Summary
Much of the effort of this laboratory in recent years has been directed towards developing a reliable protocol for the experimental analysis of factors affecting metastatic spread from naturally occurring (i.e. not transplanted) neoplasms. The objective of this has been to develop a data base on the variations in metastatic behaviour between spontaneously arising neoplasms and to examine the tumour-specific and host-specific mechanisms accounting for this. This paper details the experimental technique and underlying conceptual basis which have been developed for reproducible investigations of this subject. It also reviews our conclusions from such work on the role in metastatic spread of tumour cell surface properties, collagenase secretion, microenvironmental effects on tumour cell growth in various organs, tumour macrophage content, and degree of cell shedding into the bloodstream.
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Tarin D, Price JE: Metastatic colonization potential of primary tumour cells in mice. Br J Cancer (39): 740–754, 1979.
Tarin D, Price JE: Influence of microenvironment and vascular anatomy on ‘metastatic’ colonization potential of mammary tumors. Cancer Res (41): 3604–3609, 1981.
Price JE, Carr D, Jones LD, Messer P, Tarin D: Experimental analysis of factors affecting metastatic spread using naturally-occurring tumours. Invasion Metastasis (in press) 1982.
Price JE, Tarin D: Retention of ‘metastatic’ colonisation potential by cells of spontaneous primary tumours after cryopreservation. Br J Cancer (45): 790–793, 1982.
Heston WE, Vlahakis G: C3h-Avy—a high hepatoma and high mammary tumor strain of mice. J Natl Cancer Inst (40): 1161–1166, 1968.
Vlahakis G, Heston WE, Smith GH: Strain C3H-Avymice: ninety per cent incidence of mammary tumors transmitted by either parent. Science (179): 185–187, 1970.
Festing MFW: Inbred Strains in Biomedical Research. Macmillan Press, London, 1979.
Fidler IJ: Selection of successive tumour lines for metastasis. Nature New Biol (242): 148–149, 1973.
Fidler IJ: Biological behaviour of malignant melanoma cells correlated to their survival in vivo. Cancer Res (35): 218–224, 1975.
Fidler IJ: Patterns of tumour cell arrest and development. In: Weiss L (ed) Fundamental aspects of metastasis. North-Holland, Amsterdam, 1976, pp 275–289.
Fidler IJ: Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res (38): 2651–2660, 1978.
Kripke ML, Gruys E, Fidler IJ: Metastatic heterogeneity of cells rom an ultraviolet light-induced murine fibrosarcoma of recent origin. Cancer Res (38): 2962–2967, 1978.
Paget S: The distribution of secondary growth in cancer of the breast. Lancet (1): 571–573, 1889.
Hart IR, Fidler IJ: Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res (40): 2281–2287, 1980.
Kinsey DL: An experimental study of preferential metastasis. Cancer (13): 674–676, 1960.
Sugarbaker EV, Cohen AM, Ketcham AS: Do metastases metastasize? Ann Surg (174): 161–166, 1971.
Fidler IJ, Nicolson GL: Brief communication: organ selectivity for implantation survival and growth of B16 melanoma variant tumor lines. J Natl Cancer Inst (57): 1199–1202, 1976.
Tarin D: Stromal factors relating to invasion and metastatic spread of tumours. In: Stoll BA (ed) New aspects of breast cancer, Vol 4. Systemic control of breast cancer. William Heinemann, London, 1981, pp 21–37.
Bosmann HB, Bieber GF, Brown AE, Case KR, Gersten DM, Kimmerer TW, Lione A: Biochemical parameters correlated with tumour cell implantation. Nature (246): 487–489, 1973.
Rieber M, Rieber MS: Metastatic potential correlates with cell-surface protein alterations in B16 melanoma variants. Nature (293): 74–76, 1981.
Yogeeswaran G, Salk PL: Metastatic potential is positively correlated with cell surface sialylation of cultured murine tumor cell lines. Science (212): 1514–1516, 1981.
Kim U, Baumler A, Carruthers C, Bielat K: Immunological escape mechanism in spontaneously metastasizing mammary tumours. Proc Natl Acad Sci (72): 1012–1016, 1975.
Chatterjee SK, Kim U: Galactosyltransferase activity in metastasizing and nonmetastasizing rat mammary carcinomas and its possible relationship with tumour cell antigen shedding. J Natl Cancer Inst (58): 273–280, 1977.
Poste G, Nicholson GL: Arrest and metastasis of bloodborne tumor cells are modified by fusion of plasma membrane vesicles from highly metastatic cells. Proc Natl Acad Sci (77): 399–403, 1980.
Price JE, Tarin D: Lectin agglutinability of mammary tumours with differing metastatic colonisation potentials. Differentiation (20): 264–269, 1981.
Tarin D: Sequential electron microscopical study of experimental mouse skin carcinogenesis. Int J Cancer (2): 195–211, 1967.
Tarin D: Fine structure of murine mammary tumours: the relationship between epithelium and connective tissue in neoplasms induced by various agents. Br J Cancer (23): 417–425, 1969.
Tarin D: Morphological studies on the mechanism of carcinogenesis. In: Tarin D (ed) Tissue interactions in carcinogenesis. Academic Press, London, 1972, pp 227–289.
Tarin D: Cellular interactions in neoplasia. In: Weiss L (ed) Fundamental aspects of metastasis. North-Holland, Amsterdam, 1976, pp 151–187.
Hashimoto K, Yamanishi Y, Maeyens E, Dabbous MK, Kanzaki T. Collagenolytic activities of squamous-cell carcinoma of skin. Cancer Res (33): 2790–2801, 1973.
Yamanishi Y, Dabbous MK, Hashimoto K: Effect of collagenolytic activity in basal cell epithelioma of the skin on reconstituted collaged and physical properties and kinetics of the crude enzyme. Cancer Res (32): 2551–2560, 1972.
Dresden MH, Heilman A, Schmidt JD: Collagenolytic enzymes in human neoplasms. Cancer Res (32): 993–996, 1972.
Abramson M, Schilling RW, Huang C, Salome RG: Collagenase activity in epidermoid carcinoma of the oral cavity and larynx. Ann Otol Rhinol Laryngol (84): 158–163, 1975.
Tarin D, Hoyt BJ, Evans DJ: Correlation of collagenase secretion with metastatic colonisation potential in naturally-occurring murine mammary tumours. Br J Cancer (in press) 1982.
Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S: Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature (284): 67–68, 1980.
Mareel MM: Recent aspects of tumor invasiveness. Int Rev Exp Pathol (22): 65–129, 1980.
Mareel MM, Brabander MJ: Effect of microtubule inhibitors on malignant invasion in vitro. J Natl Cancer Inst (61): 787–792, 1978.
Hart IR, Raz A, Fidler IJ: Effect of cytoskeleton-disrupting agents on the metastatic behavior of melanoma cells. J Natl Cancer Inst (64): 891–899, 1980.
Hagmar B, Ryd W: Tumor cell locomotion: a factor in metastasis formation? Influence of cytochalasin B on a tumor dissemination pattern. Int J Cancer (19): 576–580, 1977.
Eccles SA, Alexander P: Macrophage content of tumours in relation to metastatic spread and host immune reaction. Nature (250): 667–669, 1974.
Wood GW, Gillespie GY: Studies on the role of macrophages in regulation of growth and metastasis of murine chemically-induced fibrosarcomas. Int J Cancer (16): 1022–1029, 1975.
Nash JRG, Price JE, Tarin D: Macrophage content and colony-forming potential in mouse mammary carcinomas. Br J Cancer (43): 478–485, 1981.
Dobrossy L, Pavelic ZP, Bernacki RJ: A correlation between cell surface sialyltransferase, sialic acid, and glycosidase activities and the implantability of B16 murine melanoma. Cancer Res (41): 2262–2266, 1981.
Squartini F, Bistocchi M: Bioactivity of C3H and RIII a cell-surface antigen correlated with organ-specific metastasis. Nature (286): 267–269, 1980.
Squartini F, Bistocchi M: Bioactivity of C3H and RIII mammary tumor viruses in virgin female BALB/c mice. J Natl Cancer Inst (58): 1845–1847, 1977.
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Tarin, D. Investigations of the mechanisms of metastatic spread of naturally occurring neoplasms. Cancer Metast Rev 1, 215–225 (1982). https://doi.org/10.1007/BF00046828
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DOI: https://doi.org/10.1007/BF00046828