Transforming growth factor β1 suppresses nonmetastatic colon cancer at an early stage of tumorigenesis

Cancer Research

Volumn 59, Issue 14, 1999, Pages 3379-3386

  Engle, Sandra J ^a   Hoying, James B ^a   Boivin, Gregory P ^a   Ormsby, Ilona ^a   Gartside, Peter S ^b   Doetschman, Thomas ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; COLON CARCINOGENESIS; COLON CARCINOMA; HISTOPATHOLOGY; HYPERPLASIA; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADENOCARCINOMA; ADENOMA; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; APOPTOSIS; BETA CATENIN; BIOLOGICAL MARKERS; CECUM; CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; COLON; COLONIC NEOPLASMS; CROSSES, GENETIC; CYTOSKELETAL PROTEINS; DISEASE PROGRESSION; DNA; DNA, NEOPLASM; DNA-BINDING PROTEINS; GENES, APC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; HYPERPLASIA; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MICROSATELLITE REPEATS; NEOPLASM METASTASIS; NUCLEAR PROTEINS; SPECIFIC PATHOGEN-FREE ORGANISMS; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0033565626     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Mulder, K. M., Ramey, M. K., Hoosein, N. M., Levine, A. E., Hinshaw, X. H., Brattain, D. E., and Brattain, M. G. Characterization of transforming growth factor-β-resistant subclones isolated from a transforming growth factor-β-sensitive human colon carcinoma cell line. Cancer Res., 48: 7120-7125, 1988.
2. Manning, A. M., Williams, A. C., Game, S. M., and Paraskeva, C. Differential sensitivity of human colonic adenoma and carcinoma cells to transforming growth factor β (TGF-β): conversion of an adenoma cell line to a tumorigenic phenotype is accompanied by a reduced response to the inhibitory effects of TGF-β. Oncogene, 6: 1471-1476, 1991.
3. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, L., Fan, R. S., Zborowska, E., Kinzler, K. W., and Vogelstein, B. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science (Washington DC), 268: 1336-1338, 1995.
4. Parsons, R., Myeroff, L. L., Liu, B., Willson, J. K., Markowitz, S. D., Kinzler, K. W., and Vogelstein, B. Microsatellite instability and mutations of the transforming growth factor β type II receptor gene in colorectal cancer. Cancer Res., 55: 5548-5550, 1995.
5. Akiyama, Y., Iwanaga, R., Ishikawa, T., Sakamoto, K., Nishi, N., Nihei, Z., Iwama, T., Saitoh, K., and Yuasa, Y. Mutations of the transforming growth factor-β type II receptor gene are strongly related to sporadic proximal colon carcinomas with microsatellite instability. Cancer (Phila.), 78: 2478-2484, 1996.
6. Eppert, K., Scherer, S. W., Ozcelik, H., Pirone, R., Hoodless, P., Kim, H., Tsui, L. C., Bapat, B., Gallinger, S., Andrulis, I. L., Thomsen, G. H., Wrana, J. L., and Attisano, L. MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell, 86: 543-552, 1996.
7. Thiagalingam, S., Lengauer, C., Leach, F. S., Schutte, M., Hahn, S. A., Overhauser, J., Willson, J. K., Markowitz, S., Hamilton, S. R., Kern, S. E., Kinzler, K. W., and Vogelstein, B. Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers. Nat. Genet., 13: 343-346, 1996.
8. Takagi, Y., Kohmura, H., Futamura, M., Kida, H., Tanemura, H., Shimokawa, K., and Saji, S. Somatic alterations of the DPC4 gene in human colorectal cancers in vivo. Gastroenterology, 111: 1369-1372, 1996.
9. Takaku, K., Oshima, M., Miyoshi, H., Matsui, M., Seldin, M. F., and Taketo, M. M. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell, 92: 645-656, 1998.
10. Zhu, Y., Richardson, J. A., Parada, L. F., and Graff, J. M. Smad3 mutant mice develop metastatic colorectal cancer. Cell, 94: 703-714, 1998.
11. Roberts, A. B., McCune, B. K., and Sporn, M. B. TGF-β: regulation of extracellular matrix. Kidney Int., 41: 557-559, 1992.
12. Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R., Sidman, C., Proetzel, G., Calvin, D., and Doetschman, T. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature (Lond.), 359: 693-699, 1992.
13. Kulkarni, A. B., Huh, C. G., Becker, D., Geiser, A., Lyght, M., Flanders, K. C., Roberts, A. B., Sporn, M. B., Ward, J. M., and Karlsson, S. Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA, 90: 770-774, 1993.
14. Wahl, S. M., Hunt, D. A., Wakefield, L. M., McCartney-Francis, N., Wahl, L. M., Roberts, A. B., and Sporn, M. B. Transforming growth factor type β induces monocyte chemotaxis and growth factor production. Proc. Natl. Acad. Sci. USA, 84: 5788-5792, 1987.
15. Brandes, M. E., Mai, U. E., Ohura, K., and Wahl, S. M. Type I transforming growth factor-β receptors on neutrophils mediate chemotaxis to transforming growth factor-β. J. Immunol., 147: 1600-1606, 1991.
16. Wahl, S. M. Transforming growth factor β (TGF-β) in inflammation: a cause and a cure. J. Clin. Immunol., 12: 61-74, 1992.
17. Roberts, A. B., Thompson, N. L., Heine, U., Flanders, C., and Sporn, M. B. Transforming growth factor-β: possible roles in carcinogenesis. Br. J. Cancer (Phila.), 57: 594-600, 1988.
18. Diebold, R. J., Eis, M. J., Yin, M., Ormsby, I., Boivin, G. P., Darrow, B. J., Saffitz, J. E., and Doetschman, T. Early-onset multifocal inflammation in the transforming growth factor β1-null mouse is lymphocyte mediated. Proc. Natl. Acad. Sci. USA, 92: 12215-12219, 1995.
19. Kallapur, S., Ormsby, I., and Doetschman, T. Strain dependency of TGF β1 function during embryogenesis. Mol. Reprod. Dev., 52: 341-349, 1999.
20. Shinkai, Y., Rathbun, G., Lam, K. P., Oltz, E. M., Stewan, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., and Stall, A. M. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell, 68: 855-867, 1992.
21. Sadlack, B., Merz, H., Schorle, H., Schimpl, A., Feller, A. C., and Horak, I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell, 75: 253-261, 1993.
22. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., and Muller, W. Inlerleukin-10-deficient mice develop chronic enterocolitis. Cell, 75: 263-274, 1993.
23. Mombaerts, P., Mizoguchi, E., Grusby, M. J., Glimcher, L. H., Bhan, A. K., and Tonegawa, S. Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell, 75: 274-282, 1993.
24. Fynan, T. M., and Reiss, M. Resistance to inhibition of cell growth by transforming growth factor-β and its role in oncogenesis. Crit. Rev. Oncog., 4: 493-540, 1993.
25. Barnard, J. A., Lyons, R. M., and Moses, H. L. The cell biology of transforming growth factor β. Biochim. Biophys. Acta, 1032: 79-87, 1990.
26. Krawisz, J. E., Sharon, P., and Stenson, W. F. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology, 87: 1344-1350, 1984.
27. Singer, I. I., Kawka, D. W., Scott, S., Weidner, J. R., Mumford, R. A., Riehl, T. E., and Stenson, W. F. Expression of inducible nitric oxide synthase and nitrotyrosine in colonie epithelium in inflammatory bowel disease. Gastroenterology, 111: 871-885, 1996.
28. Miller, M. J., Thompson, J. H., Zhang, X. J., Sadowska-Krowicka, H., Kakkis, J. L., Munshi, U. K., Sandoval, M., Rossi, J. L., Eloby-Childress, S., and Beckman, J. S. Role of inducible nitric oxide synthase expression and peroxynitrite formation in guinea pig ileitis. Gastroenterology, 109: 1475-1483, 1995.
29. Beckman, J. S., and Koppenol, W. H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol., 271: C1424-C1437, 1996.
30. Miyaki, M., Konishi, M., Kikuchi-Yanoshita, R., Enomoto, M., Igari, T., Tanaka, K., Muraoka, M., Takahashi, H., Amada, Y., and Fukayama, M. Characteristics of somatic mutation of the adenomatous polyposis coli gene in colorectal tumors. Cancer Res., 54: 3011-3020, 1994.
31. Beroud, C., and Soussi, T. APC gene: database of germline and somatic mutations in human tumors and cell lines. Nucleic Acids Res., 24: 121-124, 1996.
32. Miyoshi, Y., Nagase, H., Ando, H., Horii, A., Ichii, S., Nakatsuru, S., Aoki, T., Miki, Y., Mori, T., and Nakamura, Y. Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum. Mol. Genet., 1: 229-233, 1992.
33. Powell, S. M., Zilz, N., Beazer-Barclay, Y., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B., and Kinzler, K. W. APC mutations occur early during colorectal tumorigenesis. Nature (Lond.), 359: 235-237, 1992.
34. Luongo, C., Moser, A. R., Gledhill, S., and Dove, W. F. Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res., 54: 5947-5952, 1994.
35. Oshima, M., Oshima, H., Kitagawa, K., Kobayashi, M., Itakura, C., and Taketo, M. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc. Natl. Acad. Sci. USA, 92: 4482-4486, 1995.
36. Levy, D. B., Smith, K. J., Beazer-Barclay, Y., Hamilton, S. R., Vogelstein, B., and Kinzler, K. W. Inactivation of both APC alleles in human and mouse tumors. Cancer Res., 54: 5953-5958, 1994.
37. Bullions, L. C., and Levine, A. J. The role of β-catenin in cell adhesion, signal transduction, and cancer. Curr. Opin. Oncol., 10: 81-87, 1998.
38. McCrea, P. D., Turck, C. W., and Gumbiner, B. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science (Washington DC), 254: 1359-1361, 1991.
39. Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R., and Birchmeier, W. Functional interaction of β-catenin with the transcription factor LEF-1. Nature (Lond.), 382: 638-642, 1996.
40. Inomata, M., Ochiai, A., Akimoto, S., Kitano, S., and Hirohashi, S. Alteration of β-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients. Cancer Res., 56: 2213-2217, 1996.
41. Senda, T., Miyashiro, I., Matsumine, A., Baeg, G. H., Monden, T., Kobayashil, S., Monden, M., Toyoshima, K., and Akiyama, T. The tumor suppressor protein APC colocalizes with β-catenin in the colon epithelial cells. Biochem. Biophys. Res. Commun., 223: 329-334, 1996.
42. Lin, H. Y., Moustakas, A., Knaus, P., Wells, R. G., Henis, Y. I., and Lodish, H. F. The soluble exoplasmic domain of the type II transforming growth factor (TGF)-β receptor. A heterogeneously glycosylated protein with high affinity and selectivity for TGF-β ligands. J. Biol. Chem., 270: 2747-2754, 1995.
43. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L., and Doetschman, T. TGF/β2 knockout mice have multiple developmental defects that are non-overlapping with other TGFβ knockout phenotypes. Development (Camb.), 124: 2659-2670, 1997.
44. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N., and Groffen, J. Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet., 11: 415-421, 1995.
45. Proetzel, G., Pawlowski, S. A., Wiles, M. V., Yin, M., Boivin, G. P., Howles, P. N., Ding, J., Ferguson, M. W., and Doetschman, T. Transforming growth factor-β3 is required for secondary palate fusion. Nat. Genet., 11: 409-414, 1995.
46. Chang, W. W. Histogenesis of colon cancer in experimental animals. Scand. J. Gastroenterol. Suppl., 104: 27-43, 1984.
47. Maskens, A. P. Histogenesis of colon glands during postnatal growth. Acta Anat. (Basel), 100: 17-26, 1978.
48. Thorup, I. Histomorphological and immunohistochemical characterization of colonic aberrant crypt foci in rats: relationship to growth factor expression. Carcinogenesis (Lond.), 18: 465-472, 1997.
49. Mikhailowski, R., Shpitz, B., Polak-Charcon, S., Kost, Y., Segal, Y., Segal, C., Fich, A., and Lamprecht, S. A. Controlled release of TGF-β1 impedes rat colon carcinogenesis in vivo. Int. J. Cancer, 78: 618-623, 1998.
50. Barnard, J. A., Warwick, G. J., and Gold, L. I. Localization of transforming growth factor β isoforms in the normal murine small intestine and colon. Gastroenterology, 105: 67-73, 1993.
51. Avery, A., Paraskeva, C., Hall, P., Flanders, K. C., Sporn, M., and Moorghen, M. TGF-β expression in the human colon: differential immunostaining along crypt epithelium. Br. J. Cancer, 68: 137-139, 1993.
52. Moser, A. R., Pitot, H. C., and Dove, W. F. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science (Washington DC), 247: 322-324, 1990.