MicroRNA functions in animal development and human disease

Development

Volumn 132, Issue 21, 2005, Pages 4653-4662

  Alvarez Garcia, Ines ^a   Miska, Eric A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HOX PROTEIN; INSULIN; MICRORNA; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; RAS PROTEIN; TRANSCRIPTION FACTOR E2F;

APOPTOSIS; B CELL LYMPHOMA; CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL DIFFERENTIATION; DIGEORGE SYNDROME; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; INSULIN RELEASE; LARVAL DEVELOPMENT; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; DISEASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICRORNAS; MORPHOGENESIS;

ANIMALIA; ANURA; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; MAGNOLIOPHYTA; MAMMALIA;

EID: 28044471565     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02073     Document Type: Review

References (118)

1. Abbott, A. L., Alvarez-Saavedra, E., Miska, E. A., Lau, N. C., Bartel, D. P., Horvitz, H. R. and Ambros, V. (2005). The let-7 MicroRNA family members mir-48, mir-84 and mir-241 function together to regulate. developmental timing in Caenorhabditis elegans. Dev. Cell 9, 403-414.
2. Abrahante, J. E., Daul, A. L., Li, M., Volk, M. L., Tennessen, J. M., Miller, E. A. and Rougvie, A. E. (2003). The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev. Cell 4, 625-637.
3. Ambros, V. and Horvitz, H. R. (1984). Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409-416.
4. Antebi, A., Culotti, J. G. and Hedgecock, E. M. (1998). daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 125, 1191-1205.
5. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
6. Baulcombe, D. (2004). RNA silencing in plants. Nature 431, 356-363.
7. Beitel, G. J., Clark, S. G. and Horvitz, H. R. (1990). Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature 348, 503-509.
8. Berezikov, E., Guryev, V., van de Belt, J., Wienholds, E., Plasterk, R. H. and Cuppen, E. (2005). Phylogenetic shadowing and computational identification of human microRNA genes. Cell 120, 21-24.
9. Bernstein, E., Caudy, A. A., Hammond, S. M. and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366.
10. 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. and Hannon, G. J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215-217.
11. Bohnsack, M. T., Czaplinski, K. and Gorlich, D. (2004). Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10, 185-191.
12. Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B. and Cohen, S. M. (2003). bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila Cell 113, 25-36.
13. Brennecke, J., Stark, A., Russell, R. B. and Cohen, S. M. (2005). Principles of microRNA-target recognition. PLoS Biol. 3, E85.
14. Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M., Rai, K. et al. (2002). Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 99, 15524-15529.
15. Calin, G. A., Liu, C. G., Sevignani, C., Ferracin, M., Felli, N., Dumitru, C. D., Shimizu, M., Cimmino, A., Zupo, S., Dono, M. et al. (2004a). MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc. Natl. Acad. Sci. USA 101, 11755-11760.
16. Calin, G. A., Sevignani, C., Dumitru, C. D., Hyslop, T., Noch, E., Yendamuri, S., Shimizu, M., Rattan, S., Bullrich, F., Negrini, M. et al. (2004b). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. USA 101, 2999-3004.
17. Chalfie, M., Horvitz, H. R. and Sulston, J. E. (1981). Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 24, 59-69.
18. Chang, S., Johnston, R. J., Jr and Hobert, O. (2003). A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17, 2123-2137.
19. Chang, S., Johnston, R. J., Jr, Frokjaer-Jensen, C., Lockery, S. and Hobert, O. (2004). MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430, 785-789.
20. Chen, C. Z., Li, L., Lodish, H. F. and Bartel, D. P. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86.
21. Cobb, B. S., Nesterova, T. B., Thompson, E., Hertweck, A., O'Connor, E., Godwin, J., Wilson, C. B., Brockdorff, N., Fisher, A. G., Smale, S. T. et al. (2005). T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 201, 1367-1373.
22. Denli, A. M., Tops, B. B., Plasterk, R. H., Ketting, R. F. and Hannon, G. J. (2004). Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231-235.
23. Du, T. and Zamore, P. D. (2005). microPrimer: An introduction to microRNA. Development (in press).
24. Fukagawa, T., Nogami, M., Yoshikawa, M., Ikeno, M., Okazaki, T., Takami, Y., Nakayama, T. and Oshimura, M. (2004). Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat. Cell. Biol. 6, 784-791.
25. Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., Hammond, S. M., Bartel, D. P. and Schier, A. F. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838.
26. Gould, S. J. (2000). Of coiled oysters and big brains: how to rescue the terminology of heterochrony, now gone astray. Evol. Dev. 2, 241-248.
27. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N. and Shiekhattar, R. (2004). The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240.
28. Griffiths-Jones, S. (2004). The microRNA Registry. Nucleic Acids Res. 32, D109-D111.
29. Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D. L., Fire, A., Ruvkun, G. and Mello, C. C. (2001). Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34.
30. Grosshans, H., Johnson, T., Reinert, K. L., Gerstein, M. and Slack, F. J. (2005). The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev. Cell. 8, 321-330.
31. Han, J., Lee, Y., Yeom, K. H., Kim, Y. K., Jin, H. and Kim, V. N. (2004). The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016-3027.
32. Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E. and Tabin, C. J. (2005). The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 102, 10898-10903.
33. Hatfield, S. D., Shcherbata, H. R., Fischer, K. A., Nakahara, K., Carthew, R. W. and Ruohola-Baker, H. (2005). Stem cell division is regulated by the microRNA pathway. Nature 435, 974-978.
34. He, L., Thomson, J. M., Hemann, M. T., Hernando-Monge, E., Mu, D., Goodson, S., Powers, S., Cordon-Cardo, C., Lowe, S. W., Hannon, G. J. et al. (2005). A microRNA polycistron as a potential human oncogene. Nature 435, 828-833.
35. Hipfner, D. R., Weigmann, K. and Cohen, S. M. (2002). The bantam gene regulates Drosophila growth. Genetics 161, 1527-1537.
36. Hobert, O., Johnston, R. J., Jr and Chang, S. (2002). Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat. Rev. Neurosci. 3, 629-640.
37. Horvitz, H. R. and Sulston, J. E. (1980). Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96, 435-454.
38. Horvitz, H. R., Sternberg, P. W., Greenwald, I. S., Fixsen, W. and Ellis, H. M. (1983). Mutations that affect neural cell lineages and cell fates during the development of the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 48, 453-463.
39. Houbaviy, H. B., Murray, M. F. and Sharp, P. A. (2003). Embryonic stem cell-specific MicroRNAs. Dev. Cell 5, 351-358.
40. Hutvagner, G., Simard, M. J., Mello, C. C. and Zamore, P. D. (2004). Sequence-specific inhibition of small RNA function. PLoS Biol. 2, E98.
41. Jing, Q., Huang, S., Guth, S., Zarubin, T., Motoyama, A., Chen, J., Di Padova, F., Lin, S. C., Gram, H. and Han, J. (2005). Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120, 623-634.
42. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C. and Marks, D. S. (2004). Human MicroRNA targets. PLoS Biol. 2, E363.
43. Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., Labourier, E., Reinert, K. L., Brown, D. and Slack, F. J. (2005). RAS is regulated by the let-7 microRNA family. Cell 120, 635-647.
44. Johnston, R. J. and Hobert, O. (2003). A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426, 845-849.
45. Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D. M. and Rajewsky, K. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501.
46. Kidner, C. A. and Martienssen, R. A. (2005). The developmental role of microRNA in plants. Curr. Opin. Plant Biol. 8, 38-44.
47. Kiriakidou, M., Nelson, P. T., Kouranov, A., Fitziev, P., Bouyioukos, C., Mourelatos, Z. and Hatzigeorgiou, A. (2004). A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 18, 1165-1178.
48. Knight, S. W. and Bass, B. L. (2001). A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 293, 2269-2271.
49. Knight, S. W. and Bass, B. L. (2002). The role of RNA editing by ADARs in RNAi. Mol. Cell 10, 809-817.
50. Knust, E. (1997). Drosophila morphogenesis: movements behind the edge. Curr. Biol. 7, R558-R561.
51. Knust, E., Schrons, H., Grawe, F. and Campos-Ortega, J. A. (1992). Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132, 505-518.
52. Lagos-Quintana, M., Rauhut, R., Lendeckel, W. and Tuschl, T. (2001). Identification of novel genes coding for small expressed RNAs. Science 294, 853-858.
53. Lai, E. C. (2002). Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30, 363-364.
54. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
55. Lai, E. C. and Posakony, J. W. (1997). The Bearded box, a novel 3′ UTR sequence motif, mediates negative post-transcriptional regulation of Bearded and Enhancer of split Complex gene expression. Development 124, 4847-4856.
56. Lai, E. C., Burks, C. and Posakony, J. W. (1998). The K box, a conserved 3′ UTR sequence motif, negatively regulates accumulation of enhancer of split complex transcripts. Development 125, 4077-4088.
57. Lai, E. C., Bodner, R., Kavaler, J., Freschi, G. and Posakony, J. W. (2000a). Antagonism of notch signaling activity by members of a novel protein family encoded by the bearded and enhancer of split gene complexes. Development 127, 291-306.
58. Lai, E. C., Bodner, R. and Posakony, J. W. (2000b). The enhancer of split complex of Drosophila includes four Notch-regulated members of the bearded gene family. Development 127, 3441-3455.
59. Lai, E. C., Tam, B. and Rubin, G. M. (2005). Pervasive regulation of Drosophila Notch target genes by GY box-, Brd-box-, and K-box-class microRNAs. Genes Dev. 19, 1067-1080.
60. Landthaler, M., Yalcin, A. and Tuschl, T. (2004). The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol. 14, 2162-2167.
61. Lau, N. C., Lim, L. P., Weinstein, E. G. and Bartel, D. P. (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858-862.
62. Leaman, D., Chen, P. Y., Fak, J., Yalcin, A., Pearce, M., Unnerstall, U., Marks, D. S., Sander, C., Tuschl, T. and Gaul, U. (2005). Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121, 1097-1108.
63. Lecellier, C. H., Dunoyer, P., Arar, K., Lehmann-Che, J., Eyquem, S., Himber, C., Saib, A. and Voinnet, O. (2005). A cellular microRNA mediates antiviral defense in human cells. Science 308, 557-560.
64. Lee, R. C. and Ambros, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864.
65. Lee, R. C., Feinbaum, R. L. and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854.
66. Lee, R., Feinbaum, R. and Ambros, V. (2004a). A short history of a short RNA. Cell 116, S89-S96.
67. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S. et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419.
68. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004b). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81.
69. Leviten, M. W., Lai, E. C. and Posakony, J. W. (1997). The Drosophila gene Bearded encodes a novel small protein and shares 3′ UTR sequence motifs with multiple Enhancer of split complex genes. Development 124, 4039-4051.
70. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P. and Burge, C. B. (2003). Prediction of mammalian microRNA targets. Cell 115, 787-798.
71. Lewis, B. P., Burge, C. B. and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20.
72. Lim, L. P., Glasner, M. E., Yekta, S., Burge, C. B. and Bartel, D. P. (2003a). Vertebrate microRNA genes. Science 299, 1540.
73. Lim, L. P., Lau, N. C., Weinstein, E. G., Abdelhakim, A., Yekta, S., Rhoades, M. W., Burge, C. B. and Bartel, D. P. (2003b). The microRNAs of Caenorhabditis elegans. Genes Dev. 17, 991-1008.
74. Lin, M., Jones-Rhoades, M. W., Lau, N. C., Bartel, D. P. and Rougvie, A. E. (2005). Regulatory mutations upstream of mir-48, a C. elegans let-7 family microRNA cause developmental timing defects. Dev. Cell 9, 415-422.
75. Lin, S. Y., Johnson, S. M., Abraham, M., Vella, M. C., Pasquinelli, A., Gamberi, C., Gottlieb, E. and Slack, F. J. (2003). The C elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell 4, 639-650.
76. Lindsay, E. A. (2001). Chromosomal microdeletions: dissecting del22q11 syndrome. Nat. Rev. Genet. 2, 858-868.
77. Llave, C., Kasschau, K. D., Rector, M. A. and Carrington, J. C. (2002). Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605-1619.
78. Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A. et al. (2005). MicroRNA expression profiles classify human cancers. Nature 435, 834.
79. Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E. and Kutay, U. (2003). Nuclear export of microRNA precursors. Science 303, 95-98.
80. Mansfield, J. H., Harfe, B. D., Nissen, R., Obenauer, J., Srineel, J., Chaudhuri, A., Farzan-Kashani, R., Zuker, M., Pasquinelli, A. E., Ruvkun, G. et al. (2004). MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat. Genet. 36, 1079-1083.
81. McManus, M. T. (2003). MicroRNAs and cancer. Semin. Cancer Biol. 13, 253-258.
82. Meins, F., Jr, Si-Ammour, A. and Blevins, T. (2005). RNA silencing systems and their relevance to plant development. Annu. Rev. Cell Dev. Biol. (in press).
83. Meister, G., Landthaler, M., Dorsett, Y. and Tuschl, T. (2004). Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. Rna 10, 544-550.
84. Mochizuki, K. and Gorovsky, M. A. (2005). A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19, 77-89.
85. Muljo, S. A., Ansel, K. M., Kanellopoulou, C., Livingston, D. M., Rao, A. and Rajewsky, K. (2005). Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202, 261-269.
86. O'Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V. and Mendell, J. T. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839-843.
87. Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B., Muller, P. et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89.
88. Pasquinelli, A. E., McCoy, A., Jimenez, E., Salo, E., Ruvkun, G., Martindale, M. Q. and Baguna, J. (2003). Expression of the 22 nucleotide let-7 heterochronic RNA throughout the Metazoa: a role in life history evolution? Evol. Dev. 5, 372-378.
89. Petersen, M. and Wengel, J. (2003). LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol. 21, 74-81.
90. Pfeffer, S., Zavolan, M., Grasser, F. A., Chien, M., Russo, J. J., Ju, J., John, B., Enright, A. J., Marks, D., Sander, C. et al. (2004). Identification of virus-encoded microRNAs. Science 304, 734-736.
91. Pfeffer, S., Sewer, A., Lagos-Quintana, M., Sheridan, R., Sander, C., Grasser, F. A., van Dyk, L. F., Ho, C. K., Shuman, S., Chien, M. et al. (2005). Identification of microRNAs of the herpesvirus family. Nat. Methods 2, 269-276.
92. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E. and Filipowicz, W. (2005). Inhibition of translational initiation by let-7 microRNA in human cells. Science (in press).
93. Poy, M. N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P. E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P. et al. (2004). A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432, 226-230.
94. Provost, P., Silverstein, R. A., Dishart, D., Walfridsson, J., Djupedal, I., Kniola, B., Wright, A., Samuelsson, B., Radmark, O. and Ekwall, K. (2002). Dicer is required for chromosome segregation and gene silencing in fission yeast cells. Proc. Natl. Acad. Sci. USA 99, 16648-16653.
95. Rajewsky, N. and Socci, N. D. (2004). Computational identification of microRNA targets. Dev. Biol. 267, 529-535.
96. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R. and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906.
97. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B. and Bartel, D. P. (2002). MicroRNAs in plants. Genes Dev. 16, 1616-1626.
98. Rougvie, A. E. (2005). Keeping time with microRNAs. Development (in press).
99. Ruvkun, G., Wightman, B. and Ha, I. (2004). The 20 years it took to recognize the importance of tiny RNAs. Cell 116, S93-S96.
100. Shiohama, A., Sasaki, T., Noda, S., Minoshima, S. and Shimizu, N. (2003). Molecular cloning and expression analysis of a novel gene DGCR8 located in the DiGeorge syndrome chromosomal region. Biochem. Biophys. Res. Commun. 304, 184-190.
101. Slack, F. J., Basson, M., Liu, Z., Ambros, V., Horvitz, H. R. and Ruvkun, G. (2000). 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, 659-669.
102. Smalheiser, N. R. and Torvik, V. I. (2005). Mammalian microRNAs derived from genomic repeats. Trends Genet. 21, 322-326.
103. Stark, A., Brennecke, J., Russell, R. B. and Cohen, S. M. (2003). Identification of Drosophila microRNA targets. PLoS Biol. 1, E60.
104. Suh, M. R., Lee, Y., Kim, J. Y., Kim, S. K., Moon, S. H., Lee, J. Y., Cha, K. Y., Chung, H. M., Yoon, H. S., Moon, S. Y. et al. (2004). Human embryonic stem cells express a unique set of microRNAs. Dev. Biol. 270, 488-498.
105. Sullivan, C. S., Grundhoff, A. T., Tevethia, S., Pipas, J. M. and Ganem, D. (2005). SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435, 682-686.
106. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
107. Tanzer, A. and Stadler, P. F. (2004). Molecular evolution of a microRNA cluster. J. Mol. Biol. 339, 327-335.
108. Tanzer, A., Amemiya, C. T., Kim, C. B. and Stadler, P. F. (2005). Evolution of microRNAs located within Hox gene clusters. J. Exp. Zoolog. B Mol. Dev. Evol. 304, 75-85.
109. Watanabe, T., Takeda, A., Mise, K., Okuno, T., Suzuki, T., Minami, N. and Imai, H. (2005). Stage-specific expression of microRNAs during Xenopus development. FEBS Lett. 579, 318-324.
110. Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E. and Plasterk, R. H. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat. Genet. 35, 217-218.
111. Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., Horvitz, R. H., Kauppinen, S. and Plasterk, R. H. (2005). MicroRNA Expression in Zebrafish Embryonic Development. Science 309, 310-311.
112. Wightman, B., Ha, I. and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862.
113. Wurmbach, E., Wech, I. and Preiss, A. (1999). The Enhancer of split complex of Drosophila melanogaster harbors three classes of Notch responsive genes. Mech. Dev. 80, 171-180.
114. Xie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., Lander, E. S. and Kellis, M. (2005). Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature 434, 338-345.
115. Xu, P., Vernooy, S. Y., Guo, M. and Hay, B. A. (2003). The Drosophila MicroRNA Mir-14 Suppresses Cell Death and Is Required for Normal Fat Metabolism. Curr. Biol. 13, 790-795.
116. Yekta, S., Shih, I. H. and Bartel, D. P. (2004). MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594-596.
117. Yi, R., Qin, Y., Macara, I. G. and Cullen, B. R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011-3016.
118. Zhao, Y., Samal, E. and Srivastava, D. (2005). Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436, 214-220.