Let-7 represses Nr6a1 and a mid-gestation developmental program in adult fibroblasts

Genes and Development

Volumn 27, Issue 8, 2013, Pages 941-954

  Gurtan, Allan M ^a   Ravi, Arvind ^b   Rahl, Peter B ^c   Bosson, Andrew D ^a,b   Jnbaptiste, Courtney K ^a,b   Bhutkar, Arjun ^a   Whittaker, Charles A ^a   Young, Richard A ^c   Sharp, Phillip A ^a,b  

^a David H Koch Institute for Integrative Cancer Research   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Cancer; Dicer; Embryo; Let 7; MiRNAs; Oncofetal

Indexed keywords

DICER; LET 7; MICRORNA; NUCLEAR RECEPTOR NR6A1; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER INHIBITION; CELL TYPE; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; GESTATIONAL AGE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; ONCOGENE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN TARGETING; TRANSCRIPTION TERMINATION;

ANIMALS; ANTIGENS, NEOPLASM; CELL LINE; DEAD-BOX RNA HELICASES; FIBROBLASTS; GENE DELETION; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; MESENCHYMAL STROMAL CELLS; MICE; MICRORNAS; NUCLEAR RECEPTOR SUBFAMILY 6, GROUP A, MEMBER 1; PROTEIN BINDING; RIBONUCLEASE III;

MURINAE;

EID: 84876926693     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.215376.113     Document Type: Article

References (69)

1. Alajez NM, Shi W, Wong D, Lenarduzzi M, Waldron J, Weinreb I, Liu FF. 2012. Lin28b promotes head and neck cancer progression via modulation of the insulin-like growth factor survival pathway. Oncotarget 3: 1641-1652.
2. Ambros V. 2011. MicroRNAs and developmental timing. Curr Opin Genet Dev 21: 511-517.
3. Andl T, Murchison EP, Liu F, Zhang Y, Yunta-Gonzalez M, Tobias JW, Andl CD, Seykora JT, Hannon GJ, Millar SE. 2006. The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles. Curr Biol 16: 1041-1049.
4. Bartel DP, Chen CZ. 2004. Micromanagers of gene expression: The potentially widespread influence ofmetazoanmicroRNAs. Nat Rev Genet 5: 396-400.
5. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV, Hannon GJ. 2003. Dicer is essential for mouse development. Nat Genet 35: 215-217.
6. Boyerinas B, Park SM, Shomron N, Hedegaard MM, Vinther J, Andersen JS, Feig C, Xu J, Burge CB, Peter ME. 2008. Identification of let-7-regulated oncofetal genes. Cancer Res 68: 2587-2591.
7. Boyerinas B, Park SM, Hau A, Murmann AE, Peter ME. 2010. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer 17: F19-F36.
8. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. 2003. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113: 25-36.
9. Calabrese JM, Seila AC, Yeo GW, Sharp PA. 2007. RNA sequence analysis defines Dicer's role in mouse embryonic stem cells. Proc Natl Acad Sci 104: 18097-18102.
10. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITSCLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
11. Chung AC, Katz D, Pereira FA, Jackson KJ, DeMayo FJ, Cooney AJ, O'Malley BW. 2001. Loss of orphan receptor germ cell nuclear factor function results in ectopic development of the tail bud and a novel posterior truncation. Mol Cell Biol 21: 663-677.
12. Colas AR, McKeithan WL, Cunningham TJ, Bushway PJ, Garmire LX, Duester G, Subramaniam S, Mercola M. 2012. Wholegenome microRNA screening identifies let-7 and mir-18 as regulators of germ layer formation during early embryogenesis. Genes Dev 26: 2567-2579.
13. David R, Joos TO, Dreyer C. 1998. Anteroposterior patterning and organogenesis of Xenopus laevis require a correct dose of germ cell nuclear factor (xGCNF). Mech Dev 79: 137-152.
14. Dugas JC, Cuellar TL, Scholze A, Ason B, Ibrahim A, Emery B, Zamanian JL, Foo LC, McManus MT, Barres BA. 2010. Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination. Neuron 65: 597-611.
15. Ebert MS, Sharp PA. 2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149: 515-524.
16. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, Battista S, Ciarmiello A, Pallante P, Arra C, Melillo RM, et al. 2006. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 9: 459-471.
17. Frost RJ, Olson EN. 2011. Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci 108: 21075-21080.
18. Fuhrmann G, Chung AC, Jackson KJ, Hummelke G, Baniahmad A, Sutter J, Sylvester I, Scholer HR, Cooney AJ. 2001. Mouse germline restriction of Oct4 expression by germ cell nuclear factor. Dev Cell 1: 377-387.
19. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: An expanding universe. Nat Rev Genet 10: 94-108.
20. Gu P, LeMenuet D, Chung AC, Mancini M, Wheeler DA, Cooney AJ. 2005. Orphan nuclear receptor GCNF is required for the repression of pluripotency genes during retinoic acidinduced embryonic stem cell differentiation. Mol Cell Biol 25: 8507-8519.
21. Gurtan AM, Sharp PA. 2013. The role of miRNAs in regulating gene expression networks. J Mol Biol. doi: 10.1016/j.jmb.2013.03.007.
22. Gurtan AM, Lu V, Bhutkar A, Sharp PA. 2012. In vivo structure-function analysis of human Dicer reveals directional processing of precursor miRNAs. RNA 18: 1116-1122.
23. Hammell CM, Karp X, Ambros V. 2009. A feedback circuit involving let-7-familymiRNAs and DAF-12 integrates environmental signals and developmental timing in Caenorhabditis elegans. Proc Natl Acad Sci 106: 18668-18673.
24. Hansen TV, Hammer NA, Nielsen J, Madsen M, Dalbaeck C, Wewer UM, Christiansen J, Nielsen FC. 2004. Dwarfism and impaired gut development in insulin-like growth factor II mRNA-binding protein 1-deficient mice. Mol Cell Biol 24: 4448-4464.
25. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ. 2005. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci 102: 10898-10903.
26. Herranz H, Cohen SM. 2010. MicroRNAs and gene regulatory networks: Managing the impact of noise in biological systems. Genes Dev 24: 1339-1344.
27. Hirning-Folz U, Wilda M, Rippe V, Bullerdiek J, Hameister H. 1998. The expression pattern of the Hmgic gene during development. Genes Chromosomes Cancer 23: 350-357.
28. Irie N, Kuratani S. 2011. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2: 248.
29. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. 2005. RAS is regulated by the let-7 microRNA family. Cell 120: 635-647.
30. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, Wilson M, Wang X, Shelton J, Shingara J, et al. 2007. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 67: 7713-7722.
31. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K. 2005. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501.
32. Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, Kim CG, Cantor AB, Orkin SH. 2010. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143: 313-324.
33. Koralov SB, Muljo SA, Galler GR, Krek A, Chakraborty T, Kanellopoulou C, Jensen K, Cobb BS, Merkenschlager M, Rajewsky N, et al. 2008. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132: 860-874.
34. Lee YS, Dutta A. 2007. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 21: 1025-1030.
35. Lee RC, Feinbaum RL, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
36. Leung AK, Young AG, Bhutkar A, Zheng GX, Bosson AD, Nielsen CB, Sharp PA. 2011. Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat Struct Mol Biol 18: 237-244.
37. Li Z, Gilbert JA, Zhang Y, Zhang M, Qiu Q, Ramanujan K, Shavlakadze T, Eash JK, Scaramozza A, Goddeeris MM, et al. 2012. An HMGA2-IGF2BP2 axis regulates myoblast proliferation and myogenesis. Dev Cell 23: 1176-1188.
38. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, et al. 2008. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533.
39. Mayr C, Bartel DP. 2009. Widespread shortening of 39UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684.
40. Mayr C, Hemann MT, Bartel DP. 2007. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315: 1576-1579.
41. Melton C, Judson RL, Blelloch R. 2010. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463: 621-626.
42. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, Rajewsky K. 2005. Aberrant T cell differentiation in the absence of Dicer. J Exp Med 202: 261-269.
43. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ. 2005. Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci 102: 12135-12140.
44. Nimmo RA, Slack FJ. 2009. An elegant miRror: MicroRNAs in stem cells, developmental timing and cancer. Chromosoma 118: 405-418.
45. O'Rourke JR, Georges SA, Seay HR, Tapscott SJ, McManus MT, Goldhamer DJ, Swanson MS, Harfe BD. 2007. Essential role for Dicer during skeletal muscle development. Dev Biol 311: 359-368.
46. Peeper DS, Shvarts A, Brummelkamp T, Douma S, Koh EY, Daley GQ, Bernards R. 2002. A functional screen identifies hDRIL1 as an oncogene that rescues RAS-induced senescence. Nat Cell Biol 4: 148-153.
47. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141: 432-445.
48. Ravi A, Gurtan AM, Kumar MS, Bhutkar A, Chin C, Lu V, Lees JA, Jacks T, Sharp PA. 2012. Proliferation and tumorigenesis of a murine sarcoma cell line in the absence of DICER1. Cancer Cell 21: 848-855.
49. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906.
50. Schulman BR, Esquela-Kerscher A, Slack FJ. 2005. Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev Dyn 234: 1046-1054.
51. Shapiro JS, Langlois RA, Pham AM, Tenoever BR. 2012. Evidence for a cytoplasmic microprocessor of pri-miRNAs. RNA 18: 1338-1346.
52. Taher L, Collette NM, Murugesh D, Maxwell E, Ovcharenko I, Loots GG. 2011. Global gene expression analysis of murine limb development. PLoS ONE 6: e28358.
53. Takebe A, Era T, Okada M, Martin Jakt L, Kuroda Y, Nishikawa S. 2006. Microarray analysis of PDGFR a+ populations in ES cell differentiation culture identifies genes involved in differentiation of mesoderm and mesenchyme including ARID3b that is essential for development of embryonic mesenchymal cells. Dev Biol 293: 25-37.
54. Tessier CR, Doyle GA, Clark BA, Pitot HC, Ross J. 2004. Mammary tumor induction in transgenic mice expressing an RNA-binding protein. Cancer Res 64: 209-214.
55. Trang P, Medina PP, Wiggins JF, Ruffino L, Kelnar K, Omotola M, Homer R, Brown D, Bader AG, Weidhaas JB, et al. 2010. Regression of murine lung tumors by the let-7 microRNA. Oncogene 29: 1580-1587.
56. Viswanathan SR, Daley GQ. 2010. Lin28: A microRNA regulator with a macro role. Cell 140: 445-449.
57. Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, O'Sullivan M, Lu J, Phillips LA, Lockhart VL, et al. 2009. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet 41: 843-848.
58. Vitobello A, Ferretti E, Lampe X, Vilain N, Ducret S, Ori M, Spetz JF, Selleri L, Rijli FM. 2011. Hox and Pbx factors control retinoic acid synthesis during hindbrain segmentation. Dev Cell 20: 469-482.
59. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R. 2007. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385.
60. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. 2008. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2: 333-344.
61. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW III, et al. 2009. BioGPS: An extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
62. Wu C, Macleod I, Su AI. 2013. BioGPS and MyGene.info: Organizing online, gene-centric information. Nucleic Acids Res 41: D561-D565.
63. Yan ZH, Medvedev A, Hirose T, Gotoh H, Jetten AM. 1997. Characterization of the response element and DNA binding properties of the nuclear orphan receptor germ cell nuclear factor/retinoid receptor-related testis-associated receptor. J Biol Chem 272: 10565-10572.
64. Yi R, O'Carroll D, Pasolli HA, Zhang Z, Dietrich FS, Tarakhovsky A, Fuchs E. 2006. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat Genet 38: 356-362.
65. Zaidi MR, Okada Y, Chada KK. 2006. Misexpression of fulllength HMGA2 induces benign mesenchymal tumors in mice. Cancer Res 66: 7453-7459.
66. Zheng H, Ying H, Wiedemeyer R, Yan H, Quayle SN, Ivanova EV, Paik JH, Zhang H, Xiao Y, Perry SR, et al. 2010. PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 17: 497-509.
67. Zhou X, Benson KF, Ashar HR, Chada K. 1995. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 376: 771-774.
68. Zhu H, Shah S, Shyh-Chang N, Shinoda G, Einhorn WS, Viswanathan SR, Takeuchi A, Grasemann C, Rinn JL, Lopez MF, et al. 2010. Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat Genet 42: 626-630.
69. Zhu H, Shyh-Chang N, Segre AV, Shinoda G, Shah SP, Einhorn WS, Takeuchi A, Engreitz JM, Hagan JP, Kharas MG, et al. 2011. The Lin28/let-7 axis regulates glucose metabolism. Cell 147: 81-94.