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[Cancer Research 61, 3225-3229, April 15, 2001]
© 2001 American Association for Cancer Research

Perspectives in Cancer Research

A Gene Hypermethylation Profile of Human Cancer1

Manel Esteller2,, 3, Paul G. Corn2, Stephen B. Baylin and James G. Herman4

The Johns Hopkins Comprehensive Cancer Center, Baltimore, Maryland 21231

ABSTRACT

We are in an era where the potential exists for deriving comprehensive profiles of DNA alterations characterizing each form of human cancer. Such profiles would provide invaluable insight into mechanisms underlying the evolution of each tumor type and will provide molecular markers, which could radically improve cancer detection. To date, no one type of DNA change has been defined which accomplishes this purpose. Herein, by using a candidate gene approach, we show that one category of DNA alteration, aberrant methylation of gene promoter regions, can enormously contribute to the above goals. We have now analyzed a series of promoter hypermethylation changes in 12 genes (p16INK4a, p15INK4b, p14ARF, p73, APC,5 BRCA1, hMLH1, GSTP1, MGMT, CDH1, TIMP3, and DAPK), each rigorously characterized for association with abnormal gene silencing in cancer, in DNA from over 600 primary tumor samples representing 15 major tumor types. The genes play known important roles in processes encompassing tumor suppression, cell cycle regulation, apoptosis, DNA repair, and metastastic potential. A unique profile of promoter hypermethylation exists for each human cancer in which some gene changes are shared and others are cancer-type specific. The hypermethylation of the genes occurs independently to the extent that a panel of three to four markers defines an abnormality in 70–90% of each cancer type. Our results provide an unusual view of the pervasiveness of DNA alterations, in this case an epigenetic change, in human cancer and a powerful set of markers to outline the disruption of critical pathways in tumorigenesis and for derivation of sensitive molecular detection strategies for virtually every human tumor type.




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C. A. Righini, F. de Fraipont, J.-F. Timsit, C. Faure, E. Brambilla, E. Reyt, and M.-C. Favrot
Tumor-Specific Methylation in Saliva: A Promising Biomarker for Early Detection of Head and Neck Cancer Recurrence
Clin. Cancer Res., February 15, 2007; 13(4): 1179 - 1185.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
M. van den Donk, M. van Engeland, L. Pellis, B. J.M. Witteman, F. J. Kok, J. Keijer, and E. Kampman
Dietary Folate Intake in Combination with MTHFR C677T Genotype and Promoter Methylation of Tumor Suppressor and DNA Repair Genes in Sporadic Colorectal Adenomas
Cancer Epidemiol. Biomarkers Prev., February 1, 2007; 16(2): 327 - 333.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
W. C. Reinhold, M. A. Reimers, A. K. Maunakea, S. Kim, S. Lababidi, U. Scherf, U. T. Shankavaram, M. S. Ziegler, C. Stewart, H. Kouros-Mehr, et al.
Detailed DNA methylation profiles of the E-cadherin promoter in the NCI-60 cancer cells
Mol. Cancer Ther., February 1, 2007; 6(2): 391 - 403.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
H. Shi, J. Guo, D. J. Duff, F. Rahmatpanah, R. Chitima-Matsiga, M. Al-Kuhlani, K. H. Taylor, O. Sjahputera, M. Andreski, J. E. Wooldridge, et al.
Discovery of novel epigenetic markers in non-Hodgkin's lymphoma
Carcinogenesis, January 1, 2007; 28(1): 60 - 70.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L.-H. Wang, S.-H. Kim, J. H. Lee, Y.-L. Choi, Y. C. Kim, T. S. Park, Y.-C. Hong, C.-F. Wu, and Y. K. Shin
Inactivation of SMAD4 Tumor Suppressor Gene During Gastric Carcinoma Progression
Clin. Cancer Res., January 1, 2007; 13(1): 102 - 110.
[Abstract] [Full Text] [PDF]

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 ASH Education BookHome page
G. Garcia-Manero
Modifying the Epigenome as a Therapeutic Strategy in Myelodysplasia
Hematology, January 1, 2007; 2007(1): 405 - 411.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. R. Morey, D. J. Smiraglia, S. R. James, J. Yu, M. T. Moser, B. A. Foster, and A. R. Karpf
DNA Methylation Pathway Alterations in an Autochthonous Murine Model of Prostate Cancer
Cancer Res., December 15, 2006; 66(24): 11659 - 11667.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. Gu, D. Berman, C. Lu, I. I. Wistuba, J. A. Roth, M. Frazier, M. R. Spitz, and X. Wu
Aberrant Promoter Methylation Profile and Association with Survival in Patients with Non-Small Cell Lung Cancer
Clin. Cancer Res., December 15, 2006; 12(24): 7329 - 7338.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. D. Williams, N. Chakravarti, M. S. Kies, S.-I. Maruya, J. N. Myers, J. C. Haviland, R. S. Weber, R. Lotan, and A. K. El-Naggar
Implications of Methylation Patterns of Cancer Genes in Salivary Gland Tumors
Clin. Cancer Res., December 15, 2006; 12(24): 7353 - 7358.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Urakami, H. Shiina, H. Enokida, H. Hirata, K. Kawamoto, T. Kawakami, N. Kikuno, Y. Tanaka, S. Majid, M. Nakagawa, et al.
Wnt Antagonist Family Genes as Biomarkers for Diagnosis, Staging, and Prognosis of Renal Cell Carcinoma Using Tumor and Serum DNA
Clin. Cancer Res., December 1, 2006; 12(23): 6989 - 6997.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Y. Yuan, J. Wang, J. Li, L. Wang, M. Li, Z. Yang, C. Zhang, and J. L. Dai
Frequent Epigenetic Inactivation of Spleen Tyrosine Kinase Gene in Human Hepatocellular Carcinoma.
Clin. Cancer Res., November 15, 2006; 12(22): 6687 - 6695.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. J. Marsit, E. A. Houseman, B. C. Christensen, K. Eddy, R. Bueno, D. J. Sugarbaker, H. H. Nelson, M. R. Karagas, and K. T. Kelsey
Examination of a CpG Island Methylator Phenotype and Implications of Methylation Profiles in Solid Tumors
Cancer Res., November 1, 2006; 66(21): 10621 - 10629.
[Abstract] [Full Text] [PDF]

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 Hum Exp ToxicolHome page
T. de Almeida Simao, G. L. De Bonis Almeida Simoes, F. S. Ribeiro, D. A. de Paula Cidade, N. A. Andreollo, L. R. Lopes, J. M. B. Macedo, R. Acatauassu, A. M. R. Teixeira, I. Felzenszwalb, et al.
Lower expression of p14ARF and p16INK4a correlates with higher DNMT3B expression in human oesophageal squamous cell carcinomas
Human and Experimental Toxicology, September 1, 2006; 25(9): 515 - 522.
[Abstract] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
A. L. Fridman, L. Tang, O. I. Kulaeva, B. Ye, Q. Li, F. Nahhas, P. C. Roberts, S. J. Land, J. Abrams, and M. A. Tainsky
Expression profiling identifies three pathways altered in cellular immortalization: interferon, cell cycle, and cytoskeleton.
J. Gerontol. A Biol. Sci. Med. Sci., September 1, 2006; 61(9): 879 - 889.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
L. Lopez-Serra, E. Ballestar, M. F. Fraga, M. Alaminos, F. Setien, and M. Esteller
A Profile of Methyl-CpG Binding Domain Protein Occupancy of Hypermethylated Promoter CpG Islands of Tumor Suppressor Genes in Human Cancer.
Cancer Res., September 1, 2006; 66(17): 8342 - 8346.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
T. Rauch, H. Li, X. Wu, and G. P. Pfeifer
MIRA-Assisted Microarray Analysis, a New Technology for the Determination of DNA Methylation Patterns, Identifies Frequent Methylation of Homeodomain-Containing Genes in Lung Cancer Cells
Cancer Res., August 15, 2006; 66(16): 7939 - 7947.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Guo, J. Ren, M. G. House, Y. Qi, M. V. Brock, and J. G. Herman
Accumulation of Promoter Methylation Suggests Epigenetic Progression in Squamous Cell Carcinoma of the Esophagus
Clin. Cancer Res., August 1, 2006; 12(15): 4515 - 4522.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
C. Gebhard, L. Schwarzfischer, T. H. Pham, R. Andreesen, A. Mackensen, and M. Rehli
Rapid and sensitive detection of CpG-methylation using methyl-binding (MB)-PCR
Nucleic Acids Res., July 5, 2006; 34(11): e82 - e82.
[Abstract] [Full Text] [PDF]

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 BloodHome page
S. Niclot, Q. Pruvot, C. Besson, D. Savoy, E. Macintyre, G. Salles, N. Brousse, B. Varet, P. Landais, P. Taupin, et al.
Implication of the folate-methionine metabolism pathways in susceptibility to follicular lymphomas
Blood, July 1, 2006; 108(1): 278 - 285.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. Gebhard, L. Schwarzfischer, T.-H. Pham, E. Schilling, M. Klug, R. Andreesen, and M. Rehli
Genome-wide profiling of CpG methylation identifies novel targets of aberrant hypermethylation in myeloid leukemia.
Cancer Res., June 15, 2006; 66(12): 6118 - 6128.
[Abstract] [Full Text] [PDF]

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 Endocr Relat CancerHome page
A. S Perry, R. Foley, K. Woodson, and M. Lawler
The emerging roles of DNA methylation in the clinical management of prostate cancer.
Endocr. Relat. Cancer, June 1, 2006; 13(2): 357 - 377.
[Abstract] [Full Text] [PDF]

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 Arch Otolaryngol Head Neck SurgHome page
M. J. Worsham, K. M. Chen, V. Meduri, A. O. H. Nygren, A. Errami, J. P. Schouten, and M. S. Benninger
Epigenetic events of disease progression in head and neck squamous cell carcinoma.
Arch Otolaryngol Head Neck Surg, June 1, 2006; 132(6): 668 - 677.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
A. N. Bachman, G. M. Curtin, D. J. Doolittle, and J. I. Goodman
Altered Methylation in Gene-Specific and GC-Rich Regions of DNA Is Progressive and Nonrandom during Promotion of Skin Tumorigenesis
Toxicol. Sci., June 1, 2006; 91(2): 406 - 418.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
D.-F. Peng, Y. Kanai, M. Sawada, S. Ushijima, N. Hiraoka, S. Kitazawa, and S. Hirohashi
DNA methylation of multiple tumor-related genes in association with overexpression of DNA methyltransferase 1 (DNMT1) during multistage carcinogenesis of the pancreas
Carcinogenesis, June 1, 2006; 27(6): 1160 - 1168.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
M. Esteller
The necessity of a human epigenome project
Carcinogenesis, June 1, 2006; 27(6): 1121 - 1125.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
J. S. Jones, C. I. Amos, M. Pande, X. Gu, J. Chen, I. M. Campos, Q. Wei, M. Rodriguez-Bigas, P. M. Lynch, and M. L. Frazier
DNMT3b Polymorphism and Hereditary Nonpolyposis Colorectal Cancer Age of Onset.
Cancer Epidemiol. Biomarkers Prev., May 1, 2006; 15(5): 886 - 891.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
G. Shao, J. Berenguer, A. C. Borczuk, C. A. Powell, T. K. Hei, and Y. Zhao
Epigenetic Inactivation of Betaig-h3 Gene in Human Cancer Cells.
Cancer Res., May 1, 2006; 66(9): 4566 - 4573.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
S. Mulero-Navarro, J.M. Carvajal-Gonzalez, M. Herranz, E. Ballestar, M.F. Fraga, S. Ropero, M. Esteller, and P.M. Fernandez-Salguero
The dioxin receptor is silenced by promoter hypermethylation in human acute lymphoblastic leukemia through inhibition of Sp1 binding
Carcinogenesis, May 1, 2006; 27(5): 1099 - 1104.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. H. Wei, C. Balch, H. H. Paik, Y.-S. Kim, R. L. Baldwin, S. Liyanarachchi, L. Li, Z. Wang, J. C. Wan, R. V. Davuluri, et al.
Prognostic DNA methylation biomarkers in ovarian cancer.
Clin. Cancer Res., May 1, 2006; 12(9): 2788 - 2794.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
F. J. Reu, D. W. Leaman, R. R. Maitra, S. I. Bae, L. Cherkassky, M. W. Fox, D. R. Rempinski, N. Beaulieu, A. R. MacLeod, and E. C. Borden
Expression of RASSF1A, an Epigenetically Silenced Tumor Suppressor, Overcomes Resistance to Apoptosis Induction by Interferons.
Cancer Res., March 1, 2006; 66(5): 2785 - 2793.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Vottero, M. Capelletti, S. Giuliodori, I. Viani, M. Ziveri, T. M. Neri, S. Bernasconi, and L. Ghizzoni
Decreased Androgen Receptor Gene Methylation in Premature Pubarche: A Novel Pathogenetic Mechanism?
J. Clin. Endocrinol. Metab., March 1, 2006; 91(3): 968 - 972.
[Abstract] [Full Text] [PDF]


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