The microRNA machinery

Advances in Experimental Medicine and Biology

Volumn 887, Issue , 2015, Pages 15-30

  Roberts, Thomas C ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

AGO2; Argonaute; DGCR8; Dicer; DICER1; Drosha; Exportin 5; microRNA; XPO5

Indexed keywords

ARGONAUTE 2 PROTEIN; DICER; DICER1; DIGEORGE SYNDROME CRITICAL REGION 8 PROTEIN; EXPORTIN 5; MICRORNA; NUCLEIC ACID BINDING PROTEIN; PROTEIN DROSHA; RNA INDUCED SILENCING COMPLEX; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; CARBOXYPEPTIDASE; DEAD BOX PROTEIN; DICER1 PROTEIN, HUMAN; EIF2C2 PROTEIN, HUMAN; KARYOPHERIN; RIBONUCLEASE III; SCPEP1 PROTEIN, HUMAN; XPO5 PROTEIN, HUMAN;

CAENORHABDITIS ELEGANS; CELL NUCLEUS; CYTOPLASM; DROSOPHILA MELANOGASTER; GENE SILENCING; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA ANALYSIS; RNA CLEAVAGE; RNA DEGRADATION; RNA PROCESSING; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSPORT; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN CONFORMATION;

ANIMALS; ARGONAUTE PROTEINS; CARBOXYPEPTIDASES; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; HUMANS; KARYOPHERINS; MICRORNAS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; RIBONUCLEASE III; RNA CLEAVAGE; RNA TRANSPORT;

EID: 84949806444     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-3-319-22380-3_2     Document Type: Chapter

References (100)

1. Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol. 2005; 15: 331-41.
2. Roberts TC, Wood MJA. Therapeutic targeting of non-coding RNAs. Essays Biochem. 2013; 54: 127-45.
3. Cacchiarelli D, Incitti T, Martone J, Cesana M, Cazzella V, Santini T, Sthandier O, Bozzoni I. miR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy. EMBO Rep. 2011; 12: 136-41.
4. Wang L, Zhou L, Jiang P, Lu L, Chen X, Lan H, Guttridge DC, Sun H, Wang H. Loss of miR-29 in myoblasts contributes to dystrophic muscle pathogenesis. Mol Ther. 2012; 20: 1222-33.
5. Roberts TC, Godfrey C, McClorey G, Vader P, Briggs D, Gardiner C, Aoki Y, Sargent I, Morgan JE, Wood MJA. Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res. 2013; 41: 9500-13.
6. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008; 105: 10513-8.
7. Gilad S, Meiri E, Yogev Y, et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008; 3, e3148.
8. Lee Y, Kim M, Han J, Yeom K-H, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004; 23: 4051-60.
9. Cai X, Hagedorn CH, Cullen BR. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA. 2004; 10: 1957-66.
10. Kim Y-K, Kim VN. Processing of intronic microRNAs. EMBO J. 2007; 26: 775-83.
11. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001; 294: 853-8.
12. Mogilyansky E, Rigoutsos I. The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ. 2013; 20: 1603-14.
13. Lee Y, Jeon K, Lee J-T, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002; 21: 4663-70.
14. Olsen PH, Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol. 1999; 216: 671-80.
15. Doench JG, Sharp PA. Specificity of microRNA target selection in translational repression. Genes Dev. 2004; 18: 504-11.
16. Ohler U, Yekta S, Lim LP, Bartel DP, Burge CB. Patterns of flanking sequence conservation and a characteristic upstream motif for microRNA gene identification. RNA. 2004; 10: 1309-22.
17. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010; 466: 835-40.
18. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell. 2005; 123: 631-40.
19. Roberts TC. The microRNA biology of the mammalian nucleus. Mol Ther Nucleic Acids. 2014; 3: e188.
20. Roberts TC, Wood MJ. Non-canonical microRNA biogenesis and function. In: Arbuthnot P, Weinberg M, editors. Applied RNAi: from fundamental research to therapeutic applications. Norfolk: Caister Academic Press; 2014. p. 19-42.
21. Gregory RI, Yan K-P, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature. 2004; 432: 235-40.
22. Wu H, Xu H, Miraglia LJ, Crooke ST. Human RNase III is a 160-kDa protein involved in preribosomal RNA processing. J Biol Chem. 2000; 275: 36957-65.
23. Lee Y, Ahn C, Han J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003; 425: 415-9.
24. Dalzell JJ, Warnock ND, Stevenson MA, Mousley A, Fleming CC, Maule AG. Short interfering RNA-mediated knockdown of drosha and pasha in undifferentiated Meloidogyne incognita eggs leads to irregular growth and embryonic lethality. Int J Parasitol. 2010; 40: 1303-10.
25. Wu Q, Song R, Ortogero N, et al. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem. 2012; 287: 25173-90.
26. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 2001; 409: 363-6.
27. Han J, Lee Y, Yeom K-H, Kim Y-K, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004; 18: 3016-27.
28. Wilson DI, Burn J, Scambler P, Goodship J. DiGeorge syndrome: part of CATCH 22. J Med Genet. 1993; 30: 852-6.
29. Shiohama A, Sasaki T, Noda S, Minoshima S, Shimizu N. Molecular cloning and expression analysis of a novel gene DGCR8 located in the DiGeorge syndrome chromosomal region. Biochem Biophys Res Commun. 2003; 304: 184-90.
30. Denli AM, Tops BBJ, Plasterk RHA, Ketting RF, Hannon GJ. Processing of primary microRNAs by the microprocessor complex. Nature. 2004; 432: 231-5.
31. Landthaler M, Yalcin A, Tuschl T. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol. 2004; 14: 2162-7.
32. 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.
33. Han J, Lee Y, Yeom K-H, Nam J-W, Heo I, Rhee J-K, Sohn SY, Cho Y, Zhang B-T, Kim VN. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell. 2006; 125: 887-901.
34. Mueller GA, Miller MT, Derose EF, Ghosh M, London RE, Hall TMT. Solution structure of the Drosha double-stranded RNA-binding domain. Silence. 2010; 1: 2.
35. Sohn SY, Bae WJ, Kim JJ, Yeom K-H, Kim VN, Cho Y. Crystal structure of human DGCR8 core. Nat Struct Mol Biol. 2007; 14: 847-53.
36. Senturia R, Faller M, Yin S, Loo JA, Cascio D, Sawaya MR, Hwang D, Clubb RT, Guo F. Structure of the dimerization domain of DiGeorge critical region 8. Protein Sci. 2010; 19: 1354-65.
37. Faller M, Matsunaga M, Yin S, Loo JA, Guo F. Heme is involved in microRNA processing. Nat Struct Mol Biol. 2007; 14: 23-9.
38. Brownawell AM, Macara IG. Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J Cell Biol. 2002; 156: 53-64.
39. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science. 2004; 303: 95-8.
40. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003; 17: 3011-6.
41. Bohnsack MT, Czaplinski K, Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA. 2004; 10: 185-91.
42. Gwizdek C, Ossareh-Nazari B, Brownawell AM, Doglio A, Bertrand E, Macara IG, Dargemont C. Exportin-5 mediates nuclear export of minihelix-containing RNAs. J Biol Chem. 2003; 278: 5505-8.
43. Gwizdek C, Bertrand E, Dargemont C, Lefebvre JC, Blanchard JM, Singer RH, Doglio A. Terminal minihelix, a novel RNA motif that directs polymerase III transcripts to the cell cytoplasm. Terminal minihelix and RNA export. J Biol Chem. 2001; 276: 25910-8.
44. Lu S, Cullen BR. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J Virol. 2004; 78: 12868-76.
45. Bischoff FR, Krebber H, Kempf T, Hermes I, Ponstingl H. Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. Proc Natl Acad Sci U S A. 1995; 92: 1749-53.
46. Bischoff FR, Ponstingl H. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature. 1991; 354: 80-2.
47. Zeng Y, Cullen BR. Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 2004; 32: 4776-85.
48. Okada C, Yamashita E, Lee SJ, Shibata S, Katahira J, Nakagawa A, Yoneda Y, Tsukihara T. A high-resolution structure of the pre-microRNA nuclear export machinery. Science. 2009; 326: 1275-9.
49. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Rådmark O. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 2002; 21: 5864-74.
50. Zhang H, Kolb FA, Brondani V, Billy E, Filipowicz W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 2002; 21: 5875-85.
51. Humphreys DT, Hynes CJ, Patel HR, Wei GH, Cannon L, Fatkin D, Suter CM, Clancy JL, Preiss T. Complexity of murine cardiomyocyte miRNA biogenesis, sequence variant expression and function. PLoS One. 2012; 7, e30933.
52. Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, Ha I, Baillie DL, Fire A, Ruvkun G, Mello CC. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell. 2001; 106: 23-34.
53. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science. 2001; 293: 834-8.
54. Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 2001; 15: 2654-9.
55. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV, Hannon GJ. Dicer is essential for mouse development. Nat Genet. 2003; 35: 215-7.
56. Hatfield SD, Shcherbata HR, Fischer KA, Nakahara K, Carthew RW, Ruohola-Baker H. Stem cell division is regulated by the microRNA pathway. Nature. 2005; 435: 974-8.
57. Ma J-B, Ye K, Patel DJ. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature. 2004; 429: 318-22.
58. Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W. Single processing center models for human Dicer and bacterial RNase III. Cell. 2004; 118: 57-68.
59. MacRae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA. Structural basis for double-stranded RNA processing by Dicer. Science. 2006; 311: 195-8.
60. Basyuk E, Suavet F, Doglio A, Bordonné R, Bertrand E. Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res. 2003; 31: 6593-7.
61. Cenik ES, Fukunaga R, Lu G, Dutcher R, Wang Y, Tanaka Hall TM, Zamore PD. Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driven ribonuclease. Mol Cell. 2011; 42: 172-84.
62. MacRae IJ, Zhou K, Doudna JA. Structural determinants of RNA recognition and cleavage by Dicer. Nat Struct Mol Biol. 2007; 14: 934-40.
63. Lau P-W, Potter CS, Carragher B, MacRae IJ. Structure of the human Dicer-TRBP complex by electron microscopy. Structure. 2009; 17: 1326-32.
64. Wang H-W, Noland C, Siridechadilok B, Taylor DW, Ma E, Felderer K, Doudna JA, Nogales E. Structural insights into RNA processing by the human RISC-loading complex. Nat Struct Mol Biol. 2009; 16: 1148-53.
65. Lau P-W, Guiley KZ, De N, Potter CS, Carragher B, MacRae IJ. The molecular architecture of human Dicer. Nat Struct Mol Biol. 2012; 19: 436-40.
66. Park J-E, Heo I, Tian Y, Simanshu DK, Chang H, Jee D, Patel DJ, Kim VN. Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature. 2011; 475: 201-5.
67. Gu S, Jin L, Zhang Y, Huang Y, Zhang F, Valdmanis PN, Kay MA. The loop position of shRNAs and pre-miRNAs is critical for the accuracy of dicer processing in vivo. Cell. 2012; 151: 900-11.
68. Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science. 2001; 293: 1146-50.
69. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003; 115: 209-16.
70. 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.
71. Tokumaru S, Suzuki M, Yamada H, Nagino M, Takahashi T. let-7 regulates Dicer expression and constitutes a negative feedback loop. Carcinogenesis. 2008; 29: 2073-7.
72. Lai EC. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet. 2002; 30: 363-4.
73. Friedman RC, Farh KK-H, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009; 19: 92-105.
74. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 2002; 297: 2056-60.
75. Yekta S, Shih I-H, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science. 2004; 304: 594-6.
76. Zeng Y, Yi R, Cullen BR. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci U S A. 2003; 100: 9779-84.
77. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNAmediated translational repression in human cells subjected to stress. Cell. 2006; 125: 1111-24.
78. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell. 2004; 15: 185-97.
79. Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 2007; 17: 118-26.
80. 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.
81. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-97.
82. Krek A, Grün D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet. 2005; 37: 495-500.
83. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature. 2005; 436: 740-4.
84. Haase AD, Jaskiewicz L, Zhang H, Lainé S, Sack R, Gatignol A, Filipowicz W. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 2005; 6: 961-7.
85. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song J-J, Hammond SM, Joshua-Tor L, Hannon GJ. Argonaute2 is the catalytic engine of mammalian RNAi. Science. 2004; 305: 1437-41.
86. Swarts DC, Makarova K, Wang Y, Nakanishi K, Ketting RF, Koonin EV, Patel DJ, van der Oost J. The evolutionary journey of Argonaute proteins. Nat Struct Mol Biol. 2014; 21: 743-53.
87. Rivas FV, Tolia NH, Song J-J, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol. 2005; 12: 340-9.
88. 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.
89. Alisch RS, Jin P, Epstein M, Caspary T, Warren ST. Argonaute2 is essential for mammalian gastrulation and proper mesoderm formation. PLoS Genet. 2007; 3, e227.
90. Morita S, Horii T, Kimura M, Goto Y, Ochiya T, Hatada I. One Argonaute family member, Eif2c2 (Ago2), is essential for development and appears not to be involved in DNA methylation. Genomics. 2007; 89: 687-96.
91. Cheloufi S, Dos Santos CO, Chong MMW, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature. 2010; 465: 584-9.
92. Yang J-S, 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.
93. Schirle NT, MacRae IJ. The crystal structure of human Argonaute2. Science. 2012; 336: 1037-40.
94. Elkayam E, Kuhn C-D, Tocilj A, Haase AD, Greene EM, Hannon GJ, Joshua-Tor L. The structure of human Argonaute-2 in complex with miR-20a. Cell. 2012; 150: 100-10.
95. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005; 120: 15-20.
96. Ma J-B, Yuan Y-R, Meister G, Pei Y, Tuschl T, Patel DJ. Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature. 2005; 434: 666-70.
97. 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.
98. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T. Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA. 2008; 14: 2580-96.
99. Höck J, Weinmann L, Ender C, Rüdel S, Kremmer E, Raabe M, Urlaub H, Meister G. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 2007; 8: 1052-60.
100. Liu J, Rivas FV, Wohlschlegel J, Yates JR, Parker R, Hannon GJ. A role for the P-body component GW182 in microRNA function. Nat Cell Biol. 2005; 7: 1261-6.