Identification of an epigenetic biomarker panel with high sensitivity and specificity for colorectal cancer and adenomas

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Lind, Guro E ^a,b   Danielsen, Stine A ^a,b   Ahlquist, Terje ^a,b   Merok, Marianne A ^a,b,c   Andresen, Kim ^a,b   Skotheim, Rolf I ^a,b   Hektoen, Merete ^a,b   Rognum, Torleiv O ^b,d   Meling, Gunn I ^b,d,h   Hoff, Geir ^e,f   Bretthauer, Michael ^f,g   Thiis Evensen, Espen ^a   Nesbakken, Arild ^b,c   Lothe, Ragnhild A ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c AKER UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

^e TELEMARK HOSPITAL   (Norway)

^f CANCER REGISTRY OF NORWAY   (Norway)

^g OSLO UNIVERSITY HOSPITAL   (Norway)

^h AKERSHUS UNIVERSITY HOSPITAL   (Norway)

Author keywords

Biomarker; CNRIP1; Colorectal neoplasia; Early detection; FBN1; INA; MAL; Methylation; SNCA; SPG20

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; TRICHOSTATIN A; TUMOR MARKER;

ADENOMA; ADULT; AGED; ARTICLE; CANCER CELL; CANCER DIAGNOSIS; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENETIC MARKER; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; METHYLATION; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; CARCINOMA; CHEMISTRY; COLORECTAL TUMOR; EVALUATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; METABOLISM; MIDDLE AGED; PATHOLOGY; VALIDATION STUDY;

ADENOMA; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA; COLORECTAL NEOPLASMS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTESTINAL MUCOSA; MALE; MIDDLE AGED; SENSITIVITY AND SPECIFICITY; TUMOR MARKERS, BIOLOGICAL;

EID: 79960558168     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-85     Document Type: Article

References (55)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin 2008, 58:71-96. 10.3322/CA.2007.0010, 18287387.
2. Levin B, Lieberman DA, McFarland B, Andrews KS, Brooks D, Bond J, Dash C, Giardiello FM, Glick S, Johnson CD, Levin TR, Pickhardt PJ, Rex DK, Smith RA, Thorson A, Winawer SJ. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 2008, 134:1570-1595. 10.1053/j.gastro.2008.02.002, 18384785.
3. Bretthauer M. Evidence for colorectal cancer screening. Best Pract Res Clin Gastroenterol 2010, 24:417-425. 10.1016/j.bpg.2010.06.005, 20833346.
4. Atkin WS, Edwards R, Kralj-Hans I, Wooldrage K, Hart AR, Northover JM, Parkin DM, Wardle J, Duffy SW, Cuzick J. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 2010, 375:1624-1633. 10.1016/S0140-6736(10)60551-X, 20430429.
5. van DL, Kuipers EJ, van Leerdam ME. Performance improvements of stool-based screening tests. Best Pract Res Clin Gastroenterol 2010, 24:479-492. 10.1016/j.bpg.2010.03.009, 20833351.
6. Rashid A, Shen L, Morris JS, Issa JP, Hamilton SR. CpG island methylation in colorectal adenomas. Am J Pathol 2001, 159:1129-1135. 10.1016/S0002-9440(10)61789-0, 1850474, 11549606.
7. Chan AO, Broaddus RR, Houlihan PS, Issa JP, Hamilton SR, Rashid A. CpG island methylation in aberrant crypt foci of the colorectum. Am J Pathol 2002, 160:1823-1830. 10.1016/S0002-9440(10)61128-5, 1850869, 12000733.
8. Chang E, Park DI, Kim YJ, Kim BK, Park JH, Kim HJ, Cho YK, Sohn CI, Jeon WK, Kim BI, Kim HD, Kim DH, Kim YH. Detection of colorectal neoplasm using promoter methylation of ITGA4, SFRP2, and p16 in stool samples: a preliminary report in Korean patients. Hepatogastroenterology 2010, 57:720-727.
9. Lind GE, Raiborg C, Danielsen SA, Rognum TO, Thiis-Evensen E, Hoff G, Nesbakken A, Stenmark H, Lothe RA. SPG20, a novel biomarker in colorectal carcinogenesis, encodes a regulator of cytokinesis. Oncogene 2011, 1-12.
10. Øster B, Thorsen K, Lamy P, Wojdacz TK, Hansen LL, Birkenkamp-Demtrõder K, Sørensen KD, Laurberg S, Ørntoft TF, Andersen CL. Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas. Int J Cancer 2011, 10.
11. Müller HM, Oberwalder M, Fiegl H, Morandell M, Goebel G, Zitt M, Mühlthaler M, Öfner D, Margreiter R, Widschwendter M. Methylation changes in faecal DNA: a marker for colorectal cancer screening?. Lancet 2004, 363:1283-1285. 10.1016/S0140-6736(04)16002-9, 15094274.
12. Chen WD, Han ZJ, Skoletsky J, Olson J, Sah J, Myeroff L, Platzer P, Lu S, Dawson D, Willis J, Pretlow TP, Lutterbaugh J, Kasheri L, Willson JK, Rao JS, Shuber A, Markowitz SD. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J Natl Cancer Inst 2005, 97:1124-1132. 10.1093/jnci/dji204, 16077070.
13. Zhang W, Bauer M, Croner RS, Pelz JO, Lodygin D, Hermeking H, Sturzl M, Hohenberger W, Matzel KE. DNA Stool Test for Colorectal Cancer: Hypermethylation of the Secreted Frizzled-Related Protein-1 Gene. Dis Colon Rectum 2007, 50:1618-1626. 10.1007/s10350-007-0286-6, 17762966.
14. Kim MS, Louwagie J, Carvalho B, Terhaar Sive Droste JS, Park HL, Chae YK, Yamashita K, Liu J, Ostrow KL, Ling S, Guerrero-Preston R, Demokan S, Yalniz Z, Dalay N, Meijer GA, van Criekinge W, Sidransky D. Promoter DNA methylation of oncostatin m receptor-beta as a novel diagnostic and therapeutic marker in colon cancer. PLoS ONE 2009, 4:e6555. 10.1371/journal.pone.0006555, 2717211, 19662090.
15. Kim MS, Lee J, Sidransky D. DNA methylation markers in colorectal cancer. Cancer Metastasis Rev 2010, 29:181-206. 10.1007/s10555-010-9207-6, 20135198.
16. Tang D, Liu J, Wang DR, Yu HF, Li YK, Zhang JQ. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin Invest Med 2011, 34:E88-E95.
17. Herbst A, Rahmig K, Stieber P, Philipp A, Jung A, Ofner A, Crispin A, Neumann J, Lamerz R, Kolligs FT. Methylation of NEUROG1 in Serum Is a Sensitive Marker for the Detection of Early Colorectal Cancer. Am J Gastroenterol 2011, 106:1110-1118. 10.1038/ajg.2011.6, 21326223.
18. Tänzer M, Balluff B, Distler J, Hale K, Leodolter A, Rocken C, Molnar B, Schmid R, Lofton-Day C, Schuster T, Ebert MP. Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS ONE 2010, 5:e9061. 10.1371/journal.pone.0009061, 2816214, 20140221.
19. He Q, Chen HY, Bai EQ, Luo YX, Fu RJ, He YS, Jiang J, Wang HQ. Development of a multiplex MethyLight assay for the detection of multigene methylation in human colorectal cancer. Cancer Genet Cytogenet 2010, 202:1-10. 10.1016/j.cancergencyto.2010.05.018, 20804913.
20. Lind GE, Kleivi K, Meling GI, Teixeira MR, Thiis-Evensen E, Rognum TO, Lothe RA. ADAMTS1, CRABP1, and NR3C1 identified as epigenetically deregulated genes in colorectal tumorigenesis. Cell Oncol 2006, 28:259-272.
21. Lind GE, Ahlquist T, Lothe RA. DNA hypermethylation of MAL: a promising diagnostic biomarker for colorectal tumors. Gastroenterology 2007, 132:1631-1632. 10.1053/j.gastro.2007.03.003, 17408629.
22. Lind GE, Ahlquist T, Kolberg M, Berg M, Eknaes M, Alonso MA, Kallioniemi A, Meling GI, Skotheim RI, Rognum TO, Thiis-Evensen E, Lothe RA. Hypermethylated MAL gene - a silent marker of early colon tumorigenesis. J Transl Med 2008, 6(13):13. 2292685, 18346269.
23. Kleivi K, Teixeira MR, Eknaes M, Diep CB, Jakobsen KS, Hamelin R, Lothe RA. Genome signatures of colon carcinoma cell lines. Cancer Genet Cytogenet 2004, 155:119-131. 10.1016/j.cancergencyto.2004.03.014, 15571797.
24. Kunkel LM, Smith KD, Boyer SH, Borgaonkar DS, Wachtel SS, Miller OJ, Breg WR, Jones HW, Rary JM. Analysis of human Y-chromosome-specific reiterated DNA in chromosome variants. Proc Natl Acad Sci USA 1977, 74:1245-1249. 10.1073/pnas.74.3.1245, 430660, 265567.
25. Meling GI, Lothe RA, Børresen AL, Hauge S, Graue C, Clausen OP, Rognum TO. Genetic alterations within the retinoblastoma locus in colorectal carcinomas. Relation to DNA ploidy pattern studied by flow cytometric analysis. Br J Cancer 1991, 64:475-480. 10.1038/bjc.1991.334, 1977625, 1911187.
26. Lothe RA, Peltomäki P, Meling GI, Aaltonen LA, Nyström-Lahti M, Pylkkänen L, Heimdal K, Andersen TI, Møller P, Rognum TO, Fosså SD, Haldorsen T, Langmark F, Brøgger A, de la CHapelle A, Børresen AL. Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res 1993, 53:5849-5852.
27. Thorstensen L, Lind GE, Løvig T, Diep CB, Meling GI, Rognum TO, Lothe RA. Genetic and Epigenetic Changes of Components Affecting the WNT Pathway in Colorectal Carcinomas Stratified by Microsatellite Instability. Neoplasia 2005, 7:99-108. 10.1593/neo.04448, 1501125, 15802015.
28. Thiis-Evensen E, Hoff GS, Sauar J, Langmark F, Majak BM, Vatn MH. Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer. Telemark Polyp Study I. Scand J Gastroenterol 1999, 34:414-420. 10.1080/003655299750026443, 10365903.
29. Bretthauer M, Gondal G, Larsen K, Carlsen E, Eide TJ, Grotmol T, Skovlund E, Tveit KM, Vatn MH, Hoff G. Design, organization and management of a controlled population screening study for detection of colorectal neoplasia: attendance rates in the NORCCAP study (Norwegian Colorectal Cancer Prevention). Scand J Gastroenterol 2002, 37:568-573. 10.1080/00365520252903125, 12059059.
30. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. The human genome browser at UCSC. Genome Res 2002, 12:996-1006. 186604, 12045153.
31. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, Laird PW. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 2005, 33:6823-6836. 10.1093/nar/gki987, 1301596, 16326863.
32. Widschwendter M, Siegmund KD, Muller HM, Fiegl H, Marth C, Muller-Holzner E, Jones PA, Laird PW. Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res 2004, 64:3807-3813. 10.1158/0008-5472.CAN-03-3852, 15172987.
33. Melki JR, Vincent PC, Clark SJ. Concurrent DNA hypermethylation of multiple genes in acute myeloid leukemia. Cancer Res 1999, 59:3730-3740.
34. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999, 96:8681-8686. 10.1073/pnas.96.15.8681, 17576, 10411935.
35. Costello JF, Fruhwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomäki P, Lang JC, Schuller DE, Yu L, Bloomfield CD, Caligiuri MA, Yates A, Nishikawa R, Huang H, Petrelli NJ, Zhang X, O'Dorisio MS, Held WA, Cavenee WK, Plass C. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000, 24:132-138. 10.1038/72785, 10655057.
36. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, Herman JG, Baylin SB. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002, 31:141-149. 10.1038/ng892, 11992124.
37. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N, Jiang A, Perou CM, Kim YH, Pollack JR, Fong KM, Lam CL, Wong M, Shyr Y, Nanda R, Olopade OI, Gerald W, Euhus DM, Shay JW, Gazdar AF, Minna JD. A genome-wide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 2006, 3:e486. 10.1371/journal.pmed.0030486, 1716188, 17194187.
38. Lofton-Day C, Model F, Devos T, Tetzner R, Distler J, Schuster M, Song X, Lesche R, Liebenberg V, Ebert M, Molnar B, Grutzmann R, Pilarsky C, Sledziewski A. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin Chem 2008, 54:414-423. 10.1373/clinchem.2007.095992, 18089654.
39. Zou H, Harrington JJ, Shire AM, Rego RL, Wang L, Campbell ME, Oberg AL, Ahlquist DA. Highly methylated genes in colorectal neoplasia: implications for screening. Cancer Epidemiol Biomarkers Prev 2007, 16:2686-2696. 10.1158/1055-9965.EPI-07-0518, 18086775.
40. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, Barker M, Leggett B, Levine J, Kim M, French AJ, Thibodeau SN, Jass J, Haile R, Laird PW. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006, 38:787-793. 10.1038/ng1834, 16804544.
41. Chung W, Kwabi-Addo B, Ittmann M, Jelinek J, Shen L, Yu Y, Issa JP. Identification of novel tumor markers in prostate, colon and breast cancer by unbiased methylation profiling. PLoS ONE 2008, 3:e2079. 10.1371/journal.pone.0002079, 2323612, 18446232.
42. Ausch C, Kim YH, Tsuchiya KD, Dzieciatkowski S, Washington MK, Paraskeva C, Radich J, Grady WM. Comparative analysis of PCR-based biomarker assay methods for colorectal polyp detection from fecal DNA. Clin Chem 2009, 55:1559-1563. 10.1373/clinchem.2008.122937, 19541867.
43. Kim MS, Chang X, Nagpal JK, Yamashita K, Baek JH, Dasgupta S, Wu G, Osada M, Woo JH, Westra WH, Trink B, Ratovitski EA, Moon C, Sidransky D. The N-methyl-D-aspartate receptor type 2A is frequently methylated in human colorectal carcinoma and suppresses cell growth. Oncogene 2008, 27:2045-2054. 10.1038/sj.onc.1210842, 17922030.
44. Zitt M, Zitt M, Muller HM. DNA methylation in colorectal cancer--impact on screening and therapy monitoring modalities?. Dis Markers 2007, 23:51-71.
45. Huang Z, Li L, Wang J. Hypermethylation of SFRP2 as a potential marker for stool-based detection of colorectal cancer and precancerous lesions. Dig Dis Sci 2007, 52:2287-2291. 10.1007/s10620-007-9755-y, 17410438.
46. Oberwalder M, Zitt M, Wöntner C, Fiegl H, Goebel G, Zitt M, Köhle O, Mühlmann G, Öfner D, Margreiter R, Müller HM. SFRP2 methylation in fecal DNA-a marker for colorectal polyps. Int J Colorectal Dis 2007, 15-9.
47. Wang DR, Tang D. Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World J Gastroenterol 2008, 14:524-531. 10.3748/wjg.14.524, 2681142, 18203283.
48. Devos T, Tetzner R, Model F, Weiss G, Schuster M, Distler J, Steiger KV, Grutzmann R, Pilarsky C, Habermann JK, Fleshner PR, Oubre BM, Day R, Sledziewski AZ, Lofton-Day C. Circulating Methylated SEPT9 DNA in Plasma Is a Biomarker for Colorectal Cancer. Clin Chem 2009,
49. Lee B, Godfrey M, Vitale E, Hori H, Mattei MG, Sarfarazi M, Tsipouras P, Ramirez F, Hollister DW. Linkage of Marfan syndrome and a phenotypically related disorder to two different fibrillin genes. Nature 1991, 352:330-334. 10.1038/352330a0, 1852206.
50. Wang Y, Yu Q, Cho AH, Rondeau G, Welsh J, Adamson E, Mercola D, McClelland M. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 2005, 7:748-760. 10.1593/neo.05289, 1501885, 16207477.
51. Hellebrekers DM, Melotte V, Vire E, Langenkamp E, Molema G, Fuks F, Herman JG, van Criekinge W, Griffioen AW, van Engeland M. Identification of epigenetically silenced genes in tumor endothelial cells. Cancer Res 2007, 67:4138-4148. 10.1158/0008-5472.CAN-06-3032, 17483324.
52. Jowaed A, Schmitt I, Kaut O, Wullner U. Methylation regulates alpha-synuclein expression and is decreased in Parkinson's disease patients' brains. J Neurosci 2010, 30:6355-6359. 10.1523/JNEUROSCI.6119-09.2010, 20445061.
53. Yan PS, Venkataramu C, Ibrahim A, Liu JC, Shen RZ, Diaz NM, Centeno B, Weber F, Leu YW, Shapiro CL, Eng C, Yeatman TJ, Huang TH. Mapping geographic zones of cancer risk with epigenetic biomarkers in normal breast tissue. Clin Cancer Res 2006, 12:6626-6636. 10.1158/1078-0432.CCR-06-0467, 17121881.
54. Lind GE, Danielsen SA, Ahlquist T, Merok MA, Rognum TO, Meling GI, Bretthauer M, Thiis-Evensen E, Nesbakken A, Lothe RA. A novel epigenetic biomarker panel for early detection of colorectal cancer and adenomas. Ejc Supplements 2009, 7:145.
55. Kilpinen S, Autio R, Ojala K, Iljin K, Bucher E, Sara H, Pisto T, Saarela M, Skotheim TI, Bjorkman M, Mpindi JP, Haapa-Paananen S, Vainio P, Edgren H, Wolf M, Astola J, Nees M, Hautaniemi S, Kallioniemi O. Systematic bioinformatic analysis of expression levels of 17,330 human genes across 9,783 samples from 175 types of healthy and pathological tissues. Genome Biol 2008, 9:R139. 10.1186/gb-2008-9-9-r139, 2592717, 18803840.