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Part of the book series: Cancer Growth and Progression ((CAGP,volume 11))

Abstract

The metastatic process is a series of steps – each of which must be completed for the development of a metastatic focus. Some steps consist of stochastic elements; however, overall the process selects for cellular phenotype(s) with metastatic properties from the heterogeneous cellular populations that develop within the primary tumor. Thus, although individual metastases are of clonal origin, different metastatic foci can originate from cellular variants. The development of cellular diversity is not a process unique to tumor cells. Cellular diversity rapidly evolves due to the genetic instability of metastatic cells, the selective pressures of the metastatic process and clinical interventions, and interactions with the microenvironment, including cellular immunity and tissue and organ microenvironments that can facilitate or suppress tumor growth, metastasis, and tumor cell survival. It is the cellular heterogeneity within the primary tumor, between metastatic foci, and within individual metastatic foci that provides a significant challenge for oncologists for successful clinical intervention.

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References

  • Albino AP, Lloyd KO, Houghton AN, Oettgen HF, Old LJ (1981) Heterogeneity in surface antigen and glycoprotein expression of cell lines derived from different melanoma metastases of the same patient. Implications for the study of tumor antigens. J Exp Med 154:1764–1778.

    PubMed  CAS  Google Scholar 

  • Angello JC, Danielson KG, Anderson LW, Hosick HL (1982) Glycosaminoglycan synthesis by subpopulations of epithelial cells from a mammary adenocarcinoma. Cancer Res 42:2207–2210.

    PubMed  CAS  Google Scholar 

  • Aoudjit F, Potworowski EF, Springer TA, St Pierre Y (1998a) Protection from lymphoma cell metastasis in ICAM-1 mutant mice: a posthoming event. J Immunol 161:2333–2338.

    PubMed  CAS  Google Scholar 

  • Aoudjit F, Potworowski EF, St Pierre Y (1998b) The metastatic characteristics of murine lymphoma cell lines in vivo are manifested after target organ invasion. Blood 91:623–629.

    PubMed  CAS  Google Scholar 

  • Ashall F, Bramwell ME, Harris H (1982) A new marker for human cancer cells. 1 The Ca antigen and the Ca1 antibody. Lancet 2:1–6.

    PubMed  CAS  Google Scholar 

  • Aubert C, Rouge F, Galindo JR (1980) Tumorigenicity of human malignant melanocytes in nude mice in relation to their differentiation in vitro. J Natl Cancer Inst 64:1029–1040.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Auerbach R, Lu WC, Pardon E, et al. (1987) Specificity of adhesion between murine tumor cells and capillary endothelium: an in vitro correlate of preferential metastasis in vivo. Cancer Res 47:1492–1496.

    PubMed  CAS  Google Scholar 

  • Barranco S, Luce J, Romsdahl M, Humphrey R (1973) Bleomycin as a possible synchronizing agent for human tumor cells in vivo. Cancer Research 33(4):882–887.

    PubMed  CAS  Google Scholar 

  • Barranco SC, Haenelt BR, Gee EL (1978) Differential sensitivities of five rat hepatoma cell lines to anticancer drugs. Cancer Res 38:656–660.

    PubMed  CAS  Google Scholar 

  • Barranco SC, Ho DH, Drewinko B, Romsdahl MM, Humphrey RM (1972) Differential sensitivites of human melanoma cells grown in vitro to arabinosylcytosine. Cancer Res 32:2733–2736.

    PubMed  CAS  Google Scholar 

  • Baylin SB (1982) Clonal selection and heterogeneity of human solid neoplams. In: Fidler IJ, White RJ (eds) Design of models for testing cancer therapeutics agents, pp 50–63.

    Google Scholar 

  • Baylin SB, Abeloff MD, Wieman KC, Tomford JW, Ettinger DS (1975) Elevated histaminase (diamine oxidase) activity in small-cell carcinoma of the lung. N Engl J Med 293:1286–1290.

    Article  PubMed  CAS  Google Scholar 

  • Baylin SB, Weisburger WR, Eggleston JC, et al. (1978) 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.

    PubMed  CAS  Google Scholar 

  • Becerk AJ, McCulloch EA, Till JE (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197:452–454.

    Google Scholar 

  • Becker FF, Klein KM, Wolman SR, Asofsky R, Sell S (1973) Characterization of primary hepatocellular carcinomas and initial transplant generations. Cancer Res 33:3330–3338.

    PubMed  CAS  Google Scholar 

  • Biorklund A, Hakansson L, Stenstam B, Trope C, Akerman M (1980) On heterogeneity of non-Hodgkin’s lymphomas as regards sensitivity to cytostatic drugs. An in vitro study. Eur J Cancer 16:647–654.

    PubMed  CAS  Google Scholar 

  • Bittner M, Meltzer P, Chen Y, et al. (2000) Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 406:536–540.

    PubMed  CAS  Google Scholar 

  • Bohm N, Sandritter W (1975) DNA in human tumors: a cytophotometric study. Curr Top Pathol 60:151–219.

    PubMed  CAS  Google Scholar 

  • Bosman HB, Winston RA (1970) Synthesis of glycoprotein, glycolipid, protein, and lipid in sychronized L5178Y cells. J Cell Biol 45:23–33.

    Google Scholar 

  • Bosslet K, Schirrmacher V (1981) Escape of metastasizing clonal tumor cell variants from tumor-specific cytolytic T lymphocytes. J Exp Med 154:557–562.

    PubMed  CAS  Google Scholar 

  • Bosslet K, Schirrmacher V (1982) High-frequency generation of new immunoresistant tumor variants during metastasis of a cloned murine tumor line (esb). Int J Cancer 29:195–202.

    PubMed  CAS  Google Scholar 

  • Brattain MG, Fine WD, Khaled FM, Thompson J, Brattain DE (1981) Heterogeneity of malignant cells from a human colonic carcinoma. Cancer Res 41:1751–1756.

    PubMed  CAS  Google Scholar 

  • Brennan MJ, Donegan WL, Appleby DE (1979) The variability of estrogen receptors in metastatic breast cancer. Am J Surg 137:260–262.

    PubMed  CAS  Google Scholar 

  • Briles EB, Kornfeld S (1978) Isolation and metastatic properties of detachment variants of B16 melanoma cells. J Natl Cancer Inst 60:1217–1222.

    PubMed  CAS  Google Scholar 

  • Brock WA, Swartzendruber DE, Grdina DJ (1982) Kinetic heterogeneity in density-separated murine fibrosarcoma subpopulations. Cancer Res 42:4999–5003.

    PubMed  CAS  Google Scholar 

  • Brunson KW, Beattie G, Nicolsin GL (1978) Selection and altered properties of brain-colonising metastatic melanoma. Nature 272:543–545.

    PubMed  CAS  Google Scholar 

  • Brunson KW, Nicolson GL (1978) Selection and biologic properties of malignant variants of a murine lymphosarcoma. J Natl Cancer Inst 61:1499–1503.

    PubMed  CAS  Google Scholar 

  • Byers VS, Johnston JO (1977) Antigenic differences among osteogenic sarcoma tumor cells taken from different locations in human tumors. Cancer Res 37:3173–3183.

    PubMed  CAS  Google Scholar 

  • Cameron MD, Schmidt EE, Kerkvliet N, et al. (2000) Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res 60:2541–2546.

    PubMed  CAS  Google Scholar 

  • Cerra RF, Nathanson SD (1989) Organ-specific chemotactic factors present in lung extracellular matrix. J Surg Res 46:422–426.

    PubMed  CAS  Google Scholar 

  • Chambers AF, Hill RP, Ling V (1981) Tumor heterogeneity and stability of the metastatic phenotype of mouse KHT sarcoma cells. Cancer Res 41:1368–1372.

    PubMed  CAS  Google Scholar 

  • Chu MY, Takeuchi T, Yeskey KS, Bogaars H, and Calabresi P (1979) Tumor cell heterogeneity in human lung carcinoma LX-1 [abstract]. Proc Am Assoc Cancer Res 20:151–152.

    Google Scholar 

  • Cifone MA, Fidler IJ (1981) Increasing metastatic potential is associated with increasing genetic instability of clones isolated from murine neoplasms. Proc Natl Acad Sci USA 78:6949–6952.

    PubMed  CAS  Google Scholar 

  • Cifone MA, Kripke ML, Fidler IJ (1979) Growth rate and chromosome number of tumor cell lines with different metastatic potential. J Supramol Struct 11:467–476.

    PubMed  CAS  Google Scholar 

  • Cikes M, Klein G (1972) Quantitative studies of antigen expression in cultured murine lymphoma cells. I. Cell-surface antigens in “Asynchronous” cultures. J Natl Cancer Inst 49:1599–1606.

    PubMed  CAS  Google Scholar 

  • Clark EA, Golub TR, Lander ES, Hynes RO (2000) Genomic analysis of metastasis reveals an essential role for rhoc. Nature 406:532–535.

    PubMed  CAS  Google Scholar 

  • Clark WH (1991) Tumour progression and the nature of cancer. Br J Cancer 64:631–644.

    PubMed  CAS  Google Scholar 

  • Colcher D, Horan HP, Teramoto YA, Wunderlich D, Schlom J (1981) Use of monoclonal antibodies to define the diversity of mammary tumor viral gene products in virions and mammary tumors of the genus Mus. Cancer Res 41:1451–1459.

    PubMed  CAS  Google Scholar 

  • Danielson KG, Anderson LW, Hosick HL (1980) Selection and characterization in culture of mammary tumor cells with distinctive growth properties in vivo. Cancer Res 40:1812–1819.

    PubMed  CAS  Google Scholar 

  • Dethlefsen L (1980) The growth dynamics of murine mammary tumor cells in situ. In: McGrath CM, Brennan MJ, Rich MA (eds) Cell biology of breast cancer. Academic, New York, pp 145–160.

    Google Scholar 

  • DeWys WD (1972) Studies correlating the growth rate of a tumor and its metastases and providing evidence for tumor-related systemic growth-retarding factors. Cancer Res 32:374–379.

    PubMed  CAS  Google Scholar 

  • Dexter DL, Kowalski HM, Blazar BA, et al. (1978) Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res 38:3174–3181.

    PubMed  CAS  Google Scholar 

  • Dexter DL, Leith JT (1986) Tumor heterogeneity and drug resistance. J Clin Oncol 4:244–257.

    PubMed  CAS  Google Scholar 

  • Dexter DL, Spremulli EN, Fligiel Z, et al. (1981) Heterogeneity of cancer cells from a single human colon carcinoma. Am J Med 71:949–956.

    PubMed  CAS  Google Scholar 

  • Dominguez OV, Huseby RA (1968) Heterogeneity of induced testicular interstitial cell tumors of mice as evidenced by steroid biosynthetic enzyme activities. Cancer Res 28:348–353.

    PubMed  CAS  Google Scholar 

  • Dunn TB (1959) Morphology of mammary tumors in mice. In: Homburger F, Risheman NH (eds) Physiopathology of cancer. Karger, New York, pp 38–84.

    Google Scholar 

  • Easty DM, Easty GC, Carter RL, et al. (1981) Five human tumour cell lines derived from a primary squamous carcinoma of the tongue, two subsequent local recurrences and two nodal metastases. Br J Cancer 44:363–370.

    PubMed  CAS  Google Scholar 

  • Ekman P, Snochowski M, Zetterberg A, Hogberg B, Gustafsson JA (1979) Steroid receptor content in human prostatic carcinoma and response to endocrine therapy. Cancer 44:1173–1181.

    PubMed  CAS  Google Scholar 

  • Enders JF, Diamandopoulos GT (1969) A study of variation and progression in oncongenicity in an SV 40-transformed hamster heart cell line and its clones. Proc R Soc Lond B Biol Sci 171:431–443.

    PubMed  CAS  Google Scholar 

  • Everson LK, Plocinik BA, Rogentine GN, Jr (1974) HL-A expression on the G1, S, and G2 cell-cycle stages of human lymphoid cells. J Natl Cancer Inst 53:913–920.

    PubMed  CAS  Google Scholar 

  • Ewing SL, Sumner HW, Ophoven JJ, Mayer JE, Humphrey EW (1980) Small cell anaplastic carcinoma with differentiation: a report of 14 cases. [abstract]. Lab Invest 42:115–116.

    Google Scholar 

  • Feder MK, Gilbert F (1983) Clonal evolution in a human neuroblastoma. J Natl Cancer Inst 70:1051–1056.

    PubMed  CAS  Google Scholar 

  • Fialkow PJ (1976) Clonal origin of human tumors. Biochim Biophys Acta 458:283–321.

    PubMed  CAS  Google Scholar 

  • Fidler IJ (1973) Selection of successive tumour lines for metastasis. Nat New Biol 242:148–149.

    PubMed  CAS  Google Scholar 

  • Fidler IJ (1988) Origin of cancer metastases and its implications for therapy. Isr J Med Sci 24:456–463.

    PubMed  CAS  Google Scholar 

  • Fidler IJ (1990) Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res 50:6130–6138.

    PubMed  CAS  Google Scholar 

  • Fidler IJ (1995) Cancer biology: invasion and metastasis. In: Abeloff MD, Armitage JO, Lichter AS, Niederhuber JE (eds) Clinical oncology. Churchill Livingstone, New York, pp 55–76.

    Google Scholar 

  • Fidler IJ (2002) Critical determinants of metastasis. Semin Cancer Biol 12:89–96.

    PubMed  Google Scholar 

  • Fidler IJ, Bucana C (1977) Mechanism of tumor cell resistance to lysis by syngeneic lymphocytes. Cancer Res 37:3945–3956.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Gruys E, Cifone MA, Barnes Z, Bucana C (1981) Demonstration of multiple phenotypic diversity in a murine melanoma of recent origin. J Natl Cancer Inst 67:947–956.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Hart IR (1981) Biological and experimental consequences of the zonal composition of solid tumors. Cancer Res 41:3266–3267.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Hart IR (1981) Biological and experimental consequences of the zonal composition of solid tumors. Cancer Res 41:3266–3267.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197:893–895.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Kripke ML (2003) Genomic analysis of primary tumors does not address the prevalence of metastatic cells in the population. Nat Genet 34:23.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Nicolson GL (1981) The immunobiology of experimental metastatic melanoma. Cancer Biol Rev 2:171–234.

    Google Scholar 

  • Fidler IJ, Radinsky R (1996) Search for genes that suppress cancer metastasis. J Natl Cancer Inst 88:1700–1703.

    PubMed  CAS  Google Scholar 

  • Fidler IJ, Singh RK, Yoneda J, et al. (2000) Critical determinants of neoplastic angiogenesis. Cancer J Sci Am 6(Suppl 3):S225–S236.

    Google Scholar 

  • Filmus J, Kerbel RS (1993) Development of resistance mechanisms to the growth-inhibitory effects of transforming growth factor-beta during tumor progression. Curr Opin Oncol 5:123–129.

    PubMed  CAS  Google Scholar 

  • Fogel M, Gorelik E, Segal S, Feldman M (1979) Differences in cell surface antigens of tumor metastases and those of the local tumor. J Nat Cancer Inst 62:585–588.

    PubMed  CAS  Google Scholar 

  • Foulds L (1956a) The hisologic analysis of mammary tumors of mice. I. Scope of investigations and general principles of anlysis. J Natl Cancer Inst 17:701–712.

    PubMed  CAS  Google Scholar 

  • Foulds L (1956b) The hisologic analysis of mammary tumors of mice. II. The hisotology of responsiveness and progression. The origins of tumors. J Nat Cancer Inst 17:713–754.

    Google Scholar 

  • Foulds L (1956c) The hisologic analysis of mammary tumors of mice. III. Organoid tumors. J Nat Cancer Inst 17:755–782.

    Google Scholar 

  • Foulds L (1956d) The hisologic analysis of mammary tumors of mice. IV. Secretion. J Nat Cancer Inst 17:783–801.

    Google Scholar 

  • Franks LM (1960) Estrogen-treated prostatic cancer. Cancer 13:490–501.

    PubMed  CAS  Google Scholar 

  • Friedman JM, Fialkow PJ, Greene CL, Weinberg MN (1982) Probable clonal origin of neurofibrosarcoma in a patient with hereditary neurofibromatosis. J Natl Cancer Inst 69:1289–1292.

    PubMed  CAS  Google Scholar 

  • Frost PH, Kerbel RS (1981) Immunoselection in vitro of a nonmetastatic variant from a highly metastatic tumor. J Natl Cancer Inst 69:1289–1292.

    Google Scholar 

  • Fugmann RA, Anderson JC, Stolfi RL, Martin DS (1977) Comparison of adjuvant chemotherapeutic activity against primary and metastatic spontaneous murine tumors. Cancer Res 37:496–500.

    PubMed  CAS  Google Scholar 

  • Fuji H, Mihich E (1975) Selection for high immunogenicity in drug-resistant sublines of murine lymphomas demonstrated by plaque assay. Cancer Res 35:946–952.

    PubMed  CAS  Google Scholar 

  • Fuji H, Mihich E, Pressman D (1977) Differential tumor immunogenicity of L1210 and its sublines. I. Effect of an increased antigen density on tumor cell surfaces on primary B cell responses in vitro. J Immunol 119:983–986.

    PubMed  CAS  Google Scholar 

  • Gasic GJ (1984) Role of plasma, platelets, and endothelial cells in tumor metastasis. Cancer Metastasis Rev 3:99–114.

    PubMed  CAS  Google Scholar 

  • Geier GR, Schwarz JA, Schlag P (1979) Cytologic uniformity of breast cancer from different localizations: a pattern analysis study. Exp Cell Biol 47:241–249.

    PubMed  CAS  Google Scholar 

  • Giavazzi R, Alessandri G, Spreafico F, Garattini S, Mantovani A (1980) Metastasizing capacity of tumour cells from spontaneous metastases of transplanted murine tumours. Br J Cancer 42:462–472.

    PubMed  CAS  Google Scholar 

  • Gorelik E, Feldman M, Segal S (1982) Selection of 3LL tumor subline resistant to natural effector cells concomitantly selected for increased metastatic potency. H supramol Struct 12:385–402.

    Google Scholar 

  • Gorelik E, Fogel M, Segal S, Feldman M (1979) Tumor-associated antigenic differences between the primary and the descendant metastatic tumor cell populations. J Supramol Struct 12:385–402.

    PubMed  CAS  Google Scholar 

  • Gray JM, Pierce GB (1964) Relationship between growth rate and differentiation of melanoma in vivo. J Nat Cancer Inst 32:1201–1211.

    PubMed  CAS  Google Scholar 

  • Gunthert U, Birchmeier W, Schlag PM (1996) Attempts to understand metastasis formation. II. Regulatory factors. Introduction. Curr Top Microbiol Immunol 213(Pt 2):V–VII.

    Google Scholar 

  • Gunthert U, Hofmann M, Rudy W, et al. (1991) A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65:13–24.

    PubMed  CAS  Google Scholar 

  • Hager JC, Fligiel S, Stanley W, Richardson AM, Heppner GH (1981) Characterization of a variant-producing tumor cell line from a heterogeneous strain BALB/cfc3h mouse mammary tumor. Cancer Res 41:1293–1300.

    PubMed  CAS  Google Scholar 

  • Hager JC, Heppner GH (1982) Heterogeneity of expression and induction of mouse mammary tumor virus antigens in mouse mammary tumors. Cancer Res 42:4325–4329.

    PubMed  CAS  Google Scholar 

  • Hakansson L, Trope C (1974a) Cell clones with different sensitivity to cytostatic drugs in methylcholanthrene-induced mouse sarcomas. Acta Pathol Microbiol Scand [A] 82:41–47.

    CAS  Google Scholar 

  • Hakansson L, Trope C (1974b) On the presence within tumours of clones that differ in sensitivity to cytostatic drugs. Acta Pathol Microbiol Scand [A] 82:35–40.

    CAS  Google Scholar 

  • Hanna N, Fidler IJ (1981) Relationship between metastatic potential and resistance to KN cell-mediated cytoxicity in three murine tumor systems. J Natl Cancer Inst 66:1183–1190.

    Google Scholar 

  • Hao WM, Joshi SS (1990) Differential susceptibility of metastatic lymphoma cells to natural immunity. Oncology 47:483–487.

    PubMed  CAS  Google Scholar 

  • Harris JF, Best MW (1988) Dynamic heterogeneity: metastatic variants to liver are generated spontaneously in mouse embryonal carcinoma cells. Clin Exp Metastasis 6:451–462.

    PubMed  CAS  Google Scholar 

  • Harris JF, Chambers AF, Hill RP, Ling V (1982) Metastatic variants are generated spontaneously at a high rate in mouse KHT tumor. Proc Natl Acad Sci USA 79:5547–5551.

    PubMed  CAS  Google Scholar 

  • Hart IR (1979) The selection and characterization of an invasive variant of the B16 melanoma. Am J Pathol 97:587–600.

    PubMed  CAS  Google Scholar 

  • Hart IR (1982) ‘Seed and soil’ revisited: mechanisms of site-specific metastasis. Cancer Metastasis Rev 1:5–16.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hart IR, Talmadge JE, Fidler IJ (1981) Metastatic behavior of a murine reticulum cell sarcoma exhibiting organ-specific growth. Cancer Res 41:1281–1287.

    PubMed  CAS  Google Scholar 

  • Hastings RJ, Franks LM (1983) Cellular heterogeneity in a tissue culture cell line derived from a human bladder carcinoma. Br J Cancer 47:233–244.

    PubMed  CAS  Google Scholar 

  • Henderson JS, Rous P (1962) The plating of tumor components on the subsutaneous expanses of young mice. J Exp Med 115:1211–1230.

    PubMed  CAS  Google Scholar 

  • Heppner GH, Dexter DL, DeNucci T, Miller FR, Calabresi P (1978) Heterogeneity in drug sensitivity among tumor cell subpopulations of a single mammary tumor. Cancer Res 38:3758–3763.

    PubMed  CAS  Google Scholar 

  • Heppner GH, Miller BE (1983) Tumor heterogeneity: biological implications and therapeutic consequences. Cancer Metastasis Rev 2:5–23.

    PubMed  CAS  Google Scholar 

  • Hill HZ, Hill GJ, Miller CF, Kwong F, Purdy J (1979) Radiation and melanoma: response of B16 mouse tumor cells and clonal lines to in vitro irradiation. Radiat Res 80:259–276.

    PubMed  CAS  Google Scholar 

  • Hujanen ES, Terranova VP (1985) Migration of tumor cells to organ-derived chemoattractants. Cancer Res 45:3517–3521.

    PubMed  CAS  Google Scholar 

  • Isaacs JT, Coffey DS (1981) Adaptation versus selection as the mechanism responsible for the relapse of prostatic cancer to androgen ablation therapy as studied in the Dunning R-3327-H adenocarcinoma. Cancer Res 41:5070–5075.

    PubMed  CAS  Google Scholar 

  • Isaacs JT, Wake N, Coffey DS, Sandberg AA (1982) Genetic instability coupled to clonal selection as a mechanism for tumor progression in the Dunning R-3327 rat prostatic adenocarcinoma system. Cancer Res 42:2353–2371.

    PubMed  CAS  Google Scholar 

  • Ishidate M, Jr., Aoshima M, Sakurai Y (1974) Population changes of a rat leukemia by different routes of transplantation. J Natl Cancer Inst 53:773–781.

    PubMed  Google Scholar 

  • Ito E, Moore GE (1967) Characteristic differences in clones isolated from an S37 ascites tumor in vitro. Exp Cell Res 48:440–447.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Karpatkin S, Pearlstein E, Ambrogio C, Coller BS (1988) Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest 81:1012–1019.

    PubMed  CAS  Google Scholar 

  • Kerbel RS (1979) Implications of immunological heterogeneity of tumours. Nature 280:358–360.

    PubMed  CAS  Google Scholar 

  • Kerbel RS (1990) Growth dominance of the metastatic cancer cell: cellular and molecular aspects. Adv Cancer Res 55:87–132.

    PubMed  CAS  Google Scholar 

  • Kerbel RS (1992) Expression of multi-cytokine resistance and multi-growth factor independence in advanced stage metastatic cancer. Malignant melanoma as a paradigm. Am J Pathol 141:519–524.

    PubMed  CAS  Google Scholar 

  • Kerbel RS, Waghorne C, Korczak B, Breitman ML (1988a) Clonal changes in tumours during growth and progression evaluated by southern gel analysis of random integrations of foreign DNA. Ciba Found Symp 141:123–148.

    PubMed  CAS  Google Scholar 

  • Kerbel RS, Waghorne C, Korczak B, Lagarde A, Breitman ML (1988a) Clonal dominance of primary tumours by metastatic cells: genetic analysis and biological implications. Cancer Surv 7:597–629.

    PubMed  CAS  Google Scholar 

  • Key M, Talmadge JE, Fidler IJ (1982) Lack of correlation between the progressive growth of spontaneous metastases and their content of infiltrating macrophages. J Reticuloendothel Soc 32:387–396.

    PubMed  CAS  Google Scholar 

  • Killion JJ (1978) Immunotherapy with tumor subpopulations. I. Active, specific immunotherapy of L1210 Leukemia. Cancer Immunol Immunother 4:115–119.

    Google Scholar 

  • Killion JJ, Kollmorgen GM (1976) Isolation of immunogenic tumor cells by cell-affinity chromatography. Nature 259:674–676.

    PubMed  CAS  Google Scholar 

  • Kiricuta I, Mustea I, Rogozan I, Simu G (1965) Relations between tumor metastasis. I. Aspects of the crabtree effect. Cancer 18:978–984.

    PubMed  CAS  Google Scholar 

  • Klein E (1954) Gradual transformation of solid into ascites tumors: Permanent differences between the original and the transformed sublines. Cancer Res 14:482–485.

    PubMed  CAS  Google Scholar 

  • Klein E (1955) Gradual transformation of solid into ascites tumors: evidence favoring the mutation-selection theory. Exp Cell Res 23:188–212.

    Google Scholar 

  • Kobori O, Oota K (1979) Neuroendocrine cells in serially passaged rat stomach cancers induced by MNNG. Int J Cancer 23:536–541.

    PubMed  CAS  Google Scholar 

  • Kosh F (1939) Zur frage der metastazenbildung bei Impftumoren. Z Krebsforsch 48:495–505.

    Google Scholar 

  • Kozlowski JM, Fidler IJ, Campbell D, et al. (1984) Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res 44:3522–3529.

    PubMed  CAS  Google Scholar 

  • Kripke ML, Fidler IJ (1980) Enhanced experimental metastasis of ultraviolet light-induced fibrosarcomas in ultraviolet light-irradiated syngeneic mice. Cancer Res 40:625–629.

    PubMed  CAS  Google Scholar 

  • Kripke ML, Gruys E, Fidler IJ (1978) Metastatic heterogeneity of cells from an ultraviolet light-induced murine fibrosarcoma of recent origin. Cancer Res 38:2962–2967.

    PubMed  CAS  Google Scholar 

  • Kusyk CJ, Seski JC, Medlin WV, Edwards CL (1981) Progressive chromosome changes associated with different sites of one ovarian carcinoma. J Natl Cancer Inst 66:1021–1025.

    PubMed  CAS  Google Scholar 

  • Larner EH, Rutherford CL (1982) Implementation of micromethods to resolve problems of human breast tumor heterogeneity in analysis of cyclic 3:5 nucleotide phosphodiesterase. Cancer Res 42:1661–1668.

    PubMed  CAS  Google Scholar 

  • Lee SH (1978) Cytochemical study of estrogen receptor in human mammary cancer. Am J Clin Pathol 70:197–203.

    PubMed  CAS  Google Scholar 

  • Leith JT, Brenner HJ, DeWyngaert JK, et al. (1981) Selective modification of the X ray survival response of two mouse mammary adenocarcinoma sublines by N, N-dimethylformamide. Int J Radiat Oncol Biol Phys 7:943–947.

    PubMed  CAS  Google Scholar 

  • Leith JT, Dexter DL, DeWyngaert JK, et al. (1982a) Differential responses to x-irradiation of subpopulations of two heterogeneous human carcinomas in vitro. Cancer Res 42:2556–2561.

    PubMed  CAS  Google Scholar 

  • Leith JT, Gaskins LA, Dexter DL, Calabresi P, Glicksman AS (1982b) Alteration of the survival response of two human colon carcinoma subpopulations to x-irradiation by N, N-dimethylformamide. Cancer Res 42:30–34.

    PubMed  CAS  Google Scholar 

  • Lerner RA, Oldstone MB, Cooper NR (1971) Cell cycle-dependent immune lysis of Moloney virus-transformed lymphocytes: presence of viral antigen, accessibility to antibody, and complement activation. Proc Natl Acad Sci USA 68:2584–2588.

    PubMed  CAS  Google Scholar 

  • Li LM, Nicolson GL, Fidler IJ (1991) Direct in vitro lysis of metastatic tumor cells by cytokine-activated murine vascular endothelial cells. Cancer Res 51:245–254.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lichtner RB, Kaufmann AM, Kittmann A, et al. (1995) Ligand mediated activation of ectopic EGF receptor promotes matrix protein adhesion and lung colonization of rat mammary adenocarcinoma cells. Oncogene 10:1823–1832.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Liotta LA, Stetler-Stevenson WG (1991) Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res 51:5054s–5059s.

    PubMed  CAS  Google Scholar 

  • Lippman SM, Mendelsohn G, Trump DL, Wells SA, Jr., Baylin SB (1982) The prognostic and biological significance of cellular heterogeneity in medullary thyroid carcinoma: a study of calcitonin, L-dopa decarboxylase, and histaminase. J Clin Endocrinol Metab 54:233–240.

    PubMed  CAS  Google Scholar 

  • Loewenstein WR (1979) Junctional intercellular communication and the control of growth. Biochim Biophys Acta 560:1–65.

    PubMed  CAS  Google Scholar 

  • Lotan R (1979) Different susceptibilities of human melanoma and breast carcinoma cell lines to retinoic acid-induced growth inhibition. Cancer Res 39:1014–1019.

    PubMed  CAS  Google Scholar 

  • Lotan R, Nicolson GL (1979) Heterogeneity in growth inhibition by beta-trans-retinoic acid of metastatic B16 melanoma clones and in vivo-selected cell variant lines. Cancer Res 39:4767–4771.

    PubMed  CAS  Google Scholar 

  • Lu C, Kerbel RS (1994) Cytokines, growth factors and the loss of negative growth controls in the progression of human cutaneous malignant melanoma. Curr Opin Oncol 6:212–220.

    PubMed  CAS  Google Scholar 

  • Macinnes JI, Chan EC, Percy DH, Morris VL (1981) Mammary tumors from GR mice contain more than one population of mouse mammary tumor virus-infected cells. Virology 113:119–129.

    PubMed  CAS  Google Scholar 

  • Mackintosh FR, Louie AC, Evans TL, Amylon MD, Sikic BI (1981) Clonocal heterogeneity in a human ovarian adenocarcinoma. [abstract]. Proc AACR 22:379.

    Google Scholar 

  • MacLean GD, Seehafer J, Shaw AR, Kieran MW, Longenecker BM (1982) Antigenic heterogeneity of human colorectal cancer cell lines analyzed by a panel of monoclonal antibodies. I. Heterogeneous expression of Ia-like and HLA-like antigenic determinants. J Natl Cancer Inst 69:357–364.

    PubMed  CAS  Google Scholar 

  • Makino S (1956) Further evidence favoring the concept of the stem cell in ascites tumors of rats. Ann NY Acad Sci 63:818–830.

    PubMed  CAS  Google Scholar 

  • Mantovani A, Giavazzi R, Alessandri G, Spreafico F, Garattini S (1981) Characterization of tumor lines derived from spontaneous metastases of a transplanted murine sarcoma. Eur J Cancer 17:71–76.

    PubMed  CAS  Google Scholar 

  • Mathieson BJ, Zatz MM, Sharrow SO, et al. (1982) Separation and characterization of two component tumor lines within the AKR lymphoma, AKTB-1, by fluorescence-activated cell sorting and flow microfluorometry analysis. II. Differential histopathology of sig+ and sig− sublines. J Immunol 128:1832–1838.

    PubMed  CAS  Google Scholar 

  • McCarthy JB, Skubitz AP, Iida J, et al. (1991) Tumor cell adhesive mechanisms and their relationship to metastasis. Semin Cancer Biol 2:155–167.

    PubMed  CAS  Google Scholar 

  • McCune CS, Schapira DV, Henshaw EC (1981) Specific immunotherapy of advanced renal carcinoma: evidence for the polyclonality of metastases. Cancer 47:1984–1987.

    PubMed  CAS  Google Scholar 

  • McDowell EM, Sorokin SP, Hoyt RF, Jr., Trump BF (1981) An unusual bronchial carcinoid tumor: light and electron microscopy. Hum Pathol 12:338–348.

    PubMed  CAS  Google Scholar 

  • McGee JO, Woods JC, Ashall F, Bramwell ME, Harris H (1982) A new marker for human cancer cells, 2 immunohistochemical detection of the Ca antigen in human tissues with the Ca1 antibody. Lancet 2:7–10.

    PubMed  CAS  Google Scholar 

  • Medina D (2002) Biological and molecular characteristics of the premalignant mouse mammary gland. Biochim Biophys Acta 1603:1–9.

    PubMed  CAS  Google Scholar 

  • Michalides R, Wagenaar E, Sluyser M (1982) Mammary tumor virus DNA as a marker for genotypic variance within hormone-responsive GR mouse mammary tumors. Cancer Res 42:1154–1158.

    PubMed  CAS  Google Scholar 

  • Miller BE, Miller FR, Heppner GH (1981) Interactions between tumor subpopulations affecting their sensitivity to the antineoplastic agents cyclophosphamide and methotrexate. Cancer Res 41:4378–4381.

    PubMed  CAS  Google Scholar 

  • Miller BE, Miller FR, Leith J, Heppner GH (1980) Growth interaction in vivo between tumor subpopulations derived from a single mouse mammary tumor. Cancer Res 40:3977–3981.

    PubMed  CAS  Google Scholar 

  • Miller FR (1982) Intratumor immunologic heterogeneity. Cancer Metastasis Rev 1:319–334.

    PubMed  CAS  Google Scholar 

  • Miller FR, Heppner GH (1979) Immunologic heterogeneity of tumor cell subpopulations from a single mouse mammary tumor. J Natl Cancer Inst 63:1457–1463.

    PubMed  CAS  Google Scholar 

  • Mitelman F (1971) The chromosomes of fifty primary Rous rat sarcomas. Hereditas 69:155–186.

    PubMed  CAS  Google Scholar 

  • Morikawa K, Walker SM, Nakajima M, et al. (1988) Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res 48:6863–6871.

    PubMed  CAS  Google Scholar 

  • Naito S, Kumazawa J, von Eschenbach AC, Fidler IJ (1991) Metastatic heterogeneity of human renal cell carcinoma. Urol Int 47(Suppl 1):90–95.

    PubMed  Google Scholar 

  • Nakajima M, Morikawa K, Fabra A, Bucana CD, Fidler IJ (1990) Influence of organ environment on extracellular matrix degradative activity and metastasis of human colon carcinoma cells. J Natl Cancer Inst 82(24):1890–1898.

    PubMed  CAS  Google Scholar 

  • Natali PG, Cavaliere R, Bigotti A, et al. (1983) Antigenic heterogeneity of surgically removed primary and autologous metastatic human melanoma lesions. J Immunol 130:1462–1466.

    PubMed  CAS  Google Scholar 

  • Neri A, Welch D, Kawaguchi T, Nicolson GL (1982) Development and biologic properties of malignant cell sublines and clones of a spontaneously metastasizing rat mammary adenocarcinoma. J Natl Cancer Inst 68:507–517.

    PubMed  CAS  Google Scholar 

  • Nicolin A, Canti G, Marelli O, Veronese F, Goldin A (1981) Chemotherapy and immunotherapy of L1210 leukemic mice with antigenic tumor sublines. Cancer Res 41:1358–1362.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1984a) Cell surface molecules and tumor metastasis. Regulation of metastatic phenotypic diversity. Exp Cell Res 150:3–22.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1984b) Generation of phenotypic diversity and progression in metastatic tumor cells. Cancer Metastasis Rev 3:25–42.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1984c) Tumor progression, oncogenes and the evolution of metastatic phenotypic diversity. Clin Exp Metastasis 2:85–105.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1991a) Gene expression, cellular diversification and tumor progression to the metastatic phenotype. Bioessays 13:337–342.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1991b) Molecular mechanisms of cancer metastasis: tumor and host properties and the role of oncogenes and suppressor genes. Curr Opin Oncol 3:75–92.

    PubMed  CAS  Google Scholar 

  • Nicolson GL (1991c) Tumor and host molecules important in the organ preference of metastasis. Semin Cancer Biol 2:143–154.

    PubMed  CAS  Google Scholar 

  • Nicolson GL, Brunson KW, Fidler IJ (1978) Specificity of arrest, survival, and growth of selected metastatic variant cell lines. Cancer Res 38:4105–4111.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nicolson GL, Moustafa AS (1998) Metastasis-associated genes and metastatic tumor progression. In Vivo 12:579–588.

    PubMed  CAS  Google Scholar 

  • Nierodzik ML, Klepfish A, Karpatkin S (1994) Role of platelet integrin gpiib-gpiiia, fibronectin, von Willebrand factor, and thrombin in platelet-tumor interaction in vitro and metastasis in vivo. Semin Hematol 31:278–288.

    PubMed  CAS  Google Scholar 

  • Niles RM, Makarski JS (1978) Hormonal activation of adenylate cyclase in mouse melanoma metastatic variants. J Cell Physiol 96:355–359.

    PubMed  CAS  Google Scholar 

  • Nolibe D, Poupon MF (1986) Enhancement of pulmonary metastases induced by decreased lung natural killer cell activity. J Natl Cancer Inst 77:99–103.

    PubMed  CAS  Google Scholar 

  • Nowell PC (1976) The clonal evolution of tumor cell populations. Science 194:23–28.

    PubMed  CAS  Google Scholar 

  • Ohno S (1971) Genetic implication of karyological instability of malignant somatic cells. Physiol Rev 51:496–526.

    Google Scholar 

  • Olsson L, Ebbesen P (1979) Natural polyclonality of spontaneous AKR leukemia and its consequences for so-called specific immunotherapy. J Natl Cancer Inst 62:623–627.

    PubMed  CAS  Google Scholar 

  • Olsson L, Kiger N, Kronstrom H (1981) Sensitivity of cloned high- and low-metastatic murine Lewis lung tumor cells to lysis by cytotoxic autoreactive cells. Cancer Res 41:4706–4709.

    PubMed  CAS  Google Scholar 

  • Orr FW, Sanchez-Sweatman OH, Kostenuik P, Singh G (1995) Tumor-bone interactions in skeletal metastasis. Clin Orthop 19–33.

    Google Scholar 

  • Owens DM, Watt FM (2003) Contribution of stem cells and differentiated cells to epidermal tumours. Nat Rev Cancer 3:444–451.

    PubMed  CAS  Google Scholar 

  • Panem S, Schauf V (1974) Cell-cycle dependent appearance of murine leukemia-sarcoma virus antigens. J Virol 13:1169–1175.

    PubMed  CAS  Google Scholar 

  • Parbhoo SP (1981) Heterogeneity in human mammary cancer. In: Stoll BA (ed) Systemic control of breast cancer. William Heinemann, London, pp 55–77.

    Google Scholar 

  • Pasternak CA, Warmsley AM, Thomas DB (1971) Structural alterations in the surface membrane during the cell cycle. J Cell Biol 50:562–564.

    PubMed  CAS  Google Scholar 

  • Pathak S (1990) Cytogenetic abnormalities in cancer: with special emphasis on tumor heterogeneity. Cancer Metastasis Rev 8:299–318.

    PubMed  CAS  Google Scholar 

  • Pauli BU, Augustin-Voss HG, el Sabban ME, Johnson RC, Hammer DA (1990) Organ-preference of metastasis. The role of endothelial cell adhesion molecules. Cancer Metastasis Rev 9:175–189.

    PubMed  CAS  Google Scholar 

  • Pauli BU, Knudson W (1988) Tumor invasion: a consequence of destructive and compositional matrix alterations. Hum Pathol 19:628–639.

    PubMed  CAS  Google Scholar 

  • Pauli BU, Lee CL (1988) Organ preference of metastasis. The role of organ-specifically modulated endothelial cells. Lab Invest 58:379–387.

    PubMed  CAS  Google Scholar 

  • Perez-Losada J, Balmain A (2003) Stem-cell hierarchy in skin cancer. Nat Rev Cancer 3:434–443.

    PubMed  CAS  Google Scholar 

  • Pertschuk LP, Tobin EH, Brigati DJ, et al. (1978) Immunofluorescent detection of estrogen receptors in breast cancer. Comparison with dextran-coated charcoal and sucrose gradient assays. Cancer 41:907–911.

    PubMed  CAS  Google Scholar 

  • Phillips NC (1989) Kupffer cells and liver metastasis. Optimization and limitation of activation of tumoricidal activity. Cancer Metastasis Rev 8:231–252.

    PubMed  CAS  Google Scholar 

  • Phillips NC (1990) Macrophages, metastasis and immunity. Prog Clin Biol Res 354A:257–270.

    PubMed  CAS  Google Scholar 

  • Pierce GB (1974) Cellular heterogeneity of cancers. In: Pop T, DiPaolo JA (eds) World symposium on model studies in chemical carcinogensis. Marcel Dekker, New York, pp 463–472.

    Google Scholar 

  • Pimm MV, Baldwin RW (1980) Antigenic heterogeneity of primary and metastatic tumors and its implications for immunotherapy. In: Grundmann E (ed) Metastatic tumor growth. Gustav Fischer, Stuttgart, p 305.

    Google Scholar 

  • Pimm MV, Embleton MJ, Baldwin RW (1980) Multiple antigenic specificities within primary 3-methylcholanthrene-induced rat sarcomas and metastases. Int J Cancer 25:621–629.

    PubMed  CAS  Google Scholar 

  • Pollack VA, Fidler IJ (1982) Use of young nude mice for selection of subpopulations of cells with increased metastatic potential from nonsyngeneic neoplasms. J Natl Cancer Inst 69:137–141.

    PubMed  CAS  Google Scholar 

  • Poste G (1982) Experimental systems for analysis of the malignant phenotype. Cancer Metastasis Rev 1:141–199.

    PubMed  CAS  Google Scholar 

  • Poste G, Doll J, Fidler IJ (1981) Interactions among clonal subpopulations affect stability of the metastatic phenotype in polyclonal populations of B16 melanoma cells. Proc Natl Acad Sci USA 78:6226–6230.

    PubMed  CAS  Google Scholar 

  • Poste G, Doll J, Hart IR, Fidler IJ (1980) In vitro selection of murine B16 melanoma variants with enhanced tissue-invasive properties. Cancer Res 40:1636–1644.

    PubMed  CAS  Google Scholar 

  • Poste G, Doll J, Brown AE, Tzeng J, Zeidman I (1982a) Comparison of the metastatic properties of B16 melanoma clones isolated from cultured cell lines, subcutaneous tumors, and individual lung metastases. Cancer Res 42:2770–2778.

    PubMed  CAS  Google Scholar 

  • Poste G, Tzeng J, Doll J, et al. (1982b) Evolution of tumor cell heterogeneity during progressive growth of individual lung metastases. Proc Natl Acad Sci USA 79:6574–6578.

    PubMed  CAS  Google Scholar 

  • Prehn RT (1970) Analysis of antigenic heterogeneity within individual 3-mthylcholanthrene-induced mouse sarcomas. J Nat Cancer Inst 45:1039–1045.

    PubMed  CAS  Google Scholar 

  • Rabotti G (1959) Ploidy of primary and metastatic human tumours. Nature 183:1276–1277.

    PubMed  CAS  Google Scholar 

  • Rajotte D, Arap W, Hagedorn M, et al. (1998) Molecular heterogeneity of the vascular endothelium revealed by in vivo phage display. J Clin Invest 102:430–437.

    PubMed  CAS  Google Scholar 

  • Ramaswamy S, Ross KN, Lander ES, Golub TR (2003) A molecular signature of metastasis in primary solid tumors. Nat Genet 33:49–54.

    PubMed  CAS  Google Scholar 

  • Raz A (1982) Regional emergence of metastatic heterogeneity in a growing tumor. Cancer Lett 17:153–160.

    PubMed  CAS  Google Scholar 

  • Raz A, Hanna N, Fidler IJ (1981) In vivo isolation of a metastatic tumor cell variant involving selective and nonadaptive processes. J Natl Cancer Inst 66:183–189.

    PubMed  CAS  Google Scholar 

  • Raz A, McLellan WL, Hart IR, et al. (1980) Cell surface properties of B16 melanoma variants with differing metastatic potential. Cancer Res 40:1645–1651.

    PubMed  CAS  Google Scholar 

  • Reading CL, Belloni PN, Nicolson GL (1980a) Selection and in vivo properties of lectin-attachment variants of malignant murine lymphosarcoma cell lines. J Natl Cancer Inst 64:1241–1249.

    PubMed  CAS  Google Scholar 

  • Reading CL, Brunson KW, Torrianni M, Nicolson GL (1980b) Malignancies of metastatic murine lymphosarcoma cell lines and clones correlate with decreased cell surface display of RNA tumor virus envelope glycoprotein gp70. Proc Natl Acad Sci USA 77:5943–5947.

    PubMed  CAS  Google Scholar 

  • Reeve JG, Twentyman PR (1982) Ploidy distribution of tumour cells derived from induced and spontaneously arising metastases of a murine radiation-induced sarcoma, RIF-1. Eur J Cancer Clin Oncol 18:1001–1006.

    PubMed  CAS  Google Scholar 

  • Ridley A (2000) Molecular switches in metastasis. Nature 406:466–467.

    PubMed  CAS  Google Scholar 

  • Rusciano D, Burger MM (1992) Why do cancer cells metastasize into particular organs? Bioessays 14:185–194.

    PubMed  CAS  Google Scholar 

  • Sacchi A, Calabresi F, Greco C, Zupi G (1981) Different metastatic potential of in vitro and in vivo lines selected from Lewis lung carcinoma: correlation with response to different bleomycin schedulings. Invasion Metastasis 1:227–238.

    PubMed  CAS  Google Scholar 

  • Saiki I, Naito S, Yoneda J, et al. (1991) Characterization of the invasive and metastatic phenotype in human renal cell carcinoma. Clin Exp Metastasis 9:551–566.

    PubMed  CAS  Google Scholar 

  • Sandberg AA (1977) Chromosome markers and progression in bladder cancer. Cancer Res 37:2950–2956.

    PubMed  CAS  Google Scholar 

  • Schirrmacher V, Bosslet K (1982) Clonal analysis of expression of tumor-associated transplantation antigens and of metastatic capacity. Cancer Immunol Immunother 13:62–68.

    PubMed  CAS  Google Scholar 

  • Schirrmacher V, Bosslet K, Shantz G, Clauer K, Hubsch D (1979) Tumor metastases and cell-mediated immunity in a model system in DBA/2 mice. IV. Antigenic differences between a metastasizing variant and the parental tumor line revealed by cytotoxic T lymphocytes. Int J Cancer 23:245–252.

    PubMed  CAS  Google Scholar 

  • Schirrmacher V, Fogel M, Russmann E, et al. (1982) Antigenic variation in cancer metastasis: immune escape versus immune control. Cancer Metastasis Rev 1:241–274.

    PubMed  CAS  Google Scholar 

  • Schlag P, Schreml W (1982) Heterogeneity in growth pattern and drug sensitivity of primary tumor and metastases in the human tumor colony-forming assay. Cancer Res 42:4086–4089.

    PubMed  CAS  Google Scholar 

  • Schmitt M, Daynes RA (1981) Heterogeneity of tumorigenicity phenotype in murine tumors. I. Characterization of regressor and progressor clones isolated from a nonmutagenized ultraviolet regressor tumor. J Exp Med 153:1344–1359.

    PubMed  CAS  Google Scholar 

  • Semple TU, Moore GE, Morgan RT, Woods LK, Quinn LA (1982) Multiple cell lines from patients with malignant melanoma: morphology, karyology, and biochemical analysis. J Natl Cancer Inst 68:365–380.

    PubMed  CAS  Google Scholar 

  • Shapiro JR, Yung WK, Shapiro WR (1981) Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Res 41:2349–2359.

    PubMed  CAS  Google Scholar 

  • Shearman PJ, Longenecker BM (1980) Selection for virulence and organ-specific metastasis of herpesvirus-transformed lymphoma cells. Int J Cancer 25:363–369.

    PubMed  CAS  Google Scholar 

  • Shearman PJ, Longenecker BM (1981) Clonal variation and functional correlation of organ-specific metastasis and an organ-specific metastasis-associated antigen. Int J Cancer 27:387–395.

    PubMed  CAS  Google Scholar 

  • Sher BT, Bargatze R, Holzmann B, et al. (1988) Homing receptors and metastasis. Adv Cancer Res 51:361–390.

    PubMed  CAS  Google Scholar 

  • Shipley WU (1971) Immune cytolysis in relation to the growth cycle of Chinese hamster cells. Cancer Res 31:925–929.

    PubMed  CAS  Google Scholar 

  • Singh RK, Bucana CD, Gutman M, et al. (1994) Organ site-dependent expression of basic fibroblast growth factor in human renal cell carcinoma cells. Am J Pathol 145:365–374.

    PubMed  CAS  Google Scholar 

  • Singh RK, Fidler IJ (1996) Regulation of tumor angiogenesis by organ-specific cytokines. In: Gunthert U, Birchmeier W (eds) Attempts to understand metastasis formation II. Springer, New York, pp 1–11.

    Google Scholar 

  • Singh RK, Fidler IJ (1997) Clinical applications of ifns “Future Directions”. In: Penny R, Stuart-Harris R (eds) Clinical applications of the interferons. Chapman & Hall, London, pp 391–404.

    Google Scholar 

  • Singh RK, Tsan R, Radinsky R (1997) Influence of the host microenvironment on the clonal selection of human colon carcinoma cells during primary tumor growth and metastasis. Clin Exp Metastasis 15:140–150.

    PubMed  CAS  Google Scholar 

  • Singh RK, Tsan R, Radinsky R (1997) Influence of the host microenvironment on the clonal selection of human colon carcinoma cells during primary tumor growth and metastasis. Clin Exp Metastasis 15:140–150.

    PubMed  CAS  Google Scholar 

  • Singh RK, Varney ML (2000) IL-8 expression in malignant melanoma: implications in growth and metastasis. Histol Histopathol 15:843–849.

    PubMed  CAS  Google Scholar 

  • Siracky J (1979a) Approach to the problem of heterogeneity of human tumor-cell populations. Br J Cancer 39:570–577.

    CAS  Google Scholar 

  • Siracky J (1979b) Origin of the resistance of leukemic cells to folic acid antagonists. Nature 169:628–629.

    Google Scholar 

  • Sluyser M, Evers SG, De Goeij CC (1976) Sex hormone receptors in mammary tumours of GR mice. Nature 263:386–389.

    PubMed  CAS  Google Scholar 

  • Sluyser M, Van Nie R (1974) Estrogen receptor content and hormone-responsive growth of mouse mammary tumors. Cancer Res 34:3253–3257.

    PubMed  CAS  Google Scholar 

  • Soule HD, Maloney T, McGrath CM (1981) Phenotypic variance among cells isolated from spontaneous mouse mammary tumors in primary suspension culture. Cancer Res 41:1154–1164.

    PubMed  CAS  Google Scholar 

  • Stackpole CW (1981) Distinct lung-colonizing and lung-metastasizing cell populations in B16 mouse melanoma. Nature 289:798–800.

    PubMed  CAS  Google Scholar 

  • Stackpole CW (1983) Generation of phenotypic diversity in the B16 mouse melanoma relative to spontaneous metastasis. Cancer Res 43:3057–3065.

    PubMed  CAS  Google Scholar 

  • Starace G, Badaracco G, Greco C, Sacchi A, Zupi G (1982) DNA content distribution of in vivo and in vitro lines of Lewis lung carcinoma. Eur J Cancer Clin Oncol 18:973–978.

    PubMed  CAS  Google Scholar 

  • Stephens TC, Peacock JH (1982) Clonal variation in the sensitivity of B16 melanoma to m-AMSA. Br J Cancer 45:821–829.

    PubMed  CAS  Google Scholar 

  • Stich HF, Florian SF, Emson HE (1960) The DNA content of tumor cells. I. Polyps and adenocarcinomas of the large instestine of man. J Natl Cancer Inst 24:471–482.

    PubMed  CAS  Google Scholar 

  • Straus MJ (1977) Growth characteristics of lung cancer. In: Straus MJ (ed) Lung cancer. Gune & Stratton, New York, pp 19–32.

    Google Scholar 

  • Strzadala L, Opolski A, Radzikowski C, Mihich E (1981) Differential expression of murine leukemia antigen on L1210 parental and drug-resistant sublines. Cancer Res 41:4934–4937.

    PubMed  CAS  Google Scholar 

  • Subak-Sharpe H, Burk RR, Pitts JD (1969) Metabolic co-operation between biochemically marked mammalian cells in tissue culture. J Cell Sci 4:353–367.

    PubMed  CAS  Google Scholar 

  • Suzuki N, Withers HR, Koehler MW (1978) Heterogeneity and variability of artificial lung colony-forming ability among clones from mouse fibrosarcoma. Cancer Res 38:3349–3351.

    PubMed  CAS  Google Scholar 

  • Sweeney FL, Pot-Deprun J, Poupon MF, Chouroulinkov I (1982) Heterogeneity of the growth and metastatic behavior of cloned cell lines derived from a primary rhabdomyosarcoma. Cancer Res 42:3776–3782.

    PubMed  CAS  Google Scholar 

  • Symmans WF, Liu J, Knowles DM, Inghirami G (1995) Breast cancer heterogeneity: evaluation of clonality in primary and metastatic lesions. Hum Pathol 26:210–216.

    PubMed  CAS  Google Scholar 

  • Talmadge JE (1983) The selective nature of metastasis. Cancer Metastasis Rev 2:25–40.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Benedict K, Madsen J, Fidler IJ (1984) Development of biological diversity and susceptibility to chemotherapy in murine cancer metastases. Cancer Res 44:3801–3805.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Fidler IJ (1982a) Cancer metastasis is selective or random depending on the parent tumour population. Nature 297:593–594.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Fidler IJ (1982b) Enhanced metastatic potential of tumor cells harvested from spontaneous metastases of heterogeneous murine tumors. J Natl Cancer Inst 69:975–980.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Key ME, Hart IR (1981) Characterization of a murine ovarian reticulum cell sarcoma of histiocytic origin. Cancer Res 41:1271–1280.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Starkey JR, Davis WC, Cohen AL (1979) Introduction of metastatic heterogeneity by short-term in vivo passage of a cloned transformed cell line. J Supramol Struct 12:227–243.

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Starkey JR, Stanford DR (1981) In vitro characteristics of metastatic variant subclones of restricted genetic origin. J Supramol Struct Cell Biochem 15:139–151.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Talmadge JE, Zbar B (1987) Clonality of pulmonary metastases from the bladder 6 subline of the B16 melanoma studied by southern hybridization. J Natl Cancer Inst 78:315–320.

    PubMed  CAS  Google Scholar 

  • Tan MH, Shimano T, Chu TM (1981) Differential localization of human pancreas cancer-associated antigen and carcinoembryonic antigen in homologous pancreatic tumoral xenograft. J Natl Cancer Inst 67:563–569.

    PubMed  CAS  Google Scholar 

  • Tao TW, Burger MM (1977) Non-metastasising variants selected from metastasising melanoma cells. Nature 270:437–438.

    PubMed  CAS  Google Scholar 

  • Tarin D, Price JE (1979) Metastatic colonization potential of primary tumour cells in mice. Br J Cancer 39:740–754.

    PubMed  CAS  Google Scholar 

  • Thistlethwaithe P, Davidson DD, Fidler IJ, Roth JA (1983) Syngeneic humoral immune responses to tumor-associated antigens expressed by K-1735 UV-induced melanoma and its metastases. Cancer Immunol Immunother 15:11–16.

    PubMed  CAS  Google Scholar 

  • Trope C (1975) Different sensitivity to cytostatic drugs of primary tumor and metastasis of the Lewis carcinoma. Neoplasma 22:171–180.

    PubMed  CAS  Google Scholar 

  • Trope C (1982) Different susceptibilities of tumor cell subpopulations to sytotoxic agents. In: Fidler IJ, White RJ (eds) Design of models for testing cancer chemotherapeutic agents. D. Van Nostrand, New York, pp 64–79.

    Google Scholar 

  • Trope C, Aspegren K, Kullander S, Astedt B (1979) Heterogeneous response of disseminated human ovarian cancers to cytostatics in vitro. Acta Obstet Gynecol Scand 58:543–546.

    PubMed  CAS  Google Scholar 

  • Trope C, Hakansson L, Dencker H (1975) Heterogeneity of human adenocarcinomas of the colon and the stomach as regards sensitivity to cytostatic drugs. Neoplasma 22:423–429.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tu SM, Lin SH, Logothetis CJ (2002) Stem-cell origin of metastasis and heterogeneity in solid tumours. Lancet Oncol 3:508–513.

    PubMed  CAS  Google Scholar 

  • Valeriote F, van Putten L (1975) Proliferation-dependent cytotoxicity of anticancer agents: a review. Cancer Res 35:2619–2630.

    PubMed  CAS  Google Scholar 

  • van Lamsweerde AL, Henry N, Vaes G (1983) Metastatic heterogeneity of cells from Lewis lung carcinoma. Cancer Res 43:5314–5320.

    PubMed  Google Scholar 

  • Vaupel PW, Frinak S, Bicher HI (1981) Heterogeneous oxygen partial pressure and ph distribution in C3H mouse mammary adenocarcinoma. Cancer Res 41:2008–2013.

    PubMed  CAS  Google Scholar 

  • Vindelov LL (1977) Flow microfluorometric analysis of nuclear DNA in cells from solid tumors and cell suspensions. A new method for rapid isolation and straining of nuclei. Virchows Arch B Cell Pathol 24:227–242.

    PubMed  CAS  Google Scholar 

  • Vindelov LL, Hansen HH, Christensen IJ, et al. (1980) Clonal heterogeneity of small-cell anaplastic carcinoma of the lung demonstrated by flow-cytometric DNA analysis. Cancer Res 40:4295–4300.

    PubMed  CAS  Google Scholar 

  • Vindelov LL, Spang-Thomsen M, Visfeldt J, et al. (1982) Clonal evolution demonstrated by flow cytometric DNA analysis of a human colonic carcinoma grown in nude mice. Exp Cell Biol 50:216–221.

    PubMed  CAS  Google Scholar 

  • Wagner RK, Schulze RA (1978) Clinical relevance of androgen receptor in human prostate carcinoma. Acra Endocrinol Suppl 215:139–140.

    Google Scholar 

  • Walker JR, Rees RC, Teale D, Potter CW (1982) Properties of a Herpes virus-transformed hamster cell line–I. Growth and culture characteristics of sublines of high and low metastatic potential. Eur J Cancer Clin Oncol 18:1017–1026.

    PubMed  CAS  Google Scholar 

  • Wang N, Yu SH, Liener IE, et al. (1982) Characterization of high- and low-metastatic clones derived from a methylcholanthrene-induced murine fibrosarcoma. Cancer Res 42:1046–1051.

    PubMed  CAS  Google Scholar 

  • Ware JL, Maygarden SJ (1989) Metastatic diversity in human prostatic carcinoma: implications of growth factors and growth factor receptors for the metastatic phenotype. Pathol Immunopathol Res 8:231–249.

    PubMed  CAS  Google Scholar 

  • Weiss L (1980a) Brain Metastasis, Metastasis a monographic series. The Hague, Martinus Nijhoff 2, 30–49. 1980.

    Google Scholar 

  • Weiss L (1980b) Differences between cancer cells in primary and secondary tumors. In: Ioachim HL (ed) Pathobiology annual 1980 V 10. Raven, New York, pp 51–81.

    Google Scholar 

  • Weiss L (1980c) Cancer cell traffic from the lungs to the liver: an example of metastatic inefficiency. Int J Cancer 25:385–392.

    PubMed  CAS  Google Scholar 

  • Weiss L (1983) Random and nonrandom processes in metastasis, and metastatic inefficiency. Invasion Metastasis 3:193–207.

    PubMed  CAS  Google Scholar 

  • Weiss L (1986) Metastatic inefficiency: causes and consequences. Cancer Rev 3:1–24.

    Google Scholar 

  • Weiss L (1990) Metastatic inefficiency. Adv Cancer Res 54:159–211.

    PubMed  CAS  Google Scholar 

  • Weiss L (1996) Metastatic inefficiency: intravascular and intraperitoneal implantation of cancer cells. Cancer Treat Res 82:1–11.

    PubMed  CAS  Google Scholar 

  • Weiss L (2000) Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev 19:I–XI.

    PubMed  CAS  Google Scholar 

  • Weiss L, Holmes JC, Ward PM (1983) Do metastases arise from pre-existing subpopulations of cancer cells? Br J Cancer 47:81–89.

    PubMed  CAS  Google Scholar 

  • Weiss MA, Michael JG, Pesce AJ, DiPersio L (1981) Heterogeneity of beta 2-microglobulin in human breast carcinoma. Lab Invest 45:46–57.

    PubMed  CAS  Google Scholar 

  • Welch DR, Milas L, Tomasovic SP, Nicolson GL (1983) Heterogeneous response and clonal drift of sensitivities of metastatic 13762NF mammary adenocarcinoma clones to gamma-radiation in vitro. Cancer Res 43:6–10.

    PubMed  CAS  Google Scholar 

  • Wilmanns C, Fan D, O’Brian CA, Bucana CD, Fidler IJ (1992) Orthotopic and ectopic organ environments differentially influence the sensitivity of murine colon carcinoma cells to doxorubicin and 5- fluorouracil. Int J Cancer 52:98–104.

    PubMed  CAS  Google Scholar 

  • Wolman SR (1986) Cytogenetic heterogeneity: its role in tumor evolution. Cancer Genet Cytogenet 19:129–140.

    PubMed  CAS  Google Scholar 

  • Wong CW, Lee A, Shientag L, et al. (2001) Apoptosis: an early event in metastatic inefficiency. Cancer Res 61:333–338.

    PubMed  CAS  Google Scholar 

  • Woodruff MF (1983) Cellular heterogeneity in tumours. Br J Cancer 47:589–594.

    PubMed  CAS  Google Scholar 

  • Yu JL, Rak JW, Carmeliet P, et al. (2001) Heterogeneous vascular dependence of tumor cell populations. Am J Pathol 158:1325–1334.

    PubMed  CAS  Google Scholar 

  • Zetter BR (1990) The cellular basis of site-specific tumor metastasis. N Engl J Med 322:605–612.

    PubMed  CAS  Google Scholar 

  • Zetter BR (1993) Adhesion molecules in tumor metastasis. Semin Cancer Biol 4:219–229.

    PubMed  CAS  Google Scholar 

  • Zetter BR (1997) On target with tumor blood vessel markers. Nat Biotechnol 15:1243–1244.

    PubMed  CAS  Google Scholar 

  • Zupi G, Mauro F, Sacchi A (1980) Cloning in vitro and in vivo of Lewis lung carcinoma: properties and characteristics. Br J Cancer Suppl 41:309–310.

    Google Scholar 

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Singh, R.K., Talmadge, J.E. (2008). The evolution of diversity within tumors and metastases. In: Kaiser, H.E., Nasir, A. (eds) Selected Aspects of Cancer Progression: Metastasis, Apoptosis and Immune Response. Cancer Growth and Progression, vol 11. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6729-7_5

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