The Myc-miR-17∼92 axis blunts TGFβ signaling and production of multiple TGFβ-dependent antiangiogenic factors

Cancer Research

Volumn 70, Issue 20, 2010, Pages 8233-8246

  Dews, Michael ^a   Fox, Jamie L ^a   Hultine, Stacy ^a   Sundaram, Prema ^a   Wang, Wenge ^a,d   Liu, Yingqiu Y ^a,d   Furth, Emma ^a   Enders, Gregory H ^a,c   El Deiry, Wafik ^a,d   Schelter, Janell M ^b,e   Cleary, Michele A ^b,e   Thomas Tikhonenko, Andrei ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ROSETTA INPHARMATICS   (United States)

^c FOX CHASE CANCER CENTER   (United States)

^d PENN STATE CANCER INSTITUTE   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CLUSTERIN; MICRORNA; MYC PROTEIN; SMAD4 PROTEIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE INDUCTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANGIOGENESIS INHIBITORS; ANIMALS; BASE SEQUENCE; CLUSTERIN; COLONIC NEOPLASMS; DOWN-REGULATION; GENES, REPORTER; HUMANS; LUCIFERASES; MICE; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RIBONUCLEASE III; TRANSFORMING GROWTH FACTOR BETA; UNTRANSLATED REGIONS;

EID: 78049232281     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2412     Document Type: Article

References (63)

1. Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer 2008;8:976-90.
2. Shchors K, Evan G. Tumor angiogenesis: cause or consequence of cancer? Cancer Res 2007;67:7059-61.
3. Pelengaris S, Littlewood T, Khan M, Elia G, Evan GI. Reversible activation of c-Myc in skin: induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol Cell 1999;3:565-77. (Pubitemid 29268440)
4. Shchors K, Shchors E, Rostker F, Lawlor ER, Brown-Swigart L, Evan GI. The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1β. Genes Dev 2006;20:2527-38. (Pubitemid 44396838)
5. Brandvold KA, Neiman P, Ruddell A. Angiogenesis is an early event in the generation of myc-induced lymphomas. Oncogene 2000;19:2780-5. (Pubitemid 30339228)
6. Ngo C, Gee MS, Akhtar N, et al. An in vivo function for the transforming myc protein: elicitation of the angiogenic phenotype. Cell Growth Differ 2000;11:201-10. (Pubitemid 30211009)
7. Dews M, Homayouni A, Yu D, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006;38:1060-5. (Pubitemid 44325933)
8. Janz A, Sevignani C, Kenyon K, Ngo C, Thomas-Tikhonenko A. Activation of the Myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucleic Acids Res 2000;28:2268-75. (Pubitemid 30639360)
9. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet 2009;10:94-108.
10. Chang T-C, Yu D, Lee Y-S, et al. Widespread microRNA repression by c-Myc promotes tumorigenesis. Nat Genet 2008;40:43-50.
11. Lin CH, Jackson AL, Guo J, Linsley PS, Eisenman RN. Myc-regulated microRNAs attenuate embryonic stem cell differentiation. EMBO J 2009;28:3157-70.
12. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005;435:839-43.
13. Thomas-Tikhonenko A, Viard-Leveugle I, Dews M, et al. Myc-transformed epithelial cells down-regulate clusterin which inhibits their growth in vitro and carcinogenesis in vivo. Cancer Res 2004;64:3126-36. (Pubitemid 38581413)
14. Chayka O, Corvetta D, Dews M, et al. Clusterin, a haploinsufficient tumour suppressor gene in neuroblastomas. J Natl Cancer Inst 2009;101:663-77.
15. Trougakos IP, Djeu JY, Gonos ES, Boothman DA. Advances and challenges in basic and translational research on clusterin. Cancer Res 2009;69:403-6.
16. Sevignani C, Wlodarski P, Kirillova J, et al. Tumorigenic conversion of p53-deficient colon epithelial cells by an activated Ki-ras gene. J Clin Invest 1998;101:1572-80. (Pubitemid 28198485)
17. Cummins JM, He Y, Leary RJ, et al. The colorectal microRNAome. Proc Natl Acad Sci U S A 2006;103:3687-92.
18. Suh E, Zhengqi W, Swain GP, Tenniswood M, Traber PG. Clusterin gene transcription is activated by caudal-related homeobox genes in intestinal epithelium. Am J Physiol 2001;280:G149-56.
19. Hunter CA, Yu D, Gee M, et al. Cutting edge: systemic inhibition of angiogenesis underlies resistance to tumors during acute toxoplasmosis. J Immunol 2001;166:5878-81. (Pubitemid 32440710)
20. Hughes TR, Mao M, Jones AR, et al. Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 2001;19:342-7. (Pubitemid 32275343)
21. Wooster R. Transcript profiling of cancer cell line panel. Available from: https://array.nci.nih.gov/caarray/project/woost-00041 2008.
22. Yang CR, Leskov K, Hosley-Eberlein K, et al. Nuclear clusterin/XIP8, an X-ray-induced Ku70-binding protein that signals cell death. Proc Natl Acad Sci U S A 2000;97:5907-12. (Pubitemid 30367497)
23. Jenne DE, Tschopp J. Clusterin: the intriguing guises of a widely expressed glycoprotein. Trends Biochem Sci 1992;17:154-9.
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 2007;27:91-105. (Pubitemid 46991392)
25. Linsley PS, Schelter J, Burchard J, et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 2007;27:2240-52. (Pubitemid 46418479)
26. Chung EY, Dews M, Cozma D, et al. c-Myb oncoprotein is an essential target of the dleu2 tumor suppressor microRNA cluster. Cancer Biol Ther 2008;7:1758-64.
27. Jin G, Howe PH. Regulation of clusterin gene expression by transforming growth factor β. J Biol Chem 1997;272:26620-6. (Pubitemid 27458885)
28. Bierie B, Moses HL. Tumour microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 2006;6:506-20.
29. Massague J. TGFβ in cancer. Cell 2008;134:215-30.
30. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-61. (Pubitemid 43271657)
31. Markowitz S, Wang J, Myeroff L, et al. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science 1995;268:1336-8.
32. Schwarte-Waldhoff I, Volpert OV, Bouck NP, et al. Smad4/DPC4-mediated tumor suppression through suppression of angiogenesis. Proc Natl Acad Sci U S A 2000;97:9624-9. (Pubitemid 30650826)
33. Miranda KC, Huynh T, Tay Y, et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 2006;126:1203-17. (Pubitemid 44380294)
34. Padua D, Zhang XH, Wang Q, et al. TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 2008;133:66-77. (Pubitemid 351442989)
35. Ito Y, Oike Y, Yasunaga K, et al. Inhibition of angiogenesis and vascular leakiness by angiopoietin-related protein 4. Cancer Res 2003;63:6651-7. (Pubitemid 37322943)
36. Alexandrow MG, Kawabata M, Aakre M, Moses HL. Overexpression of the c-Myc oncoprotein blocks the growth-inhibitory response but is required for the mitogenic effects of transforming growth factor β1. Proc Natl Acad Sci U S A 1995;92:3239-43.
37. Warner BJ, Blain SW, Seoane J, Massague J. Myc downregulation by transforming growth factor β required for activation of the p15 (Ink4b) G(1) arrest pathway. Mol Cell Biol 1999;19:5913-22.
38. Seoane J, Pouponnot C, Staller P, Schader M, Eilers M, Massague J. TGFβ influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nature Cell Biol 2001;3:400-8.
39. Staller P, Peukert K, Kiermaier A, et al. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol 2001;3:392-9. (Pubitemid 32288447)
40. Amati B. Integrating Myc and TGFβ signalling in cell-cycle control. Nat Cell Biol 2001;3:E112-3.
41. Feng XH, Liang YY, Liang M, Zhai W, Lin X. Direct interaction of c-Myc with Smad2 and Smad3 to inhibit TGF-β-mediated induction of the CDK inhibitor p15(Ink4B). Mol Cell 2002;9:133-43. (Pubitemid 34127777)
42. Schuhmacher M, Kohlhuber F, Holzel M, et al. The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res 2001;29:397-406. (Pubitemid 32060926)
43. Zeller KI, Jegga AG, Aronow B, O'Donnell KA, Dang CV. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol 2003;4:R69.1-R69.10.
44. Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
45. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the Ecadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22:894-907. (Pubitemid 351482843)
46. Fontana L, Fiori ME, Albini S, et al. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 2008;3:e2236.
47. Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008;132:875-86. (Pubitemid 351312807)
48. Koralov SB, Muljo SA, Galler GR, et al. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 2008;132:860-74.
49. Xiao C, Srinivasan L, Calado DP, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 2008;9:405-14. (Pubitemid 351405110)
50. Mavrakis KJ, Wolfe AL, Oricchio E, et al. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 2010;12:372-9.
51. Inomata M, Tagawa H, Guo YM, Kameoka Y, Takahashi N, Sawada K. MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood 2009;113:396-402.
52. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008;454:56-61. (Pubitemid 351931982)
53. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor β signaling. Cancer Res 2008;68:8191-4.
54. Rai D, Kim SW, McKeller MR, Dahia PL, Aguiar RC. Targeting of SMAD5 links microRNA-155 to the TGF-β pathway and lymphomagenesis. Proc Natl Acad Sci U S A 2010;107:3111-6.
55. Rogler CE, Levoci L, Ader T, et al. MicroRNA-23b cluster microRNAs regulate transforming growth factor-β/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology 2009;50:575-84.
56. Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, 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.
57. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature 2005;435:828-33. (Pubitemid 40839734)
58. Olive V, Bennett MJ, Walker JC, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev 2009;23:2839-49.
59. Mu P, Han YC, Betel D, et al. Genetic dissection of the miR-17∼92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev 2009;23:2806-11.
60. Fontana L, Pelosi E, Greco P, et al. MicroRNAs 17-5-20a-106a control monocytopoiesis through AML1 targeting andM-CSF receptor upregulation. Nat Cell Biol 2007;9:775-87. (Pubitemid 47019464)
61. Schulte JH, Horn S, Otto T, et al. MYCN regulates oncogenic micro-RNAs in neuroblastoma. Int J Cancer 2008;122:699-704. (Pubitemid 350308967)
62. Northcott PA, Fernandez L, Hagan JP, et al. The miR-17/92 polycistron is up-regulated in sonic hedgehog-driven medulloblastomas and induced by N-myc in sonic hedgehog-treated cerebellar neural precursors. Cancer Res 2009;69:3249-55.
63. Hellebrekers DM, Melotte V, Vire E, et al. Identification of epigenetically silenced genes in tumor endothelial cells. Cancer Res 2007;67:4138-48. (Pubitemid 46815059)