Cancer-Predicting Gene Expression Changes in Colonic Mucosa of Western Diet Fed Mlh1+/- Mice

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Pussila, Marjaana ^a   Sarantaus, Laura ^a   Dermadi Bebek, Denis ^a   Valo, Satu ^a   Reyhani, Nima ^b   Ollila, Saara ^a,c   Päivärinta, Essi ^a   Peltomäki, Päivi ^a   Mutanen, Marja ^a   Nyström, Minna ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b AALTO UNIVERSITY   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

DICKKOPF 1 PROTEIN; GENOMIC DNA; MESSENGER RNA; PROTEIN MLH1; SUPPRESSOR OF CYTOKINE SIGNALING 1; TUMOR MARKER; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER SUSCEPTIBILITY; COLON CARCINOGENESIS; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; DIETARY INTAKE; DKK1 GENE; DNA METHYLATION; FEEDING; GENE EXPRESSION; GENE INACTIVATION; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HETEROZYGOTE; HOXD1 GENE; MLH1 GENE; MOUSE; NONHUMAN; PROMOTER REGION; REGULATOR GENE; SIGNAL TRANSDUCTION; SLC5A8 GENE; SOCS1 GENE; TUMOR SUPPRESSOR GENE; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CATION TRANSPORT PROTEINS; COLON; COLONIC NEOPLASMS; COLORECTAL NEOPLASMS, HEREDITARY NONPOLYPOSIS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MUCOUS MEMBRANE; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TIME FACTORS;

EID: 84885127948     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076865     Document Type: Article

References (49)

1. Bingham S, Riboli E, (2004) Diet and cancer--the European Prospective Investigation into Cancer and Nutrition. Nat Rev Cancer 4: 206-215. doi:10.1038/nrc1298. PubMed: 14993902.
2. Fearon ER, (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6: 479-507. doi:10.1146/annurev-pathol-011110-130235. PubMed: 21090969.
3. Feinberg AP, Ohlsson R, Henikoff S, (2006) The epigenetic progenitor origin of human cancer. Nat Rev Genet 7: 21-33. doi:10.1038/nrg1748. PubMed: 16369569.
4. Lao VV, Grady WM, (2011) Epigenetics and colorectal cancer. Nat. Rev Gastroenterol Hepatol 8: 686-700. doi:10.1038/nrgastro.2011.173.
5. Ahuja N, Issa JP, (2000) Aging, methylation and cancer. Histol Histopathol 15: 835-842. PubMed: 10963127.
6. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, et al. (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7: 536-540. doi:10.1038/ng0894-536. PubMed: 7951326.
7. Toyota M, Issa JP, (1999) CpG island methylator phenotypes in aging and cancer. Semin Cancer Biol 9: 349-357. doi:10.1006/scbi.1999.0135. PubMed: 10547343.
8. Arasaradnam RP, Commane DM, Bradburn D, Mathers JC, (2008) A review of dietary factors and its influence on DNA methylation in colorectal carcinogenesis. Epigenetics 3: 193-198. doi:10.4161/epi.3.4.6508. PubMed: 18682688.
9. Verma M, (2012) Cancer control and prevention by nutrition and epigenetic approaches. Antioxid Redox Signal 17: 355-364. doi:10.1089/ars.2011.4388. PubMed: 22047027.
10. Tammariello AE, Milner JA, (2010) Mouse models for unraveling the importance of diet in colon cancer prevention. J Nutr Biochem 21: 77-88. doi:10.1016/j.jnutbio.2009.09.014. PubMed: 20122631.
11. Newmark HL, Yang K, Kurihara N, Fan K, Augenlicht LH, et al. (2009) Western-style diet-induced colonic tumors and their modulation by calcium and vitamin D in C57Bl/6 mice: a preclinical model for human sporadic colon cancer. Carcinogenesis 30: 88-92. PubMed: 19017685.
12. Newmark HL, Yang K, Lipkin M, Kopelovich L, Liu Y, et al. (2001) A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice. Carcinogenesis 22: 1871-1875. doi:10.1093/carcin/22.11.1871. PubMed: 11698351.
13. Yang K, Kurihara N, Fan K, Newmark H, Rigas B, et al. (2008) Dietary induction of colonic tumors in a mouse model of sporadic colon cancer. Cancer Res 68: 7803-7810. doi:10.1158/0008-5472.CAN-08-1209. PubMed: 18829535.
14. Yang K, Yang W, Mariadason J, Velcich A, Lipkin M, et al. (2005) Dietary components modify gene expression: implications for carcinogenesis. J Nutr 135: 2710-2714. PubMed: 16251635.
15. Lynch HT, Lynch PM, Lanspa SJ, Snyder CL, Lynch JF, et al. (2009) Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications. Clin Genet 76: 1-18. doi:10.1111/j.1399-0004.2009.01230.x. PubMed: 19659756.
16. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, et al. (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134. doi:10.1016/S0092-8674(00)81312-4. PubMed: 8674118.
17. Edelmann W, Yang K, Kuraguchi M, Heyer J, Lia M, et al. (1999) Tumorigenesis in Mlh1 and Mlh1/Apc1638N mutant mice. Cancer Res 59: 1301-1307. PubMed: 10096563.
18. Reeves PG, Nielsen FH, Fahey GC Jr., (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951. PubMed: 8229312.
19. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034. PubMed: 12184808.
20. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, et al. (2005) Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci U S A 102: 15785-15790. doi:10.1073/pnas.0507816102. PubMed: 16243968.
21. Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ, (2007) Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res 35: e119. doi:10.1093/nar/gkm662. PubMed: 17855397.
22. Akilesh S, Shaffer DJ, Roopenian D, (2003) Customized molecular phenotyping by quantitative gene expression and pattern recognition analysis. Genome Res 13: 1719-1727. doi:10.1101/gr.533003. PubMed: 12840047.
23. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
24. Efron B, Tibshirani R, Storey JD, Tusher V, (2001) Empirical Bayes analysis of a microarray experiment. J Am Stat Assoc 96: 1151-1160. doi:10.1198/016214501753382129.
25. Kallio MA, Tuimala JT, Hupponen T, Klemelä P, Gentile M, et al. (2011) Chipster: user-friendly analysis software for microarray and other high-throughput data. BMC Genomics 12: 507. doi:10.1186/1471-2164-12-507. PubMed: 21999641.
26. Oyama T, Yamada Y, Hata K, Tomita H, Hirata A, et al. (2008) Further upregulation of beta-catenin/Tcf transcription is involved in the development of macroscopic tumors in the colon of ApcMin/+ mice. Carcinogenesis 29: 666-672. PubMed: 18204079.
27. Gregorieff A, Clevers H, (2005) Wnt signaling in the intestinal epithelium: from endoderm to cancer. Genes Dev 19: 877-890. doi:10.1101/gad.1295405. PubMed: 15833914.
28. Pendás-Franco N, Aguilera O, Pereira F, González-Sancho JM, Muñoz A, (2008) Vitamin D and Wnt/beta-catenin pathway in colon cancer: role and regulation of DICKKOPF genes. Anticancer Res 28: 2613-2623. PubMed: 19035286.
29. Koch S, Nava P, Addis C, Kim W, Denning TL, et al. (2011) The Wnt antagonist Dkk1 regulates intestinal epithelial homeostasis and wound repair. Gastroenterology 141: 259-268, e251-258 doi:10.1053/j.gastro.2011.03.043. PubMed: 21440550.
30. Burgess AW, Faux MC, Layton MJ, Ramsay RG, (2011) Wnt signaling and colon tumorigenesis--a view from the periphery. Exp Cell Res 317: 2748-2758. doi:10.1016/j.yexcr.2011.08.010. PubMed: 21884696.
31. Schneider MR, Dahlhoff M, Horst D, Hirschi B, Trülzsch K, et al. (2010) A key role for E-cadherin in intestinal homeostasis and Paneth cell maturation. PLOS ONE 5: e14325. doi:10.1371/journal.pone.0014325. PubMed: 21179475.
32. Baylin SB, Ohm JE, (2006) Epigenetic gene silencing in cancer- a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6: 107-116. doi:10.1038/nrc1799. PubMed: 16491070.
33. González-Sancho JM, Aguilera O, García JM, Pendás-Franco N, Peña C, et al. (2005) The Wnt antagonist DICKKOPF-1 gene is a downstream target of beta-catenin/TCF and is downregulated in human colon cancer. Oncogene 24: 1098-1103. doi:10.1038/sj.onc.1208303. PubMed: 15592505.
34. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, et al. (2004) Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36: 417-422. doi:10.1038/ng1330. PubMed: 15034581.
35. Ahuja N, Li Q, Mohan AL, Baylin SB, Issa JP, (1998) Aging and DNA methylation in colorectal mucosa and cancer. Cancer Res 58: 5489-5494. PubMed: 9850084.
36. Kawakami K, Ruszkiewicz A, Bennett G, Moore J, Grieu F, et al. (2006) DNA hypermethylation in the normal colonic mucosa of patients with colorectal cancer. Br J Cancer 94: 593-598. doi:10.1038/sj.bjc.6602940. PubMed: 16421593.
37. Worthley DL, Whitehall VL, Buttenshaw RL, Irahara N, Greco SA, 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. PubMed: 19966864.
38. Issa JP, Ahuja N, Toyota M, Bronner MP, Brentnall TA, (2001) Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res 61: 3573-3577. PubMed: 11325821.
39. Aguilera O, Fraga MF, Ballestar E, Paz MF, Herranz M, et al. (2006) Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 25: 4116-4121. doi:10.1038/sj.onc.1209439. PubMed: 16491118.
40. Maehata T, Taniguchi H, Yamamoto H, Nosho K, Adachi Y, et al. (2008) Transcriptional silencing of Dickkopf gene family by CpG island hypermethylation in human gastrointestinal cancer. World J Gastroenterol 14: 2702-2714. doi:10.3748/wjg.14.2702. PubMed: 18461655.
41. Rawson JB, Sun Z, Dicks E, Daftary D, Parfrey PS, et al. (2012) Vitamin D Intake Is Negatively Associated with Promoter Methylation of the Wnt Antagonist Gene DKK1 in a Large Group of Colorectal Cancer Patients. Nutr Cancer 64: 919-928. doi:10.1080/01635581.2012.711418. PubMed: 22966878.
42. Aguilera O, Peña C, García JM, Larriba MJ, Ordóñez-Morán P, et al. (2007) The Wnt antagonist DICKKOPF-1 gene is induced by 1alpha,25-dihydroxyvitamin D3 associated to the differentiation of human colon cancer cells. Carcinogenesis 28: 1877-1884. doi:10.1093/carcin/bgm094. PubMed: 17449905.
43. Janssens S, Denayer T, Deroo T, Van Roy F, Vleminckx K, (2010) Direct control of Hoxd1 and Irx3 expression by Wnt/beta-catenin signaling during anteroposterior patterning of the neural axis in Xenopus. Int J Dev Biol 54: 1435-1442. doi:10.1387/ijdb.092985sj. PubMed: 20979027.
44. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353. doi:10.1038/nature04733. PubMed: 16625203.
45. Jacinto FV, Ballestar E, Ropero S, Esteller M, (2007) Discovery of epigenetically silenced genes by methylated DNA immunoprecipitation in colon cancer cells. Cancer Res 67: 11481-11486. doi:10.1158/0008-5472.CAN-07-2687. PubMed: 18089774.
46. Shiraishi M, Sekiguchi A, Oates AJ, Terry MJ, Miyamoto Y, (2002) HOX gene clusters are hotspots of de novo methylation in CpG islands of human lung adenocarcinomas. Oncogene 21: 3659-3662. doi:10.1038/sj.onc.1205453. PubMed: 12032868.
47. Erdelyi I, Levenkova N, Lin EY, Pinto JT, Lipkin M, et al. (2009) Western-style diets induce oxidative stress and dysregulate immune responses in the colon in a mouse model of sporadic colon cancer. J Nutr 139: 2072-2078. doi:10.3945/jn.108.104125. PubMed: 19759248.
48. Hitchler MJ, Domann FE, (2009) Metabolic defects provide a spark for the epigenetic switch in cancer. Free Radic Biol Med 47: 115-127. doi:10.1016/j.freeradbiomed.2009.04.010. PubMed: 19362589.
49. Taniguchi K, Kakinuma S, Tokairin Y, Arai M, Kohno H, et al. (2006) Mild inflammation accelerates colon carcinogenesis in Mlh1-deficient mice. Oncology 71: 124-130. doi:10.1159/000100522. PubMed: 17347588.