Abstract
This review starts on one of our special interests, the organ preference of metastasis. We examined data on 1,117 autopsy cases and found that the organ distribution of metastasis of cancers of the lung, pancreas, stomach, colon, rectum, uterine cervix, liver, bile duct, and esophagus involved the lung, liver, adrenal gland, bone/bone marrow, lymph node, and pleura/peritoneum. Cancers of the kidney, thyroid, ovary, choriocarcinoma, and breast, however, manifested different metastatic patterns. The distribution of leukemia and lymphoma metastases was quite different from that of epithelial cancers. On the basis of experimental studies, we believe that the anatomical-mechanical hypothesis should be replaced by the microinjury hypothesis, which suggests that tissue microinjury induced by temporal tumor cell embolization is crucial for successful metastasis. This hypothesis may actually reflect the so-called inflammatory oncotaxis concept. To clarify the mechanisms underlying metastasis, we developed an experimental model system of a rat hepatoma AH7974 that embraced substrate adhesiveness. This model did not prove a relationship between substrateadhesion potential and metastatic lung-colonizing potential of tumor cells, but metastatic potential was correlated with the expression of the laminin carbohydrate that was recognized by Griffonia (Bandeiraea) simplicifolia isolectin G4. Therefore, we investigated the relationship between carbohydrate expression profiles and metastasis and prognosis. We indeed found an intimate relationship between the carbohydrate expression of cancer cells and the progression of malignant tumors, organ preference of metastasis, metastatic potential of tumor cells, and prognosis of patients.
Keywords: Anatomical-mechanical hypothesis, cancer metastasis, carbohydrates, cell adhesion molecule, organ preference of metastasis, seed-soil hypothesis, Tn antigen.
Graphical Abstract
[1]
The Editorial Board of the Cancer Statistics in Japan, Takayama,S., Editor-in-chief. Cancer Statistics in Japan 2012; Foundation for Promotion of Cancer Research, National Cancer Center: Tokyo, 2012.
[2]
Langley, R.R.; Fidler, I.J. Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr. Rev., 2007, 28, 297-321.
[3]
Nguyen, D.X.; Bos, P.D. Massagué, J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer, 2009, 9, 274-284.
[4]
Witz, I.P. The tumor microenvironment: the making of a paradigm. Cancer Microenviron., 2009, 2(1), 9-17.
[5]
Labelle, M.; Hynes, R.O. The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov., 2012, 2, 1091-1099.
[6]
Kawaguchi, T. Cancer metastasis: characterization and identification of the behavior of metastatic tumor cells and the cell adhesion molecules, including carbohydrates. Curr. Drug Targets Cardiovasc. Haematol. Disord., 2005, 5, 39-64.
[7]
Kawaguchi, T.; Takazawa, H.; Imai, S.; Morimoto, J.; Watanabe, T.; Kanno, M.; Igarashi, S. Expression of Vicia villosa agglutinin (VVA)-binding glycoprotein in primary breast cancer cells in relation to lymphatic metastasis: is atypical Muc1 bearing Tn antigen a receptor of VVA? Breast Cancer Res. Treat., 2006, 98, 31-43.
[8]
Suzuki, H.; Kawaguchi, T.; Hasegawa, T.; Yonechi, A.; Ohsugi, J.; Higuchi, M.; Yamada, F.; Shio, Y.; Fujiu, K.; Kanno, R.; Ohishi, A.; Gotoh, M. Prognostic impact of p53 protein overexpression in patients with node-negative lung adenocarcinoma. Cancer Lett., 2006, 237, 242-247.
[9]
Shio, Y.; Suzuki, H.; Kawaguchi, T.; Ohsugi, J.; Higuchi, M.; Fujiu, K.; Kanno, R.; Ohishi, A.; Gotoh, M. Carbohydrate status detecting by PNA is changeable through cancer prognosis from primary to metastatic nodal site: a possible prognostic factor in patient with node-positive lung adenocarcinoma. Lung Cancer, 2007, 57, 187-192.
[10]
Kawaguchi, T.; Imai, S.; Haga, S.; Morimoto, J.; Honda, T. Demonstration and Partial Identification of Aberrant MUC1 Bearing Tn Antigen in Rat Ascites Hepatoma AH109A Cells with Strong Lymph Node Metastasis Propensity. In: Cancer Metastasis Research; Watanabe, A., Ed.; Nova Science Publishers:Hauppauge, NY. , 2008; pp. 147-163.
[11]
Kawaguchi, T.; Honda, T.; Nishihara, M.; Yamamoto, T.; Yokoyama, M. Histological study on side effects and tumor targeting of a block copolymer micelle on rats. J. Control. Release, 2009, 136, 240-246.
[12]
Kawaguchi, T.; Kanno, M.; Asahi, S.; Honda, T. Relationship Between Carbohydrate Expression Profiles of Cancer Cells and Prognosis of Breast Cancer Patients. In: Aggressive Breast Cancer; DeFrina, R.H., Ed.; Nova Science Publishers: Hauppauge, NY, 2010; pp. 231-235.
[13]
Kawaguchi, T.; Kanno, M.; Takazawa, H.; Imai, S.; Morimoto, J.; Haga, S.; Honda, T. Lymphatic Spreading Propensity and Aberrant MUC1 Bearing TN/TN-like Carbohydrate of Aggressive Breast Cancer Cells. In: Aggressive Breast Cancer; DeFrina, R.H., Ed.; Nova Science Publishers: Hauppauge, NY, 2010; pp. 199-228.
[14]
Kawaguchi, T. Cancer Metastasis Research, Pathological Insight; Nova Science Publishers: Hauppauge, NY, 2012.
[16]
Paget, S. The distribution of secondary growths in cancer of the breast. Lancet, 1889, 133, 571-573.
[19]
Viadana, E.; Bross, I.D.J.; Pickren, J.W. Cascade Spread of Blood-borne Metastases in Solid and Nonsolid Cancers of Humans. In: Pulmonary Metastasis; Weiss, L.; Gilbert, H.A., Eds.; Martinus Nijhoff Medical Division: The Hague, 1978; pp. 142-167.
[20]
Batson, O.V. The Vertebral Vein System: Caldwell Lecture, 1956. In: Bone Metastasis; Weiss, L.; Gilbert, H.A., Eds.; GK Hall: Boston, 1981; pp. 21-48.
[21]
de la Monte, S.M.; Moore, G.W.; Hutchins, G.M. Patterned distribution of metastases from malignant melanoma in humans. Cancer Res., 1983, 43, 3427-3433.
[22]
Viadana, E.; Bross, I.D.J.; Pickren, J.W. The spread of blood-borne metastases in malignant lymphomas of man. Oncology, 1976, 33, 123-131.
[23]
Lee, Y-T.N. Breast carcinoma: pattern of metastasis at autopsy. J. Surg. Oncol., 1983, 23, 175-180.
[25]
de la Monte, S.M.; Moore, G.W.; Hutchins, G.M. Nonrandom distribution of metastases in neuroblastic tumors. Cancer, 1983, 52, 915-925.
[26]
Abrams, H.L.; Spiro, R.; Goldstein, N. Metastases in carcinoma: analysis of 1000 autopsied cases. Cancer, 1950, 3, 74-85.
[27]
Mori, W.; Adachi, Y.; Okabe, H.; Oota, K. An analysis of 755 autopsied cases of malignant tumors: a statistical study of their metastasis. Jpn. J. Cancer Clin., 1963, 9, 351-374. [in Japanese].
[28]
Urano, Y.; Fukushima, T.; Kitamura, S.; Mori, H.; Baba, K.; Aizawa, S. Recent knowledge about cancer metastasis: cancer metastasis as observed in autopsy records. Oncologia, 1985, 15, 46-71. [in Japanese].
[29]
Sugarbaker, E.V. Patterns of metastasis in human malignancies. Cancer Biol. Rev., 1981, 2, 235-278.
[30]
Hart, I.R. ‘Seed and soil’ revisited: mechanisms of site-specific metastasis. Cancer Metastasis Rev., 1982, 1, 5-16.
[31]
Zetter, B.R. The cellular basis of site-specific tumor metastasis. N. Engl. J. Med., 1990, 322, 605-612.
[32]
Nicolson, G.L. Cancer progression and growth: relationship of paracrine and autocrine growth mechanisms to organ preference of metastasis. Exp. Cell Res., 1993, 204, 171-180.
[33]
Dittmar, T.; Heyder, C.; Gloria-Maercker, E.; Hatzmann, W.; Zänker, K.S. Adhesion molecules and chemokines: the navigation system for circulating tumor (stem) cells to metastasize in an organ-specific manner. Clin. Exp. Metastasis, 2008, 25, 11-32.
[34]
Talmadge, J.E.; Fidler, I.J. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res., 2010, 70, 5649-5669.
[35]
Kawaguchi, T.; Kawaguchi, M.; Miner, K.M.; Lembo, T.M.; Nicolson, G.L. Brain meninges tumor formation by in vivo-selected metastatic B16 melanoma variants in mice. Clin. Exp. Metastasis, 1983, 1, 247-259.
[36]
Kawaguchi, T.; Ikeda, K. Experimental studies on factors affecting tumor growth in the liver I. A scrutiny of number of cells and volume of fluid inoculated. Fukushima J. Med. Sci., 1976, 23, 11-16.
[37]
Sugino, T.; Kawaguchi, T. New metastatic tumor model using cancer cell nest from C3H mammary carcinoma. Nyugan Kiso Kenkyu, 1992, 2, 34-38. [in Japanese].
[38]
Sato, H.; Suzuki, M. Deformability and Viability of Tumor Cells by Transcapillary Passage, with Reference to Organ Affinity of Metastasis in Cancer. In: Fundamental Aspects of Metastasis; Weiss, L., Ed.; North-Holland: Amsterdam, 1976; pp. 311-317.
[39]
Suzuki, M. Studies on metastasis XXIV. Experiments on the brain metastasis of the rat ascites hepatoma cells. J. Tuberculosis and Leprosy, 1968, 20, 181-194. [in Japanese].
[40]
Asahina, S. Experimental studies on relationship between tumors and organs by direct transplantation of small number of cells of ascites tumor into tissues. Fukushima Igaku Zasshi, 1967, 17, 65-89. [in Japanese].
[41]
Kawaguchi, T.; Nakamura, K. Relationship between transcerebral passage of tumor cells and brain metastasis. Gann, 1977, 68, 65-71.
[42]
Warren, B.A. Arrest and extravasation of cancer cells with special reference to brain metastasis and microinjury hypothesis. In: Brain Metastasis; Weiss, L.; Gilbert, H.A.; Posner, J.B., Eds.; GK Hall: Boston, 1980; pp. 81-99.
[43]
Sato, H.; Suzuki, M. Experimental studies on metastasis formation, with special reference to the mechanism of cancer cell lodgement in the microcirculation.In: Atherogenesis. Vol. II, International
Congress Series No. 269, Proceedings of the Second International
Symposium on Atherogenesis, Thrombogenesis and Pyridinolcarbamate
Treatment, Shimamoto, T.; Numano, F.; Addison,
G.M., Eds.; Excerpta Medica: Amsterdam. 1973, pp. 168-176.
[44]
Endo, M. Effect of dead cell embolism on formation of haematogenous metastases in the brain. Fukushima Igaku Zasshi, 1980, 30, 189-203. [in Japanese].
[45]
Kobayashi, T.; Kitamura, H.; Tobai, S.; Asahina, S.; Nakamura, K. Experimental studies on hematogenous metastasis in the kidney (1): effect of ischemia. Fukushima Igaku Zasshi, 1980, 29, 247-257. [in Japanese].
[46]
Nakamura, K.; Suzuki, K. Quantitative study on the trans-pulmonary passage of tumor cells. Gann, 1969, 60, 483-497.
[47]
Sakurai, T.; Ebina, Y.; Yokoya, S.; Nakamura, K. Electron microscopic studies on extravasation of ascites hepatomas in the kidney and lung. Fukushima J. Med. Sci., 1977, 24, 1-21.
[48]
Ogiu, T.; Nakamura, K. Growth of intraperitoneally transplanted ascites hepatoma, AH39 cells, in the area of gelatin sponge inoculation into the abdominal wall of Donryu rats. Gann, 1979, 70, 173-179.
[49]
Kawaguchi, T.; Kitamura, H.; Nakamura, K. Tumor formation of rat ascites hepatoma cells in the traumatized brain. Gann, 1979, 70, 337-342.
[50]
Kawaguchi, T.; Endo, M.; Tobai, S.; Nakamura, K. Behavior pattern of rat ascites tumor cells arrested in liver sinusoids: an electron microscopic study. Gann, 1979, 70, 277-290.
[51]
Kawaguchi, T.; Tobai, S.; Nakamura, K. Extravascular migration of tumor cells in the brain: an electron microscopic study. Invasion Metastasis, 1982, 2, 40-50.
[52]
Nakashima, Y.; Kawaguchi, T.; Nakamura, K. The mechanisms of metastasis formation in injured parietal peritoneum by Yoshida sarcoma cells: an electron microscopic study. Fukushima J. Med. Sci., 1985, 31, 17-28.
[53]
Velnar, T.; Bailey, T.; Smarkolj, V. The wound healing process: an overview of the cellular and molecular mechanisms. J. Int. Med. Res., 2009, 37, 1528-1542.
[54]
French, J.E.; Macfarlane, R.G. Haemostasis and thrombosis.In:General Pathology, 4th ed; Florey, L., Ed.; Lloyd-Luke: London, 1970, pp. 273-317.
[55]
Wood, S., Jr Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. Arch. Pathol., 1958, 66, 550-568.
[56]
Chambers, A.F.; Groom, A.C.; MacDonald, I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer, 2002, 2, 563-572.
[58]
Bendas, G.; Borsig, L. Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int. J. Cell Biol., 2012.
[http://dx.doi.org/10.1155/2012/676731]
[http://dx.doi.org/10.1155/2012/676731]
[59]
Cox, T.R.; Bird, D.; Baker, A.M.; Barker, H.E.; Ho, M-W.Y.; Lang, G.; Erler, J.T. LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res., 2013, 73, 1721-1732.
[60]
Orr, F.W.; Warner, D.J. Effects of systemic complement activation and neutrophil-mediated pulmonary injury on the retention and metastasis of circulating cancer cells in mouse lungs. Lab. Invest., 1990, 62, 331-338.
[61]
Soares, F.A.; Shaughnessy, S.G.; MacLarkey, W.R.; Orr, F.W. Quantification and morphologic demonstration of reactive oxygen species produced by Walker 256 tumor cells in vitro and during metastasis in vivo. Lab. Invest., 1994, 71, 480-489.
[62]
Dinarello, C.A. Why not treat human cancer with interleukin-1 blockade? Cancer Metastasis Rev., 2010, 29, 317-329.
[64]
Dvorak, H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med., 1986, 315, 1650-1659.
[65]
Zeamari, S.; Roos, E.; Stewart, F.A. Tumour seeding in peritoneal wound sites in relation to growth-factor expression in early granulation tissues. Eur. J. Cancer, 2004, 40, 1431-1440.
[66]
Rudenstam, C.M. Experimental studies on trauma and metastasis formation. Acta Chir. Scand. Suppl., 1968, 391, 1-83.
[67]
Hofer, S.O.P.; Molema, G.; Hermens, R.A.E.C.; Wanebo, H.J.; Reichner, J.S.; Hoekstra, H.J. The effect of surgical wounding on tumour development. Eur. J. Surg. Oncol., 1999, 25, 231-243.
[68]
Murthy, S.M.; Goldschmidt, R.A.; Rao, L.N.; Ammirati, M.; Buchmann, T.; Scanlon, E.F. The influence of surgical trauma on experimental metastasis. Cancer, 1989, 64, 2035-2044.
[69]
DerHagopian, R.P.; Sugarbaker, E.V.; Ketcham, A. Inflammatory oncotaxis. JAMA, 1978, 240, 374-375.
[70]
Poste, G. Experimental systems for analysis of the malignant phenotype. Cancer Metastasis Rev., 1982, 1, 141-199.
[71]
Nicolson, G.L. Cancer metastasis: tumor cell and host organ properties important in metastasis to specific secondary sites. Biochim. Biophys. Acta, 1988, 948, 175-224.
[72]
Matsuura, N.; Puzon-McLaughlin, W.; Irie, A.; Morikawa, Y.; Kakudo, K.; Takada, Y. Induction of experimental bone metastasis in mice by transfection of integrin α4β1 into tumor cells. Am. J. Pathol., 1996, 148, 55-61.
[74]
Odashima, S. Establishment of ascites hepatomas in the rat: 1951-1962. Natl. Cancer Inst. Monogr., 1964, 16, 51-93.
[75]
Sato, H. Experimental studies on the mechanism of metastasis formation. Acta Pathol. Jpn., 1959, 9, 685-706.
[76]
Sato, Y. Difference in Genome Between Rat Ascites Hepatoma AH7974 and AH7974F Cells Which Display Differential Liver
Metastatic Ability. PhD Thesis. No. 230, Fukushima Medical
University School of Medicine: Fukushima. 1997. (in Japanese)
[77]
Kawaguchi, T.; Endo, M.; Yokoya, S.; Nakamura, K. Influence of lodgement site on the proliferation-kinetics of tumor cells. Experientia, 1981, 37, 414-415.
[78]
Kawaguchi, T.; Endo, M.; Yokoya, S.; Nakamura, K. Difference in proliferation-kinetics between tumor cells arrested in the brain and liver. Experientia, 1982, 38, 1236-1237.
[79]
Kawaguchi, T.; Nakamura, K. Analysis of the lodgement and extravasation of tumor cells in experimental models of hematogenous metastasis. Cancer Metastasis Rev., 1986, 5, 77-94.
[80]
Kawaguchi, T.; Endo, M.; Tobai, S.; Nakamura, K. Behavior pattern of rat ascites tumor cells arrested in liver sinusoids: an electron microscopic study. Gann, 1979, 70, 277-290.
[81]
Paku, S.; Döme, B.; Tóth, R.; Timár, J. Organ-specificity of the extravasation process: an ultrastructural study. Clin. Exp. Metastasis, 2001, 18, 481-492.
[82]
Dingeman, K.P.; Roos, E.; van den Bergh Weerman, M.A.; van de Pavert, I.V. Invasion of liver tissue by tumor cells and leucocytes: comparative ultrastructure. J. Natl. Cancer Inst., 1978, 60, 583-598.
[83]
Shibue, T.; Brooks, M.W.; Inan, M.F.; Reinhardt, F.; Weinberg, R.A. The outgrowth of micrometastases is enabled by the formation of filopodium-like protrusions. Cancer Discov., 2012, 2, 706-721.
[84]
Watanabe, K. Experimental study on organ preference of cancer metastasis: establishment and characterization of highly metastatic sublines to eye ball derived from rat ascites hepatoma AH7974. Fukushima Igaku Zasshi, 1989, 39, 575-584. [in Japanese].
[85]
Saito, A. The development of useful experimental model for analysis of organ preference on cancer metastasis: the establishment of highly metastatic cell lines to rat ovary and their metastatic propensity. Fukushima Igaku Zasshi, 1989, 39, 585-595. [in Japanese].
[86]
Hoshi, N. Establishment of Highly Metastatic Subline Bo-4 from Rat Ascites Hepatoma AH7974., PhD Thesis, No. 200, Fukushima Medical
University School of Medicine: Fukushima,. 1995. (in Japanese)
[87]
Fidler, I.J. Selection of successive tumour lines for metastasis. Nat. New Biol., 1973, 242, 148-149.
[88]
Gaede, S.D.; Sholley, M.M.; Quattropani, S.L. Endothelial mitosis during the initial stages of corpus luteum neovascularization in the cycling adult rat. Am. J. Anat., 1985, 172, 173-180.
[89]
Brunson, K.W.; Nicolson, G.L. Selection of malignant melanoma variant cell lines for ovary colonization. J. Supramol. Struct., 1979, 11, 517-528.
[90]
Ferry, A.P.; Font, R.L. Carcinoma metastatic to the eye and orbit. I. A clinicopathologic study of 227 cases. Arch. Ophthalmol., 92, 276-286. 1974
[91]
Young, R.H. From Krukenberg to today: the ever present problems posed by metastatic tumors in the ovary: part I. Historical perspective, general principles, mucinous tumors including the Krukenberg tumor. Adv. Anat. Pathol., 2006, 13, 205-227.
[92]
Kawaguchi, T.; Saito, A. Pathology of organ preference metastasis. Mebio, 1992, 7, 22-30. [in Japanese].
[93]
Kizuka, F.; Tokuda, N.; Takagi, K.; Adachi, Y.; Lee, L.; Tamura, I.; Maekawa, R.; Taketani, T.; Tamura, H.; Suzuki, T.; Owada, Y.; Sugino, N. Involvement of bone marrow-derived vascular progenitor cells in neovascularization during formation of the corpus luteum in mice. Biol. Reprod., 2012, 87, 1-7.
[94]
Fidler, I.J.; Kripke, M.L. Metastasis results from preexisting variant cells within a malignant tumor. Science, 1977, 197, 893-895.
[95]
Nicolson, G.L. Tumor and host molecules important in the organ preference of metastasis. Semin. Cancer Biol., 1991, 2, 143-154.
[96]
Brunson, K.W.; Beattie, G.; Nicolson, G.L. Selection and altered properties of brain-colonising metastatic melanoma. Nature, 1978, 272, 543-545.
[97]
Miner, K.M.; Kawaguchi, T.; Uba, G.W.; Nicolson, G.L. Clonal drift of cell surface, melanogenic, and experimental metastatic properties of in vivo-selected, brain meninges-colonizing murine B16 melanoma. Cancer Res., 1982, 42, 4631-4638.
[98]
Irimura, T.; Nicolson, G.L. Carbohydrate chain analysis by lectin binding to electrophoretically separated glycoproteins from murine B16 melanoma sublines of various metastatic properties. Cancer Res., 1984, 44, 791-798.
[99]
Nicolson, G.L.; Dulski, K.; Basson, C.; Welch, D.R. Preferential organ attachment and invasion in vitro by B16 melanoma cells selected for differing metastatic colonization and invasive properties. Invasion Metastasis, 1985, 5, 144-158.
[100]
Nicolson, G.L.; Van Pelt, C.; Irimura, T.; Kawaguchi, T. Stabilities and characteristics of brain meninges-colonizing murine melanoma cells. Prog. Exp. Tumor Res., 1985, 29, 17-35.
[101]
Nicolson, G.L.; Kawaguchi, T.; Kawaguchi, M.; Van Pelt, C. Brain surface invasion and metastasis of murine malignant melanoma variants. J. Neurooncol., 1987, 4, 209-218.
[102]
Nicolson, G.L.; Inoue, T.; Van Pelt, C.S.; Cavanaugh, P.G. Differential expression of a Mr~90,000 cell surface transferrin receptor-related glycoprotein on murine B16 metastatic melanoma sublines selected for enhanced brain or ovary colonization. Cancer Res., 1990, 50, 515-520.
[103]
Marchetti, D.; Menter, D.; Jin, L.; Nakajima, M.; Nicolson, G.L. Nerve growth factor effects on human and mouse melanoma cell invasion and heparanase production. Int. J. Cancer, 1993, 55, 692-699.
[104]
Kawaguchi, T.; Kawaguchi, M.; Miner, K.M.; Lembo, T.M.; Nicolson, G.L. Brain meninges tumor formation by in vivo-selected metastatic B16 melanoma variants in mice. Clin. Exp. Metastasis, 1983, 1, 247-259.
[105]
Kawaguchi, T.; Kawaguchi, M.; Dulski, K.M.; Nicolson, G.L. Cellular behavior of metastatic B16 melanoma in experimental blood-borne implantation and cerebral invasion: an electron microscopic study. Invasion Metastasis, 1985, 5, 16-30.
[106]
Kawaguchi, T.; Kawaguchi, M.; Lembo, T.M.; Nicolson, G.L. Differential tumor growth of blood-borne B16 melanoma variants in cerebral dura mater is related to tumor-host cell reactions. Clin. Exp. Metastasis, 1989, 7, 1-14.
[107]
Benton, R.L.; Maddie, M.A.; Minnillo, D.R.; Hagg, T.; Whittemore, S.R. Griffonia simplicifolia isolectin B4 identifies a specific subpopulation of angiogenic blood vessels following contusive spinal cord injury in the adult mouse. J. Comp. Neurol., 2008, 507, 1031-1052.
[108]
Barden, H.; Levine, S. Histochemical observations on rodent brain melanin. Brain Res. Bull., 1983, 10, 847-851.
[109]
Brouland, J.P.; Megarbane, B.; Kafe, H.; Brouet, J.C.; Mikol, J. Cerebro-meningeal localization of extramedullary haematopoiesis (EMH), a rare complication of chronic idiopathic myelofibrosis (CIM). Neuropathol. Appl. Neurobiol., 2004, 30, 396-401.
[110]
Yamamura, H.; Sato, H. Quantitative studies on the developing vascular system of rat hepatoma. J. Natl. Cancer Inst., 1974, 53, 1229-1240.
[111]
Hori, K.; Suzuki, M.; Tanda, S.; Saito, S. In vivo analysis of tumor vascularization in the rat. Jpn. J. Cancer Res., 1990, 81, 279-288.
[112]
Miura, Y.; Ariga, M.; Miyauchi, M.; Arai, K.; Yagasaki, K. Isolation and characterization of subpopulations of rat ascites hepatoma cell line of AH109A with different metastatic potentials. Cytotechnology, 2003, 43, 27-32.
[113]
Hiratsuka, S.; Nakamura, K.; Iwai, S.; Murakami, M.; Itoh, T.; Kijima, H.; Shipley, J.M.; Senior, R.M.; Shibuya, M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell, 2002, 2, 289-300.
[114]
World Health Organization Classification of Tumours, Pathology
and Genetics of Tumours of the lung, pleura, thymus and heart.
Travis, W.D.; Brambilla, E.; Müller-Hermelink, H.K.; Harris, C.C.,
Eds.; IARC Press: Lyon,; , 2004.
[115]
Smid, M.; Wang, Y.; Zhang, Y.; Sieuwerts, A.M.; Yu, J.; Klijn, J.G.; Foekens, J.A.; Martens, J.W. Subtypes of breast cancer show preferential site of relapse. Cancer Res., 2008, 68, 3108-3114.
[116]
Liotta, L.A. Tumor invasion and metastases--role of the extracellular matrix: Rhoads Memorial Award lecture. Cancer Res., 1986, 46, 1-7.
[117]
Tanjore, H.; Kalluri, R. The role of type IV collagen and basement membranes in cancer progression and metastasis. Am. J. Pathol., 2006, 168, 715-717.
[118]
Nicolson, G.L. Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev., 1988, 7, 143-188.
[119]
Klein, E. Gradual transformation of solid into ascites tumors: evidence favoring the mutation-selection theory. Exp. Cell Res., 1955, 8, 188-212.
[120]
Yoshida, T. Contributions of the ascites hepatoma to the concept of malignancy of cancer. Ann. N. Y. Acad. Sci., 1956, 63, 852-881.
[121]
Raz, A.; Ben-Ze’ev, A. A modulation of the metastatic capability in B16 melanoma by cell shape. Science, 1983, 221, 1307-1310.
[122]
Kawaguchi, T.; Igarashi, S.; Wakabayashi, H.; Yokoya, S.; Fukui, K. Substrate adhesiveness and experimental metastatic potential of rat ascites hepatoma AH7974-derived variant sublines. Clin. Exp. Metastasis, 1992, 10, 225-238.
[123]
Kawaguchi, T.; Ono, T.; Wakabayashi, H.; Igarashi, S. Cell surface laminin-like substances and laminin-related carbohydrates of rat ascites hepatoma AH7974 and its variants with different lung-colonizing potential. Clin. Exp. Metastasis, 1994, 12, 203-212.
[124]
Kawaguchi, T.; Watanabe, K.; Sugino, T.; Sakuma, A.; Igarashi, S.; Ono, T.; Nakamura, K.; Kimura, A.; Yokoya, S.; Ozawa, M.; Muramatsu, T. Establishment and Characterization of Metastatic Ascites Hepatoma Variants with Different Adhesive Properties to Substrate in vitro. In: Recent Progress of Life Science Technology in Japan; Ikawa, Y.; Wada, A., Eds.; Academic Press: Tokyo, 1989; pp. 267-279.
[125]
Murray, J.C.; Liotta, L.; Rennard, S.I.; Martin, G.R. Adhesion characteristics of murine metastatic and nonmetastatic tumor cells in vitro. Cancer Res., 1980, 40, 347-351.
[126]
Bal de Kier Joffé, E.; Puricelli, L.; de Lustig, E.S. Modified adhesion behavior after in vitro passage of two related murine mammary adenocarcinomas with different metastasizing ability. Invasion Metastasis, 1986, 6, 302-312.
[127]
Terranova, V.P.; Liotta, L.A.; Russo, R.G.; Martin, G.R. Role of laminin in the attachment and metastasis of murine tumor cells. Cancer Res., 1982, 42, 2265-2269.
[128]
Kimura, A.; Kawaguchi, T.; Ono, T.; Sakuma, A.; Yokoya, Y.; Kochi, H.; Nakamura, K. Cell surface heparan sulphate and adhesive property of sublines of rat ascites hepatoma AH7974. J. Cell Sci., 1988, 90, 683-689.
[129]
Sanderson, R.D. Heparan sulfate proteoglycans in invasion and metastasis. Semin. Cell Dev. Biol., 2001, 12, 89-98.
[130]
Nakajima, M.; Irimura, T.; Di Ferrante, N.; Nicolson, G.L. Heparan sulphate degradation: relation to tumor invasive and metastatic properties of tumor cells of mouse B16 melanoma sublines. Science, 1983, 220, 611-613.
[131]
Ozawa, M.; Sato, M.; Muramatsu, H.; Hamada, H.; Muramatsu, T. A membrane glycoprotein involved in teratocarcinoma cell adhesion to substratum. Exp. Cell Res., 1985, 158, 127-143.
[132]
Rieber, M.; Castillo, M.A.; Rieber, M.S.; Irwin, J.C.; Urbina, C. Decrease in tumor-cell attachment and in a 140-kDa fibronectin receptor correlate with greater expression of multiple 34-kDa surface proteins and cytoplasmic 54-kDa components. Int. J. Cancer, 1988, 41, 96-100.
[133]
Blumenstock, F.A.; Saba, T.M.; Weber, P.; Laffin, R. Biochemical and immunological characterization of human opsonic alpha2SB glycoprotein: its identity with cold-insoluble globulin. J. Biol. Chem., 1978, 253, 4287-4291.
[134]
Varani, J.; Lovett, E.J., III; Wicha, M.; Malinoff, H.; McCoy, J.P., Jr Cell surface α-D-galactopyranosyl end groups: use as markers in the isolation of murine tumor cell lines with different cancer-causing potentials. J. Natl. Cancer Inst., 1983, 71, 1281-1287.
[135]
Kawaguchi, T.; Kanno, M.; Kimijima, I.; Abe, R. Carbohydrate expression of tumor cells and prognosis of breast cancer-analysis on human cancer and experimental certification on mechanism. Basic Invest. Breast Carcinoma, 1997, 6, 41-47. [in Japanese].
[136]
Grimstad, I.A.; Varani, J.; McCoy, J.P., Jr Contribution of α-D-galacopyranoside end groups to attachment of highly and low metastatic murine fibrosarcoma cells to various substrates. Exp. Cell Res., 1984, 155, 345-358.
[137]
Hiserodt, J.C.; Laybourn, K.A.; Varani, J. Laminin inhibits the recognition of tumor target cells by murine natural killer (NK) and natural cytotoxic (NC) lymphocytes. Am. J. Pathol., 1985, 121, 148-155.
[138]
Castronovo, V.; Colin, C.; Claysmith, A.P.; Chen, P.H.; Lifrange, E.; Lambotte, R.; Krutzsc, J.; Liotta, L.A.; Sobel, M.E. Immunodetection of the metastasis-associated laminin receptor in human breast cancer cells obtained by fine-needle aspiration biopsy. Am. J. Pathol., 1990, 137, 1373-1381.
[139]
Galili, U.; Macher, B.A. Interaction between anti-Gal and human tumor cells: a natural defense mechanism? J. Natl. Cancer Inst., 1989, 81, 178-179.
[140]
Ooishi, M.; Kawaguchi, T.; Hoshi, K.; Morimura, Y.; Sato, A.; Suzuki, T. Immunohistochemical demonstration of laminin in endometrial cancer of uterus in relation to it’s invasion and metastasis. Acta Obstet. Gynaecol. Jpn., 1995, 47, 955-956. [in Japanese].
[141]
Hakomori, S. Aberrant glycosylation in tumors and tumor-associated carbohydrate antigens. Adv. Cancer Res., 1989, 52, 257-331.
[142]
Irimura, T.; Nakamori, S.; Matsushita, Y.; Taniuchi, Y.; Todoroki, N.; Tsuji, T.; Izumi, Y.; Kawamura, Y.; Hoff, S.D.; Cleary, K.R. Colorectal cancer metastasis determined by carbohydrate-mediated cell adhesion: role of sialyl-Lex antigens. Semin. Cancer Biol., 1993, 4, 319-324.
[143]
Kannagi, R. Carbohydrate antigen sialyl Lewis a—its pathophysiological significance and induction mechanism in cancer progression. Chang Gung Med. J., 2007, 30, 189-209.
[145]
Dabelsteen, E. Cell surface carbohydrates as prognostic markers in human carcinomas. J. Pathol., 1996, 179, 358-369.
[146]
Brooks, S.A. The involvement of Helix pomatia lectin (HPA) binding N-acetylgalactosamine glycans in cancer progression. Histol. Histopathol., 2000, 15, 143-158.
[147]
Dennis, J.W.; Laferté, S.; Waghorne, C.; Breitman, M.L.; Kerbel, R.S. β1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science, 1987, 236, 582-585.
[148]
Kawaguchi, T.; Takano, Y.; Ohori, T.; Ito, F.; Koyama, S.; Kanno, T. Carbohydrate expression of cancer cells in progression of gastric cancer from early to advanced stage. Stomach and Intestine, 1997, 32, 797-808. [in Japanese].
[149]
Koyama, S.; Terashima, S.; Takano, Y.; Ohori, T.; Inoue, H.; Motoki, R.; Kawaguchi, T. P53 protein expression of carcinoma cells associated with metastasis and prognosis in gastric carcinomas: a clinicopathological study. Fukushima Igaku Zasshi, 1997, 47, 131-142. [in Japanese].
[150]
Terashima, S.; Takano, Y.; Ohori, T.; Kanno, T.; Kimura, T.; Motoki, R.; Kawaguchi, T. Soybean agglutinin binding as a useful prognostic indicator in stomach cancer. Surg. Today, 1997, 27, 293-297.
[151]
Terashima, S.; Takano, Y.; Ohori, T.; Kanno, T.; Kimura, T.; Motoki, R.; Kawaguchi, T. Sialyl-Tn antigen as a useful predictor of poor prognosis in patients with advanced stomach cancer. Surg. Today, 1998, 28, 682-686.
[152]
Ohori, T.; Kawaguchi, T. Carbohydrate expression of carcinoma cells associated with metastasis and prognosis in advanced gastric carcinomas: a clinicopathological study. Fukushima Igaku Zasshi, 1998, 48, 25-36. [in Japanese].
[153]
Takano, Y.; Teranishi, Y.; Terashima, S.; Motoki, R.; Kawaguchi, T. Lymph node metastasis-related carbohydrate epitopes of gastric cancer with submucosal invasion. Surg. Today, 2000, 30, 1073-1082.
[154]
Kanno, T. The Study on Correlation of Mucin Core Expression of Cancer Cells and Metastasis/Prognosis of Gastric Cancer. PhD
Thesis, No. 1014, Fukushima Medical University School of
Medicine: Fukushima. 1997. (in Japanese)
[155]
Itoh, F. The Study on Correlation of Blood Group Antigen ABH
Expression and Metastasis/Prognosis of Gastric Cancer.. PhD
Thesis, No.963, Fukushima Medical University School of
Medicine: Fukushima. 1996. (in Japanese)
[156]
Konno, A.; Hoshino, Y.; Terashima, S.; Motoki, R.; Kawaguchi, T. Carbohydrate expression profile of colorectal cancer cells is relevant to metastatic pattern and prognosis. Clin. Exp. Metastasis, 2002, 19, 61-70.
[157]
Kimura, T. Clinicopathological Study on Relationship Between
ABH Antigen Expression of Cancer Cells and Metastasis/Prognosis
of Colorectal Cancer..PhD Thesis, No. 1015, Fukushima Medical University School of Medicine: Fukushima. 1997. (in Japanese)
[158]
Patton, S.; Gendler, S.J.; Spicer, A.P. The epithelial mucin, MUC1, of milk, mammary gland and other tissues. Biochim. Biophys. Acta, 1995, 1241, 407-423.
[159]
Kawaguchi, T.; Takazawa, H.; Imai, S.; Morimoto, J.; Watanabe, T. Lack of polymorphism in MUC1 tandem repeats in cancer cells is related to breast cancer progression in Japanese women. Breast Cancer Res. Treat., 2005, 92, 223-230.
[160]
Tsuchiya, A.; Kanno, M.; Kawaguchi, T.; Endo, Y.; Zhang, G.J.; Ohtake, T.; Kimijima, I. Prognostic relevance of Tn expression in breast cancer. Breast Cancer, 1999, 6, 175-180.
[161]
Kawaguchi, T. Liver Metastatic Breast Cancer Cells Express
Atypical MUC1 with Vicia villosa Agglutinin-Binding
Carbohydrate(s), Proceedings of the 95th Annual Meeting of the
American Association of Cancer Research, March 2004; AACR:
Orlando, FL,. 2004, 45, p. 52.
[162]
Holdsworth, P.J.; Thorogood, J.; Benson, E.A.; Clayden, A.D. Blood group as a prognostic indicator in breast cancer. Br. Med. J., 1985, 290, 671-773.
[163]
Lee, J.S.; Ro, J.Y.; Sahin, A.A.; Hong, W.K.; Brown, B.W.; Mountain, C.F.; Hittelman, W.N. Expression of blood-group antigen A—a favorable prognostic factor in non-small-cell lung cancer. N. Engl. J. Med., 1991, 324, 1084-1090.
[164]
Goldstein, I.J.; Blake, D.A.; Ebisu, S.; Williams, T.J.; Murphy, L.A. Carbohydrate binding studies on the Bandeiraea simplicifolia I isolectins. Lectins which are mono-, di-, tri-, and tetravalent for N-acetyl-D-galactosamine. J. Biol. Chem., 1981, 256, 3890-3893.
[165]
Hedlund, M.; Ng, E.; Varki, A.; Varki, N.M. α2-6-Linked sialic acids on N-glycans modulate carcinoma differentiation in vivo. Cancer Res., 2008, 68, 388-394.
[167]
Madsen, C.B.; Lavrsen, K.; Steentoft, C.; Vester-Christensen, M.B.; Clausen, H.; Wandall, H.H.; Pedersen, A.E. Glycan elongation beyond the mucin associated Tn antigen protects tumor cells from immune-mediated killing. PLoS One, 2013, 8e72413
[168]
Fujita-Yamaguchi, Y. Renewed interest in basic and applied research involving monoclonal antibodies against an oncofetal Tn-antigen. J. Biochem., 2013, 154, 103-105.
Article Metrics
145
5