Myc-regulated microRNAs attenuate embryonic stem cell differentiation

EMBO Journal

Volumn 28, Issue 20, 2009, Pages 3157-3170

  Lin, Chin Hsing ^a   Jackson, Aimee L ^b,c   Guo, Jie ^b   Linsley, Peter S ^b,c   Eisenman, Robert N ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b ROSETTA INPHARMATICS   (United States)

^c REGULUS THERAPEUTICS   (United States)

Author keywords

Differentiation; Embryonic stem cell; MicroRNA; Myc

Indexed keywords

MICRORNA; MYC PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME; NONHUMAN; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ASSAY; REGULATORY MECHANISM;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; EMBRYONIC STEM CELLS; IMMUNOHISTOCHEMISTRY; MICE; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-MYC;

MURINAE;

EID: 70350302617     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.254     Document Type: Article

References (82)

1. Adhikary S, Eilers M (2005) Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 6: 635-645
2. Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, Larsson LG, Wright AP (2005) c-Myc associates with ribosomal DNA and activates RNA poly-merase I transcription. Nat Cell Biol 7: 303-310
3. Arnold I, Watt FM (2001) c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr Biol 11 : 558-568
4. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538
5. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326
6. Boscher C, Mege RM (2008) Cadherin-11 interacts with the FGF receptor and induces neurite outgrowth through associated downstream signalling. Cell Signal 20: 1061-1072
7. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353 (Pubitemid 44050199)
8. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136
9. Burt RK, Verda L, Kim DA, Oyama Y, Luo K, Link C (2004) Embryonic stem cells as an alternate marrow donor source: engraftment without graft-versus-host disease. J Exp Med 199: 895-904
10. 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 USA 104: 18097-18102
11. Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866
12. Cao X, Pfaff SL, Gage FH (2007) A functional study of miR-124 in the developing neural tube. Genes Dev 21: 531-536
13. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301: 336-338
14. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, Dalton S (2005) LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132: 885-896
15. Chang TC, Mendell JT (2007) microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet 8: 215-239
16. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, Dang CV, Thomas-Tikhonenko A, Mendell JT (2008) Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 40: 43-50
17. Chen C, Ridzon D, Lee CT, Blake J, Sun Y, Strauss WM (2007) Defining embryonic stem cell identity using differentiation-related microRNAs and their potential targets. Mamm Genome 18: 316-327
18. Chen CZ, Li L, Lodish HF, Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86
19. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK et al (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117
20. Cole MD, Nikiforov MA (2006) Transcriptional activation by the Myc oncoprotein. Curr Top Microbiol Immunol 302: 33-50
21. Dubois NC, Adolphe C, Ehninger A, Wang RA, Robertson EJ, Trumpp A (2008) Placental rescue reveals a sole requirement for c-Myc in embryonic erythroblast survival and hematopoietic stem cell function. Development 135: 2455-2465
22. Dykxhoorn DM, Novina CD, Sharp PA (2003) Killing the messenger: short RNAs that silence gene expression. Nat Rev Mol Cell Biol 4: 457-467
23. Eilers M, Eisenman RN (2008) Myc?s broad reach. Genes Dev 22: 2755-2766
24. Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269
25. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B (2001) Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 15: 2069-2082
26. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van Eyk JE, Mendell JT, Dang CV (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458: 762-765
27. Gomez-Roman N, Grandori C, Eisenman RN, White RJ (2003) Direct activation of RNA polymerase III transcription by c-Myc. Nature 421: 290-294
28. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ (2005) c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 7: 311-318
29. Grewal SI, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 301: 798-802
30. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ (2007) A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134
31. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM (2005) A microRNA polycistron as a potential human oncogene. Nature 435: 828-833
32. Houbaviy HB, Murray MF, Sharp PA (2003) Embryonic stem cell-specific MicroRNAs. Dev Cell 5: 351-358
33. Hwang HW, Mendell JT (2007) MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 96 (Suppl): R40-R44
34. Ibarra I, Erlich Y, Muthuswamy SK, Sachidanandam R, Hannon GJ (2007) A role for microRNAs in maintenance of mouse mammary epithelial progenitor cells. Genes Dev 21 : 3238-3243
35. Judson RL, Babiarz JE, Venere M, Blelloch R (2009) Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 27: 459-461
36. 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
37. Kato M, Slack FJ (2008) microRNAs: small molecules with big roles-C. elegans to human cancer. Biol Cell 100: 71-81
38. Kim J, Chu J, Shen X, Wang J, Orkin SH (2008) An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061
39. Kleine-Kohlbrecher D, Adhikary S, Eilers M (2006) Mechanisms of transcriptional repression by Myc. Curr Top Microbiol Immunol 302: 51-62
40. Knoepfler PS, Cheng PF, Eisenman RN (2002) N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 16: 2699-2712
41. Kushida T, Inaba M, Hisha H, Ichioka N, Esumi T, Ogawa R, Iida H, Ikehara S (2001) Intra-bone marrow injection of allogeneic bone marrow cells: a powerful new strategy for treatment of intractable autoimmune diseases in MRL/lpr mice. Blood 97: 3292-3299
42. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K et al (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313 (Pubitemid 44313811)
43. Lien WH, Gelfand VI, Vasioukhin V (2008) Alpha-E-catenin binds to dynamitin and regulates dynactin-mediated intracellular traffic. J Cell Biol 183: 989-997
44. Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP (2003) Vertebrate microRNA genes. Science 299: 1540
45. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773
46. Liu N, Bezprozvannaya S, Williams AH, Qi X, Richardson JA, Bassel-Duby R, Olson EN (2008) microRNA-133a regulates cardi-omyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 22: 3242-3254
47. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872
48. Lotterman CD, Kent OA, Mendell JT (2008) Functional integration of microRNAs into oncogenic and tumor suppressor pathways. Cell Cycle 7: 2493-2499
49. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533
50. Medina PP, Slack FJ (2008) microRNAs and cancer: an overview. Cell Cycle 7: 2485-2492
51. Mendell JT (2005) MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle 4: 1179-1184
52. Mizui M, Kikutani H (2008) Neuropilin-1: the glue between regulatory T cells and dendritic cells? Immunity 28: 302-303
53. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci USA 102: 12135-12140
54. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2008) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26: 101-106
55. O?Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435: 839-843
56. Okubo T, Knoepfler PS, Eisenman RN, Hogan BL (2005) Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132: 1363-1374
57. Ormestad M, Astorga J, Carlsson P (2004) Differences in the embryonic expression patterns of mouse Foxf1 and -2 match their distinct mutant phenotypes. Dev Dyn 229: 328-333
58. Ormestad M, Astorga J, Landgren H, Wang T, Johansson BR, Miura N, Carlsson P (2006) Foxf1 and Foxf2 control murine gut development by limiting mesenchymal Wnt signaling and promoting extracellular matrix production. Development 133: 833-843
59. Pellet-Many C, Frankel P, Jia H, Zachary I (2008) Neuropilins: structure, function and role in disease. Biochem J 411: 211-226
60. Pickford AS, Cogoni C (2003) RNA-mediated gene silencing. Cell Mol Life Sci 60: 871-882
61. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P, Stoffel M (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432: 226-230
62. Raymond CK, Roberts BS, Garrett-Engele P, Lim LP, Johnson JM (2005) Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs. RNA 1 1 : 1737-1744
63. Sampson VB, Rong NH, Han J, Yang Q, Aris V, Soteropoulos P, Petrelli NJ, Dunn SP, Krueger LJ (2007) MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 67: 9762-9770
64. Scacheri PC, Crawford GE, Davis S (2006a) Statistics for ChIP-chip and DNase hypersensitivity experiments on NimbleGen arrays. Methods Enzymol 411 : 270-282
65. Scacheri PC, Davis S, Odom DT, Crawford GE, Perkins S, Halawi MJ, Agarwal SK, Marx SJ, Spiegel AM, Meltzer PS, Collins FS (2006b) Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet 2: e51
66. Schwarz Q, Vieira JM, Howard B, Eickholt BJ, Ruhrberg C (2008) Neuropilin 1 and 2 control cranial gangliogenesis and axon guidance through neural crest cells. Development 135: 1605-1613
67. Solter D, Knowles BB (1978) Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 75: 5565-5569
68. Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9: 219-230
69. Suh MR, Lee Y, Kim JY, Kim SK, Moon SH, Lee JY, Cha KY, Chung HM, Yoon HS, Moon SY, Kim VN, Kim KS (2004) Human embryonic stem cells express a unique set of microRNAs. Dev Biol 270: 488-498
70. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872
71. Taniguchi H, Kawauchi D, Nishida K, Murakami F (2006) Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain. Development 133: 1923-1931
72. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J (2008) Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152
73. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455: 1124-1128
74. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM (2006) Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 20: 2202-2207
75. Vasudevan S, Tong Y, Steitz JA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318: 1931-1934
76. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21: 744-749
77. Viswanathan SR, Daley GQ, Gregory RI (2008) Selective blockade of microRNA processing by Lin28. Science 320: 97-100
78. Wang T, Tamakoshi T, Uezato T, Shu F, Kanzaki-Kato N, Fu Y, Koseki H, Yoshida N, Sugiyama T, Miura N (2003) Forkhead transcription factor Foxf2 (LUN)-deficient mice exhibit abnormal development of secondary palate. Dev Biol 259: 83-94
79. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R (2008) Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 40: 1478-1483
80. 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
81. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R (2007) In vitro repro-gramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324
82. Ziegelbauer JM, Sullivan CS, Ganem D (2009) Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat Genet 41: 130-134