MiR-34a and miR-34b/c suppress intestinal tumorigenesis

Cancer Research

Volumn 77, Issue 10, 2017, Pages 2746-2758

  Jiang, Longchang ^a   Hermeking, Heiko ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; MICRORNA; MICRORNA 34A; MICRORNA 34B; MICRORNA 34C; UNCLASSIFIED DRUG; MIRN34 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GRADING; CANCER SURVIVAL; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; IMMUNOCOMPETENT CELL; LYMPH NODE METASTASIS; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; SMALL INTESTINE CANCER; TUMOR VOLUME; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; BIOLOGICAL MODEL; CELL PROLIFERATION; CELL TRANSFORMATION; CLUSTER ANALYSIS; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; INTESTINE TUMOR; KNOCKOUT MOUSE; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; REPRODUCIBILITY; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; WNT SIGNALING;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; INTESTINAL MUCOSA; INTESTINAL NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; MODELS, BIOLOGICAL; PROGNOSIS; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; WNT SIGNALING PATHWAY;

EID: 85020214949     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-2183     Document Type: Article

References (50)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016;66:7-30.
2. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996;87:159-70.
3. Bienz M, Clevers H. Linking colorectal cancer to Wnt signaling. Cell 2000;103:311-20.
4. Moser AR, Mattes EM, Dove WF, Lindstrom MJ, Haag JD, Gould MN. ApcMin, a mutation in the murine Apc gene, predisposes to mammary carcinomas and focal alveolar hyperplasias. Proc Natl Acad Sci U S A 1993;90:8977-81.
5. Luongo C, Moser AR, Gledhill S, Dove WF. Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res 1994;54:5947-52.
6. Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, Dove WF. ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 1995;31A:1061-4.
7. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-10.
8. Hermeking H.MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 2012;12:613-26.
9. Hunten S, Kaller M, Drepper F, Oeljeklaus S, Bonfert T, Erhard F, et al. p53- Regulated networks of protein, mRNA, miRNA, and lncRNA expression revealed by integrated pulsed stable isotope labeling with amino acids in cell culture (pSILAC) and next generation sequencing (NGS) analyses.Mol Cell Proteomics 2015;14:2609-29.
10. Rokavec M, Li H, Jiang L, Hermeking H. The p53/miR-34 axis in development and disease. J Mol Cell Biol 2014;6:214-30.
11. Hermeking H.p53 enters the microRNA world. Cancer Cell 2007;12: 414-8.
12. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, et al. Differential regulation ofmicroRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007;6:1586-93.
13. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, et al. miR- 34 and SNAIL form a double-negative feedback loop to regulate epithelialmesenchymal transitions. Cell Cycle 2011;10:4256-71.
14. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011;17:211-5.
15. Bu P, Wang L, Chen KY, Srinivasan T, Murthy PK, Tung KL, et al. A miR-34anumb feedforward loop triggered by inflammation regulates asymmetric stem cell division in intestine and colon cancer. Cell Stem Cell 2016;18: 189-202.
16. Cheng CY, Hwang CI, Corney DC, Flesken-Nikitin A, Jiang L, Oner GM, et al. miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep 2014;6:1000-7.
17. Choi YJ, Lin CP, HoJJ, He X, Okada N, Bu P, et al.miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 2011;13:1353-60.
18. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H, et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell cycle 2008;7:2591-600.
19. Siemens H, Neumann J, Jackstadt R, Mansmann U, Horst D, Kirchner T, et al. Detection of miR-34a promoter methylation in combination with elevated expression of c-Met and b-catenin predicts distant metastasis of colon cancer. Clin Cancer Res 2013;19:710-20.
20. Adams BD, Parsons C, Slack FJ. The tumor-suppressive and potential therapeutic functions of miR-34a in epithelial carcinomas. Expert Opin Ther Targets 2016;20:737-53.
21. Rokavec M, Oner MG, Li H, Jackstadt R, Jiang L, Lodygin D, et al. IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest 2014;124:1853-67.
22. Gregorieff A, Clevers H. In situ hybridization to identify gut stem cells. Curr Protoc Stem Cell Biol 2010;Chapter 2:Unit 2F 1.
23. Risso D, Ngai J, Speed TP, Dudoit S. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat Biotechnol 2014;32:896-902.
24. Kallio MA, Tuimala JT, Hupponen T, Klemela P, Gentile M, Scheinin I, et al. Chipster: user-friendly analysis software for microarray and other highthroughput data. BMC Genom 2011;12:507.
25. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009;37:1-13.
26. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50.
27. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20.
28. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 2011;141:1762-72.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))Method.Methods 2001;25:402-8.
30. Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487:330-7.
31. Vogt M, Munding J, Gruner M, Liffers ST, Verdoodt B, Hauk J, et al. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 2011;458:313-22.
32. Lee SH, Hu LL, Gonzalez-Navajas J, Seo GS, Shen C, Brick J, et al. ERK activation drives intestinal tumorigenesis in Apc(min/+) mice. Nat Med 2010;16:665-70.
33. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014;15:550.
34. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139-40.
35. Munoz J, Stange DE, Schepers AG, van de Wetering M, Koo BK, Itzkovitz S, et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+4' cell markers. EMBO J 2012;31:3079-91.
36. Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011;8:511-24.
37. Kim NH, Kim HS, Kim N-G, Lee I, Choi H-S, Li X-Y, et al. p53 and miRNA- 34 are Suppressors of Canonical Wnt Signaling. Sci Signal 2011;4:ra71.
38. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009;457:608-11.
39. Garofalo M, Jeon YJ, NuovoGJ, Middleton J, Secchiero P, Joshi P, et al. MiR- 34a/c-Dependent PDGFR-alpha/beta downregulation inhibits tumorigenesis and enhances TRAIL-Induced apoptosis in lung cancer. PloS One 2013;8:e67581.
40. Kaller M, Liffers S-T, Oeljeklaus S, Kuhlmann K, Röh S, Hoffmann R, et al. Genome-wide characterization ofmiR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol Cell Proteo 2011;10:M111. 010462.
41. Zhang J, Zhou S, Tang L, Shen L, Xiao L, Duan Z, et al.WAVE1gene silencing via RNA interference reduces ovarian cancer cell invasion, migration and proliferation. Gynecol Oncol 2013;130:354-61.
42. Corrales L, Matson V, Flood B, Spranger S, Gajewski TF. Innate immune signaling and regulation in cancer immunotherapy. Cell Res 2016; 27:96-108.
43. Craven RJ, Xu LH, Weiner TM, Fridell YW, Dent GA, Srivastava S, et al. Receptor tyrosine kinases expressed in metastatic colon cancer. Int J Cancer 1995;60:791-7.
44. Grose R, Dickson C. Fibroblast growth factor signaling in tumorigenesis. Cytokine Growth Factor Rev 2005;16:179-86.
45. OlivoMarston SE, Hursting SD, Lavigne J, Perkins SN, Maarouf RS, Yakar S, et al. Genetic reduction of circulating insulinlike growth factor1 inhibits azoxymethaneinduced colon tumorigenesis in mice. Mol Carcinogen 2009;48:1071-6.
46. Tamura S, Oshima T, Yoshihara K, Kanazawa A, Yamada T, Inagaki D, et al. Clinical significance of STC1 gene expression in patients with colorectal cancer. Anticancer Res 2011;31:325-9.
47. Warnier M, Roudbaraki M, Derouiche S, Delcourt P, Bokhobza A, Prevarskaya N, et al. CACNA2D2 promotes tumorigenesis by stimulating cell proliferation and angiogenesis. Oncogene 2015;34:5383-94.
48. Worthley DL, Giraud AS, Wang TC. The extracellular matrix in digestive cancer. Cancer Microenviron 2010;3:177-85.
49. Togashi Y, Kogita A, Sakamoto H, Hayashi H, Terashima M, de Velasco MA, et al. Activin signal promotes cancer progression and is involved in cachexia in a subset of pancreatic cancer. Cancer Lett 2015;356:819-27.
50. DuY-Z, GuX-H, Cheng S-F, Li L, Liu H, HuL-P, et al. The oncogenetic role of stanniocalcin 1 in lung adenocarcinoma: a promising serum candidate biomarker for tracking lung adenocarcinoma progression. Tumor Biol 2015:1-12.