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Department of Cell Biology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030
The process of metastasis is not random. Rather, it consists of a series of linked, sequential steps that must be completed by tumor cells if a metastasis is to develop. Although some of the steps in this process contain stochastic elements, as a whole, metastasis favors the survival and growth of a few subpopulations of cells that preexist within the parent neoplasm. Moreover, metastases can have a clonal origin, and different metastases can originate from the proliferation of single cells. The outcome of metastasis depends on the interaction of metastatic cells with different organ environments. Organ-specific metastases have been demonstrated in a variety of experimental tumor systems. Moreover, we have found tumor growth that is specific to a particular site within one organ. Whether the same conclusions can be reached for human cancers remained unanswered until very recently.
Studies from our laboratory and from others have shown that the implantation of human cancer cells derived from surgical specimens into correct anatomical sites of nude mice can provide a suitable model of metastasis of human tumors. Clonal analysis of a human renal carcinoma, colon carcinomas, and melanomas has revealed that these tumors are indeed heterogeneous for metastatic properties, an observation made only after orthotopic implantation. Thus, growth in the environment of specific organs can be selective and the environment per se influences this process.
While it is clear that vascularity and local immunity can facilitate or retard tumor growth, we have concentrated on understanding how damage to an organ and the subsequent repair process can facilitate tumor cell proliferation. Accelerated growth of human colon cancer cells was found in hepatectomized nude mice, whereas accelerated growth of human renal cancer cells was found in nephrectomized nude mice. These data suggest that systemic physiological signals can be recognized by neoplastic cells presumably by mechanisms similar to those shared by their normal cell counterparts. In summary, the critical factors that regulate metastasis are the intrinsic properties of metastatic cells and host factors involved in homeostasis. The recent increase in our understanding of metastasis should provide important leads for developing more effective approaches to the treatment of disseminated cancer.
1 Financial support of this research was provided by Grant R35-CA 42107 from the National Cancer Institute, NIH. Presented at the Seventy-ninth Annual Meeting of the American Association for Cancer Research, May 26, 1988, in New Orleans, LA.
Received 6/26/90. Accepted 6/27/90.
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 L. Borsig, R. Wong, R. O. Hynes, N. M. Varki, and A. Varki Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis PNAS, February 19, 2002; 99(4): 2193 - 2198. [Abstract] [Full Text] [PDF]
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 S. Mechtersheimer, P. Gutwein, N. Agmon-Levin, A. Stoeck, M. Oleszewski, S. Riedle, R. Postina, F. Fahrenholz, M. Fogel, V. Lemmon, et al. Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins J. Cell Biol., November 12, 2001; 155(4): 661 - 674. [Abstract] [Full Text] [PDF]
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K. A. Olson, H. R. Byers, M. E. Key, and J. W. Fett Prevention of Human Prostate Tumor Metastasis in Athymic Mice by Antisense Targeting of Human Angiogenin Clin. Cancer Res., November 1, 2001; 7(11): 3598 - 3605. [Abstract] [Full Text] [PDF]
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A. Li, M. L. Varney, and R. K. Singh Expression of Interleukin 8 and Its Receptors in Human Colon Carcinoma Cells with Different Metastatic Potentials Clin. Cancer Res., October 1, 2001; 7(10): 3298 - 3304. [Abstract] [Full Text] [PDF]
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S. W. Nam, T. Clair, Y.-S. Kim, A. McMarlin, E. Schiffmann, L. A. Liotta, and M. L. Stracke Autotaxin (NPP-2), a Metastasis-enhancing Motogen, Is an Angiogenic Factor Cancer Res., September 1, 2001; 61(18): 6938 - 6944. [Abstract] [Full Text] [PDF]
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I. J. Fidler Angiogenic Heterogeneity: Regulation of Neoplastic Angiogenesis by the Organ Microenvironment J Natl Cancer Inst, July 18, 2001; 93(14): 1040 - 1041. [Full Text] [PDF]
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S. A. Tahir, G. Yang, S. Ebara, T. L. Timme, T. Satoh, L. Li, A. Goltsov, M. Ittmann, J. D. Morrisett, and T. C. Thompson Secreted Caveolin-1 Stimulates Cell Survival/Clonal Growth and Contributes to Metastasis in Androgen-insensitive Prostate Cancer Cancer Res., May 1, 2001; 61(10): 3882 - 3885. [Abstract] [Full Text]
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S. Engler, C. Thiel, K. Förster, K. David, R. Bredehorst, and H. Juhl A Novel Metastatic Animal Model Reflecting the Clinical Appearance of Human Neuroblastoma: Growth Arrest of Orthotopic Tumors by Natural, Cytotoxic Human Immunoglobulin M Antibodies Cancer Res., April 1, 2001; 61(7): 2968 - 2973. [Abstract] [Full Text]
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L. Borsig, R. Wong, J. Feramisco, D. R. Nadeau, N. M. Varki, and A. Varki Heparin and cancer revisited: Mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis PNAS, March 13, 2001; 98(6): 3352 - 3357. [Abstract] [Full Text] [PDF]
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 J. I. Izawa and C. P.N. Dinney The role of angiogenesis in prostate and other urologic cancers: a review Can. Med. Assoc. J., March 1, 2001; 164(5): 662 - 670. [Abstract] [Full Text] [PDF]
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H. Yonou, T. Yokose, T. Kamijo, N. Kanomata, T. Hasebe, K. Nagai, T. Hatano, Y. Ogawa, and A. Ochiai Establishment of a Novel Species- and Tissue-specific Metastasis Model of Human Prostate Cancer in Humanized Non-Obese Diabetic/Severe Combined Immunodeficient Mice Engrafted with Human Adult Lung and Bone Cancer Res., March 1, 2001; 61(5): 2177 - 2182. [Abstract] [Full Text]
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J. W. Slaton, K. Inoue, P. Perrotte, A. K. El-Naggar, D. A. Swanson, I. J. Fidler, and C. P. N. Dinney Expression Levels of Genes that Regulate Metastasis and Angiogenesis Correlate with Advanced Pathological Stage of Renal Cell Carcinoma Am. J. Pathol., February 1, 2001; 158(2): 735 - 743. [Abstract] [Full Text] [PDF]
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J. Friederichs, Y. Zeller, A. Hafezi-Moghadam, H.-J. Gröne, K. Ley, and P. Altevogt The CD24/P-selectin Binding Pathway Initiates Lung Arrest of Human A125 Adenocarcinoma Cells Cancer Res., December 1, 2000; 60(23): 6714 - 6722. [Abstract] [Full Text]
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K. Kuba, K. Matsumoto, K. Date, H. Shimura, M. Tanaka, and T. Nakamura HGF/NK4, a Four-Kringle Antagonist of Hepatocyte Growth Factor, Is an Angiogenesis Inhibitor that Suppresses Tumor Growth and Metastasis in Mice Cancer Res., December 1, 2000; 60(23): 6737 - 6743. [Abstract] [Full Text]
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H. Nokihara, H. Yanagawa, Y. Nishioka, S. Yano, N. Mukaida, K. Matsushima, and S. Sone Natural Killer Cell-dependent Suppression of Systemic Spread of Human Lung Adenocarcinoma Cells by Monocyte Chemoattractant Protein-1 Gene Transfection in Severe Combined Immunodeficient Mice Cancer Res., December 1, 2000; 60(24): 7002 - 7007. [Abstract] [Full Text]
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 I. J. Fidler Regulation of Neoplastic Angiogenesis J Natl Cancer Inst Monographs, December 1, 2000; 2000(28): 10 - 14. [Abstract] [Full Text] [PDF]
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B. A. Yoshida, M. M. Sokoloff, D. R. Welch, and C. W. Rinker-Schaeffer Metastasis-Suppressor Genes: a Review and Perspective on an Emerging Field J Natl Cancer Inst, November 1, 2000; 92(21): 1717 - 1730. [Abstract] [Full Text] [PDF]
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S. Yano, H. Shinohara, R. S. Herbst, H. Kuniyasu, C. D. Bucana, L. M. Ellis, D. W. Davis, D. J. McConkey, and I. J. Fidler Expression of Vascular Endothelial Growth Factor Is Necessary but not Sufficient for Production and Growth of Brain Metastasis Cancer Res., September 1, 2000; 60(17): 4959 - 4967. [Abstract] [Full Text]
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K. Gohji, M. Nomi, Y. Niitani, S. Kitazawa, A. Fujii, Y. Katsuoka, and M. Nakajima Independent Prognostic Value of Serum Hepatocyte Growth Factor in Bladder Cancer J. Clin. Oncol., August 16, 2000; 18(16): 2963 - 2971. [Abstract] [Full Text] [PDF]
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B. Cady Sentinel Lymph Node Procedure in Squamous Cell Carcinoma of the Vulva J. Clin. Oncol., August 15, 2000; 18(15): 2795 - 2797. [Full Text] [PDF]
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Y. Kitadai, K. Haruma, N. Mukaida, Y. Ohmoto, N. Matsutani, W. Yasui, S. Yamamoto, K. Sumii, G. Kajiyama, I. J. Fidler, et al. Regulation of Disease-Progression Genes in Human Gastric Carcinoma Cells by Interleukin 8 Clin. Cancer Res., July 1, 2000; 6(7): 2735 - 2740. [Abstract] [Full Text]
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H. Kuniyasu, P. Troncoso, D. Johnston, C. D. Bucana, E. Tahara, I. J. Fidler, and C. A. Pettaway Relative Expression of Type IV Collagenase, E-cadherin, and Vascular Endothelial Growth Factor/Vascular Permeability Factor in Prostatectomy Specimens Distinguishes Organ-confined from Pathologically Advanced Prostate Cancers Clin. Cancer Res., June 1, 2000; 6(6): 2295 - 2308. [Abstract] [Full Text]
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S. Huang, A. DeGuzman, C. D. Bucana, and I. J. Fidler Nuclear Factor-{{kappa}}B Activity Correlates with Growth, Angiogenesis, and Metastasis of Human Melanoma Cells in Nude Mice Clin. Cancer Res., June 1, 2000; 6(6): 2573 - 2581. [Abstract] [Full Text]
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K. Inoue, J. W. Slaton, B. Y. Eve, S. J. Kim, P. Perrotte, M. D. Balbay, S. Yano, M. Bar-Eli, R. Radinsky, C. A. Pettaway, et al. Interleukin 8 Expression Regulates Tumorigenicity and Metastases in Androgen-independent Prostate Cancer Clin. Cancer Res., May 1, 2000; 6(5): 2104 - 2119. [Abstract] [Full Text] [PDF]
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 A. S. Boehle, P. Dohrmann, I. Leuschner, H. Kalthoff, and D. Henne-Bruns An improved orthotopic xenotransplant procedure for human lung cancer in SCID bg mice Ann. Thorac. Surg., April 1, 2000; 69(4): 1010 - 1015. [Abstract] [Full Text] [PDF]
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K. Inoue, J. W. Slaton, S. J. Kim, P. Perrotte, B. Y. Eve, M. Bar-Eli, R. Radinsky, and C. P. N. Dinney Interleukin 8 Expression Regulates Tumorigenicity and Metastasis in Human Bladder Cancer Cancer Res., April 1, 2000; 60(8): 2290 - 2299. [Abstract] [Full Text]
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M. Morifuji, S.’i. Taniguchi, H. Sakai, Y. Nakabeppu, and M. Ohishi Differential Expression of Cytokeratin after Orthotopic Implantation of Newly Established Human Tongue Cancer Cell Lines of Defined Metastatic Ability Am. J. Pathol., April 1, 2000; 156(4): 1317 - 1326. [Abstract] [Full Text] [PDF]
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J. Yokota Tumor progression and metastasis Carcinogenesis, March 1, 2000; 21(3): 497 - 503. [Abstract] [Full Text] [PDF]
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R. S. Herbst, S. Yano, H. Kuniyasu, F. R. Khuri, C. D. Bucana, F. Guo, D. Liu, B. Kemp, J. J. Lee, W. K. Hong, et al. Differential Expression of E-cadherin and Type IV Collagenase Genes Predicts Outcome in Patients with Stage I Non-Small Cell Lung Carcinoma Clin. Cancer Res., March 1, 2000; 6(3): 790 - 797. [Abstract] [Full Text]
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L. C. L. T. van Kempen, J. J. van den Oord, G. N. P. van Muijen, U. H. Weidle, H. P. J. Bloemers, and G. W. M. Swart Activated Leukocyte Cell Adhesion Molecule/CD166, a Marker of Tumor Progression in Primary Malignant Melanoma of the Skin Am. J. Pathol., March 1, 2000; 156(3): 769 - 774. [Abstract] [Full Text] [PDF]
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R. J. Guan, H. L. Ford, Y. Fu, Y. Li, L. M. Shaw, and A. B. Pardee Drg-1 as a Differentiation-related, Putative Metastatic Suppressor Gene in Human Colon Cancer Cancer Res., February 1, 2000; 60(3): 749 - 755. [Abstract] [Full Text]
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Z.-Z. Su, N. I. Goldstein, H. Jiang, M.-N. Wang, G. J. Duigou, C. S. H. Young, and P. B. Fisher PEG-3, a nontransforming cancer progression gene, is a positive regulator of cancer aggressiveness and angiogenesis PNAS, December 21, 1999; 96(26): 15115 - 15120. [Abstract] [Full Text] [PDF]
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J. W. Slaton, P. Perrotte, K. Inoue, C. P. N. Dinney, and I. J. Fidler Interferon-{{alpha}}-mediated Down-Regulation of Angiogenesis-related Genes and Therapy of Bladder Cancer Are Dependent on Optimization of Biological Dose and Schedule Clin. Cancer Res., October 1, 1999; 5(10): 2726 - 2734. [Abstract] [Full Text] [PDF]
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H. Miyake, I. Hara, K. Gohji, K. Yamanaka, S. Hara, S. Arakawa, M. Nakajima, and S. Kamidono Relative Expression of Matrix Metalloproteinase-2 and Tissue Inhibitor of Metalloproteinase-2 in Mouse Renal Cell Carcinoma Cells Regulates Their Metastatic Potential Clin. Cancer Res., October 1, 1999; 5(10): 2824 - 2829. [Abstract] [Full Text] [PDF]
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Y. J. Kim, L. Borsig, H.-L. Han, N. M. Varki, and A. Varki Distinct Selectin Ligands on Colon Carcinoma Mucins Can Mediate Pathological Interactions among Platelets, Leukocytes, and Endothelium Am. J. Pathol., August 1, 1999; 155(2): 461 - 472. [Abstract] [Full Text] [PDF]
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C.-J. Tseng, C. C. Pao, J.-D. Lin, Y.-K. Soong, J.-H. Hong, and S. Hsueh Detection of Human Papillomavirus Types 16 and 18 mRNA in Peripheral Blood of Advanced Cervical Cancer Patients and Its Association With Prognosis J. Clin. Oncol., May 1, 1999; 17(5): 1391 - 1391. [Abstract] [Full Text] [PDF]
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J. M. Jessup, P. Battle, H. Waller, K. H. Edmiston, D. B. Stolz, S. C. Watkins, J. Locker, and K. Skena Reactive Nitrogen and Oxygen Radicals Formed during Hepatic Ischemia-Reperfusion Kill Weakly Metastatic Colorectal Cancer Cells Cancer Res., April 1, 1999; 59(8): 1825 - 1829. [Abstract] [Full Text] [PDF]
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