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Mutational Analysis of the APC/ß-Catenin/Tcf Pathway in Colorectal Cancer¹

Johns Hopkins Oncology Center, Baltimore, Maryland 21231 [A. B. S., P. J. M., B. V., K. W. K.], and Howard Hughes Medical Institutes, Johns Hopkins University, Baltimore, Maryland 20815 [B. V.]

Mutation of the adenomatous polyposis coli (APC) tumor suppressor gene initiates the majority of colorectal (CR) cancers. One consequence of this inactivation is constitutive activation of ß-catenin/Tcf-mediated transcription. To further explore the role of the APC/ß-catenin/Tcf pathway in CR tumorigenesis, we searched for mutations in genes implicated in this pathway in CR tumors lacking APC mutations. No mutations of the -catenin (CTNNG1), GSK-3 (GSK3A), or GSK-3ß (GSK3B) genes were detected. In contrast, mutations in the NH₂-terminal regulatory domain of ß-catenin (CTNNB1) were found in 13 of 27 (48%) CR tumors lacking APC mutations. Mutations in the ß-catenin regulatory domain and APC were observed to be mutually exclusive, consistent with their equivalent effects on ß-catenin stability and Tcf transactivation. In addition, we found that CTNNB1 mutations can occur in the early, adenomatous stage of CR neoplasia, as has been observed previously with APC mutations. These results suggest that CTNNB1 mutations can uniquely substitute for APC mutations in CR tumors and that ß-catenin signaling plays a critical role in CR tumorigenesis.

¹ This work was supported by NIH Grant CA57345. B. V. is an investigator of the Howard Hughes Medical Institutes.

² These authors contributed equally to this work.

³ To whom requests for reprints should be addressed, at the Johns Hopkins Oncology Center, 424 North Bond Street, Baltimore, MD 21231-1001.

Received 12/ 2/97. Accepted 1/23/98.

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				Y. Zhai, R. Wu, D. R. Schwartz, D. Darrah, H. Reed, F. T. Kolligs, M. T. Nieman, E. R. Fearon, and K. R. Cho Role of {beta}-Catenin/T-Cell Factor-Regulated Genes in Ovarian Endometrioid Adenocarcinomas Am. J. Pathol., April 1, 2002; 160(4): 1229 - 1238. [Abstract] [Full Text] [PDF]

				S. C. Abraham, D. S. Klimstra, R. E. Wilentz, C. J. Yeo, K. Conlon, M. Brennan, J. L. Cameron, T.-T. Wu, and R. H. Hruban Solid-Pseudopapillary Tumors of the Pancreas Are Genetically Distinct from Pancreatic Ductal Adenocarcinomas and Almost Always Harbor {beta}-catenin Mutations Am. J. Pathol., April 1, 2002; 160(4): 1361 - 1369. [Abstract] [Full Text] [PDF]

				J. Park, D. Betel, R. Gryfe, K. Michalickova, N. Di Nicola, S. Gallinger, C. W. V. Hogue, and M. Redston Mutation Profiling of Mismatch Repair-deficient Colorectal Cancers Using an in Silico Genome Scan to Identify Coding Microsatellites Cancer Res., March 1, 2002; 62(5): 1284 - 1288. [Abstract] [Full Text] [PDF]

				N. A. C. S. Wong and M. Pignatelli {beta}-Catenin--A Linchpin in Colorectal Carcinogenesis? Am. J. Pathol., February 1, 2002; 160(2): 389 - 401. [Abstract] [Full Text] [PDF]

				H. Usadel, J. Brabender, K. D. Danenberg, C. Jeronimo, S. Harden, J. Engles, P. V. Danenberg, S. Yang, and D. Sidransky Quantitative Adenomatous Polyposis Coli Promoter Methylation Analysis in Tumor Tissue, Serum, and Plasma DNA of Patients with Lung Cancer Cancer Res., January 1, 2002; 62(2): 371 - 375. [Abstract] [Full Text] [PDF]

				T. Hinoi, M. Tani, P. C. Lucas, K. Caca, R. L. Dunn, E. Macri¶, M. Loda¶, H. D. Appelman, K. R. Cho, and E. R. Fearon Loss of CDX2 Expression and Microsatellite Instability Are Prominent Features of Large Cell Minimally Differentiated Carcinomas of the Colon Am. J. Pathol., December 1, 2001; 159(6): 2239 - 2248. [Abstract] [Full Text] [PDF]

				G. G. Chung, E. Provost, E. P. Kielhorn, L. A. Charette, B. L. Smith, and D. L. Rimm Tissue Microarray Analysis of {beta}-Catenin in Colorectal Cancer Shows Nuclear Phospho-{beta}-catenin Is Associated with a Better Prognosis Clin. Cancer Res., December 1, 2001; 7(12): 4013 - 4020. [Abstract] [Full Text] [PDF]

				X. P. Hao, T. G. Pretlow, J. S. Rao, and T. P. Pretlow {beta}-Catenin Expression Is Altered in Human Colonic Aberrant Crypt Foci Cancer Res., November 1, 2001; 61(22): 8085 - 8088. [Abstract] [Full Text] [PDF]

				R. Koesters, M. A. Hans, A. Benner, R. Prosst, J. Boehm, J. Gahlen, and M. von Knebel Doeberitz Predominant mutation of codon 41 of the {beta}-catenin proto-oncogene in rat colon tumors induced by 1,2-dimethylhydrazine using a complete carcinogenic protocol Carcinogenesis, November 1, 2001; 22(11): 1885 - 1890. [Abstract] [Full Text] [PDF]

				S. C. Abraham, T.-T. Wu, D. S. Klimstra, L. S. Finn, J.-H. Lee, C. J. Yeo, J. L. Cameron, and R. H. Hruban Distinctive Molecular Genetic Alterations in Sporadic and Familial Adenomatous Polyposis-Associated Pancreatoblastomas : Frequent Alterations in the APC/{beta}-Catenin Pathway and Chromosome 11p Am. J. Pathol., November 1, 2001; 159(5): 1619 - 1627. [Abstract] [Full Text] [PDF]

				E. Sadot, B. Geiger, M. Oren, and A. Ben-Ze'ev Down-Regulation of {beta}-Catenin by Activated p53 Mol. Cell. Biol., October 15, 2001; 21(20): 6768 - 6781. [Abstract] [Full Text] [PDF]

				A. M. Carothers, K. A. Melstrom Jr., J. D. Mueller, M. J. Weyant, and M. M. Bertagnolli Progressive Changes in Adherens Junction Structure during Intestinal Adenoma Formation in Apc Mutant Mice J. Biol. Chem., October 12, 2001; 276(42): 39094 - 39102. [Abstract] [Full Text] [PDF]

				H. Shiina, M. Igawa, S. Urakami, K. Shigeno, T. Yoneda, M. Terashima, M. Deguchi, L. Ribeiro-Filho, and R. Dahiya Alterations of {beta}- and {gamma}-Catenin in N-Butyl-N-(-4-hydroxybutyl)nitrosamine-induced Murine Bladder Cancer Cancer Res., October 1, 2001; 61(19): 7101 - 7109. [Abstract] [Full Text] [PDF]

				T. Liu, J. Chen, S. Salahshor, S. Kuismanen, E. Holmberg, H. Gronberg, P. Peltomaki, and A. Lindblom Screening families with endometrial and colorectal cancers for germline mutations J. Med. Genet., September 1, 2001; 38(9): e29 - 29. [Full Text] [PDF]

				R.-H. Chen and F. McCormick Selective Targeting to the Hyperactive {beta}-Catenin/T-Cell Factor Pathway in Colon Cancer Cells Cancer Res., June 1, 2001; 61(11): 4445 - 4449. [Abstract] [Full Text] [PDF]

				D. Arango, G. A. Corner, S. Wadler, P. J. Catalano, and L. H. Augenlicht c-myc/p53 Interaction Determines Sensitivity of Human Colon Carcinoma Cells to 5-Fluorouracil in Vitro and in Vivo Cancer Res., June 1, 2001; 61(12): 4910 - 4915. [Abstract] [Full Text] [PDF]

				L. Zhang, J. Yu, J. K. V. Willson, S. D. Markowitz, K. W. Kinzler, and B. Vogelstein Short Mononucleotide Repeat Sequence Variability in Mismatch Repair-deficient Cancers Cancer Res., May 1, 2001; 61(9): 3801 - 3805. [Abstract] [Full Text]

				W. Szeto, W. Jiang, D. A. Tice, B. Rubinfeld, P. G. Hollingshead, S. E. Fong, D. L. Dugger, T. Pham, D. G. Yansura, T. A. Wong, et al. Overexpression of the Retinoic Acid-responsive Gene Stra6 in Human Cancers and Its Synergistic Induction by Wnt-1 and Retinoic Acid Cancer Res., May 1, 2001; 61(10): 4197 - 4205. [Abstract] [Full Text]

				L. Lehnert, M. M. Lerch, Y. Hirai, M.-L. Kruse, W. Schmiegel, and H. Kalthoff Autocrine Stimulation of Human Pancreatic Duct-Like Development by Soluble Isoforms of Epimorphin in Vitro J. Cell Biol., March 5, 2001; 152(5): 911 - 922. [Abstract] [Full Text] [PDF]

				D. F. Calvisi, V. M. Factor, R. Loi, and S. S. Thorgeirsson Activation of {beta}-Catenin during Hepatocarcinogenesis in Transgenic Mouse Models: Relationship to Phenotype and Tumor Grade Cancer Res., March 1, 2001; 61(5): 2085 - 2091. [Abstract] [Full Text]

				R. A. Wagenaar, H. C. Crawford, and L. M. Matrisian Stabilized {beta}-Catenin Immortalizes Colonic Epithelial Cells Cancer Res., March 1, 2001; 61(5): 2097 - 2104. [Abstract] [Full Text]

				Y. Naishiro, T. Yamada, A. S. Takaoka, R. Hayashi, F. Hasegawa, K. Imai, and S. Hirohashi Restoration of Epithelial Cell Polarity in a Colorectal Cancer Cell Line by Suppression of {beta}-catenin/T-Cell Factor 4-mediated Gene Transactivation Cancer Res., March 1, 2001; 61(6): 2751 - 2758. [Abstract] [Full Text]

				Y.-H. Ling, Y. Zhong, and R. Perez-Soler Disruption of Cell Adhesion and Caspase-Mediated Proteolysis of {beta}- and {gamma}-Catenins and APC Protein in Paclitaxel-Induced Apoptosis Mol. Pharmacol., March 1, 2001; 59(3): 593 - 603. [Abstract] [Full Text]

				G. Garcia-Rostan, R. L. Camp, A. Herrero, M. L. Carcangiu, D. L. Rimm, and G. Tallini {beta}-Catenin Dysregulation in Thyroid Neoplasms : Down-Regulation, Aberrant Nuclear Expression, and CTNNB1 Exon 3 Mutations Are Markers for Aggressive Tumor Phenotypes and Poor Prognosis Am. J. Pathol., March 1, 2001; 158(3): 987 - 996. [Abstract] [Full Text] [PDF]

				S. C. Abraham, B. Nobukawa, F. M. Giardiello, S. R. Hamilton, and T.-T. Wu Sporadic Fundic Gland Polyps : Common Gastric Polyps Arising Through Activating Mutations in the {beta}-Catenin Gene Am. J. Pathol., March 1, 2001; 158(3): 1005 - 1010. [Abstract] [Full Text] [PDF]

				S. C. Abraham, E. A. Montgomery, F. M. Giardiello, and T.-T. Wu Frequent {beta}-Catenin Mutations in Juvenile Nasopharyngeal Angiofibromas Am. J. Pathol., March 1, 2001; 158(3): 1073 - 1078. [Abstract] [Full Text] [PDF]