Alternative miRNA Biogenesis Pathways and the Interpretation of Core miRNA Pathway Mutants

Molecular Cell

Volumn 43, Issue 6, 2011, Pages 892-903

  Yang, Jr Shiuan ^a,b   Lai, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DICER; DOUBLE STRANDED RNA; DROSHA; MICRORNA; RIBONUCLEASE III; SHORT HAIRPIN RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

BIOGENESIS; CONTROLLED STUDY; DROSOPHILA; GENE CONTROL; GENE EXPRESSION; GENE LOSS; GENOTYPE; KNOCKOUT GENE; MUTANT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY SYSTEM; OOCYTE; PHENOTYPE; REVIEW; RNA CLEAVAGE; RNA PROCESSING;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EUKARYOTIC INITIATION FACTORS; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; MODELS, GENETIC; MUTATION; OLFACTORY PATHWAYS; RIBONUCLEASE III; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; RNA-INDUCED SILENCING COMPLEX;

ANIMALIA;

EID: 80052996141     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.07.024     Document Type: Review

References (109)

1. Axtell M.J., Westholm J.O., Lai E.C. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 2011, 12:221.
2. Babiarz J.E., Ruby J.G., Wang Y., Bartel D.P., Blelloch R. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev. 2008, 22:2773-2785.
3. Babiarz J.E., Hsu R., Melton C., Thomas M., Ullian E.M., Blelloch R. A role for noncanonical microRNAs in the mammalian brain revealed by phenotypic differences in Dgcr8 versus Dicer1 knockouts and small RNA sequencing. RNA 2011, 17:1489-1501.
4. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
5. Bejarano F., Smibert P., Lai E.C. miR-9a prevents apoptosis during wing development by repressing Drosophila LIM-only. Dev. Biol. 2010, 338:63-73.
6. Bennasser Y., Chable-Bessia C., Triboulet R., Gibbings D., Gwizdek C., Dargemont C., Kremer E.J., Voinnet O., Benkirane M. Competition for XPO5 binding between Dicer mRNA, pre-miRNA and viral RNA regulates human Dicer levels. Nat. Struct. Mol. Biol. 2011, 18:323-327.
7. Berdnik D., Fan A.P., Potter C.J., Luo L. MicroRNA processing pathway regulates olfactory neuron morphogenesis. Curr. Biol. 2008, 18:1754-1759.
8. Berezikov E., Guryev V., van de Belt J., Wienholds E., Plasterk R.H., Cuppen E. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005, 120:21-24.
9. Berezikov E., Chung W.-J., Willis J., Cuppen E., Lai E.C. Mammalian mirtron genes. Mol. Cell 2007, 28:328-336.
10. Berezikov E., Robine N., Samsonova A., Westholm J.O., Naqvi A., Hung J.H., Okamura K., Dai Q., Bortolamiol-Becet D., Martin R., et al. Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res. 2011, 21:203-215.
11. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., Mills A.A., Elledge S.J., Anderson K.V., Hannon G.J. Dicer is essential for mouse development. Nat. Genet. 2003, 35:215-217.
12. Biryukova I., Asmar J., Abdesselem H., Heitzler P. Drosophila mir-9a regulates wing development via fine-tuning expression of the LIM only factor, dLMO. Dev. Biol. 2009, 327:487-496.
13. Bogerd H.P., Karnowski H.W., Cai X., Shin J., Pohlers M., Cullen B.R. A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral MicroRNAs. Mol. Cell 2010, 37:135-142.
14. Brameier M., Herwig A., Reinhardt R., Walter L., Gruber J. Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res. 2011, 39:675-686.
15. Cheloufi S., Dos Santos C.O., Chong M.M., Hannon G.J. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589.
16. Choi W.Y., Giraldez A.J., Schier A.F. Target protectors reveal dampening and balancing of Nodal agonist and antagonist by miR-430. Science 2007, 318:271-274.
17. Chong M.M., Rasmussen J.P., Rudensky A.Y., Littman D.R. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 2008, 205:2005-2017.
18. Chong M.M., Zhang G., Cheloufi S., Neubert T.A., Hannon G.J., Littman D.R. Canonical and alternate functions of the microRNA biogenesis machinery. Genes Dev. 2010, 24:1951-1960.
19. Chung W.J., Okamura K., Martin R., Lai E.C. Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr. Biol. 2008, 18:795-802.
20. Chung W.J., Agius P., Westholm J.O., Chen M., Okamura K., Robine N., Leslie C.S., Lai E.C. Computational and experimental identification of mirtrons in Drosophila melanogaster and Caenorhabditis elegans. Genome Res. 2011, 21:286-300.
21. Cifuentes D., Xue H., Taylor D.W., Patnode H., Mishima Y., Cheloufi S., Ma E., Mane S., Hannon G.J., Lawson N.D., et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 2010, 328:1694-1698.
22. Cole C., Sobala A., Lu C., Thatcher S.R., Bowman A., Brown J.W., Green P.J., Barton G.J., Hutvagner G. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 2009, 15:2147-2160.
23. Couvillion M.T., Sachidanandam R., Collins K. A growth-essential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev. 2010, 24:2742-2747.
24. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 2011, 12:19-31.
25. Czech B., Malone C.D., Zhou R., Stark A., Schlingeheyde C., Dus M., Perrimon N., Kellis M., Wohlschlegel J.A., Sachidanandam R., et al. An endogenous small interfering RNA pathway in Drosophila. Nature 2008, 453:798-802.
26. Diederichs S., Haber D.A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007, 131:1097-1108.
27. Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
28. Drider D., Condon C. The continuing story of endoribonuclease III. J. Mol. Microbiol. Biotechnol. 2004, 8:195-200.
29. Drinnenberg I.A., Weinberg D.E., Xie K.T., Mower J.P., Wolfe K.H., Fink G.R., Bartel D.P. RNAi in budding yeast. Science 2009, 326:544-550.
30. Ender C., Krek A., Friedländer M.R., Beitzinger M., Weinmann L., Chen W., Pfeffer S., Rajewsky N., Meister G. A human snoRNA with microRNA-like functions. Mol. Cell 2008, 32:519-528.
31. Fabian M.R., Sonenberg N., Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 2010, 79:351-379.
32. Flynt A.S., Lai E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 2008, 9:831-842.
33. Flynt A.S., Liu N., Martin R., Lai E.C. Dicing of viral replication intermediates during silencing of latent Drosophila viruses. Proc. Natl. Acad. Sci. USA 2009, 106:5270-5275.
34. Flynt A.S., Greimann J.C., Chung W.J., Lima C.D., Lai E.C. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol. Cell 2010, 38:900-907.
35. Fukuda T., Yamagata K., Fujiyama S., Matsumoto T., Koshida I., Yoshimura K., Mihara M., Naitou M., Endoh H., Nakamura T., et al. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat. Cell Biol. 2007, 9:604-611.
36. Ghildiyal M., Zamore P.D. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 2009, 10:94-108.
37. Ghildiyal M., Seitz H., Horwich M.D., Li C., Du T., Lee S., Xu J., Kittler E.L., Zapp M.L., Weng Z., Zamore P.D. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008, 320:1077-1081.
38. Giraldez A.J., Cinalli R.M., Glasner M.E., Enright A.J., Thomson J.M., Baskerville S., Hammond S.M., Bartel D.P., Schier A.F. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308:833-838.
39. Glazov E.A., Cottee P.A., Barris W.C., Moore R.J., Dalrymple B.P., Tizard M.L. A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res. 2008, 18:957-964.
40. Halic M., Moazed D. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 2010, 140:504-516.
41. Han J., Lee Y., Yeom K.H., Nam J.W., Heo I., Rhee J.K., Sohn S.Y., Cho Y., Zhang B.T., Kim V.N. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125:887-901.
42. Han J., Pedersen J.S., Kwon S.C., Belair C.D., Kim Y.K., Yeom K.H., Yang W.Y., Haussler D., Blelloch R., Kim V.N. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 2009, 136:75-84.
43. Harfe B.D., McManus M.T., Mansfield J.H., Hornstein E., Tabin C.J. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 2005, 102:10898-10903.
44. Haussecker D., Huang Y., Lau A., Parameswaran P., Fire A.Z., Kay M.A. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 2010, 16:673-695.
45. Kadener S., Rodriguez J., Abruzzi K.C., Khodor Y.L., Sugino K., Marr M.T., Nelson S., Rosbash M. Genome-wide identification of targets of the drosha-pasha/DGCR8 complex. RNA 2009, 15:537-545.
46. Kaneko H., Dridi S., Tarallo V., Gelfand B.D., Fowler B.J., Cho W.G., Kleinman M.E., Ponicsan S.L., Hauswirth W.W., Chiodo V.A., et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 2011, 471:325-330.
47. Kanellopoulou C., Muljo S.A., Kung A.L., Ganesan S., Drapkin R., Jenuwein T., Livingston D.M., Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 2005, 19:489-501.
48. Karginov F.V., Cheloufi S., Chong M.M., Stark A., Smith A.D., Hannon G.J. Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol. Cell 2010, 38:781-788.
49. Kataoka Y., Takeichi M., Uemura T. Developmental roles and molecular characterization of a Drosophila homologue of Arabidopsis Argonaute1, the founder of a novel gene superfamily. Genes Cells 2001, 6:313-325.
50. Kawamura Y., Saito K., Kin T., Ono Y., Asai K., Sunohara T., Okada T.N., Siomi M.C., Siomi H. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 2008, 453:793-797.
51. Koralov S.B., Muljo S.A., Galler G.R., Krek A., Chakraborty T., Kanellopoulou C., Jensen K., Cobb B.S., Merkenschlager M., Rajewsky N., Rajewsky K. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 2008, 132:860-874.
52. Lai E.C., Posakony J.W. The Bearded box, a novel 3' UTR sequence motif, mediates negative post-transcriptional regulation of Bearded and Enhancer of split Complex gene expression. Development 1997, 124:4847-4856.
53. Lai E.C., Burks C., Posakony J.W. The K box, a conserved 3' UTR sequence motif, negatively regulates accumulation of enhancer of split complex transcripts. Development 1998, 125:4077-4088.
54. Lai E.C., Tomancak P., Williams R.W., Rubin G.M. Computational identification of Drosophila microRNA genes. Genome Biol. 2003, 4:R42.
55. Lee Y.S., Shibata Y., Malhotra A., Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 2009, 23:2639-2649.
56. Lee H.C., Li L., Gu W., Xue Z., Crosthwaite S.K., Pertsemlidis A., Lewis Z.A., Freitag M., Selker E.U., Mello C.C., Liu Y. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 2010, 38:803-814.
57. Leung A.K., Young A.G., Bhutkar A., Zheng G.X., Bosson A.D., Nielsen C.B., Sharp P.A. Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat. Struct. Mol. Biol. 2011, 18:237-244.
58. Li Y., Wang F., Lee J.A., Gao F.B. MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev. 2006, 20:2793-2805.
59. Lim L.P., Burge C.B. A computational analysis of sequence features involved in recognition of short introns. Proc. Natl. Acad. Sci. USA 2001, 98:11193-11198.
60. Lin Y.T., Sullivan C.S. Expanding the role of Drosha to the regulation of viral gene expression. Proc. Natl. Acad. Sci. USA 2011, 108:11229-11234.
61. Ma J., Flemr M., Stein P., Berninger P., Malik R., Zavolan M., Svoboda P., Schultz R.M. MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 2010, 20:265-270.
62. Medina M.F., Joshi S. RNA-polymerase III-driven expression cassettes in human gene therapy. Curr. Opin. Mol. Ther. 1999, 1:580-594.
63. Meyer W.J., Schreiber S., Guo Y., Volkmann T., Welte M.A., Müller H.A. Overlapping functions of argonaute proteins in patterning and morphogenesis of Drosophila embryos. PLoS Genet. 2006, 2:e134.
64. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 2005, 102:12135-12140.
65. Murchison E.P., Stein P., Xuan Z., Pan H., Zhang M.Q., Schultz R.M., Hannon G.J. Critical roles for Dicer in the female germline. Genes Dev. 2007, 21:682-693.
66. Nakagawa A., Shi Y., Kage-Nakadai E., Mitani S., Xue D. Caspase-dependent conversion of Dicer ribonuclease into a death-promoting deoxyribonuclease. Science 2010, 328:327-334.
67. Okamura K., Lai E.C. Endogenous small interfering RNAs in animals. Nat. Rev. Mol. Cell Biol. 2008, 9:673-678.
68. Okamura K., Ishizuka A., Siomi H., Siomi M.C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 2004, 18:1655-1666.
69. Okamura K., Hagen J.W., Duan H., Tyler D.M., Lai E.C. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007, 130:89-100.
70. Okamura K., Balla S., Martin R., Liu N., Lai E.C. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat. Struct. Mol. Biol. 2008, 15:581-590.
71. Okamura K., Chung W.-J., Ruby J.G., Guo H., Bartel D.P., Lai E.C. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 2008, 453:803-806.
72. Ono M., Scott M.S., Yamada K., Avolio F., Barton G.J., Lamond A.I. Identification of human miRNA precursors that resemble box C/D snoRNAs. Nucleic Acids Res. 2011, 39:3879-3891.
73. Paddison P.J., Caudy A.A., Hannon G.J. Stable suppression of gene expression by RNAi in mammalian cells. Proc. Natl. Acad. Sci. USA 2002, 99:1443-1448.
74. Patrick D.M., Zhang C.C., Tao Y., Yao H., Qi X., Schwartz R.J., Jun-Shen Huang L., Olson E.N. Defective erythroid differentiation in miR-451 mutant mice mediated by 14-3-3zeta. Genes Dev. 2010, 24:1614-1619.
75. Pederson T. Regulatory RNAs derived from transfer RNA?. RNA 2010, 16:1865-1869.
76. Persson H., Kvist A., Vallon-Christersson J., Medstrand P., Borg A., Rovira C. The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat. Cell Biol. 2009, 11:1268-1271.
77. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grässer F.A., van Dyk L.F., Ho C.K., Shuman S., Chien M., et al. Identification of microRNAs of the herpesvirus family. Nat. Methods 2005, 2:269-276.
78. Rasmussen K.D., Simmini S., Abreu-Goodger C., Bartonicek N., Di Giacomo M., Bilbao-Cortes D., Horos R., Von Lindern M., Enright A.J., O'Carroll D. The miR-144/451 locus is required for erythroid homeostasis. J. Exp. Med. 2010, 207:1351-1358.
79. Reese T.A., Xia J., Johnson L.S., Zhou X., Zhang W., Virgin H.W. Identification of novel microRNA-like molecules generated from herpesvirus and host tRNA transcripts. J. Virol. 2010, 84:10344-10353.
80. Ruby J.G., Jan C.H., Bartel D.P. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86.
81. Saraiya A.A., Wang C.C. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 2008, 4:e1000224.
82. Scherer L.J., Frank R., Rossi J.J. Optimization and characterization of tRNA-shRNA expression constructs. Nucleic Acids Res. 2007, 35:2620-2628.
83. Scott M.S., Avolio F., Ono M., Lamond A.I., Barton G.J. Human miRNA precursors with box H/ACA snoRNA features. PLoS Comput. Biol. 2009, 5:e1000507.
84. Shapiro J.S., Varble A., Pham A.M., Tenoever B.R. Noncanonical cytoplasmic processing of viral microRNAs. RNA 2010, 16:2068-2074.
85. Shenoy A., Blelloch R. Genomic analysis suggests that mRNA destabilization by the microprocessor is specialized for the auto-regulation of Dgcr8. PLoS ONE 2009, 4:e6971.
86. Shi W., Hendrix D., Levine M., Haley B. A distinct class of small RNAs arises from pre-miRNA-proximal regions in a simple chordate. Nat. Struct. Mol. Biol. 2009, 16:183-189.
87. Shin C., Nam J.W., Farh K.K., Chiang H.R., Shkumatava A., Bartel D.P. Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 2010, 38:789-802.
88. Smibert P., Lai E.C. Lessons from microRNA mutants in worms, flies and mice. Cell Cycle 2008, 7:2500-2508.
89. Su H., Trombly M.I., Chen J., Wang X. Essential and overlapping functions for mammalian Argonautes in microRNA silencing. Genes Dev. 2009, 23:304-317.
90. Suh N., Baehner L., Moltzahn F., Melton C., Shenoy A., Chen J., Blelloch R. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 2010, 20:271-277.
91. Svoboda P., Stein P., Hayashi H., Schultz R.M. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 2000, 127:4147-4156.
92. Taft R.J., Glazov E.A., Lassmann T., Hayashizaki Y., Carninci P., Mattick J.S. Small RNAs derived from snoRNAs. RNA 2009, 15:1233-1240.
93. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.
94. Tan G.S., Garchow B.G., Liu X., Yeung J., Morris J.P., Cuellar T.L., McManus M.T., Kiriakidou M. Expanded RNA-binding activities of mammalian Argonaute 2. Nucleic Acids Res. 2009, 37:7533-7545.
95. Tang F., Kaneda M., O'Carroll D., Hajkova P., Barton S.C., Sun Y.A., Lee C., Tarakhovsky A., Lao K., Surani M.A. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007, 21:644-648.
96. Triboulet R., Chang H.M., Lapierre R.J., Gregory R.I. Post-transcriptional control of DGCR8 expression by the Microprocessor. RNA 2009, 15:1005-1011.
97. Ventura A., Young A.G., Winslow M.M., Lintault L., Meissner A., Erkeland S.J., Newman J., Bronson R.T., Crowley D., Stone J.R., et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008, 132:875-886.
98. Wang X.H., Aliyari R., Li W.X., Li H.W., Kim K., Carthew R., Atkinson P., Ding S.W. RNA interference directs innate immunity against viruses in adult Drosophila. Science 2006, 312:452-454.
99. Wang Y., Medvid R., Melton C., Jaenisch R., Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 2007, 39:380-385.
100. Wang Y., Baskerville S., Shenoy A., Babiarz J.E., Baehner L., Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 2008, 40:1478-1483.
101. Watanabe T., Totoki Y., Toyoda A., Kaneda M., Kuramochi-Miyagawa S., Obata Y., Chiba H., Kohara Y., Kono T., Nakano T., et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543.
102. Wu H., Xu H., Miraglia L.J., Crooke S.T. Human RNase III is a 160-kDa protein involved in preribosomal RNA processing. J. Biol. Chem. 2000, 275:36957-36965.
103. Yang S., Tutton S., Pierce E., Yoon K. Specific double-stranded RNA interference in undifferentiated mouse embryonic stem cells. Mol. Cell. Biol. 2001, 21:7807-7816.
104. Yang J.S., Maurin T., Robine N., Rasmussen K.D., Jeffrey K.L., Chandwani R., Papapetrou E.P., Sadelain M., O'Carroll D., Lai E.C. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc. Natl. Acad. Sci. USA 2010, 107:15163-15168.
105. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
106. Yi R., O'Carroll D., Pasolli H.A., Zhang Z., Dietrich F.S., Tarakhovsky A., Fuchs E. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat. Genet. 2006, 38:356-362.
107. Yi R., Pasolli H.A., Landthaler M., Hafner M., Ojo T., Sheridan R., Sander C., O'Carroll D., Stoffel M., Tuschl T., Fuchs E. DGCR8-dependent microRNA biogenesis is essential for skin development. Proc. Natl. Acad. Sci. USA 2009, 106:498-502.
108. Yu D., dos Santos C.O., Zhao G., Jiang J., Amigo J.D., Khandros E., Dore L.C., Yao Y., D'Souza J., Zhang Z., et al. miR-451 protects against erythroid oxidant stress by repressing 14-3-3zeta. Genes Dev. 2010, 24:1620-1633.
109. Yuan Y.R., Pei Y., Ma J.B., Kuryavyi V., Zhadina M., Meister G., Chen H.Y., Dauter Z., Tuschl T., Patel D.J. Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 2005, 19:405-419.