Role of pri-miRNA tertiary structure in miR-17∼92 miRNA biogenesis

RNA Biology

Volumn 8, Issue 6, 2011, Pages 1105-1114

  Chaulk, Steven G ^a   Thede, Gina L ^a   Kent, Oliver A ^c   Xu, Zhizhong ^a   Gesner, Emily M ^a   Veldhoen, Richard A ^a   Khanna, Suneil K ^a   Goping, Ing Swie ^a   MacMillan, Andrew M ^a   Mendell, Joshua T ^d   Young, Howard S ^a,b   Fahlman, Richard P ^a,b   Glover, J N Mark ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Drosha; miRNA biogenesis; miRNA cluster; Pri miRNA structure

Indexed keywords

ALPHA5 INTEGRIN; MICRORNA; MICRORNA 17 92; PRIMARY MICRORNA; UNCLASSIFIED DRUG; DROSHA PROTEIN, HUMAN; MESSENGER RNA; MIRN17 MICRORNA, HUMAN; MIRN92 MICRORNA, HUMAN; RIBONUCLEASE III;

ARTICLE; HUMAN; HUMAN CELL; RNA PROCESSING; RNA SEQUENCE; RNA STRUCTURE; RNA SYNTHESIS; STRUCTURE ANALYSIS; BIOGENESIS; CELL LINE; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; RNA FOLDING;

BASE SEQUENCE; BIOGENESIS; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN ALPHA5; MICRORNAS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NUCLEIC ACID CONFORMATION; RIBONUCLEASE III; RNA FOLDING; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

EID: 81255210927     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.8.6.17410     Document Type: Article

References (62)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism and function. Cell 2004; 116:281-97.
2. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008; 9:219-30. (Pubitemid 351301826)
3. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, 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)
4. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med 2009; 60:167-79.
5. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005; 6:376-85. (Pubitemid 40637855)
6. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008; 133:217-22. (Pubitemid 351508308)
7. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406-15. (Pubitemid 37442169)
8. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009; 10:126-39.
9. Kim VN. MicroRNA precursors in motion: exportin-5 mediates their nuclear export. Trends Cell Biol 2004; 14:156-9. (Pubitemid 38447114)
10. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-14.
11. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006; 6:259-69.
12. Kent OA, Mendell JT. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene 2006; 25:6188-96. (Pubitemid 44527849)
13. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435:828-33. (Pubitemid 40839734)
14. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006; 38:1060-5. (Pubitemid 44325933)
15. Uziel T, Karginov FV, Xie S, Parker JS, Wang YD, Gajjar A, et al. The miR-17~92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma. Proc Natl Acad Sci USA 2009; 106:2812-7.
16. Yu J, Wang F, Yang GH, Wang FL, Ma YN, Du ZW, et al. Human microRNA clusters: genomic organization and expression profile in leukemia cell lines. Biochem Biophys Res Commun 2006; 349:59-68. (Pubitemid 44331762)
17. Zhang Y, Zhang R, Su B. Diversity and evolution of MicroRNA gene clusters. Sci China C Life Sci 2009; 52:261-6.
18. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, et al. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006; 125:887-901. (Pubitemid 43810154)
19. Zeng Y, Cullen BR. Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences. J Biol Chem 2005; 280:27595-603. (Pubitemid 41076871)
20. Zeng Y, Yi R, Cullen BR. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J 2005; 24:138-48. (Pubitemid 40188471)
21. Trujillo RD, Yue SB, Tang Y, O'Gorman WE, Chen CZ. The potential functions of primary microRNAs in target recognition and repression. EMBO J 29:3272-85.
22. Liu G, Min H, Yue S, Chen CZ. Pre-miRNA loop nucleotides control the distinct activities of mir-181a-1 and mir-181c in early T cell development. PLoS One 2008; 3:3592.
23. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, et al. Functional links between clustered microRNAs: suppression of cell cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009; 37:1672-81.
24. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 2008; 68:8191-4.
25. Lee Y, Kim VN. In vitro and in vivo assays for the activity of Drosha complex. Methods Enzymol 2007; 427:89-106.
26. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003; 425:415-9. (Pubitemid 37187272)
27. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004; 432:235-40. (Pubitemid 39545855)
28. Buchmueller KL, Webb AE, Richardson DA, Weeks KM. A collapsed non-native RNA folding state. Nat Struct Biol 2000; 7:362-6. (Pubitemid 30249996)
29. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007; 129:1401-14. (Pubitemid 46970709)
30. Feng Y, Zhang X, Song Q, Li T, Zeng Y. Drosha processing controls the specificity and efficiency of global microRNA expression. Biochim Biophys Acta.
31. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435:839-43. (Pubitemid 40839736)
32. Stahley MR, Adams PL, Wang J, Strobel SA. Structural metals in the group I intron: a ribozyme with a multiple metal ion core. J Mol Biol 2007; 372:89-102. (Pubitemid 47223219)
33. Batey RT, Rambo RP, Doudna JA. Tertiary Motifs in RNA Structure and Folding. Angew Chem Int Ed Engl 1999; 38:2326-43. (Pubitemid 29399554)
34. Battle DJ, Doudna JA. Specificity of RNA-RNA helix recognition. Proc Natl Acad Sci USA 2002; 99:11676-81. (Pubitemid 34994458)
35. Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, et al. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 2000; 16:1046-7. (Pubitemid 32051021)
36. Kieft JS, Zhou K, Jubin R, Murray MG, Lau JY, Doudna JA. The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J Mol Biol 1999; 292:513-29. (Pubitemid 29457315)
37. Chaulk SG, MacMillan AM. Kinetic Footprinting of an RNA-Folding Pathway Using Peroxynitrous Acid. Angew Chem Int Ed Engl 2000; 39:521-3. (Pubitemid 30101728)
38. Latham JA, Cech TR. Defining the inside and outside of a catalytic RNA molecule. Science 1989; 245:276-82. (Pubitemid 19196644)
39. Chaulk SG, MacMillan AM. Characterization of the Tetrahymena ribozyme folding pathway using the kinetic footprinting reagent peroxynitrous acid. Biochemistry 2000; 39:2-8. (Pubitemid 30033313)
40. Hyeon C, Dima RI, Thirumalai D. Size, shape and flexibility of RNA structures. J Chem Phys 2006; 125:194905.
41. Ballarino M, Pagano F, Girardi E, Morlando M, Cacchiarelli D, Marchioni M, et al. Coupled RNA processing and transcription of intergenic primary microRNAs. Mol Cell Biol 2009; 29:5632-8.
42. Morlando M, Ballarino M, Gromak N, Pagano F, Bozzoni I, Proudfoot NJ. Primary microRNA transcripts are processed co-transcriptionally. Nat Struct Mol Biol 2008; 15:902-9.
43. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009; 324:1710-3.
44. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, et al. The myc-miR-17~92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res 70:8233-46.
45. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007; 282:2130-4. (Pubitemid 47076737)
46. 1 checkpoint to regulate cell cycle progression. Oncogene 2009; 28:140-5.
47. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137:1005-17.
48. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 2009; 8:129-38.
49. Guttilla IK, White BA. Coordinate regulation of FOXO1 by miR-27a, miR-96 and miR-182 in breast cancer cells. J Biol Chem 2009; 284:23204-16.
50. Ji J, Zhang J, Huang G, Qian J, Wang X, Mei S. Overexpressed microRNA-27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation. FEBS Lett 2009; 583:759-66.
51. Liu T, Tang H, Lang Y, Liu M, Li X. MicroRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett 2009; 273:233-42.
52. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O'Day E, et al. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell cycle genes via binding to "seedless" 3'UTR microRNA recognition elements. Mol Cell 2009; 35:610-25.
53. Lal A, Pan Y, Navarro F, Dykxhoorn DM, Moreau L, Meire E, et al. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat Struct Mol Biol 2009; 16:492-8.
54. Huang S, He X, Ding J, Liang L, Zhao Y, Zhang Z, et al. Upregulation of miR-23a approximately 27a approximately 24 decreases transforming growth factor-beta-induced tumor-suppressive activities in human hepatocellular carcinoma cells. Int J Cancer 2008; 123:972-8. (Pubitemid 352032429)
55. Pratt ZL, Kuzembayeva M, Sengupta S, Sugden B. The microRNAs of Epstein-Barr Virus are expressed at dramatically differing levels among cell lines. Virology 2009; 386:387-97.
56. Ludtke SJ, Baldwin PR, Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 1999; 128:82-97. (Pubitemid 30013436)
57. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, Ladjadj M, et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 1996; 116:190-9. (Pubitemid 26093143)
58. Bottcher B, Wynne SA, Crowther RA. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 1997; 386:88-91. (Pubitemid 27130926)
59. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004; 25:1605-12.
60. Graham FL, van der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 1973; 52:456-67.
61. Tsuge M, Hamamoto R, Silva FP, Ohnishi Y, Chayama K, Kamatani N, et al. A variable number of tandem repeats polymorphism in an E2F-1 binding element in the 5' flanking region of SMYD3 is a risk factor for human cancers. Nat Genet 2005; 37:1104-7. (Pubitemid 41486663)
62. West S, Gromak N, Norbury CJ, Proudfoot NJ. Adenylation and exosome-mediated degradation of cotranscriptionally cleaved pre-messenger RNA in human cells. Mol Cell 2006; 21:437-43. (Pubitemid 43163538)