© 2001 by Oxford University Press
Journal of the National Cancer Institute, Vol. 93, No. 9, 691-699,
May 2, 2001
© 2001 Oxford University Press
Epigenetic Inactivation of RASSF1A in Lung and Breast Cancers and Malignant Phenotype Suppression
Affiliations of authors: D. G. Burbee, E. Forgacs, S. Zöchbauer-Müller, B. Gao, D. Randle, M. Kondo, A. Virmani, S. Bader, Y. Sekido, S. Toyooka, A. F. Gazdar, J. D. Minna (Hamon Center for Therapeutic Oncology Research), L. Shivakumar, M. White (Department of Cell Biology), S. Milchgrub (Department of Pathology), The University of Texas Southwestern Medical Center at Dallas; K. Fong, Department of Thoracic Medicine, The Prince Charles Hospital, Queensland, Australia; F. Latif, Department of Reproductive and Child Health, University of Birmingham, U.K.; M. Lerman, Laboratory of Immunobiology, National Cancer Institute-Frederick Cancer Research and Development Center, Frederick, MD; E. Zabarovsky, Karolinska Institute, Stockholm, Sweden.
Correspondence to: John D. Minna, M.D., Hamon Center for Therapeutic Oncology Research, The University of Texas Southwestern Medical Center at Dallas, 6000 Harry Hines Blvd., Dallas, TX 75390-8593 (e-mail: John.Minna@ UTSouthwestern.edu).
Background: The recently identified RASSF1 locus is located within a 120-kilobase region of chromosome 3p21.3 that frequently undergoes allele loss in lung and breast cancers. We explored the hypothesis that RASSF1 encodes a tumor suppressor gene for lung and breast cancers. Methods: We assessed expression of two RASSF1 gene products, RASSF1A and RASSF1C, and the methylation status of their respective promoters in 27 non-small-cell lung cancer (NSCLC) cell lines, in 107 resected NSCLCs, in 47 small-cell lung cancer (SCLC) cell lines, in 22 breast cancer cell lines, in 39 resected breast cancers, in 104 nonmalignant lung samples, and in three breast and lung epithelial cultures. We also transfected a lung cancer cell line that lacks RASSF1A expression with vectors containing RASSF1A complementary DNA to determine whether exogenous expression of RASSF1A would affect in vitro growth and in vivo tumorigenicity of this cell line. All statistical tests were two-sided. Results: RASSF1A messenger RNA was expressed in nonmalignant epithelial cultures but not in 100% of the SCLC, in 65% of the NSCLC, or in 60% of the breast cancer lines. By contrast, RASSF1C was expressed in all nonmalignant cell cultures and in nearly all cancer cell lines. RASSF1A promoter hypermethylation was detected in 100% of SCLC, in 63% of NSCLC, in 64% of breast cancer lines, in 30% of primary NSCLCs, and in 49% of primary breast tumors but in none of the nonmalignant lung tissues. RASSF1A promoter hypermethylation in resected NSCLCs was associated with impaired patient survival (P = .046). Exogenous expression of RASSF1A in a cell line lacking expression decreased in vitro colony formation and in vivo tumorigenicity. Conclusion: RASSF1A is a potential tumor suppressor gene that undergoes epigenetic inactivation in lung and breast cancers through hypermethylation of its promoter region.
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A. Dallol, A. Agathanggelou, S. L. Fenton, J. Ahmed-Choudhury, L. Hesson, M. D. Vos, G. J. Clark, J. Downward, E. R. Maher, and F. Latif RASSF1A Interacts with Microtubule-Associated Proteins and Modulates Microtubule Dynamics Cancer Res., June 15, 2004; 64(12): 4112 - 4116. [Abstract] [Full Text] [PDF]
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R. Pio, I. Zudaire, I. Pino, Z. Castano, N. Zabalegui, S. Vicent, F. Garcia-Amigot, M. D. Odero, M. D. Lozano, J. Garcia-Foncillas, et al. {alpha}CP-4, Encoded by a Putative Tumor Suppressor Gene at 3p21, But Not Its Alternative Splice Variant {alpha}CP-4a, Is Underexpressed in Lung Cancer Cancer Res., June 15, 2004; 64(12): 4171 - 4179. [Abstract] [Full Text] [PDF]
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N. Sunaga, K. Miyajima, M. Suzuki, M. Sato, M. A. White, R. D. Ramirez, J. W. Shay, A. F. Gazdar, and J. D. Minna Different Roles for Caveolin-1 in the Development of Non-Small Cell Lung Cancer versus Small Cell Lung Cancer Cancer Res., June 15, 2004; 64(12): 4277 - 4285. [Abstract] [Full Text] [PDF]
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M. Suzuki, N. Sunaga, D. S. Shames, S. Toyooka, A. F. Gazdar, and J. D. Minna RNA Interference-Mediated Knockdown of DNA Methyltransferase 1 Leads to Promoter Demethylation and Gene Re-Expression in Human Lung and Breast Cancer Cells Cancer Res., May 1, 2004; 64(9): 3137 - 3143. [Abstract] [Full Text] [PDF]
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J. C. Lindsey, M. E. Lusher, J. A. Anderton, S. Bailey, R. J. Gilbertson, A. D.J. Pearson, D. W. Ellison, and S. C. Clifford Identification of tumour-specific epigenetic events in medulloblastoma development by hypermethylation profiling Carcinogenesis, May 1, 2004; 25(5): 661 - 668. [Abstract] [Full Text] [PDF]
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T. Takahashi, N. Shivapurkar, J. Reddy, H. Shigematsu, K. Miyajima, M. Suzuki, S. Toyooka, S. Zochbauer-Muller, J. Drach, G. Parikh, et al. DNA Methylation Profiles of Lymphoid and Hematopoietic Malignancies Clin. Cancer Res., May 1, 2004; 10(9): 2928 - 2935. [Abstract] [Full Text] [PDF]
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S. Yegnasubramanian, J. Kowalski, M. L. Gonzalgo, M. Zahurak, S. Piantadosi, P. C. Walsh, G. S. Bova, A. M. De Marzo, W. B. Isaacs, and W. G. Nelson Hypermethylation of CpG Islands in Primary and Metastatic Human Prostate Cancer Cancer Res., March 15, 2004; 64(6): 1975 - 1986. [Abstract] [Full Text] [PDF]
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M. J. Shrubsole, Y.-T. Gao, Q. Cai, X. O. Shu, Q. Dai, J. R. Hebert, F. Jin, and W. Zheng MTHFR Polymorphisms, Dietary Folate Intake, and Breast Cancer Risk: Results from the Shanghai Breast Cancer Study Cancer Epidemiol. Biomarkers Prev., February 1, 2004; 13(2): 190 - 196. [Abstract] [Full Text] [PDF]
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I. H. N. Wong, J. Chan, J. Wong, and P. K. H. Tam Ubiquitous Aberrant RASSF1A Promoter Methylation in Childhood Neoplasia1 Clin. Cancer Res., February 1, 2004; 10(3): 994 - 1002. [Abstract] [Full Text] [PDF]
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S. L. Fenton, A. Dallol, A. Agathanggelou, L. Hesson, J. Ahmed-Choudhury, S. Baksh, C. Sardet, R. Dammann, J. D. Minna, J. Downward, et al. Identification of the E1A-Regulated Transcription Factor p120E4F as an Interacting Partner of the RASSF1A Candidate Tumor Suppressor Gene Cancer Res., January 1, 2004; 64(1): 102 - 107. [Abstract] [Full Text] [PDF]
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C. Garnis, C. Baldwin, L. Zhang, M. P. Rosin, and W. L. Lam Use of Complete Coverage Array Comparative Genomic Hybridization to Define Copy Number Alterations on Chromosome 3p in Oral Squamous Cell Carcinomas Cancer Res., December 15, 2003; 63(24): 8582 - 8585. [Abstract] [Full Text] [PDF]
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Y. Liu, Q. An, L. Li, D. Zhang, J. Huang, X. Feng, S. Cheng, and Y. Gao Hypermethylation of p16INK4a in Chinese lung cancer patients: biological and clinical implications Carcinogenesis, December 1, 2003; 24(12): 1897 - 1901. [Abstract] [Full Text] [PDF]
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P. S. Yan, H. Shi, F. Rahmatpanah, T. H-C. Hsiau, A. H-A. Hsiau, Y.-W. Leu, J. C. Liu, and T. H.-M. Huang Differential Distribution of DNA Methylation within the RASSF1A CpG Island in Breast Cancer Cancer Res., October 1, 2003; 63(19): 6178 - 6186. [Abstract] [Full Text] [PDF]
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D.-H. Kim, J. S. Kim, J.-H. Park, S. K. Lee, Y.-I. Ji, Y. M. Kwon, Y. M. Shim, J. Han, and J. Park Relationship of Ras Association Domain Family 1 Methylation and K-Ras Mutation in Primary Non-Small Cell Lung Cancer Cancer Res., October 1, 2003; 63(19): 6206 - 6211. [Abstract] [Full Text] [PDF]
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A. Agathanggelou, I. Bieche, J. Ahmed-Choudhury, B. Nicke, R. Dammann, S. Baksh, B. Gao, J. D. Minna, J. Downward, E. R. Maher, et al. Identification of Novel Gene Expression Targets for the Ras Association Domain Family 1 (RASSF1A) Tumor Suppressor Gene in Non-Small Cell Lung Cancer and Neuroblastoma Cancer Res., September 1, 2003; 63(17): 5344 - 5351. [Abstract] [Full Text] [PDF]
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S. M. Dong, D.-I. Sun, N. E. Benoit, I. Kuzmin, M. I. Lerman, and D. Sidransky Epigenetic Inactivation of RASSF1A in Head and Neck Cancer Clin. Cancer Res., September 1, 2003; 9(10): 3635 - 3640. [Abstract] [Full Text] [PDF]
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W. A. Palmisano, K. P. Crume, M. J. Grimes, S. A. Winters, M. Toyota, M. Esteller, N. Joste, S. B. Baylin, and S. A. Belinsky Aberrant Promoter Methylation of the Transcription Factor Genes PAX5 {alpha} and {beta} in Human Cancers Cancer Res., August 1, 2003; 63(15): 4620 - 4625. [Abstract] [Full Text] [PDF]
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Y. Cohen, G. Singer, O. Lavie, S. M. Dong, U. Beller, and D. Sidransky The RASSF1A Tumor Suppressor Gene Is Commonly Inactivated in Adenocarcinoma of the Uterine Cervix Clin. Cancer Res., August 1, 2003; 9(8): 2981 - 2984. [Abstract] [Full Text] [PDF]
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S. Zhong, W. Yeo, M. W. Tang, N. Wong, P. B. S. Lai, and P. J. Johnson Intensive Hypermethylation of the CpG Island of Ras Association Domain Family 1A in Hepatitis B Virus-associated Hepatocellular Carcinomas Clin. Cancer Res., August 1, 2003; 9(9): 3376 - 3382. [Abstract] [Full Text] [PDF]
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T. Kuroki, F. Trapasso, S. Yendamuri, A. Matsuyama, H. Alder, M. Mori, and C. M. Croce Allele Loss and Promoter Hypermethylation of VHL, RAR-{beta}, RASSF1A, and FHIT Tumor Suppressor Genes on Chromosome 3p in Esophageal Squamous Cell Carcinoma Cancer Res., July 1, 2003; 63(13): 3724 - 3728. [Abstract] [Full Text] [PDF]
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D.-H. Kim, J. S. Kim, Y.-I. Ji, Y. M. Shim, H. Kim, J. Han, and J. Park Hypermethylation of RASSF1A Promoter Is Associated with the Age at Starting Smoking and a Poor Prognosis in Primary Non-Small Cell Lung Cancer Cancer Res., July 1, 2003; 63(13): 3743 - 3746. [Abstract] [Full Text] [PDF]
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M. D. Vos, A. Martinez, C. A. Ellis, T. Vallecorsa, and G. J. Clark The Pro-apoptotic Ras Effector Nore1 May Serve as a Ras-regulated Tumor Suppressor in the Lung J. Biol. Chem., June 6, 2003; 278(24): 21938 - 21943. [Abstract] [Full Text] [PDF]
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I. Kuzmin, L. Liu, R. Dammann, L. Geil, E. J. Stanbridge, S. P. Wilczynski, M. I. Lerman, and G. P. Pfeifer Inactivation of RAS Association Domain Family 1A Gene in Cervical Carcinomas and the Role of Human Papillomavirus Infection Cancer Res., April 15, 2003; 63(8): 1888 - 1893. [Abstract] [Full Text] [PDF]
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M. Spugnardi, S. Tommasi, R. Dammann, G. P. Pfeifer, and D. S. B. Hoon Epigenetic Inactivation of RAS Association Domain Family Protein 1 (RASSF1A) in Malignant Cutaneous Melanoma Cancer Res., April 1, 2003; 63(7): 1639 - 1643. [Abstract] [Full Text] [PDF]
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T. Kuroki, F. Trapasso, S. Yendamuri, A. Matsuyama, H. Alder, M. Mori, and C. M. Croce Promoter Hypermethylation of RASSF1A in Esophageal Squamous Cell Carcinoma Clin. Cancer Res., April 1, 2003; 9(4): 1441 - 1445. [Abstract] [Full Text] [PDF]
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E. C. Chan, S. Y. Lam, K. W. Tsang, B. Lam, J. C. M. Ho, K. H. Fu, W. K. Lam, and Y. L. Kwong Aberrant Promoter Methylation in Chinese Patients with Non-Small Cell Lung Cancer: Patterns in Primary Tumors and Potential Diagnostic Application in Bronchoalevolar Lavage Clin. Cancer Res., December 1, 2002; 8(12): 3741 - 3746. [Abstract] [Full Text] [PDF]
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A. Rathi, A. K. Virmani, J. O. Schorge, K. J. Elias, R. Maruyama, J. D. Minna, S. C. Mok, L. Girard, D. A. Fishman, and A. F. Gazdar Methylation Profiles of Sporadic Ovarian Tumors and nonmalignant Ovaries from High-Risk Women Clin. Cancer Res., November 1, 2002; 8(11): 3324 - 3331. [Abstract] [Full Text] [PDF]
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K. Harada, S. Toyooka, N. Shivapurkar, A. Maitra, J. L. Reddy, H. Matta, K. Miyajima, C. F. Timmons, G. E. Tomlinson, D. Mastrangelo, et al. Deregulation of Caspase 8 and 10 Expression in Pediatric Tumors and Cell Lines Cancer Res., October 15, 2002; 62(20): 5897 - 5901. [Abstract] [Full Text] [PDF]
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M. E. Lusher, J. C. Lindsey, F. Latif, A. D. J. Pearson, D. W. Ellison, and S. C. Clifford Biallelic Epigenetic Inactivation of the RASSF1A Tumor Suppressor Gene in Medulloblastoma Development Cancer Res., October 15, 2002; 62(20): 5906 - 5911. [Abstract] [Full Text] [PDF]
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S. Sarkar, B. C. Roy, N. Hatano, T. Aoyagi, K. Gohji, and R. Kiyama A Novel Ankyrin Repeat-containing Gene (Kank) Located at 9p24 Is a Growth Suppressor of Renal Cell Carcinoma J. Biol. Chem., September 20, 2002; 277(39): 36585 - 36591. [Abstract] [Full Text] [PDF]
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R. Diaz, D. Ahn, L. Lopez-Barcons, M. Malumbres, I. Perez de Castro, J. Lue, N. Ferrer-Miralles, R. Mangues, J. Tsong, R. Garcia, et al. The N-ras Proto-oncogene Can Suppress the Malignant Phenotype in the Presence or Absence of Its Oncogene Cancer Res., August 1, 2002; 62(15): 4514 - 4518. [Abstract] [Full Text] [PDF]
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