Aberrant methylation of NPY, PENK, and WIF1 as a promising marker for blood-based diagnosis of colorectal cancer

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Roperch, Jean Pierre ^a   Incitti, Roberto ^b   Forbin, Solène ^c   Bard, Floriane ^c   Mansour, Hicham ^b,c   Mesli, Farida ^d   Baumgaertner, Isabelle ^d   Brunetti, Francesco ^d   Sobhani, Iradj ^c,d  

^a Paris Biotech   (France)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d HENRI MONDOR HOSPITAL   (France)

Author keywords

Circulating DNA methylation; Colorectal cancer; Epigenetic markers; QM MSP

Indexed keywords

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; COLONOSCOPY; COLORECTAL CANCER; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MIDDLE AGED; NPY GENE; PATHOLOGY; PENK GENE; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; VERY ELDERLY; WIF1 GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; COLORECTAL NEOPLASMS; DNA; DNA METHYLATION; ENKEPHALINS; FEMALE; HUMANS; MALE; MIDDLE AGED; MOLECULAR DIAGNOSTIC TECHNIQUES; MULTIPLEX POLYMERASE CHAIN REACTION; NEOPLASM STAGING; NEUROPEPTIDE Y; PROMOTER REGIONS, GENETIC; PROTEIN PRECURSORS; REPRESSOR PROTEINS; ROC CURVE; SEQUENCE ANALYSIS, DNA; TUMOR MARKERS, BIOLOGICAL;

EID: 84888356699     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-566     Document Type: Article

References (57)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden:Globocan 2000. Int J Cancer 2001, 94(2):153-156. 10.1002/ijc.1440, 11668491.
2. Boyle P, Leon ME. Epidemiology of colorectal cancer. Br Med Bull 2002, 64:1-25. 10.1093/bmb/64.1.1, 12421722.
3. Jemal A, Siegel R, Xu J, Ward E. Cancer Statistics, 2010. Cancer J Clin 2010, 60(5):277-300.
4. Winawer S, Fletcher R, Rex D, Bond J, Burt R, Ferrucci J, et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale-update based on new evidence. Gastroenterology 2003, 124(2):544-560. 10.1053/gast.2003.50044, 12557158.
5. Osborn NK, Ahlquist DA. Stool screening for colorectal cancer: molecular approaches. Gastroenterology 2005, 128(1):192-206. 10.1053/j.gastro.2004.10.041, 15633136.
6. Sobhani I, Alzahouri K, Ghout I, Charles DJ, Durand-Zaleski I. Cost-effectiveness of mass screening for colorectal cancer: choice of fecal occult blood test and screening strategy. Dis Colon Rectum 2011, 54(7):876-886. 10.1007/DCR.0b013e31820fd2bc, 21654256.
7. Faivre J, Dancourt V, Lejeune C, Tazi MA, Lamour J, Gerard D, et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study. Gastroenterology 2004, 126(6):1674-1680.
8. Frazier AL, Colditz GA, Fuchs CS, Kuntz KM. Cost-effectiveness of screening for colorectal cancer in the general population. JAMA 2000, 284(15):1954-1961. 10.1001/jama.284.15.1954, 11035892.
9. Desch CE, Benson AB, Somerfield MR, Flynn PJ, Krause C, Loprinzi CL, et al. Colorectal cancer surveillance: 2005 update of an American society of clinical oncology practice guideline. J Clin Oncol 2005, 23(33):8512-8519. 10.1200/JCO.2005.04.0063, 16260687.
10. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood: Minnesota colon cancer control study. N Engl J Med 2005, 328(19):1365-1371.
11. Clerc L, Jooste V, Lejeune C, Schmitt B, Arveux P, Quantin C, et al. Cost of care of colorectal cancers according to health care patterns and stage at diagnosis in France. Eur J Health Econ 2008, 9(4):361-367. 10.1007/s10198-007-0083-0, 18030510.
12. Hardcastle JD, Thomas WM, Chamberlain J, Pye G, Sheffield J, James PD, et al. Ramdomised, controlled trial of faecal occult blood screening for colorectal cancer: results for first 107,349 subjects. Lancet 1989, 1(8648):1160-1164.
13. Esteller M. DNA methylation and cancer therapy: new developments and expectations. Curr Opin Oncol 2005, 17(1):55-60. 10.1097/01.cco.0000147383.04709.10, 15608514.
14. Baylin SB, Esteller M, Rountree MR, Bachman KE, Schuebel K, Herman JG. Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet 2001, 10(7):687-692. 10.1093/hmg/10.7.687, 11257100.
15. Wong JJ, Hawkins NJ, Ward RL. Colorectal cancer: a model for epigenetic tumorigenesis. Gut 2007, 56(1):140-148. 10.1136/gut.2005.088799, 1856668, 16840508.
16. Muller HM, Widschwendter M. Methylated DNA as a possible screening marker for neoplastic disease in several body fluids. Expert Rev Mol Diagn 2003, 3(4):443-458. 10.1586/14737159.3.4.443, 12877384.
17. Fackler MJ, Malone K, Zhang Z, Schilling E, Garrett-Mayer E, Swift-Scanlan T, et al. Quantitative multiplex methylation-specific PCR analysis doubles detection of tumor cells in breast ductal fluid. Clin Cancer Res 2006, 12(11 Pt 1):3306-3310.
18. Hoque MO, Begum S, Topaloglu O, Chatterjee A, Rosenbaum E, Van CW, et al. Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J Natl Cancer Inst 2006, 98(14):996-1004. 10.1093/jnci/djj265, 16849682.
19. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, et al. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 1999, 398(6726):431-436. 10.1038/18899, 10201374.
20. He B, Reguart N, You L, Mazieres J, Xu Z, Lee AY, et al. Blockade of Wnt-1 signaling induces apoptosis in human colorectal cancer cells containing downstream mutations. Oncogene 2005, 24(18):3054-3058. 10.1038/sj.onc.1208511, 15735684.
21. Taniguchi H, Yamamoto H, Hirata T, Miyamoto N, Oki M, Nosho K, et al. Frequent epigenetic inactivation of Wnt inhibitory factor-1 in human gastrointestinal cancers. Oncogene 2005, 24(53):7946-7952. 10.1038/sj.onc.1208910, 16007117.
22. Cebrat M, Strzadala L, Kisielow P. Wnt inhibitory factor-1: a candidate for a new player in tumorigenesis of intestinal epithelial cells. Cancer Lett 2004, 206(1):107-113. 10.1016/j.canlet.2003.10.024, 15019166.
23. Ding Z, Qian YB, Zhu LX, Xiong QR. Promoter methylation and mRNA expression of DKK-3 and WIF-1 in hepatocellular carcinoma. World J Gastroenterol 2009, 15(21):2595-2601. 10.3748/wjg.15.2595, 2691489, 19496188.
24. Kansara M, Tsang M, Kodjabachian L, Sims NA, Trivett MK, Ehrich M, et al. Wnt inhibitory factor 1 is epigenetically silenced in human osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice. Clin Invest 2009, 119:837-851.
25. Yang Z, Wang Y, Fang J, Chen F, Liu J, Wu J. Expression and aberrant promoter methylation of Wnt inhibitory factor-1 in human astrocytomas. J Exp Clin Cancer Res 2010, 29:26. 10.1186/1756-9966-29-26, 2851677, 20334650.
26. Delmas AL, Riggs BM, Pardo CE, Dyer LM, Darst RP, Izumchenko EG, et al. WIF1 is a frequent target for epigenetic silencing in squamous cell carcinoma of the cervix. Carcinogenesis 2011, 32(11):1625-1633. 10.1093/carcin/bgr193, 3204350, 21873353.
27. Wissmann C, Wild PJ, Kaiser S, Roepcke S, Stoehr R, Woenckhaus M, et al. WIF1, a component of the Wnt pathway, is down-regulated in prostate, breast, lung, and bladder cancer. J Pathol 2003, 201:204-212. 10.1002/path.1449, 14517837.
28. Mazieres J, He B, You L, Xu Z, Lee AY, Mikami I, et al. Wnt inhibitory factor-1 is silenced by promoter hypermethylation in human lung cancer. Cancer Res 2004, 64(14):4717-4720. 10.1158/0008-5472.CAN-04-1389, 15256437.
29. Veeck J, Wild PJ, Fuchs T, Schuffler PJ, Hartmann A, Knüchel R, Dahl E. Prognostic relevance of Wnt-inhibitory factor-1 (WIF1) and Dickkopf-3 (DKK3) promoter methylation in human breast cancer. BMC cancer 2009, 9:217. 10.1186/1471-2407-9-217, 2717119, 19570204.
30. Lambiv WL, Vassallo I, Delorenzi M, Shay T, Diserens AC, Misra A, et al. The Wnt inhibitory factor 1 (WIF1) is targeted in glioblastoma and has a tumor suppressing function potentially by induction of senescence. Neuro Oncol 2011, 13(7):736-747. 10.1093/neuonc/nor036, 3129269, 21642372.
31. Lee BB, Lee EJ, Jung EH, Chun HK, Chang DK, Song SY, et al. Aberrant methylation of APC, MGMT, RASSF2A, and Wif-1 genes in plasma as a biomarker for early detection of colorectal cancer. Clin Cancer Res 2009, 15(19):6185-6191. 10.1158/1078-0432.CCR-09-0111, 19773381.
32. Jones PA. DNA methylation and cancer. Oncogene 2002, 21(35):5358-5360. 10.1038/sj.onc.1205597, 12154398.
33. Byun T, Karimi M, Marsh JL, Milovanovic T, Lin F, Holcombe RF. Expression of secreted Wnt antagonists in gastrointestinal tissues: potential role in stem cell homeostasis. J Clin Pathol 2005, 58:515-519. 10.1136/jcp.2004.018598, 1770654, 15858124.
34. Powell SM, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992, 359:235-237. 10.1038/359235a0, 1528264.
35. Sansom OJ, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004, 18:1385-1390. 10.1101/gad.287404, 423189, 15198980.
36. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004, 20:781-810. 10.1146/annurev.cellbio.20.010403.113126, 15473860.
37. Segditsas S, Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006, 25(57):7531-7537. 10.1038/sj.onc.1210059, 17143297.
38. Gregorieff A, Pinto D, Begthel H, Destree O, Kielman M, Clevers H. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 2005, 129(2):626-638.
39. Chan AO, Rashid A. CpG island methylation in precursors of gastrointestinal malignancies. Curr Mol Med 2006, 6:401-408. 10.2174/156652406777435417, 16900663.
40. Kalra SP, Kalra PS. Neuropeptide Y: a physiological orexigen modulated by the feedback action of ghrelin and leptin. Endocrine 2003, 22(1):49-56. 10.1385/ENDO:22:1:49, 14610298.
41. Ukkola O, Ravussin E, Jacobson P, Perusse L, Rankinen T, Tschop M, et al. Role of ghrelin polymorphisms in obesity based on three different studies. Obes Res 2002, 10(8):782-791. 10.1038/oby.2002.106, 12181387.
42. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008, 371(9612):569-578. 10.1016/S0140-6736(08)60269-X, 18280327.
43. Hallden G, Hadi M, Hong HT, Aponte GW. Y receptor-mediated induction of CD63 transcripts, a tetraspanin determined to be necessary for differentiation of the intestinal epithelial cell line, hBRIE 380i cells. J Biol Chem 1999, 274:27914-27924. 10.1074/jbc.274.39.27914, 10488139.
44. Ogasawara M, Murata J, Ayukawa K, Saiki I. Differential effect of intestinal neuropeptides on invasion and migration of colon carcinoma cells in vitro. Cancer Lett 1997, 119:125-130. 10.1016/S0304-3835(97)81762-4, 18372531.
45. Liu AJ, Furusato B, Ravindranath L, Chen YM, Srikantan V, McLeod DG, Petrovics G, Srivastava S. Quantitative analysis of a panel of gene expression in prostate cancer with emphasis on NPY expression analysis. J Zhejiang Univ Sci B 2007, 8:853-859. 10.1631/jzus.2007.B0853, 2100155, 18257117.
46. Abe M, Watanabe N, McDonell N, Takato T, Ohira M, Nakagawara A, Ushijima T. Identification of genes targeted by CpG island methylator phenotype in neuroblastomas, and their possible integrative involvement in poor prognosis. Oncology 2008, 74:50-60. 10.1159/000139124, 18544995.
47. Shin SH, Kim BH, Jang JJ, Suh KS, Kang GH. Identification of novel methylation markers in hepatocellular carcinoma using a methylation array. J Korean Med Sci 2010, 25(8):1152-1159. 10.3346/jkms.2010.25.8.1152, 2908783, 20676325.
48. DeMorrow S, Onori P, Venter J, Invernizzi P, Frampton G, White M, Franchitto A, et al. Neuropeptide Y inhibits cholangiocarcinoma cell growth and invasion. Am J Physiol Cell Physiol 2011, 300(5):1078-1089.
49. Tegeder I, Geisslinger G. Opioids as modulators of cell death and survival-unraveling mechanisms and revealing new indications. Pharmacol Rev 2004, 56(3):351-369. 10.1124/pr.56.3.2, 15317908.
50. Bottger A, Spruce BA. Proenkephalin is a nuclear protein responsive to growth arrest and differentiation signals. J Cell Biol 1995, 130(6):1251-1262. 10.1083/jcb.130.6.1251, 2120573, 7559749.
51. Mc Tavish N, Copeland LA, Saville MK, Perkins ND, Spruce BA. Proenkephalin assists stress-activated apoptosis through transcriptional repression of NF-KappaB and p53-related genes targets. Cell Death Differ 2007, 14(9):1700-1710. 10.1038/sj.cdd.4402172, 2695322, 17599100.
52. Sonneberg JL, Rauscher FJ, Morgan JI, Curran T. Regulation of proenkephalin by fos and Jun. Science 1989, 246(4937):1622-1625. 10.1126/science.2512642, 2512642.
53. Goo YA, Goodlett DR, Pascal LE, et al. Stromal mesenchyme cell genes of the human prostate and bladder. BMC Urol 2005, 5:17. 10.1186/1471-2490-5-17, 1327674, 16343351.
54. Chung W, Bondaruk J, Jelinek J, Lotan Y, Liang S, Czerniak B, Issa JP. Detection of bladder cancer using novel DNA methylation biomarkers in urine sediments. Cancer Epidemiol Biomarkers 2011, 20(7):1483-1491.
55. Ueki T, Toyata M, Skinner H, et al. Identification and characterization of differentially methylated CpG islands in pancreatic carcinoma. Cancer Res 2001, 61(23):8540-8546.
56. Fukushima N, Sato N, Ueki T, et al. Aberrant methylation of preproenkephalin and p16 genes in pancreatic intraepithelial neoplasia and pancreatic ductal adenocarcinoma. Am J Pathol 2002, 160(5):1573-1581. 10.1016/S0002-9440(10)61104-2, 1850889, 12000709.
57. Tan AC, Jimeno A, Lin SH, Wheelhouse J, Chan F, Solomon A, et al. Characterizing DNA methylation patterns in pancreatic cancer genome. Mol Oncol 2009, 3(5-6):425-438.