Argonaute-3 activates the let-7a passenger strand microRNA

RNA Biology

Volumn 10, Issue 10, 2013, Pages 1631-1643

  Winter, Julia ^a   Diederichs, Sven ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Argonaute 3; Let 7a; MicroRNA; Passenger strand; Thermodynamic stability

Indexed keywords

ARGONAUTE 3 PROTEIN; ARGONAUTE PROTEIN; MICRORNA; REGULATOR PROTEIN; UNCLASSIFIED DRUG; EIF2C3 PROTEIN, HUMAN; HEMIN; MIRNLET7 MICRORNA, HUMAN;

ARTICLE; EMBRYO; HUMAN; HUMAN CELL; REGULATORY MECHANISM; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

ARGONAUTE PROTEINS; HEMIN; HUMANS; MICRORNAS; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84886037550     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.26424     Document Type: Article

References (94)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97; PMID:14744438; http://dx.doi.org/10.1016/S0092-8674 (04) 00045-5
2. 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; PMID:18197166; http://dx.doi.org/10.1038/nrg2290
3. Winter J, Diederichs S. MicroRNA biogenesis and cancer. Methods Mol Biol 2011;676:3-22; PMID:20931386; http://dx.doi.org/10.1007/978-1-60761-863-8-1
4. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009;11:228-34; PMID:19255566; http://dx.doi.org/10.1038/ncb0309-228
5. * species has substantial influence on microRNA and 3' UTR evolution. Nat Struct Mol Biol 2008;15:354-63; PMID:18376413; http://dx.doi.org/10.1038/nsmb.1409 (Pubitemid 351483397)
6. * species. RNA 2011;17:312-26; PMID:2117 7881; http://dx.doi.org/10.1261/rna. 2537911
7. Okamura K, Ladewig E, Zhou L, Lai EC. Functional small RNAs are generated from select miRNA hairpin loops in flies and mammals. Genes Dev 2013;27:778-92; PMID:23535236; http://dx.doi. o r g/10.1101/g a d. 2116 98.11 2
8. Winter J, Link S, Witzigmann D, Hildenbrand C, Previti C, Diederichs S. Loop-miRs: active microRNAs generated from single-stranded loop regions. Nucleic Acids Res 2013;41:5503-12; PMID:23580554; http://dx.doi.org/10.1093/nar/g kt 251
9. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007;129:1401-14; PMID:17604727; http://dx.doi.org/10.1016/j.cell.2007.04.040 (Pubitemid 46970709)
10. * species and their role in myeloid cells. Blood 2011;118:3350-8; PMID:21628414; http://dx.doi.org/10.1182/blood-2010-10-312454
11. Kuchenbauer F, Morin RD, Argiropoulos B, Petriv OI, Griffith M, Heuser M, Yung E, Piper J, Delaney A, Prabhu AL, et al. In-depth characterization of the microRNA transcriptome in a leukemia progression model. Genome Res 2008;18:1787-97; PMID:18849523; http://dx.doi.org/10.1101/gr.077578.108
12. Ro S, Park C, Young D, Sanders KM, Yan W. Tissuedependent paired expression of miRNAs. Nucleic Acids Res 2007;35:5944-53; PMID:17726050; http://dx.doi.org/10.1093/nar/gkm641
13. * with elevated expression in patients with pulmonary tuberculosis. Mol Immunol 2011;48:1084-90; PMID: 21367459; http://dx.doi.org/10.1016/j. molimm.2011.02.001
14. *, an intronic product of the vascular endothelial EGF-like 7 gene, regulates prostein translation and invasiveness of prostate cancer LNCaP cells. J Mol Med (Berl) 2008;86:313-22; PMID:18193184; http://dx.doi.org/10. 1007/s00109-007-0296-9
15. * regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci 2008;28:14341-6; PMID:19118166; http://dx.doi.org/10.1523/JNEUROSCI.2390-08.2008
16. * is linked to the prognosis of malignant pleural mesothelioma. Cancer Res 2010;70:1916-24; PMID:20160038; http://dx.doi.org/10.1158/0008-5472. CAN-09-3993
17. * microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 2009;30:953-9; PMID:19372139; http://dx.doi.org/10.1093/carcin/bgp094
18. * suppresses tumorigenicity of prostate cancer by inhibiting mitochondrial antioxidant enzymes. PLoS One 2010;5:e14356; PMID:21203553; http://dx.doi.org/10.1371/journal. pone.0014356
19. * mediates metabolic shift in breast cancer cells via the PGC-1β/ERR? transcriptional pathway. Cell Metab 2010;12:352-61; PMID:20889127; http://dx.doi.org/10.1016/j. cmet.2010.09.002
20. * regulates the MET proto-oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 2008;283:18158-66; PMID:18456660; http://dx.doi.org/10.1074/jbc. M800186200
21. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003;115:209-16; PMID:14567918; http://dx.doi.org/10.1016/ S0092-8674 (03) 00801-8 (Pubitemid 37329584)
22. Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD. Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003;115:199-208; PMID:145 67 917; http://dx.doi.org/10.1016/S0092-8674 (03) 00759-1 (Pubitemid 37329583)
23. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000;408:86-9; PMID: 11 0 8151 2; http://dx.doi.org/10.1038/35040556
24. Griffiths-Jones S. miRBase: the microRNA sequence database. Methods Mol Biol 2006;342:129-38; PMID:16957372
25. Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA, Jacks T. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A 2008;105:3903-8; PMID:18308936; http://dx.doi.org/10.1073/pnas.0712321105 (Pubitemid 351723497)
26. Esquela-Kerscher A, Trang P, Wiggins JF, Patrawala L, Cheng A, Ford L, Weidhaas JB, Brown D, Bader AG, Slack FJ. The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 2008;7:759-64; PMID:18344688; http://dx.doi.org/10.4161/cc.7.6.5834 (Pubitemid 351520040)
27. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007;21:1025-30; PMID:17437991; http://dx.doi.org/10.1101/ gad.1540407 (Pubitemid 46686471)
28. Mayr C, Hemann MT, Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 2007;315:1576-9; PMID:17322030; http://dx.doi.org/10.1126/science.1137999 (Pubitemid 46449474)
29. Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, Jewell DA, Feig C, Lengyel E, Peter ME. Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci U S A 2007;104:11400-5; PMID:17600087; http://dx.doi.org/10.1073/pnas.0704372104 (Pubitemid 47175152)
30. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, Knuutila S. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma-A miRNA microarray analysis. Genes Chromosomes Cancer 2009;48:615-2 3; PMID: 19 39 6 8 6 4; http://dx.doi.org/10.1002/gcc.20669
31. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, Dang CV, Thomas-Tikhonenko A, Mendell JT. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008;40:43-50; PMID:18066065; http://dx.doi.org/10.1038/ng.2007.30
32. Sampson VB, Rong NH, Han J, Yang Q, Aris V, Soteropoulos P, Petrelli NJ, Dunn SP, Krueger LJ. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 2007;67:9762-70; PMID:17942906; http://dx.doi.org/10.1158/0008-5472. CAN-07-2462 (Pubitemid 47621223)
33. Guil S, Cáceres JF. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat Struct Mol Biol 2007;14:591-6; PMID:17558416; http://dx.doi.org/10.1038/nsmb1250 (Pubitemid 47037061)
34. Michlewski G, Guil S, Semple CA, Cáceres JF. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 2008;32:383-93; PMID:18995836; http://dx.doi.org/10.1016/j. molcel.2008.10.013
35. Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A, Gherzi R, Rosenfeld MG. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009;459:1010-4; PMID:19458619; http://dx.doi.org/10.1038/nature08025
36. Heo I, Joo C, Cho J, Ha M, Han J, Kim VN. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol Cell 2008;32:276-84; PMID:18951094; http://dx.doi.org/10.1016/j. molcel.2008.09.014
37. Höck J, Meister G. The Argonaute protein family. Genome Biol 2008;9:210; PMID:18304383; http://dx.doi.org/10.1186/gb-2008-9-2-210
38. Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 2008;9:22-32; PMID:18073770; http://dx.doi.org/10.1038/ nrm2321
39. Winter J, Diederichs S. Argonaute proteins regulate microRNA stability: Increased microRNA abundance by Argonaute proteins is due to microRNA stabilization. RNA Biol 2011;8:1149-57; PMID: 21941127; http://dx.doi.org/10. 4161/rna.8.6.17665
40. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007;131:1097-108; PMID:18 0 8310 0; http://d x.doi.org/10.1016/j. cell.20 07.10.032 (Pubitemid 350235019)
41. Diederichs S, Jung S, Rothenberg SM, Smolen GA, Mlody BG, Haber DA. Coexpression of Argonaute-2 enhances RNA interference toward perfect match binding sites. Proc Natl Acad Sci U S A 2008;105:9284-9; PMID:18591665; http://dx.doi.org/10.1073/pnas.0800803105
42. O'Carroll D, Mecklenbrauker I, Das PP, Santana A, Koenig U, Enright AJ, Miska EA, Tarakhovsky A. A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev 2007;21:1999-2004; PMID:17626790; http://dx.doi.org/10.1101/gad.1565607 (Pubitemid 47267286)
43. Zhou Y, Chen L, Barlogie B, Stephens O, Wu X, Williams DR, Cartron MA, Van Rhee F, Nair B, Waheed S, et al. High-risk myeloma is associated with global elevation of miRNAs and overexpression of EIF2C2/AGO2. Proc Natl Acad Sci U S A 2010;107:7904-9; PMID:20385818; http://dx.doi.org/10.1073/pnas.0908441107
44. Leuschner PJ, Ameres SL, Kueng S, Martinez J. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep 2006;7:314-20; PMID:16439995; http://dx.doi.org/10.1038/sj.embor.7400637
45. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 2005;123:607-20; PMID:16271386; http://dx.doi.org/10.1016/j. cell.2005.08.044 (Pubitemid 41608464)
46. Rand TA, Petersen S, Du F, Wang X. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 2005;123:621-9; PMID:16271385; http://dx.doi.org/10.1016/j.cell.2005.10.020 (Pubitemid 41608465)
47. Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev 2005;19:2837-48; PMID:16287716; http://dx.doi.org/10.1101/gad.1370605 (Pubitemid 41739969)
48. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010;465:584-9; PMID:20424607; http://dx.doi.org/10.1038/nature09092
49. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 2010;328:1694-8; PMID:20448148; http://dx.doi.org/10.1126/science.1190809
50. Yang JS, Maurin T, Robine N, Rasmussen KD, Jeffrey KL, Chandwani R, Papapetrou EP, Sadelain M, O'Carroll D, Lai EC. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci U S A 2010;107:15163-8; PMID:20699384; http://dx.doi.org/10. 1073/pnas.1006432107
51. Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE. Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 2012;486:541-4; PMID:22722835
52. Hauptmann J, Dueck A, Harlander S, Pfaff J, Merkl R, Meister G. Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nat Struct Mol Biol 2013;20:814-7; PMID:23665583; http://dx.doi.org/10.1038/nsmb. 2577
53. Schürmann N, Trabuco LG, Bender C, Russell RB, Grimm D. Molecular dissection of human Argonaute proteins by DNA shuffling. Nat Struct Mol Biol 2013;20:818-26; PMID:23748378; http://dx.doi.org/10.1038/nsmb.2607
54. Yi R, Doehle BP, Qin Y, Macara IG, Cullen BR. Overexpression of exportin 5 enhances RNA interference mediated by short hairpin RNAs and microR-NAs. RNA 2005;11:220-6; PMID:15613540; http://dx.doi.org/10.1261/rna.7233305 (Pubitemid 40165636)
55. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-8; PMID: 15 9 4 4 70 8; http://dx.doi.org/10. 1038/nature03702 (Pubitemid 40839735)
56. Azuma-Mukai A, Oguri H, Mituyama T, Qian ZR, Asai K, Siomi H, Siomi MC. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci U S A 2008;105:7964-9; PMID:18524951; http://dx.doi.org/10.1073/pnas.0800334105 (Pubitemid 351904690)
57. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T. Molecular characterization of human Argonautecontaining ribonucleoprotein complexes and their bound target mRNAs. RNA 2008;14:2580-96; PMID:18978028; http://dx.doi.org/10.1261/rna.1351608
58. Breving K, Esquela-Kerscher A. The complexities of microRNA regulation: mirandering around the rules. Int J Biochem Cell Biol 2010;42:1316-29; PMID:19800023; http://dx.doi.org/10.1016/j. biocel.2009.09.016
59. Piskounova E, Viswanathan SR, Janas M, LaPierre RJ, Daley GQ, Sliz P, Gregory RI. Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J Biol Chem 2008;283:21310-4; PMID:18550544; http://dx.doi.org/10.1074/jbc. C800108200
60. Förstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 2007;130:287-97; PMID:176 629 4 3; http://dx.doi.org/10.1016/j. cell.2007.05.056 (Pubitemid 47086327)
61. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell 2008;133:116-27; PMID: 18 3 4 23 61; http://dx.doi.org/10.1016/j. cell.2008.02.034
62. Tomari Y, Matranga C, Haley B, Martinez N, Zamore PD. A protein sensor for siRNA asymmetry. Science 2004;306:1377-80; PMID:15550672; http://dx.doi.org/10.1126/scienc e.1102755 (Pubitemid 39532515)
63. Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson EN, Wang S. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23-27-24 clusters. Proc Natl Acad Sci U S A 2011;108:8287-92; PMID: 2153 6 891; http://dx.doi.org/10.1073/pnas.1105254108
64. Westholm JO, Lai EC. Mirtrons: microRNA biogenesis via splicing. Biochimie 2011;93:1897-904; PMID:21712066; http://dx.doi.org/10.1016/j. biochi.2011.06.017
65. Veronese A, Lupini L, Consiglio J, Visone R, Ferracin M, Fornari F, Zanesi N, Alder H, D'Elia G, Gramantieri L, et al. Oncogenic role of miR-483-3p at the IGF2/483 locus. Cancer Res 2010;70:3140-9; PMID:20388800; http://dx.doi.org/10.1158/0008-5472. CAN-09-4456
66. Sangokoya C, Telen MJ, Chi JT. microRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease. Blood 2010;116:4338-48; PMID:20709907; http://dx.doi.org/10.1182/blood-2009-04- 214817
67. Miko E, Margitai Z, Czimmerer Z, Várkonyi I, Dezso B, Lányi A, Bacsó Z, Scholtz B. miR-126 inhibits proliferation of small cell lung cancer cells by targeting SLC7A5. FEBS Lett 2011;585:1191-6; PMID: 214 39283; http://dx.doi.org/10.1016/j. febslet.2011.03.039
68. Kondo N, Toyama T, Sugiura H, Fujii Y, Yamashita H. miR-206 Expression is down-regulated in estrogen receptor alpha-positive human breast cancer. Cancer Res 2008;68:5004-8; PMID:18593897; http://dx.doi.org/10.1158/0008-5472. CAN-08-0180
69. Jones D, Li Y, He Y, Xu Z, Chen H, Min W. Mirtron microRNA-1236 inhibits VEGFR-3 signaling during inflammatory lymphangiogenesis. Arterioscler Thromb Vasc Biol 2012;32:633-42; PMID:22223733; http://dx.doi.org/10.1161/AT V BA H A.111.243576
70. Chen X, Yan Q, Li S, Zhou L, Yang H, Yang Y, Liu X, Wan X. Expression of the tumor suppressor miR-206 is associated with cellular proliferative inhibition and impairs invasion in ERα-positive endometrioid adenocarcinoma. Cancer Lett 2012;314:41-53; PMID: 2198313 0; http://dx.doi.org/10.1016/j. canlet.2011.09.014
71. Addya S, Keller MA, Delgrosso K, Ponte CM, Vadigepalli R, Gonye GE, Surrey S. Erythroidinduced commitment of K562 cells results in clusters of differentially expressed genes enriched for specific transcription regulatory elements. Physiol Genomics 2004;19:117-30; PMID:15252187; http://dx.doi.org/10. 1152/physiolgenomics.00028.2004 (Pubitemid 40039918)
72. Subramani D, Alahari SK. Integrin-mediated function of Rab GTPases in cancer progression. Mol Cancer 2010;9:312; PMID:21143914; http://dx.doi.org/10. 1186/1476-4598-9-312
73. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 2008;133:128-41; PMID:18342362; http://dx.doi.org/10.1016/j.cell.2008.02.033
74. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 2008;49:493-500; PMID:18344228; http://dx.doi.org/10.1093/pcp/pcn043
75. Czech B, Zhou R, Erlich Y, Brennecke J, Binari R, Villalta C, Gordon A, Perrimon N, Hannon GJ. Hierarchical rules for Argonaute loading in Drosophila. Mol Cell 2009;36:445-56; PMID:19917252; http://dx.doi.org/10.1016/j. molcel.2009.09.028
76. * strands into the RNA interference pathway. RNA 2010;16:43-56; PMID:19917635; http://dx.doi.org/10. 1261/rna.1972910
77. Okamura K, Liu N, Lai EC. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol Cell 2009;36:431-44; PMID:19917251; http://dx.doi.org/10.1016/j.molcel.2009.09.027
78. Frank F, Sonenberg N, Nagar B. Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 2010;465:818-22; PMID:20505670; http://dx.doi.org/10.1038/nature09039
79. *-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 2011;42:356-66; PMID:21549312; http://dx.doi.org/10.1016/j. molcel.2011.04.010
80. Czech B, Hannon GJ. Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 2011;12:19-31; PMID: 21116 3 0 5; http://d x.doi.org/10.1038/nrg2916
81. Axtell MJ, Westholm JO, Lai EC. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 2011;12:221; PMID: 21554756; http://dx.doi.org/10.1186/gb-2011-12-4-221
82. Gu S, Jin L, Zhang F, Huang Y, Grimm D, Rossi JJ, Kay MA. Thermodynamic stability of small hairpin RNAs highly influences the loading process of different mammalian Argonautes. Proc Natl Acad Sci U S A 2011;108:9208-13; PMID: 21576 45 9; http://dx.doi.org/10.1073/pnas.1018023108
83. Su H, Trombly MI, Chen J, Wang X. Essential and overlapping functions for mammalian Argonautes in microRNA silencing. Genes Dev 2009;23:304-17; PMID:19174539; http://dx.doi.org/10.1101/g a d.1749 8 0 9
84. Yoda M, Kawamata T, Paroo Z, Ye X, Iwasaki S, Liu Q, Tomari Y. ATP-dependent human RISC assembly pathways. Nat Struct Mol Biol 2010;17:17-23; PMID:19966796; http://dx.doi.org/10.1038/nsmb.1733
85. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008;454:56-61; PMID:18548003; http://dx.doi.org/10.1038/nature07086 (Pubitemid 351931982)
86. Hagan JP, Piskounova E, Gregory RI. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 2009;16:1021-5; PMID:19713958; http://dx.doi.org/10.1038/nsmb.1676
87. Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 2008;14:1539-49; PMID:18566191; http://dx.doi.org/10.1261/rna.1155108
88. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 2008;10:987-93; PMID:18604195; http://dx.doi.org/10.1038/ncb1759
89. Sakamoto S, Aoki K, Higuchi T, Todaka H, Morisawa K, Tamaki N, Hatano E, Fukushima A, Taniguchi T, Agata Y. The NF90-NF45 complex functions as a negative regulator in the microRNA processing pathway. Mol Cell Biol 2009;29:3754-69; PMID:19398578; http://dx.doi.org/10.1128/MCB.01836-08
90. Trabucchi M, Briata P, Filipowicz W, Rosenfeld MG, Ramos A, Gherzi R. How to control miRNA maturation? RNA Biol 2009;6:536-40; PMID:19875945; http://dx.doi.org/10.4161/rna.6.5.10080
91. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008;320:97-100; PMID:18292307; http://dx.doi. or g/10.1126/scienc e.1154040 (Pubitemid 351490762)
92. Yamagata K, Fujiyama S, Ito S, Ueda T, Murata T, Naitou M, Takeyama K, Minami Y, O'Malley BW, Kato S. Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol Cell 2009;36:340-7; PMID:19854141; http://dx.doi.org/ 10.1016/j. molcel.2009.08.017
93. Müller-Tidow C, Diederichs S, Schrader MG, Vogt U, Miller K, Berdel WE, Serve H. Cyclin A1 is highly expressed in aggressive testicular germ cell tumors. Cancer Lett 2003;190:89-95; PMID:12536081; http://dx.doi.org/10.1016/ S0304-3835 (02) 00582-7 (Pubitemid 36106559)
94. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005;33:e179; PMID:16314309; http://dx.doi.org/10.1093/nar/gni178