Novel candidate colorectal cancer biomarkers identified by methylation microarray-based scanning

Endocrine-Related Cancer

Volumn 18, Issue 4, 2011, Pages 465-478

  Mori, Yuriko ^a   Olaru, Alexandru V ^a   Cheng, Yulan ^a   Agarwal, Rachana ^a   Yang, Jian ^a   Luvsanjav, Delgermaa ^a   Yu, Wayne ^b   Selaru, Florin M ^a   Hutfless, Susan ^a   Lazarev, Mark ^a   Kwon, John H ^a   Brant, Steven R ^a   Marohn, Michael R ^c   Hutcheon, David F ^a   Duncan, Mark D ^d   Goel, Ajay ^e   Meltzer, Stephen J ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d JOHNS HOPKINS BAYVIEW MEDICAL CENTER   (United States)

^e BAYLOR RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; MICRORNA; PENTRAXIN; PROTEIN HOMER 2; ZINC FINGER PROTEIN;

AREA UNDER THE CURVE; ARTICLE; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA MICROARRAY; GENE LOCUS; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY;

ADENOMA; ADULT; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; COLON; COLORECTAL NEOPLASMS; DNA METHYLATION; DNA, NEOPLASM; EPIGENOMICS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MICRORNAS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RECTUM; TUMOR MARKERS, BIOLOGICAL;

EID: 80052174886     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-11-0083     Document Type: Article

References (54)

1. Ahlquist DA, Sargent DJ, Loprinzi CL, Levin TR, Rex DK, Ahnen DJ, Knigge K, Lance MP, Burgart LJ, Hamilton SR et al. 2008a Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Annals of Internal Medicine 149 441-450.
2. Ahlquist T, Lind GE, Costa VL, Meling GI, Vatn M, Hoff GS, Rognum TO, Skotheim RI, Thiis-Evensen E & Lothe RA 2008b Gene methylation profiles of normal mucosa, and benign and malignant colorectal tumors identify early onset markers. Molecular Cancer 7 94. (doi:10.1186/1476-4598-7-94)
3. Ahuja N, Li Q, Mohan AL, Baylin SB & Issa JP 1998 Aging DNA methylation in colorectal mucosa and cancer. Cancer Research 58 5489-5494. (Pubitemid 28551135)
4. Ayala JE, Bracy DP, James FD, Burmeister MA, Wasserman DH & Drucker DJ 2010 Glucagon-like peptide-1 receptor knockout mice are protected from high-fat diet-induced insulin resistance. Endocrinology 151 4678-4687. (doi:10.1210/en.2010-0289)
5. Baek YH, Chang E, Kim YJ, Kim BK, Sohn JH & Park DI 2009 Stool methylation-specific polymerase chain reaction assay for the detection of colorectal neoplasia in Korean patients. Diseases of the Colon and Rectum 52 1452-1459; discussion 1459-1463. (doi:10.1007/DCR.0b013e3181a79533)
6. Belshaw NJ, Elliott GO, Foxall RJ, Dainty JR, Pal N, Coupe A, Garg D, Bradburn DM, Mathers JC &Johnson IT 2008 Profiling CpG island field methylation in both morphologically normal and neoplastic human colonic mucosa. British Journal of Cancer 99 136-142. (doi:10.1038/sj.bjc.6604432)
7. Belshaw NJ, Pal N, Tapp HS, Dainty JR, Lewis MP, Williams MR, Lund EK & Johnson IT 2010 Patterns of DNA methylation in individual colonic crypts reveal aging and cancer-related field defects in the morphologically normal mucosa. Carcinogenesis 31 1158-1163. (doi:10.1093/carcin/bgq077)
8. Campos RV, Lee YC & Drucker DJ 1994 Divergent tissue-specific and developmental expression of receptors for glucagon and glucagon-like peptide-1 in the mouse. Endocrinology 134 2156-2164. (doi:10.1210/en.134.5.2156)
9. Chen WD, Han ZJ, Skoletsky J, Olson J, Sah J, Myeroff L, Platzer P, Lu S, Dawson D, Willis J et al. 2005 Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. Journal of National Cancer Institute 97 1124-1132. (doi:10.1093/jnci/dji204)
10. DeLong ER, DeLong DM & Clarke-Pearson DL 1988 Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44 837-845. (doi:10.2307/2531595)
11. Dong W, Tu S, Xie J, Sun P, Wu Y & Wang L 2009 Frequent promoter hypermethylation and transcriptional downregulation of BTG4 gene in gastric cancer. Biochemical and Biophysical Research Communications 387 132-138. (doi:10.1016/j.bbrc.2009.06.140)
12. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV & Laird PW 2000 MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Research 28 E32. (doi:10.1093/nar/28.8.e32)
13. Ebert MP, Model F, Mooney S, Hale K, Lograsso J, Tonnes-Priddy L, Hoffmann J, Csepregi A, Rocken C, Molnar B et al. 2006 Aristaless-like homeobox-4 gene methylation is a potential marker for colorectal adenocarcinomas. Gastroenterology 131 1418-1430. (doi:10.1053/j.gastro.2006.08. 034)
14. Estecio MR, Yan PS, Ibrahim AE, Tellez CS, Shen L, Huang TH & Issa JP 2007 High-throughput methylation profiling by MCA coupled to CpG island microarray. Genome Research 17 1529-1536. (doi:10.1101/gr.6417007)
15. Fraga MF & Esteller M 2007 Epigenetics and aging: the targets and the marks. Trends in Genetics 23 413-418. (doi:10.1016/j.tig.2007.05.008)
16. Gomes GR, Yasuhara F, Siu ER, Fernandes SA, Avellar MC, Lazari MF & Porto CS 2011 In vivo treatments with fulvestrant and anastrozole differentially affect gene expression in the rat efferent ductules. Biology of Reproduction 84 52-61. (doi:10.1095/biolreprod.110.085340)
17. Hadjiyanni I, Siminovitch KA, Danska JS & Drucker DJ 2010 Glucagon-like peptide-1 receptor signalling selectively regulates murine lymphocyte proliferation and maintenance of peripheral regulatory T cells. Diabetologia 53 730-740. (doi:10.1007/s00125-009-1643-x)
18. Hagihara A, Miyamoto K, Furuta J, Hiraoka N, Wakazono K, Seki S, Fukushima S, Tsao MS, Sugimura T & Ushijima T 2004 Identification of 27 50 CpG islands aberrantly methylated and 13 genes silenced in human pancreatic cancers. Oncogene 23 8705-8710. (doi:10.1038/sj.onc.1207783)
19. Hiyama K, Tanimoto K, Nishimura Y, Tsugane M, Fukuba I, Sotomaru Y, Hiyama E & Nishiyama M 2008 Exploration of the genes responsible for unlimited proliferation of immortalized lung fibroblasts. Experimental Lung Research 34 373-390. (doi:10.1080/01902140802221912)
20. Hogan AM, Collins D, Baird AW & Winter DC 2009 Estrogen and gastrointestinal malignancy. Molecular and Cellular Endocrinology 307 19-24. (doi:10.1016/j.mce.2009.03.016)
21. Huang Z, Li L & Wang J 2007 Hypermethylation of SFRP2 as a potential marker for stool-based detection of colorectal cancer and precancerous lesions. Digestive Diseases and Sciences 52 2287-2291. (doi:10.1007/s10620-007-9755-y)
22. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE & Baylin SB 1994 Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nature Genetics 7 536-540. (doi:10.1038/ng0894-536)
23. Itzkowitz SH & Yio X 2004 Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. American Journal of Physiology. Gastrointestinal and Liver Physiology 287 G7-17. (doi:10.1152/ajpgi.00079.2004)
24. Itzkowitz SH, Present DH & Colitis Foundation of America Colon Cancer in IBDSG 2005 Consensus conference: colorectal cancer screening and surveillance in inflammatory bowel disease. Inflammatory Bowel Diseases 11 314-321. (doi:10.1097/01.MIB.0000160811.76729.d5)
25. Itzkowitz SH, Jandorf L, Brand R, Rabeneck L, Schroy PC III, Sontag S, Johnson D, Skoletsky J, Durkee K, Markowitz S et al. 2007 Improved fecal DNA test for colorectal cancer screening. Clinical Gastroenterology and Hepatology 5 111-117. (doi:10.1016/j.cgh.2006.10.006)
26. Jemal A, Siegel R, Hao Y, Murray T & Thun MJ 2008 Cancer statistics 2008. CA: A Cancer Journal for Clinicians 58 71-96. (doi:10.3322/CA.2007.0010)
27. Kahi CJ, Rex DK & Imperiale TF 2008 Screening, surveillance, and primary prevention for colorectal cancer: a review of the recent literature. Gastroenterology 135 380-399. (doi:10.1053/j.gastro.2008.06.026)
28. Kim YH, Petko Z, Dzieciatkowski S, Lin L, Ghiassi M, Stain S, Chapman WC, Washington MK, Willis J, Markowitz SD et al. 2006 CpG island methylation of genes accumulates during the adenoma progression step of the multistep pathogenesis of colorectal cancer. Genes, Chromosomes & Cancer 45 781-789. (doi:10.1002/gcc.20341)
29. Kozaki K, Imoto I, Mogi S, Omura K & Inazawa J 2008 Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Research 68 2094-2105. (doi:10.1158/0008-5472.CAN-07-5194)
30. Larsson SC, Orsini N & Wolk A 2005 Diabetes mellitus and risk of colorectal cancer: a meta-analysis. Journal of National Cancer Institute 97 1679-1687. (doi:10.1093/jnci/dji375)
31. Li M, Chen WD, Papadopoulos N, Goodman SN, Bjerregaard NC, Laurberg S, Levin B, Juhl H, Arber N, Moinova H et al. 2009 Sensitive digital quantification of DNA methylation in clinical samples. Nature Biotechnology 27 858-863. (doi:10.1038/nbt.1559)
32. Lin KJ, Cheung WY, Lai JY & Giovannucci EL 2011 The effect of estrogen versus combined estrogen-progestogen therapy on the risk of colorectal cancer. International Journal of Cancer [in press]. (doi:10.1002/ijc.26026)
33. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ et al. 2008 A microRNA DNA methylation signature for human cancer metastasis. PNAS 105 13556-13561. (doi:10.1073/pnas.0803055105)
34. Maher SG, Gillham CM, Duggan SP, Smyth PC, Miller N, Muldoon C, O'Byrne KJ, Sheils OM, Hollywood D &Reynolds JV 2009 Gene expression analysis of diagnostic biopsies predicts pathological response to neoadjuvant chemoradiotherapy of esophageal cancer. Annals of Surgery 250 729-737. (doi:10.1097/SLA.0b013e3181bce7e1)
35. Menigatti M, Pedroni M, Verrone AM, Borghi F, Scarselli A, Benatti P, Losi L, Di Gregorio C, Schar P, Marra G et al. 2007 O6-methylguanine-DNA methyltransferase promoter hypermethylation in colorectal carcinogenesis. Oncology Reports 17 1421-1427.
36. Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, Jin Z, Sato F, Berki AT, Kan T et al. 2006 Agenome-wide search identifies epigenetic silencing of somatostatin, tachykinin-1, and 5 other genes in colon cancer. Gastroenterology 131 797-808. (doi:10.1053/j.gastro.2006.06.006)
37. Muller HM, Oberwalder M, Fiegl H, Morandell M, Goebel G, Zitt M, Muhlthaler M, Ofner D, Margreiter R &Widschwendter M 2004 Methylation changes in faecal DNA: a marker for colorectal cancer screening? Lancet 363 1283-1285. (doi:10.1016/S0140-6736(04)16002-9)
38. Nagasaka T, Tanaka N, Cullings HM, Sun DS, Sasamoto H, Uchida T, Koi M, Nishida N, Naomoto Y, Boland CR et al. 2009 Analysis of fecal DNA methylation to detect gastrointestinal neoplasia. Journal of National Cancer Institute 101 1244-1258. (doi:10.1093/jnci/djp265)
39. Nosho K, Kure S, Irahara N, Shima K, Baba Y, Spiegelman D, Meyerhardt JA, Giovannucci EL, Fuchs CS & Ogino S 2009 A prospective cohort study shows unique epigenetic, genetic, and prognostic features of synchronous colorectal cancers. Gastroenterology 137 1609-1620. (doi:10.1053/j.gastro.2009.08.002)
40. Ogawa R, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Mori Y, Mori R, Tomoda K, Katada T, Harada K et al. 2008 Identification of candidate genes involved in the radiosensitivity of esophageal cancer cells by microarray analysis. Diseases of the Esophagus 21 288-297. (doi:10.1111/j.1442-2050.2007. 00759.x)
41. Ongenaert M, Wisman GB, Volders HH, Koning AJ, Zee AG, van Criekinge W & Schuuring E 2008 Discovery of DNA methylation markers in cervical cancer using relaxation ranking. BMC Medical Genomics 1 57. (doi:10.1186/1755-8794-1- 57)
42. Shen L, Kondo Y, Rosner GL, Xiao L, Hernandez NS, Vilaythong J, Houlihan PS, Krouse RS, Prasad AR, Einspahr JG et al. 2005 MGMT promoter methylation and field defect in sporadic colorectal cancer. Journal of National Cancer Institute 97 1330-1338. (doi:10.1093/jnci/dji275)
43. Svrcek M, Buhard O, Colas C, Coulet F, Dumont S, Massaoudi I, Lamri A, Hamelin R, Cosnes J, Oliveira C et al. 2010 Methylation tolerance due to an O6-methylguanine DNA methyltransferase (MGMT) field defect in the colonic mucosa: an initiating step in the development of mismatch repair-deficient colorectal cancers. Gut 59 1516-1526. (doi:10.1136/gut.2009.194787)
44. Takahashi K, Kohno T, Ajima R, Sasaki H, Minna JD, Fujiwara T, Tanaka N & Yokota J 2006 Homozygous deletion and reduced expression of the DOCK8 gene in human lung cancer. International Journal of Oncology 28 321-328.
45. Tanzer M, Balluff B, Distler J, Hale K, Leodolter A, Rocken C, Molnar B, Schmid R, Lofton-Day C, Schuster T et al. 2010 Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS ONE 5 e9061. (doi:10.1371/journal.pone.0009061)
46. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y & Tokino T 2008 Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Research 68 4123-4132. (doi:10.1158/0008-5472.CAN-08-0325)
47. Uhlmann K, Brinckmann A, Toliat MR, Ritter H & Nurnberg P 2002 Evaluation of a potential epigenetic biomarker by quantitative methyl-single nucleotide polymorphism analysis. Electrophoresis 23 4072-4079. (doi:10.1002/elps.200290023)
48. Wang DR & Tang D 2008 Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World Journal of Gastroenterology 14 524-531. (doi:10.3748/wjg.14.524)
49. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D et al. 2006 CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nature Genetics 38 787-793. (doi:10.1038/ng1834)
50. Wimmer K, Zhu Xx XX, Rouillard JM, Ambros PF, Lamb BJ, Kuick R, Eckart M, Weinhausl A, Fonatsch C & Hanash SM 2002 Combined restriction landmark genomic scanning and virtual genome scans identify a novel human homeobox gene, ALX3, that is hypermethylated in neuroblastoma. Genes, Chromosomes & Cancer 33 285-294. (doi:10.1002/gcc.10030)
51. Worthley DL, Whitehall VL, Buttenshaw RL, Irahara N, Greco SA, Ramsnes I, Mallitt KA, Le Leu RK, Winter J, Hu Y et al. 2010 DNA methylation within the normal colorectal mucosa is associated with pathway-specific predisposition to cancer. Oncogene 29 1653-1662. (doi:10.1038/onc.2009.449)
52. Xu G, Kaneto H, Laybutt DR, Duvivier-Kali VF, Trivedi N, Suzuma K, King GL, Weir GC & Bonner-Weir S 2007 Downregulation of GLP-1 and GIP receptor expression by hyperglycemia: possible contribution to impaired incretin effects in diabetes. Diabetes 56 1551-1558. (doi:10.2337/db06-1033)
53. Yang N, Eijsink JJ, Lendvai A, Volders HH, Klip H, Buikema HJ, van Hemel BM, Schuuring E, van der Zee AG & Wisman GB 2009 Methylation markers for CCNA1 and C13ORF18 are strongly associated with high-grade cervical intraepithelial neoplasia and cervical cancer in cervical scrapings. Cancer Epidemiology, Biomarkers & Prevention 18 3000-3007. (doi:10.1158/1055-9965. EPI-09-0405)
54. Yasuhara F, Gomes GR, Siu ER, Suenaga CI, Marostica E, Porto CS & Lazari MF 2008 Effects of the antiestrogen fulvestrant (ICI 182 780) on gene expression of the rat efferent ductules. Biology of Reproduction 79 432-441. (doi:10.1095/biolreprod.107.067413)