Analysis of the lodgement and extravasation of tumor cells in experimental models of hematogenous metastasis

Odashima S: Establishment of ascites hepatomas in the rat, 1951–1962. J Natl Cancer Inst Monogr 16: 51–93, 1964 Isaka H, Satoh H, Hirai H: Variants of Yoshida ascites sarcoma and α-feto protein. In: Nakahara W, Ono T, Sugimura T (eds): Differentiation and control of malignancy of tumor cells. Univ of Tokyo Press, Tokyo, 1974 pp 311–323 Sato H: Cancer metastasis from pathological studies on ascites tumors (in Japanese). Nippon Byori-Gakkai Kaishi (Trans Soc Jpn) 56: 9–36, 1967 Kanzaki K: Distribution of tumors in various organs foltowing the transplantation into the left chamber of the heart (studies with the Yoshida sarcoma and the ascites hepatoma). Gann 44: 445–463, 1953 Kurata T: Hematogenous dissemination of tumor cells (studies with the ascites hepatoma of the rat). Tr Soc Path Jpn 48: 1329–1337, 1959 Yamada T, Adachi L, Yoshino S: Distribution of tumor growth in various organ following injection of rat ascites hepatomas into the left chamber of the rat's heart. Bull Tokyo Med Dental Univ 9: 483–495, 1962 Yoshida K: Experimental studies on metastasis formation in the liver and lung by means of portal injection of the rat ascites hepatomas. Tohoku Igaku Zasshi 64: 107–118, 1961 Asahina S: An experimental study on relationship between tumors and organs by direct transplantation of small number of cells of ascites tumors into tissues. Fukushima Igaku Zasshi 17: 65–89, 1967 Khato J, Suzuki M, Sato H: Quantitative study on thromboplastin in various strains of Yoshida ascites hepatoma cells of rat. Gann 65: 289–294, 1974 Sato H, Suzuki M: Deformability and viability of tumor cells by transcapillary passage, with reference to organ affinity of metastasis in cancer. In: Weiss L (ed): Fundamental aspects of metastasis. North-Holland. Amsterdam, 1976, pp 311–317 Kohga S: Thromboplastic and fibrinolytic activities of ascites tumor cells of rat, with reference to their role in metastasis formation. Gann 65: 289–294, 1978 Khato J, Sato H, Suzuki M, Sato H: Filtrability and flow characteristics of leukemic and non-leukemic tumor cell suspension through polycarbonate filters in relation to hematogenous spread of cancer. Tohoku J Exp Med 128: 273–294, 1979 Griffiths JD, Salsbury AJ: Results of investigations into circulating cancer cells. In: Griffiths JD, Salsbury AJ (eds). Circulating cancer cells. Charles C Thomas, Springfield, 1965, pp 53–99 Agostino D: Are the showers of cancer cells in the blood responsible for an increase in metastasis? Tumori 54: 427–440, 1968 Engell HC: Cancer cells in the circulating blood. Acta Chir Scand 201 (Suppl): 9–70, 1955 Watne AL, Sandberg AA, Moore GE: The prognostic value of tumor cells in the blood. Arch Surg 83: 190–195, 1961 Besarga R, Kisieleski WE, Harvorsen K: A study on the establishment and growth of tumor metastases with tritiated thymidine. Cancer Res 20: 910–917, 1960 Munakata H: Studies on metastasis of cancer XII: experiments on the outcomes of tumor cells in the blood. Fukushima Igaku Zasshi 11: 1281–1285, 1961 Hofer KG, Prensky W, Hughas WL: Death and metastatic distrubution of tumor cells in mice monitored with 131I-tododeoxyuridine. J Natl Cancer Inst 43: 763–773, 1969 Fidler IJ: Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125I-5-iodo-2-deoxyuridine. J Natl Cancer Inst 45: 773–762, 1970 Sadler TE, Alexander P: Trapping and destruction of blood-borne syngeneic leukemic cells in lung, liver and spleen of normal and leukemic rats. Br J Cancer 33: 512–520, 1976 Hanna N, Fidler IJ: Role of natural killer cells in the destruction of circulating tumor emboli. J Natl Cancer Inst 65: 801–809, 1980 Zeidman I: The fate of circulating tumor cells I. Passage of cells through capillaries. Cancer Res 21: 38–39, 1961 Zeidman I: The fate of circulating tumor cells II. A mechanisms of cortison action in increasing metastases. Cancer Res 22: 501–503, 1962 Sato H, Suzuki M: Experimental studies on metastasis formation, with special reference to the mechanism of cancer cell lodgement in microcirculation. In: Shimamoto T, Numano F, Addison GM (eds): Atherogenesis, Vol II, international congress series No 269 (Proc of the second international symposium on atherogenesis, thrombogenesis and pridinol carbamate). Excerpta Medica, Amsterdam, 1973, pp 168–176 Nakamura K, Iino M, Suzuki K, Asahina H, Munakata H: An experimental study on factors affecting to metastasis formation (in Japanese). Nihhon Rinsho 24: 227–232, 1966 Nakamura K, Iino M, Suzuki K, Asahina S: The mechanisms of hematogenous metastasis in cancer (in Japanese). Igaku-no-Ayumi 59: 223–228, 1966 Nakamura K, Suzuki K: Quantitative study on transpulmonary passage of tumor cells. Gann 60: 483–497, 1969 Fidler IJ: The relationship of embolic homogeneity, number, size, and viability to the incidence of experimental metastasis. Eur J Cancer 9: 223–227, 1973 Liotta LA, Kleinerman J, Saidel GM: The significance of hematogenous tumor cell clumps in the metastasis process. Cancer Res 36: 889–894, 1976 Coman DR, Eisenberg RB, McCutcheon M: Factors affecting the distribution of tumor metastasis. Experiments with V2 carcinoma of rabbits. Cancer Res 9: 649–651, 1949 deLong RP, Coman DR: Relative susceptibility of various organs to tumor transplantation. Cancer Res 10: 512–515, 1950 Coman DR, deLong RP, McCutcheon M: Studies on the mechanisms of metastasis. The distribution of tumors in various organs in relation to the distribution of arterial emboli. Cancer Res 11: 648–651, 1951 Coman DR: Mechanisms responsible for the origin and distribution of blood-borne tumor metastasis: a review. Cancer Res 13, 397–404, 1953 Green HSN, Harvey EK: The relationship between the dissemination of tumor cells and the distribution of metastasis. Cancer Res 24: 799–811, 1964 Fisher B, Fisher E: The organ distribution of disseminated 51Cr-labeled tumor cells. Cancer Res 27: 412–420, 1967 Suemasu K, Katagiri M, Shimosato Y, Mikuni M, Ishikawa S: Initial stage of hematogenous metastasis of 51Cr-labeled tumor cells. Gann 61: 7–15, 1970 Baba T, Ishii M: Experimental tumor metastasis I. Triphenyl-tetrazolium chloride (TTC) staining as an ultravitally labeling method for tumor cells. Fukuoka Acta Medica 61: 307–317, 1970 Liotta LA, Kleinerman J, Saidel GM: Quantitative relationship of intravascular tumor cells, tumor vessels, and pulmonary metastasis following tumor implantation. Cancer Res 34: 997–1004, 1974 Fidler IJ, Nicolson GL: Organ selectivity for survival and growth of B16 melanoma variant tumor lines. J Natl Cancer Inst 57: 1199–1202, 1976 Suzuki M: Studies on metastasis XXIV. Experiments on the brain metastasis of the rat ascites hepatoma cells. Kosankin-byo-Kenkyu Zasshi 20: 181–194, 1968 Kawaguchi T, Nakamura K: Relationship between transcerebral passage of tumor cells and brain metastasis. Gann 68: 65–71, 1977 Luck B, Breedis C, Woo ZP, Berwick L, Nowell P: Differential growth of metastatic tumors in liver and lung. Experiments with rabbit V2 carcinoma. Cancer Res 12: 734–738, 1952 Bellamy D, Hinsull SM: Influence of lodgement site in the proliferation of metastases of Walker 256 carcinoma in the rat. Br J Cancer 37: 81–85, 1978 Kawaguchi T, Endo M, Yokoya S, Nakamura K: Influence of lodgement site in the proliferation-kinetics of tumor cells. Experientia 37: 414–415, 1981 Kawaguchi T, Endo M, Yokoya S, Nakamura K: Difference in proliferation-kinetics between tumor cells arrested in the brain and liver. Experientia 38: 1236–1237, 1982 Kawaguchi T, Nakamura K: Histological and electron microscopical studies of brain metastasis preceded by injury. In: Proceedings of the 31th annual meeting of the Japanese Cancer Association, Nagoya. Japanese Cancer Association, Tokyo, 1972, p 293 Kawaguchi T, Kitamura H, Nakamura K: Tumor formation of rat ascites hepatoma cells in the traumatized brain. Gann 70: 337–342, 1979 Kobavashi T, Kitamura H, Tobai S, Asahina S, Nakamura K: Experimental studies on hematogenous metastasis in the kidney (1). Effect of ischemia. Fukushima Igaku Zasshi 29: 247–257, 1980 Endo M: Effect of dead cell embloism of formation of hematogenous metastasis in the brain. Fukushima Igaku Zasshi 30: 189–203, 1980 Nakashima Y, Kawaguchi T, Nakamura K: The mechanisms of metastasis formation in injured parietal peritoneum by Yoshida sarcoma cells: an clectron microscopic study. Fukushima J Med Sci 31: 17–28, 1985 Fisher ER, Fisher B: Experimental studies of factors influencing the development of hepatic metastasis III. Effect of surgical trauma with special reference to liver injury. Ann Sur 150: 731–744, 1959 Warren BA: Arrest and extravasation of cancer cells with special reference to brain metastases and the microinjury hypothesis. In: Weiss L, Gilbert HA, Posner JB (eds): Brain metastasis, Martinus Nijhoff, The Hague, 1980, pp 81–99 Pajet S: Distribution of secondary growth in cancer of the breast. Lancet 1: 571–573, 1889 Fidler IJ: Selection of successive tumor lines for metastasis. Nature 242: 148–149, 1973 Kawaguchi T, Watanabe K, Nakamura K: Biological and metastatic properties of rat ascites hepatoma sublines with different adhessiveness. In: Proceedings of the 42th annual meeting of the Japanese Cancer Association, Nagoya. Japanese Cancer Association, Tokyo, 1982, p 425 Watanabe K, Kawaguchi T, Nakamura K: Selection and establishment of rat ascites hepatoma AH7974 variant sublines highly metastatic to the eye and its mechanisms involved in the process. In: Proceedings of the 43th annual meeting of the Japanese Cancer Association, Fukuoka. Japanese Cancer Association. Tokyo, 1983, p 428 Kawaguchi T, Watanabe K, Igarashi S, Nakamura K: Selection and establishment of highly metastatic rat ascites hepatoma variant subline to the peritoneum. In: Proceedings of the 43th annual meeting of the Japanese Cancer Association, Fukuoka. Japanese Cancer Association, Tokyo, 1983. p 437 Sakuma A, Kawaguchi T: Metastatic potential to ovary of rat ascites hepatoma AH7974 variant cell line selected in vivo. In preparation for submission Proctor JW: Rat sarcoma model supports both ‘soil seed’ and ‘mechanical’ theories of metastatic spread. Br J Cancer 34: 651–654, 1976 Kawaguchi T, Kawaguchi M, Lembo TM, Nicolson GL: Brain meninges tumor formation by in vivo-selected metastatic B16 melanoma variants in mice. Clin Exp Metastasis 1: 247–259, 1983 Tarin D, Price JE: Influence of microenvironment and vascular anatomy on ‘metastatic’ colonization potential of mammary tumors. Cancer Res 41: 3604–3609, 1981 Brunson KW, Beattie G, Nicolson GL: Selection and altered properties of brain-colonizing metastatic melanoma. Nature 272: 543–545, 1978 Irimura T, Gonzalez R, Nicolson GL: Effect of tunicamycin on B16 metastatic melanoma cell surface glycoproteins and blood-borne arrest and survival properties. Cancer Res 41: 3411–3418, 1981 Nakamura K: Invasion and metastasis (in Japanese). In: Sugano H, Kobayashi H (eds): Shuyo-Biryori-Gaku. Asakura Pub, Tokyo, 1970, pp 61–72 Sakurai T, Ebina Y, Yokoya S, Nakamura K: Electron microscopic studies on extravasation of ascites hepatoma in the kidney and lung. Fukushima J Med Sci 24: 1–21, 1977 Nakamura K, Kawaguchi T, Asahina S, Sakurai T, Ebina Y, Yokoya S, Morita M: Electronmicroscopic studies on extravasation of tumor cells and early foci of hematogenous metastasis. Gann Monogr Cancer Res 20: 57–71, 1977 Kawaguchi T, Tobai S, Nakamura K: Electron microscopic studies on stickness of tumor cells to normal cells. Saibo 10: 573–579, 1978 Kawaguchi T, Endo M, Tobai S, Nakamura K: Behavior pattern of rat ascites tumor cells arrested in liver sinusoids: an electron microscopic study. Gann 70: 277–290, 1979 Kawaguchi T, Tobai S, Nakamura K: Extravascular migration of tumor cells in the brain: an electron microscopic study. Invasion Metastasis 2: 40–50, 1982 Warren BA, Guldner FH: Ultrastructure of the adhesion of Hela cells to human vein wall. Angiologica 6: 32–53, 1969 Warren BA, Vales O: The adhesion of thromboplastic tumor emboli to vessel wall in vivo. Br J Exp Pathol 53: 301–313, 1972 Cotmore SF, Carter RL: Mechanisms of enhanced intrahepatic metastasis in surfactant-treated hamsters: an electron microscopy study. Int J Cancer 11: 725–738, 1973 Sindelar WF, Tralka TS, Ketcham AS: Electron microscopic observations on formation of pulmonary metastases. J Sur Res 18: 137–161, 1975 Eguchi G, Okada T: Ultrastructure of the differentiated colony derived from a single isolated chondrocyte in in vitro culture. Dev Growth Diff 12: 297–312, 1971 Abercrombie M, Ambrose EJ: The surface properties of cancer cells: a review. Cancer Res 22: 525–548, 1962 Roos E, Dingeman KP, van de Pavert IV, van den Bergh-Weerman M: Invasion of lymphosarcoma cells into the perfused mouse liver. J Natl Cancer Inst 58: 399–407, 1977 Roos E, Dingemans KP, de Pavert IV: Mammary-carcinoma cells in mouse liver; intiltration of liver tissue and interaction with Kupffer cells. Br J Cancer 38: 88–99, 1978 Dingemans KP, Ross E: Ultrastructural aspects of the invasion of liver by cancer cells (II). In: Liver metastasis. Weiss L. Gilbert HA (eds). Martinus Nijhoff, 1982, pp 51–76 Wallace EC, Chew EC, Jones DS: Arrest and extravasation of cancer cells in the lung. In: Pulmonary metastasis. Weiss L, Gilbert HA (eds). Martinus Nijhoff, The Hague. 1978, pp 26–42 Kinjo M: Lodgement and extravasation of tumor cells in blood-borne metastasis: an electron microscopic study. Br J Cancer 38: 293–301, 1978 Foidart JM, Bere EW, Yaar M, Rennard SI, Gullino M, Martin GR, Katz SI: Distribution and immunoelectron microscopic localization of laminin, a noncollagenous basement membrane glycoprotein. Lab Invest 42: 336–342, 1980 Dingemans KP: Behavior of intravenously injected malignant lymphoma cells. A morphologic study. J Natl Cancer Inst 51: 1883–1895, 1973 Dingemans KP: Invasion of liver tissue by blood-borne mammary carcinoma cells. J Natl Cancer Inst 53: 1813–1824, 1974 Dingemans KP, Roos E, van den Bergh Weerman MA, van de Pavert IV: Invasion of liver tissue by tumor cells and leukocytes: comparative ultrastructure. J Natl Cancer Inst 60: 583–598, 1978 Chew EC, Josephson RL, Wallace AC: Morphological aspects of the arrest of circulating cancer cells. In: Weiss L (ed): Fundamental aspect of metastasis. North Holland, Amsterdam, 1976, pp 121–150 Locker J, Goldblatt PJ, Leighton J: Ultrastructural features of invasion in chick embryo liver metastasis of Yoshida ascites hepatoma. Cancer Res 30: 1632–1644, 1970 Jones DS, Wallace AC, Fraser EE: Sequence of events in experimental metastases of Walker 256 tumor: light, immunofluorescent, and electron microscopic observations. J Natl Cancer Inst 46: 493–504, 1971 Tobai S, Kobayashi T, Kitamura H, Asahina S, Nakamura K: Electronmicroscopic studies on metastatic lesions in glomeruli of ascites hepatoma AH130. In: Proceeding of the 36th annual meeting of the Japanese Cancer Association, Tokyo. Japanese Cancer Association, Tokyo, 1977, p 250 Wood S: Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. Arch Path 66: 550–568, 1958 Ludatsher RM, Luse SA, Suntzeff V: An electron microscopic study of pulmonary tumor emboli from transplantable Morris hepatoma 5123. Cancer Res 27: 1939–1952, 1967 Brooks RE: Mouse mammary tumor metastases in lung: an electron microscopic study. Cancer Res 30: 2156–2165, 1970 Sarker K: Tumor cell invasion of hepatocytes in transplantable plasma cell neoplasm of mice. Virchows Arch Abst B 11: 303–309, 1972 Carr I, McGinty F, Norris P: The fine structure of neoplastic invasion: invasion of liver, skeletal rauscle and lymphatic vessels by the Rd/3 tumor. J Patho 118: 91–97, 1976 Cambell FR: Ultrastructural study of liver sinusoids of mice during invasion of leukemic myelocytes. J Natl Cancer Inst 58: 369–376, 1977 Machade EA, Gerard DA, Mitchell JR: Arrest and extravasation of neoplastic cells: an electron microscopy study of serial sections at sequential stages. Virchows Arch (Pathol A) 396: 73–89, 1982 Azzarelli B, Muller J, Mirkin LD, Goheen MP: Transvascular migration of L2C leukemic cells studied in the liver of the guinea pig. Virchows Arch (Pathol Anat) 406: 425–440, 1985 Carter RL: General pathology of the metastatic process. In: Baldwin RW (ed): Secondary spread of cancer. Academic press, London, 1978, pp 1–52 Warren BA: Environment of the blood-borne tumor embolus adherent to vessel wall. J Med 4: 150–177, 1973 Marchesi VT, Florey HW: Electron microscopic observations on the migration of leukocytes. Quert J Exp Physiol 45: 343–348, 1960 Kramer RH, Nicolson GL: Interactions of tumor cells with vascular endothelial cell monolayers: a model for metastatic invasion. Proc Natl Acad Sci 76: 5704–5708, 1979 Tarin D: Sequential electron microscopical study of experimental mouse skin carcinogenesis. Int J Cancer 2: 195–211, 1967 Ozzello L: Electron microscopic study of functional and dysfunctional human mammary glands. J Invest Dermatol 63: 19–26, 1974 Sigino T, Kawaguchi T, Nakamura K: Expression of metastatic potential of mammary carcinoma spontaneously developed in C3H mouse. In. Proceedings of the 44th annual meeting of the Japanese Cancer Association, Tokyo. Japanese Cancer Association, Tokyo, 1985, p 470 Araki K: An ultrastructural evaluation of experimentally induced cancer cell invasion into the lymphatic vessel in rats. Bull Osaka Med School 28: 7–13, 1982 Carr I, Carr J: Experimental lymphatic invasion and metastasis. In: Weiss L, Gilbert S, Ballon C (eds): Lymphatic system metastasis. GK Hall, Boston, 1980, pp 41–73 Peter PH, Bruyn D, Cho Y: Entry of metastatic malignant cells into the circulation from a subcutaneously growing myelogeneous tumor. J Natl Cancer Inst 62: 1221–1227, 1979 Babai F, Tremblay G: Ultrastructural study of liver invasion by Novikoff hepatoma. Cancer Res 32: 2765–2770, 1972 Kawaguchi T, Kawaguchi M, Dulski KM, Nicolson GL: Cellular behavior of metastatic B16 melanoma in experimental blood-borne implantation and cerebral invasion: an electron microscopic study. Invasion Metastasis 5: 16–30, 1985 Woolley DE: Proteolytic enzymes of invasive cells. In: Mareel M, Calman KC (eds): Invasion experimental and clinical implications. Oxford Medical Pub, Oxford, 1984, pp 228–251 Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S: Metastatic potential correlates with enzymatic degradation of membrane collagen. Nature 284: 67–68, 1980 Nakajima M, Irimura T, Di Ferrante DT, Di Ferrante N, Nicolson GL: Heparan sulfate degradation correlates with tumor invasion and metastatic properties of B16 melanoma sublines. Science 202: 611–613, 1983 Kramer RH, Vogal KG, Nicolson GL: Solubilization and degradation of subendothelial glycoproteins and proteoglycans by metastatic tumor cells. J Biol Chem 257: 2678–2686, 1982 Kawaguchi T, Tobai S, Nakamura K: Cell surface structure of Yoshida sarcoma cells arrested in the liver sinusoids. In: Proceedings of the 39th annual meeting of the Japanese Cancer Association, Tokyo. Japanese Cancer Association, Tokyo, 1980, p 172 Poste G: We wish to thank Dr G Poste for the edited version