MicroRNAs: Genomics, Biogenesis, Mechanism, and Function

Cell

Volumn 116, Issue 2, 2004, Pages 281-297

  Bartel, David P ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; SMALL INTERFERING RNA;

BIOGENESIS; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE REPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC CODE; GENOMICS; HUMAN; INTRON; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PLANT; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REVIEW; RNA ANALYSIS; RNA CLEAVAGE; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; STEM CELL; TRANSLATION REGULATION;

ANIMALIA;

EID: 0347444723     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(04)00045-5     Document Type: Review

References (132)

1. Abrahante J.E., Daul A.L., Li M., Volk M.L., Tennessen J.M., Miller E.A., Rougvie A.E. The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev. Cell. 4:2003;625-637.
2. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 57:1989;49-57.
3. Ambros V., Bartel B., Bartel D.P., Burge C.B., Carrington J.C., Chen X., Dreyfuss G., Eddy S.R., Griffiths-Jones S., Marshall M.et al. A uniform system for microRNA annotation. RNA. 9:2003;277-279. a.
4. Ambros V., Lee R.C., Lavanway A., Williams P.T., Jewell D. MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr. Biol. 13:2003;807-818. b.
5. Aravin A.A., Naumova N.M., Tulin A.V., Vagin V.V., Rozovsky Y.M., Gvozdev V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in Drosophila melanogaster germline. Curr. Biol. 11:2001;1017-1027.
6. Aravin A.A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder B., Gaasterland T., Meyer J., Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev. Cell. 5:2003;337-350.
7. Aukerman M.J., Sakai H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell. 10:2003;10.
8. Bartel B., Bartel D.P. MicroRNAs. At the root of plant development? Plant Physiol. 132:2003;709-717.
9. Bashirullah A., Pasquinelli A.E., Kiger A.A., Perrimon N., Ruvkun G., Thummel C.S. Coordinate regulation of small temporal RNAs at the onset of Drosophila metamorphosis. Dev. Biol. 259:2003;1-8.
10. Basyuk E., Suavet F., Doglio A., Bordonne R., Bertrand E. Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res. 31:2003;6593-6597.
11. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 409:2001;295-296.
12. Bohmert K., Camus I., Bellini C., Bouchez D., Caboche M., Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17:1998;170-180.
13. Bollman K.M., Aukerman M.J., Park M.Y., Hunter C., Berardini T.Z., Poethig R.S. HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development. 130:2003;1493-1504.
14. Brennecke J., Hipfner D.R., Stark A., Russell R.B., Cohen S.M. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell. 113:2003;25-36.
15. Calin G.A., Dumitru C.D., Shimizu M., Bichi R., Zupo S., Noch E., Aldler H., Rattan S., Keating M., Rai K.et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA. 99:2002;15524-15529.
16. Catalanotto C., Azzalin G., Macino G., Cogoni C. Gene silencing in worms and fungi. Nature. 404:2000;245.
17. Caudy A.A., Myers M., Hannon G.J., Hammond S.M. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16:2002;2491-2496.
18. Caudy A.A., Ketting R.F., Hammond S.M., Denli A.M., Bathoorn A.M., Tops B.B., Silva J.M., Myers M.M., Hannon G.J., Plasterk R.H. A micrococcal nuclease homologue in RNAi effector complexes. Nature. 425:2003;411-414.
19. Cerutti L., Mian N., Bateman A. Domains in gene silencing and cell differentiation proteins. the novel PAZ domain and redefinition of the Piwi domain Trends Biochem. Sci. 25:2000;481-482.
20. Chalfie M., Horvitz H.R., Sulston J.E. Mutations that lead to reiterations in the cell lineages of C. elegans. Cell. 24:1981;59-69.
21. Chen, X. (2003). A MicroRNA as a Translational Repressor of APETALA2 in Arabidopsis Flower Development. Science. Published online September 11, 2003. 10.1126/science.1088060 .
22. Chen C.Z., Li L., Lodish H.F., Bartel D.P. MicroRNAs modulate hematopoietic lineage differentiation. Science. 303:2004;83-86.
23. Cogoni C., Macino G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature. 399:1999;166-169.
24. Dalmay T., Hamilton A., Rudd S., Angell S., Baulcombe D.C. An RNA-dependent RNA polymerase in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell. 101:2000;543-553.
25. Doench J.G., Peterson C.P., Sharp P.A. siRNAs can function as miRNAs. Genes Dev. 17:2003;438-442.
26. Dostie J., Mourelatos Z., Yang M., Sharma A., Dreyfuss G. Numerous microRNPs in neuronal cells containing novel microRNAs. RNA. 9:2003;631-632.
27. Dykxhoorn D.M., Novina C.D., Sharp P.A. Killing the messenger. short RNAs that silence gene expression Nat. Rev. Mol. Cell Biol. 4:2003;457-467.
28. Elbashir S.M., Leneckel W., Tuschl T. RNA interference is mediated by 21- and 22- nucleotide RNAs. Genes Dev. 15:2001;188-200. a.
29. Elbashir S.M., Martinez J., Patkaniowska A., Lendeckel W., Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 20:2001;6877-6888. b.
30. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. Radial patterning of arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13:2003;1768-1774.
31. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 5:2003;R1.
32. Fagard M., Boutet S., Morel J.B., Bellini C., Vaucheret H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. USA. 97:2000;11650-11654.
33. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 391:1998;806-811.
34. Gauwerky C.E., Huebner K., Isobe M., Nowell P.C., Croce C.M. Activation of MYC in a masked t(8;17) translocation results in an aggressive B-cell leukemia. Proc. Natl. Acad. Sci. USA. 86:1989;8867-8871.
35. Grad Y., Aach J., Hayes G.D., Reinhart B.J., Church G.M., Ruvkun G., Kim J. Computational and experimental identification of C. elegans microRNAs. Mol. Cell. 11:2003;1253-1263.
36. Griffiths-Jones S. The microRNA registry. Nucleic Acids Res. 32:2004;D109-D111.
37. Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I., Baillie D.L., Fire A., Ruvkun G., Mello C.C. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell. 106:2001;23-34.
38. Hall I.M., Shankaranarayana G.D., Noma K., Ayoub N., Cohen A., Grewal S.I. Establishment and maintenance of a heterochromatin domain. Science. 297:2002;2232-2237.
39. Hamilton A.J., Baulcombe D.C. A novel species of small antisense RNA in posttranscriptional gene silencing. Science. 286:1999;950-952.
40. Hamilton A., Voinnet O., Chappell L., Baulcombe D. Two classes of short interfering RNA in RNA silencing. Embo J. 21:2002;4671-4679.
41. Hammond S.C., Bernstein E., Beach D., Hannon G.J. An RNA-directed nuclease mediates posttranscriptional gene silencing in Drosophila cells. Nature. 404:2000;293-296.
42. Hammond S.M., Boettcher S., Caudy A.C., Kobayashi R., Hannon G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science. 293:2001;1146-1150.
43. Hipfner D.R., Weigmann K., Cohen S.M. The bantam gene regulates Drosophila growth. Genetics. 161:2002;1527-1537.
44. Houbaviy H.B., Murray M.F., Sharp P.A. Embryonic stem cell-specific microRNAs. Dev. Cell. 5:2003;351-358.
45. Hutvágner G., Zamore P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 297:2002;2056-2060.
46. Hutvágner G., McLachlan J., Pasquinelli A.E., Balint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science. 293:2001;834-838.
47. Ishizuka A., Siomi M.C., Siomi H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16:2002;2497-2508.
48. Jackson A.L., Bartz S.R., Schelter J., Kobayashi S.V., Burchard J., Mao M., Li B., Cavet G., Linsley P.S. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21:2003;635-637.
49. Jacobsen S.E., Running M.P., Meyerowitz E.M. Disruption of an RNA helicase/RNAseIII gene in Arabidopsis causes unregulated cell division in floral meristems. Development. 126:1999;5231-5243.
50. Johnson S.M., Lin S.Y., Slack F.J. The time of appearance of the C. elegans let-7 microRNA is transcriptionally controlled utilizing a temporal regulatory element in its promoter. Dev. Biol. 259:2003;364-379.
51. Johnston R.J., Hobert O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature. 426:2003;845-849.
52. Kasschau K.D., Xie Z., Allen E., Llave C., Chapman E.J., Krizan K.A., Carrington J.C. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell. 4:2003;205-217.
53. Kawasaki H., Taira K. Hes1 is a target of microRNA-23 during retinoic-acid-induced neuronal differentiation of NT2 cells. Nature. 423:2003;838-842. a.
54. Kawasaki H., Taira K. retraction. Hes1 is a target of microRNA-23 during retinoic-acid-induced neuronal differentiation of NT2 cells Nature. 426:2003;100. b.
55. Ketting R.F., Haverkamp T.H., vanLuenen H.G., Plasterk R.H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner sydrome helicase and RNaseD. Cell. 99:1999;133-141.
56. Ketting R.F., Fischer S.E.J., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H.A. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15:2001;2654-2659.
57. Khvorova A., Reynolds A., Jayasena S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell. 115:2003;209-216.
58. Kim J., Krichevsky A., Grad Y., Hayes G.D., Kosik K.S., Church G.M., Ruvkun G. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc. Natl. Acad. Sci. USA. Published online December. 22:2003;2003. 10.1073/pnas.2333854100.
59. Knight S.W., Bass B.L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development, in caenorhabditis elegens. Science. 293:2001;2269-2271.
60. Krichevsky A.M., King K.S., Donahue C.P., Khrapko K., Kosik K.S. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA. 9:2003;1274-1281.
61. Kuersten S., Goodwin E.B. The power of the 3′ UTR. translational control and development Nat. Rev. Genet. 4:2003;626-637.
62. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 294:2001;853-858.
63. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12:2002;735-739.
64. Lagos-Quintana M., Rauhut R., Meyer J., Borkhardt A., Tuschl T. New microRNAs from mouse and human. RNA. 9:2003;175-179.
65. Lai E.C. MicroRNAs are complementary to 3′UTR motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30:2002;363-364.
66. Lai E.C., Tomancak P., Williams R.W., Rubin G.M. Computational identification of Drosophila microRNA genes. Genome Biol. 4:R42:2003;1-20.
67. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science. 294:2001;858-862.
68. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science. 294:2001;862-864.
69. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:1993;843-854.
70. Lee Y., Jeon K., Lee J.T., Kim S., Kim V.N. MicroRNA maturation. stepwise processing and subcellular localization EMBO J. 21:2002;4663-4670.
71. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature. 425:2003;415-419.
72. Lewis B.P., Shih I., Jones-Rhoades M.W., Bartel D.P., Burge C.B. Prediction of mammalian microRNA targets. Cell. 115:2003;787-798.
73. Li H., Li W.X., Ding S.W. Induction and suppression of RNA silencing by an animal virus. Science. 296:2002;1319-1321.
74. Lim L.P., Lau N.C., Weinstein E.G., Abdelhakim A., Yekta S., Rhoades M.W., Burge C.B., Bartel D.P. The microRNAs of Caenorhabditis elegans. Genes Dev. 17:2003;991-1008. a.
75. Lim L.P., Glasner M.E., Yekta S., Burge C.B., Bartel D.P. Vertebrate microRNA genes. Science. 299:2003;1540. b.
76. Lin S.Y., Johnson S.M., Abraham M., Vella M.C., Pasquinelli A., Gamberi C., Gottlieb E., Slack F.J. The C. elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell. 4:2003;639-650.
77. Lingel A., Simon B., Izaurralde E., Sattler M. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature. 426:2003;465-469.
78. Llave C., Kasschau K.D., Rector M.A., Carrington J.C. Endogenous and silencing-associated small RNAs in plants. Plant Cell. 14:2002;1605-1619. a.
79. Llave C., Xie Z., Kasschau K.D., Carrington J.C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science. 297:2002;2053-2056. b.
80. Lund E., Güttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science. 303:2004;95-98.
81. Martinez J., Patkaniowska A., Urlaub H., Luhrmann R., Tuschl T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell. 110:2002;563-574.
82. McConnell J.R., Emery J., Eshed Y., Bao N., Bowman J., Barton M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature. 411:2001;709-713.
83. Meneely P.M., Herman R.K. Lethals, steriles and deficiencies in a region of the X chromosome of Caenorhabditis elegans. Genetics. 92:1979;99-115.
84. Mette M.F., Aufsatz W., Winden J.v.d., Matzke M.A., Matzke A.J. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19:2000;5194-5201.
85. Mette M.F., van der Winden J., Matzke M., Matzke A.J. Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol. 130:2002;6-9.
86. Michael M.Z., O'Connor S.M., van Holst Pellekaan N.G., Young G.P., James R.J. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol. Cancer Res. 1:2003;882-891.
87. Mochizuki K., Fine N.A., Fujisawa T., Gorovsky M.A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell. 110:2002;689-699.
88. Moss E.G., Lee R.C., Ambros V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell. 88:1997;637-646.
89. Mourelatos Z., Dostie J., Paushkin S., Sharma A., Charroux B., Abel L., Rappsilber J., Mann M., Dreyfuss G. miRNPs. a novel class of ribonucleoproteins containing numerous microRNAs Genes Dev. 16:2002;720-728.
90. Mourrain P., Beclin C., Elmayan T., Feuerbach F., Godon C., Morel J.B., Jouette D., Lacombe A.M., Nikic S., Picault N.et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell. 101:2000;533-542.
91. Nykänen A., Haley B., Zamore P.D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell. 107:2001;309-321.
92. Ohler U., Yekta S., Lim L.P., Bartel D.P., Burge C.B. Patterns of flanking sequence conservation and a characteristic upstream motif for microRNA gene identification. RNA. in press:2004.
93. Olsen P.H., 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. 216:1999;671-680.
94. Palatnik J.F., Allen E., Wu X., Schommer C., Schwab R., Carrington J.C., Weigel D. Control of leaf morphogenesis by microRNAs. Nature. 425:2003;257-263.
95. Papp I., Mette M.F., Aufsatz W., Daxinger L., Schauer S.E., Ray A., van der Winden J., Matzke M., Matzke A.J. Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol. 132:2003;1382-1390.
96. Park W., Li J., Song R., Messing J., Chen X. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12:2002;1484-1495.
97. Parrish S., Fleenor J., Xu S., Mello C., Fire A. Functional anatomy of a dsRNA trigger. differential requirement for the two trigger strands in RNA interference Mol. Cell. 6:2000;1077-1087.
98. Pasquinelli A.E., Reinhart B.J., Slack F., Martindale M.Q., Kuroda M., Maller B., Srinivasan A., Fishman M., Hayward D., Ball E.et al. Conservation across animal phylogeny of the sequence and temporal regulation of the 21 nucleotide let-7 heterochronic regulatory RNA. Nature. 408:2000;86-89.
99. Pickford A.S., Catalanotto C., Cogoni C., Macino G. Quelling in Neurospora crassa. Adv. Genet. 46:2002;277-303.
100. Pusch O., Boden D., Silbermann R., Lee F., Tucker L., Ramratnam B. Nucleotide sequence homology requirements of HIV-1-specific short hairpin RNA. Nucleic Acids Res. 31:2003;6444-6449.
101. Reinhart B.J., Bartel D.P. Small RNAs correspond to centromere heterochromatic repeats. Science. 297:2002;1831.
102. Reinhart B.J., Slack F.J., Basson M., Bettinger J.C., Pasquinelli A.E., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21 nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403:2000;901-906.
103. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B., Bartel D.P. MicroRNAs in plants. Genes Dev. 16:2002;1616-1626.
104. Rhoades M.W., Reinhart B.J., Lim L.P., Burge C.B., Bartel B., Bartel D.P. Prediction of plant microRNA targets. Cell. 110:2002;513-520.
105. Saxena S., Jonsson Z.O., Dutta A. Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off-target activity of small inhibitory RNA in mammalian cells. J. Biol. Chem. 278:2003;44312-44319.
106. Schauer S.E., Jacobsen S.E., Meinke D.W., Ray A. DICER-LIKE1. blind men and elephants in Arabidopsis development Trends Plant Sci. 7:2002;487-491.
107. Schwarz D.S., Hutvágner G., Haley B., Zamore P.D. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell. 10:2002;537-548.
108. Schwarz D.S., Hutvagner G., Du T., Xu Z., Aronin N., Zamore P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 115:2003;199-208.
109. Seggerson K., Tang L., Moss E.G. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243:2002;215-225.
110. Seitz H., Youngson N., Lin S.P., Dalbert S., Paulsen M., Bachellerie J.P., Ferguson-Smith A.C., Cavaille J. Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat. Genet. 34:2003;261-262.
111. Sempere L.F., Sokol N.S., Dubrovsky E.B., Berger E.M., Ambros V. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev. Biol. 259:2003;9-18.
112. Slack F.J., Basson M., Liu Z., Ambros V., Horvitz H.R., Ruvkun G. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell. 5:2000;659-669.
113. Smardon A., Spoerke J.M., Stacey S.C., Klein M.E., Mackin N., Maine E.M. EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr. Biol. 10:2000;169-178.
114. Song J.J., Liu J., Tolia N.H., Schneiderman J., Smith S.K., Martienssen R.A., Hannon G.J., Joshua-Tor L. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10:2003;1026-1032.
115. Stark A., Brennecke J., Russell R.B., Cohen S.M. Identification of Drosophila microRNA targets. PLOS Biol. 1:2003;E60.
116. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 99:1999;123-132.
117. Tang G., Reinhart B.J., Bartel D.P., Zamore P.D. A biochemical framework for RNA silencing in plants. Genes Dev. 17:2003;49-63.
118. Vance V., Vaucheret H. RNA silencing in plants - defense and counterdefense. Science. 292:2001;2277-2280.
119. Volpe T., Kidner C., Hall I., Teng G., Grewal S., Martienssen R. Heterochromatic silencing and histone H3 lysine 9 methylation are regulated by RNA interference. Science. 297:2002;1833-1837.
120. Weigel D., Ahn J.H., Blazquez M.A., Borevitz J.O., Christensen S.K., Fankhauser C., Ferrandiz C., Kardailsky I., Malancharuvil E.J., Neff M.M.et al. Activation tagging in Arabidopsis. Plant Physiol. 122:2000;1003-1013.
121. Wightman B., Burglin T.R., Gatto J., Arasu P., Ruvkun G. Negative regulatory sequences in the lin-14 3′-untranslated region are necessary to generate a temporal switch during Caenorhabditis elegans development. Genes Dev. 5:1991;1813-1824.
122. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75:1993;855-862.
123. Xie Z., Kasschau K.D., Carrington J.C. Negative feedback regulation of Dicer-like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 13:2003;784-789.
124. Xu P., Vernooy S.Y., Guo M., Hay B.A. The Drosophila microRNA mir-14 suppresses cell death and is required for normal fat metabolism. Curr. Biol. 13:2003;790-795.
125. Yan K.S., Yan S., Farooq A., Han A., Zeng L., Zhou M.M. Structure and conserved RNA binding of the PAZ domain. Nature. 426:2003;468-474.
126. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17:2003;3011-3016.
127. Zamore P.D., Tuschl T., Sharp P.A., Bartel D.P. Rnai. double-stranded rna directs the atp-dependent cleavage of mRNA at 21 to 23 nucleotide intervals Cell. 101:2000;25-33.
128. Zeng Y., Cullen B.R. Sequence requirements for micro RNA processing and function in human cells. RNA. 9:2003;112-123.
129. Zeng Y., Wagner E.J., Cullen B.R. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell. 9:2002;1327-1333.
130. Zeng Y., Yi R., Cullen B.R. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc. Natl. Acad. Sci. USA. 100:2003;9779-9784.
131. Zhang H., Kolb F.A., Brondani V., Billy E., Filipowicz W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 21:2002;5875-5885.
132. Zilberman D., Cao X., Jacobsen S.E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 299:2003;716-719.