Functional screening identifies miRNAs influencing apoptosis and proliferation in colorectal cancer

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Christensen, Lise Lotte ^a   Holm, Anja ^b,c   Rantala, Juha ^d   Kallioniemi, Olli ^d   Rasmussen, Mads H ^a   Ostenfeld, Marie S ^a   Dagnaes Hansen, Frederik ^e   Øster, Bodil ^a   Schepeler, Troels ^a   Tobiasen, Heidi ^a   Thorsen, Kasper ^a   Sieber, Oliver M ^f,g   Gibbs, Peter ^f,g,h   Lamy, Philippe ^a   Hansen, Torben F ⁱ   Jakobsen, Anders ⁱ   Riising, Eva M ^j   Helin, Kristian ^j   Lubinski, Jan ^k   Hagemann Madsen, Rikke ^a   Laurberg, Søren ^a   Ørntoft, Torben F ^a   Andersen, Claus L ^a   more..

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b GLOSTRUP UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^e AARHUS UNIVERSITY   (Denmark)

^f LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h ROYAL MELBOURNE HOSPITAL   (Australia)

ⁱ UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^j UNIVERSITY OF COPENHAGEN   (Denmark)

^k POMERANIAN MEDICAL UNIVERSITY   (Poland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CASPASE 3; CASPASE 7; LACTATE DEHYDROGENASE; MICRORNA; MICRORNA 375; RNA; TRANSCRIPTION FACTOR YAP1; MESSENGER RNA; SMALL INTERFERING RNA; TUMOR PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER STAGING; CELL GROWTH; CELL PROLIFERATION; COLON MUCOSA; COLORECTAL CANCER; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENETIC TRANSFECTION; HCT116 CELL LINE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE MARKER; MIDDLE AGED; MOUSE; NONHUMAN; PHENOTYPE; PLASMID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA ISOLATION; TUMOR GROWTH; TUMOR XENOGRAFT; VERY ELDERLY; WESTERN BLOTTING; ANIMAL; COLORECTAL TUMOR; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; INTESTINE MUCOSA; LASER CAPTURE MICRODISSECTION; METABOLISM; PATHOLOGY; REPRODUCIBILITY;

AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DNA METHYLATION; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INTESTINAL MUCOSA; LASER CAPTURE MICRODISSECTION; MALE; MICE; MICRORNAS; MIDDLE AGED; NEOPLASM PROTEINS; NEOPLASM STAGING; PHENOTYPE; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84902477980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096767     Document Type: Article

References (62)

1. Boyle P, Langman JS (2000) ABC of colorectal cancer: Epidemiology. BMJ 321: 805-808.
2. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
3. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
4. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
5. Bueno MJ, Perez dC, I, Malumbres M (2008) Control of cell proliferation pathways by microRNAs. Cell Cycle 7: 3143-3148.
6. Suarez Y, Sessa WC (2009) MicroRNAs as novel regulators of angiogenesis. Circ Res 104: 442-454.
7. Subramanian S, Steer CJ (2010) MicroRNAs as gatekeepers of apoptosis. J Cell Physiol 223: 289-298.
8. Garzon R, Calin GA, Croce CM (2009) MicroRNAs in Cancer. Annu Rev Med 60: 167-179.
9. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA Jr, et al. (2006) The colorectal microRNAome. Proc Natl Acad Sci U S A 103: 3687-3692. (Pubitemid 43376616)
10. Schepeler T, Reinert JT, Ostenfeld MS, Christensen LL, Silahtaroglu AN, et al. (2008) Diagnostic and prognostic microRNAs in stage II colon cancer. Cancer Res 68: 6416-6424.
11. Arndt GM, Dossey L, Cullen LM, Lai A, Druker R, et al. (2009) Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer. BMC Cancer 9: 374.
12. Schetter AJ, Nguyen GH, Bowman ED, Mathe EA, Yuen ST, et al. (2009) Association of inflammation-related and microRNA gene expression with cancer-specific mortality of colon adenocarcinoma. Clin Cancer Res 15: 5878-5887.
13. Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, et al. (2006) Prognostic Values of microRNAs in Colorectal Cancer. Biomark Insights 2: 113-121.
14. Motoyama K, Inoue H, Takatsuno Y, Tanaka F, Mimori K, et al. (2009) Over- and under-expressed microRNAs in human colorectal cancer. Int J Oncol 34: 1069-1075.
15. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, et al. (2008) MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 299: 425-436. (Pubitemid 351185951)
16. Izumiya M, Tsuchiya N, Okamoto K, Nakagama H (2011) Systematic exploration of cancer-associated microRNA through functional screening assays. Cancer Sci 102: 1615-1621.
17. Nakano H, Miyazawa T, Kinoshita K, Yamada Y, Yoshida T (2009) Functional screening identifies a microRNA, miR-491 that induces apoptosis by targeting Bcl-X(L) in colorectal cancer cells. Int J Cancer 127: 1072-1080.
18. Cekaite L, Rantala JK, Bruun J, Guriby M, Agesen TH, et al. (2012) MiR-9, -31, and -182 deregulation promote proliferation and tumor cell survival in colon cancer. Neoplasia 14: 868-879.
19. Voorhoeve PM, le SC, Schrier M, Gillis AJ, Stoop H, et al. (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124: 1169-1181.
20. Izumiya M, Okamoto K, Tsuchiya N, Nakagama H (2010) Functional screening using a microRNA virus library and microarrays: a new high-throughput assay to identify tumor-suppressive microRNAs. Carcinogenesis 31: 1354-1359.
21. Rantala JK, Makela R, Aaltola AR, Laasola P, Mpindi JP, et al. (2011) A cell spot microarray method for production of high density siRNA transfection microarrays. BMC Genomics 12: 162.
22. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179.
23. Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250. (Pubitemid 39006544)
24. Ostenfeld MS, Fehrenbacher N, Hoyer-Hansen M, Thomsen C, Farkas T, et al. (2005) Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res 65: 8975-8983. (Pubitemid 41377389)
25. Schepeler T, Holm A, Halvey P, Nordentoft I, Lamy P, et al. (2011) Attenuation of the beta-catenin/TCF4 complex in colorectal cancer cells induces several growth-suppressive microRNAs that target cancer promoting genes. Oncogene 31: 2750-2760.
26. TargetScan v5.2. Available: http://www.targetscan.org/. Accessed 2011 Aug 1.
27. Ensembl 62. Available: http://www.ensembl.org/index.html. Accessed 2011 Apr 20.
28. Zhang S, Nohturfft A (2008) Studying Membrane Biogenesis with a Luciferase-Based Reporter Gene Assay. J Vis Exp 19: e920.
29. Meerbrey KL, Hu G, Kessler JD, Roarty K, Li MZ, et al. (2011) The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Proc Natl Acad Sci U S A 108: 3665-3670.
30. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, et al. (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
31. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
32. Saldanha AJ (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
33. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, et al. (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827. (Pubitemid 44742407)
34. Wang S, Wang L, Zhu T, Gao X, Li J, et al. (2010) Improvement of tissue preparation for laser capture microdissection: application for cell type-specific miRNA expression profiling in colorectal tumors. BMC Genomics 11: 163.
35. Chang KH, Miller N, Kheirelseid EA, Lemetre C, Ball GR, et al. (2011) MicroRNA signature analysis in colorectal cancer: identification of expression profiles in stage II tumors associated with aggressive disease. Int J Colorectal Dis 26: 1415-1422.
36. Sarver AL, French AJ, Borralho PM, Thayanithy V, Oberg AL, et al. (2009) Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer 9: 401.
37. Li X, Lin R, Li J (2011) Epigenetic Silencing of MicroRNA-375 Regulates PDK1 Expression in Esophageal Cancer. Dig Dis Sci 56: 2849-2856.
38. de Souza Rocha SP, Breiling A, Gupta N, Malekpour M, Youns M, et al. (2010) Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res 70: 9175-9184.
39. Sandoval J, Heyn HA, Moran S, Serra-Musach J, Pujana MA, et al. (2011) Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 6: 692-702.
40. Mazar J, DeBlasio D, Govindarajan SS, Zhang S, Perera RJ (2011) Epigenetic regulation of microRNA-375 and its role in melanoma development in humans. FEBS Lett 585: 2467-2476.
41. Avnit-Sagi T, Kantorovich L, Kredo-Russo S, Hornstein E, Walker MD (2009) The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. PLoS One 4: e5033.
42. Kong KL, Kwong DL, Chan TH, Law SY, Chen L, et al. (2012) MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 61: 33-42.
43. Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, et al. (2008) MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 47: 1955-1963. (Pubitemid 351952843)
44. Hatzis P, van der Flier LG, van Driel MA, Guryev V, Nielsen F, et al. (2008) Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol Cell Biol 28: 2732-2744. (Pubitemid 351542371)
45. Yochum GS, Cleland R, Goodman RH (2008) A genome-wide screen for beta-catenin binding sites identifies a downstream enhancer element that controls c-Myc gene expression. Mol Cell Biol 28: 7368-7379.
46. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
47. Vergoulis T, Vlachos IS, Alexiou P, Georgakilas G, Maragkakis M, et al. (2012) TarBase 6.0: capturing the exponential growth of miRNA targets with experimental support. Nucleic Acids Res 40: D222-D229.
48. Rosenbluh J, Nijhawan D, Cox AG, Li X, Neal JT, et al. (2012) beta-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151: 1457-1473.
49. Liu AM, Poon RT, Luk JM (2010) MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem Biophys Res Commun 394: 623-627.
50. Ding L, Xu Y, Zhang W, Deng Y, Si M, et al. (2010) MiR-375 frequently downregulated in gastric cancer inhibits cell proliferation by targeting JAK2. Cell Res 20: 784-793.
51. Hui AB, Lenarduzzi M, Krushel T, Waldron L, Pintilie M, et al. (2010) Comprehensive MicroRNA profiling for head and neck squamous cell carcinomas. Clin Cancer Res 16: 1129-1139.
52. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, et al. (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70: 2339-2349.
53. Yan H, Choi AJ, Lee BH, Ting AH (2011) Identification and Functional Analysis of Epigenetically Silenced MicroRNAs in Colorectal Cancer Cells. PLoS One 6: e20628.
54. Faltejskova P, Svoboda M, Srutova K, Mlcochova J, Besse A, et al. (2012) Identification and functional screening of microRNAs highly deregulated in colorectal cancer. J Cell Mol Med 16: 2655-2666.
55. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500. (Pubitemid 40617277)
56. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, et al. (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125: 1253-1267. (Pubitemid 43929093)
57. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, et al. (2008) Expression of Yes-associated protein in common solid tumors. Hum Pathol 39: 1582-1589.
58. Nishimura Y, Komatsu S, Ichikawa D, Nagata H, Hirajima S, et al. (2013) Overexpression of YWHAZ relates to tumor cell proliferation and malignant outcome of gastric carcinoma. Br J Cancer 108: 1324-1331.
59. von EB, Maaskola J, Memczak S, Mollmann K, Schuetz A, et al. (2012) The SNF2-like helicase HELLS mediates E2F3-dependent transcription and cellular transformation. EMBO J 31: 972-985.
60. Hwang YC, Lu TY, Huang DY, Kuo YS, Kao CF, et al. (2009) NOLC1, an enhancer of nasopharyngeal carcinoma progression, is essential for TP53 to regulate MDM2 expression. Am J Pathol 175: 342-354.
61. Abdelmohsen K, Hutchison ER, Lee EK, Kuwano Y, Kim MM, et al. (2010) miR-375 inhibits differentiation of neurites by lowering HuD levels. Mol Cell Biol 30: 4197-4210.
62. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, et al. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432: 226-230. (Pubitemid 39545853)