MicroRNA-17 is the most up-regulated member of the miR-17-92 cluster during early colon cancer evolution

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Knudsen, Kirsten Nguyen ^a,b   Nielsen, Boye Schnack ^c   Lindebjerg, Jan ^a   Hansen, Torben Frøstrup ^a   Holst, René ^b   Sørensen, Flemming Brandt ^a,b  

^a LILLEBAELT HOSPITAL   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c BIONEER A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MICRORNA; MICRORNA 135B; MICRORNA 145; MICRORNA 17; MICRORNA 17 92; MICRORNA 18; MICRORNA 19; MICRORNA 19B; MICRORNA 20; MICRORNA 20A; MICRORNA 21; MICRORNA 31; MICRORNA 92; MICRORNA 92A; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG; MIRN17 MICRORNA, HUMAN;

ADULT; AGED; AMINO ACID SEQUENCE; ARTICLE; CHROMOGENIC IN SITU HYBRIDIZATION; CLINICAL ARTICLE; COLON ADENOCARCINOMA; COLON ADENOMA; COLON CANCER; COLON POLYP; CONTROLLED STUDY; EARLY CANCER; EPITHELIUM CELL; FEMALE; GENE CLUSTER; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN SITU HYBRIDIZATION; MALE; MOLECULAR EVOLUTION; PROTEIN EXPRESSION; RNA ANALYSIS; TISSUE DISTRIBUTION; UPREGULATION; VALIDATION PROCESS; CANCER GRADING; CANCER STAGING; CELL TRANSFORMATION; COLON TUMOR; GENETICS; METABOLISM; MOLECULAR IMAGING; MULTIGENE FAMILY; PATHOLOGY; REPRODUCIBILITY; TUMOR INVASION;

BETA CATENIN; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION; MALE; MICRORNAS; MOLECULAR IMAGING; MULTIGENE FAMILY; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PTEN PHOSPHOHYDROLASE; REPRODUCIBILITY OF RESULTS;

EID: 84949034887     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140503     Document Type: Article

References (58)

1. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014; 383: 1490-502. doi: 10.1016/S0140-6736(13)61649-9
2. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990; 61: 759-67.
3. Imai K, Yamamoto H. Carcinogenesis and microsatellite instability: The interrelationship between genetics and epigenetics. Carcinogenesis. 2008; 29: 673-80.
4. Goel A, Boland CR. Epigenetics of colorectal cancer. Gastroenterology. 2012; 143: 1442-60. doi: 10. 1053/j.gastro.2012.09.032
5. Schetter AJ, Okayama H, Harris CC. The role of microRNAs in colorectal cancer. Cancer J. 2012; 18: 244-52. doi: 10.1097/PPO.0b013e318258b78f
6. Faber C, Kirchner T, Hlubek F. The impact of microRNAs on colorectal cancer. Virchows Arch. 2009; 454: 359-67. doi: 10.1007/s00428-009-0751-9
7. Slaby O, Svoboda M, Michalek J, Vyzula R. MicroRNAs in colorectal cancer: Translation of molecular biology into clinical application. Mol Cancer. 2009; 8: 102. doi: 10.1186/1476-4598-8-102
8. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of micro-RNAs. Genome Res. 2009; 19: 92-105. doi: 10.1101/gr.082701.108
9. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 2006; 6: 259-69.
10. Olive V, Li Q, He L. mir-17-92: A polycistronic oncomir with pleiotropic functions. Immunol Rev. 2013; 253: 158-66. doi: 10.1111/imr.12054
11. Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, Mongera S, Postma C, Meijerink WJ, et al. MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. Br J Cancer. 2009; 101: 707-14. doi: 10.1038/sj.bjc.6605037
12. Yu G, Tang JQ, Tian ML, Li H, Wang X, Wu T, et al. Prognostic values of the miR-17-92 cluster and its paralogs in colon cancer. J Surg Oncol. 2012; 106: 232-7. doi: 10.1002/jso.22138
13. Humphreys KJ, McKinnon RA, Michael MZ. miR-18a inhibits CDC42 and plays a tumour suppressor role in colorectal cancer cells. PLoS One. 2014; 9: e112288. doi: 10.1371/journal.pone.0112288
14. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008; 299: 425-36. doi: 10.1001/jama.299.4.425
15. Bandres E, Cubedo E, Agirre X, Malumbres R, Zarate R, Ramirez N, et al. Identification by Real-Time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-Tumoral tissues. Mol Cancer. 2006; 5: 29.
16. Slaby O, Svoboda M, Fabian P, Smerdova T, Knoflickova D, Bednarikova M, et al. Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology. 2007; 72: 397-402. doi: 10.1159/000113489
17. Michael MZ, O'Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res. 2003; 1: 882-91.
18. Chang KH, Miller N, Kheirelseid EA, Lemetre C, Ball GR, Smith MJ, et al. MicroRNA signature analysis in colorectal cancer: identification of expression profiles in stage II tumors associated with aggressive disease. Int J Colorectal Dis. 2011; 26: 1415-22. doi: 10.1007/s00384-011-1279-4
19. Nagel R, le SC, Diosdado B, van der WM, Oude Vrielink JA, Bolijn A, et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res. 2008; 68: 5795-802. doi: 10.1158/0008-5472.CAN-08-0951
20. Aslam MI, Hussein S, West K, Singh B, Jameson JS, Pringle JH. MicroRNAs associated with initiation and progression of colonic polyp: A feasibility study. Int J Surg. 2014; 13C: 272-9.
21. Bartley AN, Yao H, Barkoh BA, Ivan C, Mishra BM, Rashid A, et al. Complex patterns of altered Micro-RNA expression during the adenoma-Adenocarcinoma sequence for microsatellite-stable colorectal cancer. Clin Cancer Res. 2011; 17: 7283-93. doi: 10.1158/1078-0432.CCR-11-1452
22. Oberg AL, French AJ, Sarver AL, Subramanian S, Morlan BW, Riska SM, et al. miRNA expression in colon polyps provides evidence for a multihit model of colon cancer. PLoS One. 2011; 6: e20465. doi: 10.1371/journal.pone.0020465
23. Chang KH, Miller N, Kheirelseid EA, Ingoldsby H, Hennessy E, Curran CE, et al. MicroRNA-21 and PDCD4 expression in colorectal cancer. Eur J Surg Oncol. 2011; 37: 597-603. doi: 10.1016/j.ejso. 2011.04.001
24. Gattolliat CH, Uguen A, Pesson M, Trillet K, Simon B, Doucet L, et al. MicroRNA and targeted mRNA expression profiling analysis in human colorectal adenomas and adenocarcinomas. Eur J Cancer. 2015; 51: 409-20. doi: 10.1016/j.ejca.2014.12.007
25. Cekaite L, Rantala JK, Bruun J, Guriby M, Agesen TH, Danielsen SA, et al. MiR-9,-31, and-182 deregulation promote proliferation and tumor cell survival in colon cancer. Neoplasia. 2012; 14: 868-79.
26. Yamamichi N, Shimomura R, Inada K, Sakurai K, Haraguchi T, Ozaki Y, et al. Locked nucleic acid in situ hybridization analysis of miR-21 expression during colorectal cancer development. Clin Cancer Res. 2009; 15: 4009-16. doi: 10.1158/1078-0432.CCR-08-3257
27. Nielsen BS, Jorgensen S, Fog JU, Sokilde R, Christensen IJ, Hansen U, et al. High levels of micro-RNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clin Exp Metastasis. 2011; 28: 27-38. doi: 10.1007/s10585-010-9355-7
28. Schee K, Fodstad O, Flatmark K. MicroRNAs as biomarkers in colorectal cancer. Am J Pathol. 2010; 177: 1592-9. doi: 10.2353/ajpath.2010.100024
29. Yang L, Belaguli N, Berger DH. MicroRNA and colorectal cancer. World J Surg. 2009; 33: 638-46. doi: 10.1007/s00268-008-9865-5
30. Ma Y, Zhang P, Yang J, Liu Z, Yang Z, Qin H. Candidate microRNA biomarkers in human colorectal cancer: systematic review profiling studies and experimental validation. Int J Cancer. 2012; 130: 2077-87 doi: 10.1002/ijc.26232
31. Fang L, Li H, Wang L, Hu J, Jin T, Wang J, et al. MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget. 2014; 5: 2974-87.
32. Xiong B, Cheng Y, Ma L, Zhang C. MiR-21 regulates biological behavior through the PTEN/PI-3 K/Akt signaling pathway in human colorectal cancer cells. Int J Oncol. 2013; 42: 219-28. doi: 10.3892/ijo. 2012.1707
33. Tsuchida A, Ohno S, Wu W, Borjigin N, Fujita K, Aoki T, et al. miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci. 2011; 102: 2264-71. doi: 10.1111/j.1349-7006. 2011.02081.x
34. Ma Y, Zhang P, Wang F, Zhang H, Yang Y, Shi C, et al. Elevated oncofoetal miR-17-5p expression regulates colorectal cancer progression by repressing its target gene P130. Nat Commun. 2012; 3: 1291. doi: 10.1038/ncomms2276
35. Monzo M, Navarro A, Bandres E, Artells R, Moreno I, Gel B, et al. Overlapping expression of micro-RNAs in human embryonic colon and colorectal cancer. Cell Res. 2008; 18: 823-33. doi: 10.1038/cr. 2008.81
36. Bramis J, Zacharatos P, Papaconstantinou I, Kotsinas A, Sigala F, Korkolis DP, et al. E2F-1 transcription factor immunoexpression is inversely associated with tumor growth in colon adenocarcinomas. Anticancer Res. 2004; 24: 3041-7.
37. Xanthoulis A, Tiniakos DG. E2F transcription factors and digestive system malignancies: how much do we know? World J Gastroenterol. 2013; 19: 3189-98. doi: 10.3748/wjg.v19.i21.3189
38. Diaz R, Silva J, Garcia JM, Lorenzo Y, Garcia V, Pena C, et al. Deregulated expression of miR-106a predicts survival in human colon cancer patients. Genes Chromosomes Cancer. 2008; 47: 794-802. doi: 10.1002/gcc.20580
39. Kanaan Z, Rai SN, Eichenberger MR, Barnes C, Dworkin AM, Weller C, et al. Differential microRNA expression tracks neoplastic progression in inflammatory bowel disease-Associated colorectal cancer. Hum Mutat. 2012; 33: 551-60. doi: 10.1002/humu.22021
40. Trompeter HI, Abbad H, Iwaniuk KM, Hafner M, Renwick N, Tuschl T, et al. MicroRNAs MiR-17, MiR-20a, and MiR-106b act in concert to modulate E2F activity on cell cycle arrest during neuronal lineage differentiation of USSC. PLoS One. 2011; 6: e16138. doi: 10.1371/journal.pone.0016138
41. Kjaer-Frifeldt S, Hansen TF, Nielsen BS, Joergensen S, Lindebjerg J, Soerensen FB, et al. The prognostic importance of miR-21 in stage II colon cancer: A population-based study. Br J Cancer. 2012; 107: 1169-74. doi: 10.1038/bjc.2012.365
42. Kang W, Lee J, Oh S, Lee S, Jung C. Stromal expression of miR-21 in T3-4a colorectal cancer is an independent predictor of early tumor relapse. BMC Gastroenterol. 2015; 15: 2. doi: 10.1186/s12876-015-0227-0
43. Kent OA, McCall MN, Cornish TC, Halushka MK. Lessons from miR-143/145: The importance of celltype localization of miRNAs. Nucleic Acids Res. 2014; 42: 7528-38. doi: 10.1093/nar/gku461
44. Chivukula RR, Shi G, Acharya A, Mills EW, Zeitels LR, Anandam JL, et al. An essential mesenchymal function for miR-143/145 in intestinal epithelial regeneration. Cell. 2014; 157: 1104-16. doi: 10.1016/j. cell.2014.03.055
45. Wu CW, Ng SC, Dong Y, Tian L, Ng SS, Leung WW, et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma. Clin Cancer Res. 2014; 20: 2994-3002. doi: 10.1158/1078-0432.CCR-13-1750
46. Xu XM, Qian JC, Deng ZL, Cai Z, Tang T, Wang P, et al. Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancer. Oncol Lett. 2012; 4: 339-45.
47. Slattery ML, Herrick JS, Mullany LE, Valeri N, Stevens J, Caan BJ, et al. An evaluation and replication of miRNAs with disease stage and colorectal cancer-specific mortality. Int J Cancer. 2014. doi: 10. 1002/ijc.29384
48. Wang CJ, Zhou ZG, Wang L, Yang L, Zhou B, Gu J, et al. Clinicopathological significance of micro-RNA-31,-143 and-145 expression in colorectal cancer. Dis Markers. 2009; 26: 27-34. doi: 10.3233/DMA-2009-0601
49. Ito M, Mitsuhashi K, Igarashi H, Nosho K, Naito T, Yoshii S, et al. MicroRNA-31 expression in relation to BRAF mutation, CpG island methylation and colorectal continuum in serrated lesions. Int J Cancer. 2014; 135: 2507-15. doi: 10.1002/ijc.28920
50. Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, et al. APC mutations occur early during colorectal tumorigenesis. Nature. 1992; 359: 235-7.
51. Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007; 19: 150-8.
52. Valentini AM, Pirrelli M, Renna L, Armentano R, Caruso ML. P53 and beta-catenin in colorectal cancer progression. Curr Pharm Des. 2003; 9: 1932-6.
53. Herter P, Kuhnen C, Muller KM, Wittinghofer A, Muller O. Intracellular distribution of beta-catenin in colorectal adenomas, carcinomas and Peutz-Jeghers polyps. J Cancer Res Clin Oncol. 1999; 125: 297-304.
54. Hao X, Tomlinson I, Ilyas M, Palazzo JP, Talbot IC. Reciprocity between membranous and nuclear expression of beta-catenin in colorectal tumours. Virchows Arch. 1997; 431: 167-72.
55. Molinari F, Frattini M. Functions and Regulation of the PTEN Gene in Colorectal Cancer. Front Oncol. 2013; 3: 326. doi: 10.3389/fonc.2013.00326
56. Jang KS, Song YS, Jang SH, Min KW, Na W, Jang SM, et al. Clinicopathological significance of nuclear PTEN expression in colorectal adenocarcinoma. Histopathology. 2010; 56: 229-39. doi: 10.1111/j. 1365-2559.2009.03468.x
57. Zhang J, Xiao Z, Lai D, Sun J, He C, Chu Z, et al. miR-21, miR-17 and miR-19a induced by phosphatase of regenerating liver-3 promote the proliferation and metastasis of colon cancer. Br J Cancer. 2012; 107: 352-9. doi: 10.1038/bjc.2012.251
58. Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009; 23: 2839-49. doi: 10.1101/gad.1861409