Loss of imprinting and marked gene elevation are 2 forms of aberrant IGF2 expression in colorectal cancer

International Journal of Cancer

Volumn 127, Issue 3, 2010, Pages 568-577

  Cheng, Yu Wei ^a   Idrees, Kamran ^b   Shattock, Richard ^a   Khan, Sajid A ^c   Zeng, Zhaoshi ^d   Brennan, Cameron W ^d   Paty, Philip ^d   Barany, Francis ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Kentucky   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Colorectal cancer; CpG methylation; IGF2; Imprinting; LDR

Indexed keywords

RNA H19; SOMATOMEDIN B;

ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; DNA METHYLATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA METHYLATION; UPREGULATION;

COLORECTAL NEOPLASMS; DNA METHYLATION; GENOMIC IMPRINTING; HUMANS; INSULIN-LIKE GROWTH FACTOR II; POLYMORPHISM, GENETIC; PROMOTER REGIONS, GENETIC;

EID: 77954435392     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25086     Document Type: Article

References (43)

1. Rainier S, Johnson LA, Dobry CJ, Ping AJ, Grundy PE, Feinberg AP. Relaxation of imprinted genes in human cancer. Nature 1993;362:747-9.
2. Ogawa O, Eccles MR, Szeto J, McNoe LA, Yun K, Maw MA, Smith PJ, Reeve AE. Relaxation of insulin-like growth factor II gene imprinting implicated in Wilms' tumour. Nature 1993;362:749-51.
3. Ferguson-Smith AC. Genetic imprinting: silencing elements have their say. Curr Biol 2000;10:R872-5.
4. Cui H, Onyango P, Brandenburg S, Wu Y, Hsieh CL, Feinberg AP. Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res 2002;62:6442-6. (Pubitemid 35364103)
5. Murphy SK, Huang Z, Wen Y, Spillman MA, Whitaker RS, Simel LR, Nichols TD, Marks JR, Berchuck A. Frequent IGF2/H19 domain epigenetic alterations and elevated IGF2 expression in epithelial ovarian cancer. Mol Cancer Res 2006;4:283-92.
6. Nakagawa H, Chadwick RB, Peltomaki P, Plass C, Nakamura Y, de La Chapelle A. Loss of imprinting of the insulin-like growth factor II gene occurs by biallelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer. Proc Natl Acad Sci USA 2001;98: 591-6.
7. Sullivan MJ, Taniguchi T, Jhee A, Kerr N, Reeve AE. Relaxation of IGF2 imprinting in Wilms tumours associated with specific changes in IGF2 methylation. Oncogene 1999;18:7527-34. (Pubitemid 30035053)
8. Steenman MJ, Rainier S, Dobry CJ, Grundy P, Horon IL, Feinberg AP. Loss of imprinting of IGF2 is linked to reduced expression and abnormal methylation of H19 in Wilms' tumour. Nat Genet 1994;7: 433-9.
9. Moulton T, Crenshaw T, Hao Y, Moosikasuwan J, Lin N, Dembitzer F, Hensle T, Weiss L, McMorrow L, Loew T, Kraus W, Gerald W, et al. Epigenetic lesions at the H19 locus in Wilms' tumour patients. Nat Genet 1994;7:440-7.
10. Bell AC, Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the IGF2 gene. Nature 2000;405:482-5.
11. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/IGF2 locus. Nature 2000;405:486-9.
12. Kim HT, Choi BH, Niikawa N, Lee TS, Chang SI. Frequent loss of imprinting of the H19 and IGF-II genes in ovarian tumors. Am J Med Genet 1998;80:391-5.
13. Elkin M, Shevelev A, Schulze E, Tykocinsky M, Cooper M, Ariel I, Pode D, Kopf E, de Groot N, Hochberg A. The expression of the imprinted H19 and IGF-2 genes in human bladder carcinoma. FEBS Lett 1995;374:57-61.
14. Kondo M, Suzuki H, Ueda R, Osada H, Takagi K, Takahashi T, Takahashi T. Frequent loss of imprinting of the H19 gene is often associated with its overexpression in human lung cancers. Oncogene 1995;10:1193-8.
15. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 1995;375:34-9.
16. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001;17:520-7.
17. Reik W, Murrell A. Genomic imprinting. Silence across the border. Nature 2000;405: 408-9.
18. Cui H, Cruz-Correa M, Giardiello FM, Hutcheon DF, Kafonek DR, Brandenburg S, Wu Y, He X, Powe NR, Feinberg AP. Loss of IGF2 imprinting: a potential marker of colorectal cancer risk. Science 2003;299:1753-5.
19. Ravenel JD, Broman KW, Perlman EJ, Niemitz EL, Jayawardena TM, Bell DW, Haber DA, Uejima H, Feinberg AP. Loss of imprinting of insulin-like growth factor-II (IGF2) gene in distinguishing specific biologic subtypes of Wilms tumor. J Natl Cancer Inst 2001;93:1698-703.
20. Fottner C, Hoeflich A, Wolf E, Weber MM. Role of the insulin-like growth factor system in adrenocortical growth control and carcinogenesis. Horm Metab Res 2004;36:397-405. (Pubitemid 38932097)
21. Cheng YW, Pincas H, Bacolod MD, Schemmann G, Giardina SF, Huang J, Barral S, Idrees K, Khan SA, Zeng Z, Rosenberg S, Notterman DA, et al. CpG island methylator phenotype associates with low-degree chromosomal abnormalities in colorectal cancer. Clin Cancer Res 2008;14:6005-13.
22. Woodson K, Flood A, Green L, Tangrea JA, Hanson J, Cash B, Schatzkin A, Schoenfeld P. Loss of insulin-like growth factor-II imprinting and the presence of screen-detected colorectal adenomas in women. J Natl Cancer Inst 2004;96:407-10. (Pubitemid 38351303)
23. Cheng YW, Shawber C, Notterman D, Paty P, Barany F. Multiplexed profiling of candidate genes for CpG island methylation status using a flexible PCR/ LDR/Universal Array assay. Genome Res 2006;16:282-9.
24. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006;38:787-93.
25. MacDonald JW, Ghosh D. COPA-cancer outlier profile analysis. Bioinformatics 2006; 22:2950-1.
26. Tsafrir D, Bacolod M, Selvanayagam Z, Tsafrir I, Shia J, Zeng Z, Liu H, Krier C, Stengel RF, Barany F, Gerald WL, Paty PB, et al. Relationship of gene expression and chromosomal abnormalities in colorectal cancer. Cancer Res 2006;66:2129-37.
27. Haruta M, Arai Y, Sugawara W, Watanabe N, Honda S, Ohshima J, Soejima H, Nakadate H, Okita H, Hata J, Fukuzawa M, Kaneko Y. Duplication of paternal IGF2 or loss of maternal IGF2 imprinting occurs in half of Wilms tumors with various structural WT1 abnormalities. Genes Chromosomes Cancer 2008;47:712-27.
28. Issa JP, Vertino PM, Boehm CD, Newsham IF, Baylin SB. Switch from monoallelic to biallelic human IGF2 promoter methylation during aging and carcinogenesis. Proc Natl Acad Sci USA 1996;93:11757-62.
29. Rowley JD. Chromosome translocations: dangerous liaisons revisited. Nat Rev Cancer 2001;1:245-50.
30. Rowley JD. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973;243:290-3 (letter).
31. de Klein A, van Kessel AG, Grosveld G, Bartram CR, Hagemeijer A, Bootsma D, Spurr NK, Heisterkamp N, Groffen J, Stephenson JR. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature 1982;300:765-7.
32. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310: 644-8.
33. Ling JQ, Li T, Hu JF, Vu TH, Chen HL, Qiu XW, Cherry AM, Hoffman AR. CTCF mediates interchromosomal colocalization between IGF2/H19 and Wsb1/Nf1. Science 2006;312:269-72.
34. Lopes S, Lewis A, Hajkova P, Dean W, Oswald J, Forne T, Murrell A, Constancia M, Bartolomei M, Walter J, Reik W. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum Mol Genet 2003;12: 295-305.
35. Murrell A, Heeson S, Reik W. Interaction between differentially methylated regions partitions the imprinted genes IGF2 and H19 into parent-specific chromatin loops. Nat Genet 2004;36:889-93.
36. Sasaki H, Ishihara K, Kato R. Mechanisms of IGF2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. J Biochem 2000; 127:711-5. (Pubitemid 30317892)
37. Grande MA, van der Kraan I, de Jong L, van Driel R. Nuclear distribution of transcription factors in relation to sites of transcription and RNA polymerase II. J Cell Sci 1997;110 (Part 15):1781-91.
38. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 2004;36:1065-71.
39. Kaneda A, Wang CJ, Cheong R, Timp W, Onyango P, Wen B, Iacobuzio-Donahue CA, Ohlsson R, Andraos R, Pearson MA, Sharov AA, Longo DL, et al. Enhanced sensitivity to IGF-II signaling links loss of imprinting of IGF2 to increased cell proliferation and tumor risk. Proc Natl Acad Sci USA 2007;104:20926-31.
40. Gabory A, Ripoche MA, Yoshimizu T, Dandolo L. The H19 gene: regulation and function of a non-coding RNA. Cytogenet Genome Res 2006;113:188-93.
41. Cui H, Horon IL, Ohlsson R, Hamilton SR, Feinberg AP. Loss of imprinting in normal tissue of colorectal cancer patients with microsatellite instability. Nat Med 1998;4: 1276-80.
42. Nishihara S, Hayashida T, Mitsuya K, Schulz TC, Ikeguchi M, Kaibara N, Oshimura M. Multipoint imprinting analysis in sporadic colorectal cancers with and without microsatellite instability. Int J Oncol 2000;17:317-22.
43. Sasaki J, Konishi F, Kawamura YJ, Kai T, Takata O, Tsukamoto T. Clinicopathological characteristics of colorectal cancers with loss of imprinting of insulin-like growth factor 2. Int J Cancer 2006;119:80-3.