Integrated microRNA and mRNA expression profiling in a rat colon carcinogenesis model: Effect of a chemo-protective diet

Physiological Genomics

Volumn 43, Issue 10, 2011, Pages 640-654

  Shah, Manasvi S ^a   Schwartz, Scott L ^a   Zhao, Chen ^a   Davidson, Laurie A ^a   Zhou, Beiyan ^b   Lupton, Joanne R ^a   Ivanov, Ivan ^a,b   Chapkin, Robert S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Epigenetics; Fish oil; N 3 polyunsaturated fatty acids; Pectin

Indexed keywords

AZOXYMETHANE; CARCINOGEN; CELLULOSE; CORN OIL; FISH OIL; MESSENGER RNA; MICRORNA; MICRORNA 21; MIR 203; MIR 26B; MIR 27B; MIR 93; PECTIN; PHOSPHODIESTERASE IV; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CHEMOPROPHYLAXIS; COLON CANCER; CONTROLLED STUDY; DIET THERAPY; FAT INTAKE; GENE EXPRESSION PROFILING; MALE; NONHUMAN; POLYSOME; PRIORITY JOURNAL; RAT; RNA SYNTHESIS;

ADENOCARCINOMA; ANIMALS; CHEMOPREVENTION; COLONIC NEOPLASMS; DIET; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; MALE; MICROARRAY ANALYSIS; MICRORNAS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SYSTEMS INTEGRATION;

RATTUS; ZEA MAYS;

EID: 79957645229     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00213.2010     Document Type: Article

References (88)

1. Ahnen DJ. Are animal models of colon cancer relevant to human disease. Dig Dis Sci 30: 103S-106S, 1985.
2. Anti M, Armelao F, Marra G, Percesepe A, Bartoli GM, Palozza P, Parrella P, Canetta C, Gentiloni N, De Vitis I, Gasbarrini G. Effects of different doses of fish oil on rectal cell proliferation in patients with sporadic colonic adenomas. Gastroenterology 107: 1709-1718, 1994.
3. Anti M, Marra G, Armelao F, Bartoli GM, Ficarelli R, Percesepe A, De Vitis I, Maria G, Sofo L, Rapaccini GL, Gentiloni N, Miggiano G. Effect of omega-3 fatty acids on rectal mucosal cell proliferation in subjects at risk for colon cancer. Gastroenterology 103: 883-891, 1992.
4. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H. MicroRNA-21 (miR-21) post-transcriptionally down-regulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136, 2008.
5. Aslam MI, Taylor K, Pringle JH, Jameson JS. MicroRNAs are novel biomarkers of colorectal cancer. Br J Surg 96: 702-710, 2009.
6. Barbato C, Arisi I, Frizzo ME, Brandi R, Da Sacco L, Masotti A. Computational challenges in miRNA target predictions: to be or not to be a true target? J Biomed Biotechnol 2009: 803069, 2009.
7. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaur-ralde E. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20: 1885-1898, 2006.
8. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjonneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 361: 1496-1501, 2003.
9. Bonauer A, Dimmeler S. The microRNA-17-92 cluster: still a miRacle? Cell Cycle 8: 3866-3873, 2009.
10. Chang NW, Huang PC. Effects of the ratio of polyunsaturated and monounsaturated fatty acid to saturated fatty acid on rat plasma and liver lipid concentrations. Lipids 33: 481-487, 1998.
11. Chang WC, Chapkin RS, Lupton JR. Predictive value of proliferation, differentiation and apoptosis as intermediate markers for colon tumori-genesis. Carcinogenesis 18: 721-730, 1997.
12. Chapkin RS, McMurray DN, Lupton JR. Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroenterol 23: 48-54, 2007.
13. Cloonan N, Brown MK, Steptoe AL, Wani S, Chan WL, Forrest AR, Kolle G, Gabrielli B, Grimmond SM. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 9: R127, 2008.
14. Crim KC, Sanders LM, Hong MY, Taddeo SS, Turner ND, Chapkin RS, Lupton JR. Upregulation of p21Waf1/Cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. Carcinogenesis 29: 1415-1420, 2008.
15. Davidson LA, Nguyen DV, Hokanson RM, Callaway ES, Isett RB, Turner ND, Dougherty ER, Wang N, Lupton JR, Carroll RJ, Chapkin RS. Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat. Cancer Res 64: 6797-6804, 2004.
16. Davidson LA, Wang N, Ivanov I, Goldsby J, Lupton JR, Chapkin RS. Identification of actively translated mRNA transcripts in a rat model of early-stage colon carcinogenesis. Cancer Prev Res (Phila Pa) 2: 984-994, 2009.
17. Davidson LA, Wang N, Shah MS, Lupton JR, Ivanov I, Chapkin RS. n-3 Polyunsaturated fatty acids modulate carcinogen-directed non-coding microRNA signatures in rat colon. Carcinogenesis 30: 2077-2084, 2009.
18. Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, Hamilton SR. Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn 12: 433-440, 2010.
19. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269, 2006.
20. Fontana L, Fiori ME, Albini S, Cifaldi L, Giovinazzi S, Forloni M, Boldrini R, Donfrancesco A, Federici V, Giacomini P, Peschle C, Fruci D. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 3: e2236, 2008.
21. Gaur A, Jewell DA, Liang Y, Ridzon D, Moore JH, Chen C, Ambros VR, Israel MA. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res 67: 2456-2468, 2007.
22. Gregorieff A, Clevers H. Wnt signaling in the intestinal epithelium: from endoderm to cancer. Genes Dev 19: 877-890, 2005.
23. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-D158, 2008.
24. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105, 2007.
25. Gunter MJ, Hayes RB, Chatterjee N, Yeager M, Welch R, Schoen RE, Yakochi L, Schatzkin A, Peters U. Insulin resistance-related genes and advanced left-sided colorectal adenoma. Cancer Epidemiol Biomarkers Prev 16: 703-708, 2007.
26. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840, 2010.
27. Hanlon K, Rudin CE, Harries LW. Investigating the targets of MIR-15a and MIR-16-1 in patients with chronic lymphocytic leukemia (CLL). PLoS One 4: e7169, 2009.
28. Huang JC, Morris QD, Frey BJ. Bayesian inference of MicroRNA targets from sequence and expression data. J Comput Biol 14: 550-563, 2007.
29. Joo M, Shahsafaei A, Odze RD. Paneth cell differentiation in colonic epithelial neoplasms: evidence for the role of the Apc/beta-catenin/Tcf pathway. Hum Pathol 40: 872-880, 2009.
30. Khokhlatchev A, Rabizadeh S, Xavier R, Nedwidek M, Chen T, Zhang XF, Seed B, Avruch J. Identification of a novel Ras-regulated proapoptotic pathway. Curr Biol 12: 253-265, 2002.
31. Kim S, Choi M, Cho KH. Identifying the target mRNAs of microRNAs in colorectal cancer. Comput Biol Chem 33: 94-99, 2009.
32. 2+ accumulation in colonocytes. Am J Physiol Gastrointest Liver Physiol 293: G935-G943, 2007.
33. Koon N, Schneider-Stock R, Sarlomo-Rikala M, Lasota J, Smolkin M, Petroni G, Zaika A, Boltze C, Meyer F, Andersson L, Knuutila S, Miettinen M, El-Rifai W. Molecular targets for tumour progression in gastrointestinal stromal tumours. Gut 53: 235-240, 2004.
34. Kort EJ, Farber L, Tretiakova M, Petillo D, Furge KA, Yang XJ, Cornelius A, Teh BT. The E2F3-Oncomir-1 axis is activated in Wilms' tumor. Cancer Res 68: 4034-4038, 2008.
35. Kren BT, Wong PY, Shiota A, Zhang X, Zeng Y, Steer CJ. Polysome trafficking of transcripts and microRNAs in regenerating liver after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 297: G1181-G1192, 2009.
36. Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, Jacob ST, Ghoshal K. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem 99: 671-678, 2006.
37. Lanza G, Ferracin M, Gafa R, Veronese A, Spizzo R, Pichiorri F, Liu CG, Calin GA, Croce CM, Negrini M. mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer. Mol Cancer 6: 54, 2007.
38. Latham P, Lund EK, Johnson IT. Dietary n-3 PUFA increases the apoptotic response to 1,2-dimethylhydrazine, reduces mitosis and suppresses the induction of carcinogenesis in the rat colon. Carcinogenesis 20: 645-650, 1999.
39. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20, 2005.
40. Lindow M, Jacobsen A, Nygaard S, Mang Y, Krogh A. Intragenomic matching reveals a huge potential for miRNA-mediated regulation in plants. PLoS Comput Biol 3: e238, 2007.
41. Maragkakis M, Reczko M, Simossis VA, Alexiou P, Papadopoulos GL, Dalamagas T, Giannopoulos G, Goumas G, Koukis E, Kourtis K, Vergoulis T, Koziris N, Sellis T, Tsanakas P, Hatzigeorgiou AG. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 37: W273-W276, 2009.
42. Maroney PA, Yu Y, Fisher J, Nilsen TW. Evidence that microRNAs are associated with translating messenger RNAs in human cells. Nat Struct Mol Biol 13: 1102-1107, 2006.
43. Mayr C, Bartel DP. Widespread shortening of 3=UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684, 2009.
44. Mendes ND, Freitas AT, Sagot MF. Current tools for the identification of miRNA genes and their targets. Nucleic Acids Res 37: 2419-2433, 2009.
45. Nakamoto M, Jin P, O'Donnell WT, Warren ST. Physiological identification of human transcripts translationally regulated by a specific microRNA. Hum Mol Genet 14: 3813-3821, 2005.
46. Narita M, Murata T, Shimizu K, Nakagawa T, Sugiyama T, Inui M, Hiramoto K, Tagawa T. A role for cyclic nucleotide phosphodiesterase 4 in regulation of the growth of human malignant melanoma cells. Oncol Rep 17: 1133-1139, 2007.
47. Navarro D, Agra N, Pestana A, Alonso J, Gonzalez-Sancho JM. The EWS/FLI1 oncogenic protein inhibits expression of the Wnt inhibitor DICKKOPF-1 gene and antagonizes beta-catenin/TCF-mediated transcription. Carcinogenesis 31: 394-401, 2010.
48. Nelson PT, Hatzigeorgiou AG, Mourelatos Z. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 10: 387-394, 2004.
49. Ng EK, Tsang WP, Ng SS, Jin HC, Yu J, Li JJ, Rocken C, Ebert MP, Kwok TT, Sung JJ. MicroRNA-143 targets DNA methyltransferases 3A in colorectal cancer. Br J Cancer 101: 699-706, 2009.
50. Nicolas FE, Pais H, Schwach F, Lindow M, Kauppinen S, Moulton V, Dalmay T. Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA 14: 2513-2520, 2008.
51. Nikiforova MN, Chiosea SI, Nikiforov YE. MicroRNA expression profiles in thyroid tumors. Endocr Pathol 20: 85-91, 2009.
52. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435: 839-843, 2005.
53. Olsen PH, Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216: 671-680, 1999.
54. Orom UA, Lund AH. Experimental identification of microRNA targets. Gene 451: 1-5, 2010.
55. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21: 533-542, 2006.
56. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309: 1573-1576, 2005.
57. Reddy BS. Chemoprevention of colon cancer by dietary fatty acids. Cancer Metastasis Rev 13: 285-302, 1994.
58. Reddy BS, Burill C, Rigotty J. Effect of diets high in omega-3 and omega-6 fatty acids on initiation and postinitiation stages of colon carci-nogenesis. Cancer Res 51: 487-491, 1991.
59. Ritchie W, Flamant S, Rasko JE. Predicting microRNA targets and functions: traps for the unwary. Nat Meth 6: 397-398, 2009.
60. Saunders LR, Sharma AD, Tawney J, Nakagawa M, Okita K, Ya-manaka S, Willenbring H, Verdin E. miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues. Aging (Albany NY) 2: 415-431, 2010.
61. Sengupta P, Xu Y, Wang L, Widom R, Smith BD. Collagen alpha1(I) gene (COL1A1) is repressed by RFX family. J Biol Chem 280: 21004-21014, 2005.
62. Sethupathy P, Megraw M, Hatzigeorgiou AG. A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Meth 3: 881-886, 2006.
63. Shahi P, Loukianiouk S, Bohne-Lang A, Kenzelmann M, Kuffer S, Maertens S, Eils R, Grone HJ, Gretz N, Brors B. Argonaute-a database for gene regulation by mammalian microRNAs. Nucleic Acids Res 34: D115-D118, 2006.
64. Sinha AU, Kaimal V, Chen J, Jegga AG. Dissecting microregulation of a master regulatory network. BMC Genomics 9: 88, 2008.
65. Slaby O, Svoboda M, Michalek J, Vyzula R. MicroRNAs in colorectal cancer: translation of molecular biology into clinical application. Mol Cancer 8: 102, 2009.
66. Smith PG, Wang F, Wilkinson KN, Savage KJ, Klein U, Neuberg DS, Bollag G, Shipp MA, Aguiar RC. The phosphodiesterase PDE4B limits cAMP-associated PI3K/AKT-dependent apoptosis in diffuse large B-cell lymphoma. Blood 105: 308-316, 2005.
67. Song B, Wang Y, Titmus MA, Botchkina G, Formentini A, Kornmann M, Ju J. Molecular mechanism of chemoresistance by miR-215 in osteosarcoma and colon cancer cells. Mol Cancer 9: 96, 2010.
68. Sood P, Krek A, Zavolan M, Macino G, Rajewsky N. Cell-type-specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci USA 103: 2746-2751, 2006.
69. Sun M Estrov Z, Ji Y, Coombes KR, Harris DH, Kurzrock R. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol Cancer Ther 7: 464-473, 2008.
70. Tanigawa Y, Yakura R, Komiya T. The bHLH transcription factor Tcf12 (ME1) mRNA is abundantly expressed in Paneth cells of mouse intestine. Gene Expr Patterns 7: 709-713, 2007.
71. Tavani A, Pelucchi C, Parpinel M, Negri E, Franceschi S, Levi F, La Vecchia C. n-3 polyunsaturated fatty acid intake and cancer risk in Italy and Switzerland. Int J Cancer 105: 113-116, 2003.
72. Thermann R, Hentze MW. Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447: 875-878, 2007.
73. Trimarchi JM, Lees JA. Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3: 11-20, 2002.
74. Tsang WP, Kwok TT. The miR-18a* microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 30: 953-959, 2009.
75. Vanamala J, Glagolenko A, Yang P, Carroll RJ, Murphy ME, Newman RA, Ford JR, Braby LA, Chapkin RS, Turner ND, Lupton JR. Dietary fish oil and pectin enhance colonocyte apoptosis in part through suppression of PPARdelta/PGE2 and elevation of PGE3. Carcinogenesis 29: 790-796, 2008.
76. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, Ganser A, Eder M, Scherr M. Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood 109: 4399-4405, 2007.
77. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103: 2257-2261, 2006.
78. Vos MD, Clark GJ. RASSF family proteins and Ras transformation. Methods Enzymol 407: 311-322, 2006.
79. Wang H, Huang S, Shou J, Su EW, Onyia JE, Liao B, Li S. Comparative analysis and integrative classification of NCI60 cell lines and primary tumors using gene expression profiling data. BMC Genomics 7: 166, 2006.
80. Wang Y, Lee AT, Ma JZ, Wang J, Ren J, Yang Y, Tantoso E, Li KB, Ooi LL, Tan P, Lee CG. Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis in-hibitor-5 as a microRNA-224-specific target. J Biol Chem 283: 13205-13215, 2008.
81. West NJ, Clark SK, Phillips RK, Hutchinson JM, Leicester RJ, Belluzzi A, Hull MA. Eicosapentaenoic acid reduces rectal polyp number and size in familial adenomatous polyposis. Gut 59: 918-925, 2010.
82. Whelan J, McEntee MF. Dietary (n-6) PUFA and intestinal tumorigen-esis. J Nutr 134: 3421S-3426S, 2004.
83. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234, 2009.
84. Wu H, Ye C, Ramirez D, Manjunath N. Alternative processing of primary microRNA transcripts by Drosha generates 5' end variation of mature microRNA. PLoS One 4: e7566, 2009.
85. Yamada Y, Yoshimi N, Hirose Y, Kawabata K, Matsunaga K, Shi-mizu M, Hara A, Mori H. Frequent beta-catenin gene mutations and accumulations of the protein in the putative preneoplastic lesions lacking macroscopic aberrant crypt foci appearance, in rat colon carcinogenesis. Cancer Res 60: 3323-3327, 2000.
86. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, Huso D, Lowenstein CJ. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci USA 107: 6334-6339, 2010.
87. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. McroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359, 2008.
88. Zinovyev A, Morozova N, Nonne N, Barillot E, Harel-Bellan A, Gorban AN. Dynamical modeling of microRNA action on the protein translation process. BMC Syst Biol 4: 13, 2010.