubMed  Google Scholar 

  26. Hanna N: Role of natural killer cells in control of cancer metastasis. Cancer Met Rev 1: 45–65, 1981

    Google Scholar 

  27. Fidler IJ: Macrophages and metastasis — A biological approach to cancer therapy: Presidential address. Cancer Res 45: 4714–4725, 1985

    PubMed  Google Scholar 

  28. Turley EA: Proteoglycans and cell adhesion: Their putative role during tumorigenesis. Cancer Met Res 3: 325–340, 1985

    Google Scholar 

  29. Nicolson GL: Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayer. J Histochem Cytochem 30: 214–220, 1982

    PubMed  Google Scholar 

  30. Kramer RH, Gonzalez R, Nicolson GL: Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells. Int J Cancer 26: 639–645, 1980

    PubMed  Google Scholar 

  31. Butler T, Gullino P: Quantitation of cell-shedding into efferent blood of mammary adenocarcinoma. Cancer Res 35: 512–517, 1975

    PubMed  Google Scholar 

  32. Weiss L: A pathobiologic overview of metastasis. Semin Oncol 4: 5–17, 1977

    PubMed  Google Scholar 

  33. Fidler IJ: Selection of successive tumor lines for metastasis. Nature (New Biol) 242: 148–149, 1973

    Google Scholar 

  34. Talmadge JE, Fidler IJ: Cancer metastasis is selective or random depending on the parent tumour population. Nature 27: 593–594, 1982

    Google Scholar 

  35. Fidler IJ, Kripke ML: Metastasis results from pre-existing variant cells within a malignant tumor. Science 197: 893–895, 1977

    PubMed  Google Scholar 

  36. Luria SE, Delbruck M: Mutations of bacteria from virus sensitivity to virus resistant. Genetics 28: 491–511, 1943

    Google Scholar 

  37. Fidler IJ: Rationale and methods for the use of nude mice to study the biology and therapy of human cancer metastasis. Cancer Met Rev 5: 29–49, 1986

    Google Scholar 

  38. Talmadge JE, Wolman SR, Fidler IJ: Evidence for the clonal origin of spontaneous metastases. Science 217: 361–363, 1982

    PubMed  Google Scholar 

  39. Poste G, Tzeng J, Doll J, Greig R, Rieman D, and Zeidman I: Evolution of tumor cell heterogeneity during progressive growth of individual lung metastases. Proc Natl Acad Sci USA 79: 6574–6578

  40. Fidler IJ, Talmadge JE: Evidence that intravenously derived murine pulmonary melanoma metastases can originate from the expansion of a single tumor cell. Cancer Res 46: 5167–5171, 1986

    PubMed  Google Scholar 

  41. Fidler IJ: The relationship of embolic homeogeneity, number, size and viability to the incidence of experimental metastasis. Eur J Cancer 9: 233–227, 1973

    PubMed  Google Scholar 

  42. Liotta LA, Kleinerman J, Saidel G: The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res 36: 889–894, 1976

    PubMed  Google Scholar 

  43. Foulds L: The experimental study of tumor progression. A review. Cancer Res: 14: 327–339

  44. Klein G, Klein E: Immune surveillance against virus-induced tumors and nonrejectability of spontaneous tumors: Contrasting consequences of host-versus-tumor evolution. Proc Natl Acad Sci USA 74: 2121–2125

  45. Nowell PC: The clonal evolution of tumor cell populations: Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression. Science 194: 23–29, 1976

    PubMed  Google Scholar 

  46. Prehn RT: Tumor progression and homeostasis. Adv Cancer Res 23: 203–236, 1976

    PubMed  Google Scholar 

  47. Wolman SR: Karyotypic progression in human tumors. Cancer Met Rev 2: 257–293, 1983

    Google Scholar 

  48. Yunis JJ: The chromosomal basis of human neoplasia. Science 221: 227–236, 1983

    PubMed  Google Scholar 

  49. Cifone MA, Fidler IJ: Increasing metastatic potential is associated with increasing genetic instability of clones isolated from murine neoplasms. Proc Natl Acad Sci USA 78: 6949–6952, 1982

    Google Scholar 

  50. Yamashina K, Heppner GH: Correlation of frequency of induced mutation and metastatic potential in tumor cell lines from a single mouse mammary tumor. Cancer Res 45: 4015–4019, 1985

    PubMed  Google Scholar 

  51. Boon T, Kellerman O: Rejection by syngeneic mice of cell variants obtained by mutagenesis of a malignant teratocarcinoma cell line. Proc Natl Acad Sci USA 74: 272–275, 1977

    PubMed  Google Scholar 

  52. Boon T, Van Snick J, Pel AV, Uyttenhove C, Marchand M: Immunogenic variants obtained by mutagenesis of mouse mastocytoma P815. II. T lymphocyte mediated cytolysis. J Exp Med 152: 1184–1193, 1980

    PubMed  Google Scholar 

  53. Fisher MS, Cifone MA: Enhanced metastatic potential of murine fibrosarcoma treatedin vitro with ultraviolet radiation. Cancer Res 41: 3018–3023

  54. Frost P, Kerbel RS: On a possible epigenetic mechanism(s) of tumor cell heterogeneity: The role of DNA methylation. Cancer Met Rev 2: 375–378, 1983

    Google Scholar 

  55. Frost P, Liteplo RG, Donaghue TP, Kerbel RS: Selection of strongly immunogenic ‘Tum’ variants from tumors at high frequency using 5-azacytidine. J Exp Med 159: 1491–1501, 1984

    PubMed  Google Scholar 

  56. Olsson L, Forchhammer J: Induction of the metastatic phenotype in a mouse tumor model by 5-azacytidine, and characterization of an antigen associated with metastatic activity. Proc Natl Acad Sci USA 81: 3389–3393, 1984

    PubMed  Google Scholar 

  57. Ormerod EJ, Everett CA, Hart IR: Enhanced experimental metastatic capacity of a human tumor line following treatment with 5-azacytidine. Cancer Res 46: 884–890, 1986

    PubMed  Google Scholar 

  58. Lavia P, Ferraro M, Micheli A, Oliveri G: Effect of 5-azacytidine (5-azaC) on the induction of chromatid aberrations (CA) and sister-chromatid exchanges (SCE). Mutat Res 149: 463–467

  59. Poste G, Nicolson GL: Modification of the arrest of metastatic tumor cells in the microcirculation after treatment with plasma membrane vesicles from highly metastatic cells. Proc Natl Acad Sci USA 77: 399–403, 1980

    PubMed  Google Scholar 

  60. Reif A: Evidence for organ specificity of defense against tumors. In: Water H (ed): The Handbook of Cancer Immunology, vol 1, Garland STPM Press, New York, 1978, pp 174–240

    Google Scholar 

  61. Ioachim HL, Pearse A, Keller SE: Role of immune mechanisms in metastatic patterns of hemopoietic tumors in rats. Cancer Res 36: 2854–2862, 1976

    PubMed  Google Scholar 

  62. Bellamy D, Hinsull SM: Influence of lodgement site on the proliferation of metastases of Walker 256 carcinoma in the rat. Br J Cancer 37: 81–85, 1978

    PubMed  Google Scholar 

  63. Brambilla C, Delena M, Rossi A, Valagussa P, Bonadonna G: Response and survival in advanced breast cancer after two non-cross resistant drug combinations. Br Med J 1: 801–804, 1976

    PubMed  Google Scholar 

  64. Canellos GP, Devita VT, Gold GL, Chabner BA, Schein PS, Young RC: Cyclical combination chemotherapy for advanced breast carcinoma. Br Med J 1: 218–220, 1974

    PubMed  Google Scholar 

  65. Slack NH, Bross JBJ: The influence of site of metastasis on tumor growth and response to chemotherapy. Br J Cancer 32: 78–82, 1975

    PubMed  Google Scholar 

  66. Donelli MG, Rosso R, Garattino S: Selective chemotherapy in relation to the site of tumor transplantation. Int J Cancer 2: 421–424, 1967

    PubMed  Google Scholar 

  67. Donelli MG, Colombo T, Broggini M, Garattini S: Differential distribution of antitumor agents in primary and secondary tumors. Cancer Treat Rep 61: 1319–1324, 1977

    PubMed  Google Scholar 

  68. Suzuki M, Hori K, Abe I, Saito S, Sato H: A new approach to cancer chemotherapy: Selective enhancement of tumor blood flow with angiotensin II. JNCI 67: 663–669, 1981

    PubMed  Google Scholar 

  69. Baylin SB, Weisburger WR, Eggleston JC, Mendelsohn G, Beaven MA, Abeloff MD, Ettinger DS: Variable content of histaminase, L-Dopa decarboxylase and calcitonin in small-cell carcinoma of the lung. Biologic and clinical implications. N Engl J Med 299: 105–110, 1978

    PubMed  Google Scholar 

  70. Hockey MS, Stokes HJ, Thompson H, Woodhouse CS, Macdonald F, Fielding JWL, Ford CHJ: Carcinoembryonic antigen (CEA) expression and heterogeneity in primary adn autologous metastatic gastric tumours demonstrated by a monoclonal antibody. Br J Cancer 49: 129–133, 1984

    PubMed  Google Scholar 

  71. Gold DV, Shochat D, Primus FJ, Dexter DL, Calabresi P, Goldenberg DM: Differential expression of tumor-associated antigens in human colon carcinomas xenografted into nude mice. JNCI 71: 117–124, 1983

    PubMed  Google Scholar 

  72. Edwards PAW: Heterogeneous expression of cell surface antigens in normal epithelia and their tumors, revealed by monoclonal antibodies. Br J Cancer 51: 149–160, 1985

    PubMed  Google Scholar 

  73. Czerniak B, Darzynkiewicz Z, Staiano-Coico L, Herz F, Koss LG: Expression of Ca antigen in relation to the cell cycle in cultured human tumor cells. Cancer Res 44: 4342–4346, 1984

    PubMed  Google Scholar 

  74. Tanigawa N, Mizuno Y, Hashimura T, Hondo K, Satomura K, Hikasa Y, Niwa O, Sugahara T, Yoshida O, Kern DH, Morton DL: Comparison of drug sensitivity among tumor cells within a tumor between primary tumor and metastases, and between different metastases in the human tumor colony-forming assay. Cancer Res 44: 2309–2312, 1984

    PubMed  Google Scholar 

  75. Trope C, Hakansson L, Dencker H: Heterogeneity of human adenocarcinomas of the colon and the stomach as regards sensitivity to cytostatic drugs. Neoplasma 22: 423–430, 1975

    PubMed  Google Scholar 

  76. Abe I, Suzuki M, Hori K, Saito S, Sato H: Some aspects of size-dependent differential drug response in primary and metastatic tumors. Cancer Met Rev 4: 27–40, 1985

    Google Scholar 

  77. Donelli MG, Colombo T, Broggini M, Garattinni S: Differential distribution of antitumor agents in primary and secondary tumors. Cancer Treat Rep 61: 1319–1324, 1977

    PubMed  Google Scholar 

  78. Fugmann RA, Anderson JC, Stoli R, Martin DS: Comparison of adjuvant chemotherapeutic activity against primary and metastatic spontaneous murine tumors. Cancer Res 37: 496–500, 1977

    PubMed  Google Scholar 

  79. Smith KA, Begg AC, Denekamp J: Differences in chemosensitivity between subcutaneous and pulmonary tumours. Eur J Cancer Clin Oncol 21: 249–256, 1985

    PubMed  Google Scholar 

  80. Tsuruo T, Fidler IJ: Differences in drug sensitivity among tumor cells from parental tumors, selected variants, and spontaneous metastases. Cancer Res 41: 3058–3064, 1981

    PubMed  Google Scholar 

  81. Weichselbaum RR, Dahlberg W, Little JB: Inherently radioresistant cells exist in some human tumors. Proc Natl Acad Sci USA 82: 4732–4735, 1985

    PubMed  Google Scholar 

  82. Welch DR, Milas L, Tomasovic SP, Nicolson GL: Heterogeneous response and clonal drift of sensitivities of metastatic 13762NF mammary adenocarcinoma clones to γ-radiationin vitro. Cancer Res 43: 6–10, 1983

    PubMed  Google Scholar 

  83. Morstyn G, Russo A, Carney DN, Karawya E, Wilson SH, Mitchell JB: Heterogeneity in the radiation survival curves and biochemical properties of human lung cancer cell lines. JNCI 73: 801–807, 1984

    PubMed  Google Scholar 

  84. Fidler IJ, Hart IR: Biological and experimental consequence of the zonal composition of solid tumors. Cancer Res 41: 3266–3267, 1981

    PubMed  Google Scholar 

  85. Bradley EC, Issell BF, Hellman R: The human tumor colony-forming chemosensitivity assay: A biological and clinical review. Investigational New Drugs 2: 59–70, 1984

    PubMed  Google Scholar 

  86. Bertelsen CA, Sondak VK, Mann BD: Chemosensitivity testing of human solid tumors. A review of 1582 assays with 258 clinical correlations. Cancer 53: 1240–1245, 1984

    PubMed  Google Scholar 

  87. Rosenberg S: Lymphokine-activated killer cells: A new approach to immunotherapy of cancer. JNCI 75: 595–603, 1985

    PubMed  Google Scholar 

  88. Cheever MA, Greenberg PD, Fefer A: Potential for specific cancer therapy with immune T lymphocytes. J Biol Resp Mod 3: 113–127, 1984

    Google Scholar 

  89. Oldham RK: Biologicals and biological response modifiers: Design of clinical trials. J Biol Resp Mod 4: 117–128, 1985

    Google Scholar 

  90. Miller FR: Intratumor immunologic heterogeneity. Cancer Met Rev 1: 319–334, 1982

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology, The University of Texas M.D. Anderson Hospital and Tumor Institute at Houston, 1515 Holcombe Boulevard, 77030, Houston, TX, USA

    Isaiah J. Fidler

Authors
  1. Isaiah J. Fidler
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fidler, I.J. Review: Biologic heterogeneity of cancer metastases. Breast Cancer Res Tr 9, 17–26 (1987). https://doi.org/10.1007/BF01806690

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01806690

Keywords

Search

Navigation