Systematic study of Drosophila MicroRNA functions using a collection of targeted knockout mutations

Developmental Cell

Volumn 31, Issue 6, 2014, Pages 784-800

  Chen, Ya Wen ^a   Song, Shilin ^a   Weng, Ruifen ^a   Verma, Pushpa ^a   Kugler, Jan Michael ^a   Buescher, Marita ^a   Rouam, Sigrid ^c   Cohen, StephenM ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c PROCTER AND GAMBLE COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

ARTICLE; BLOOD BRAIN BARRIER; CHROMOSOME DELETION; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; FEMALE; FEMALE FERTILITY; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GERMLINE STEM CELL; HOMOLOGOUS RECOMBINATION; LARVAL DEVELOPMENT; MALE; MALE FERTILITY; NONHUMAN; PRIMORDIAL GERM CELL; RNA SPLICING; ALLELE; ANIMAL; BIOLOGY; GENE VECTOR; GENETIC RECOMBINATION; GENETICS; METABOLISM; MULTIGENE FAMILY; MUTATION; PHENOTYPE;

ANIMALIA;

ALLELES; ANIMALS; COMPUTATIONAL BIOLOGY; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VECTORS; MALE; MICRORNAS; MULTIGENE FAMILY; MUTATION; PHENOTYPE; RECOMBINATION, GENETIC;

EID: 84919481618     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.11.029     Document Type: Article

References (90)

1. Abbott A.L., Alvarez-Saavedra E., Miska E.A., Lau N.C., Bartel D.P., Horvitz H.R., Ambros V. The let-7 MicroRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev. Cell 2005, 9:403-414.
2. Alvarez-Saavedra E., Horvitz H.R. Many families of C. elegans microRNAs are not essential for development or viability. Curr. Biol. 2010, 20:367-373.
3. Arif S., Murat S., Almudi I., Nunes M.D., Bortolamiol-Becet D., McGregor N.S., Currie J.M., Hughes H., Ronshaugen M., Sucena É., et al. Evolution of mir-92a underlies natural morphological variation in Drosophila melanogaster. Curr. Biol. 2013, 23:523-528.
4. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71.
5. Bainton R.J., Tsai L.T., Schwabe T., DeSalvo M., Gaul U., Heberlein U. moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 2005, 123:145-156.
6. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
7. Becam I., Rafel N., Hong X., Cohen S.M., Milán M. Notch-mediated repression of bantam miRNA contributes to boundary formation in the Drosophila wing. Development 2011, 138:3781-3789.
8. 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.
9. Bejarano F., Bortolamiol-Becet D., Dai Q., Sun K., Saj A., Chou Y.T., Raleigh D.R., Kim K., Ni J.Q., Duan H., et al. A genome-wide transgenic resource for conditional expression of Drosophila microRNAs. Development 2012, 139:2821-2831.
10. Bender W. MicroRNAs in the Drosophila bithorax complex. Genes Dev. 2008, 22:14-19.
11. Boehm M., Slack F. A developmental timing microRNA and its target regulate life span in C. elegans. Science 2005, 310:1954-1957.
12. 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 2003, 113:25-36.
13. Brennecke J., Stark A., Russell R.B., Cohen S.M. Principles of microRNA-target recognition. PLoS Biol. 2005, 3:e85.
14. Brenner J.L., Jasiewicz K.L., Fahley A.F., Kemp B.J., Abbott A.L. Loss of individual microRNAs causes mutant phenotypes in sensitized genetic backgrounds in C. elegans. Curr. Biol. 2010, 20:1321-1325.
15. Broughton S.J., Piper M.D., Ikeya T., Bass T.M., Jacobson J., Driege Y., Martinez P., Hafen E., Withers D.J., Leevers S.J., Partridge L. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad. Sci. USA 2005, 102:3105-3110.
16. Bushati N., Cohen S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
17. Bushati N., Stark A., Brennecke J., Cohen S.M. Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition inDrosophila. Curr. Biol. 2008, 18:501-506.
18. Caygill E.E., Johnston L.A. Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr. Biol. 2008, 18:943-950.
19. Cayirlioglu P., Kadow I.G., Zhan X., Okamura K., Suh G.S., Gunning D., Lai E.C., Zipursky S.L. Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 2008, 319:1256-1260.
20. Chen Y.W., Weng R., Cohen S.M. Protocols for use of homologous recombination gene targeting to produce microRNA mutants in Drosophila. Methods Mol. Biol. 2011, 732:99-120.
21. Choi I.K., Hyun S. Conserved microRNA miR-8 in fat body regulates innate immune homeostasis in Drosophila. Dev. Comp. Immunol. 2012, 37:50-54.
22. 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.
23. Coulom H., Birman S. Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J.Neurosci. 2004, 24:10993-10998.
24. 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.
25. Da Ros V.G., Gutierrez-Perez I., Ferres-Marco D., Dominguez M. Dampening the signals transduced through hedgehog via microRNA miR-7 facilitates notch-induced tumourigenesis. PLoS Biol. 2013, 11:e1001554.
26. de Lencastre A., Pincus Z., Zhou K., Kato M., Lee S.S., Slack F.J. MicroRNAs both promote and antagonize longevity in C. elegans. Curr. Biol. 2010, 20:2159-2168.
27. Ebert M.S., Sharp P.A. Roles for microRNAs in conferring robustness to biological processes. Cell 2012, 149:515-524.
28. Farh K.K., Grimson A., Jan C., Lewis B.P., Johnston W.K., Lim L.P., Burge C.B., Bartel D.P. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 2005, 310:1817-1821.
29. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
30. Flynt A.S., Lai E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 2008, 9:831-842.
31. Friggi-Grelin F., Lavenant-Staccini L., Therond P. Control of antagonistic components of the hedgehog signaling pathway by microRNAs in Drosophila. Genetics 2008, 179:429-439.
32. Ge W., Chen Y.W., Weng R., Lim S.F., Buescher M., Zhang R., Cohen S.M. Overlapping functions of microRNAs in control of apoptosis during Drosophila embryogenesis. Cell Death Differ. 2012, 19:839-846.
33. 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.
34. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van Dongen S., Inoue K., Enright A.J., Schier A.F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79.
35. Gong W.J., Golic K.G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 2003, 100:2556-2561.
36. Granzotto A., Lopes F.R., Lerat E., Vieira C., Carareto C.M. The evolutionary dynamics of the Helena retrotransposon revealed by sequenced Drosophila genomes. BMC Evol. Biol. 2009, 9:174.
37. Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158.
38. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
39. Hébert S.S., Horré K., Nicolaï L., Papadopoulou A.S., Mandemakers W., Silahtaroglu A.N., Kauppinen S., Delacourte A., De Strooper B. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. USA 2008, 105:6415-6420.
40. Herranz H., Cohen S.M. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 2010, 24:1339-1344.
41. Herranz H., Hong X., Cohen S.M. Mutual repression by bantam miRNA and Capicua links the EGFR/MAPK and Hippo pathways in growth control. Curr. Biol. 2012, 22:651-657.
42. Herranz H., Hong X., Hung N.T., Voorhoeve P.M., Cohen S.M. Oncogenic cooperation between SOCS family proteins and EGFR identified using a Drosophila epithelial transformation model. Genes Dev. 2012, 26:1602-1611.
43. Hilgers V., Bushati N., Cohen S.M. Drosophila microRNAs 263a/b confer robustness during development by protecting nascent sense organs from apoptosis. PLoS Biol. 2010, 8:e1000396.
44. Huang J., Zhou W., Watson A.M., Jan Y.N., Hong Y. Efficient ends-out gene targeting in Drosophila. Genetics 2008, 180:703-707.
45. Hyun S., Lee J.H., Jin H., Nam J., Namkoong B., Lee G., Chung J., Kim V.N. Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 2009, 139:1096-1108.
46. Iovino N., Pane A., Gaul U. miR-184 has multiple roles in Drosophila female germline development. Dev. Cell 2009, 17:123-133.
47. Jin H., Kim V.N., Hyun S. Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev. 2012, 26:1427-1432.
48. Karr J., Vagin V., Chen K., Ganesan S., Olenkina O., Gvozdev V., Featherstone D.E. Regulation of glutamate receptor subunit availability by microRNAs. J.Cell Biol. 2009, 185:685-697.
49. Karres J.S., Hilgers V., Carrera I., Treisman J., Cohen S.M. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 2007, 131:136-145.
50. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:D152-D157.
51. Kugler J.M., Chen Y.W., Weng R., Cohen S.M. Maternal loss of miRNAs leads to increased variance in primordial germ cell numbers in Drosophila melanogaster. G3 (Bethesda) 2013, 3:1573-1576.
52. Kugler J.M., Verma P., Chen Y.W., Weng R., Cohen S.M. miR-989 is required for border cell migration in the Drosophila ovary. PLoS ONE 2013, 8:e67075.
53. Lasko P. Posttranscriptional regulation in Drosophila oocytes and early embryos. Wiley Interdiscip Rev RNA 2011, 2:408-416.
54. 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 1993, 75:843-854.
55. Li X., Carthew R.W. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 2005, 123:1267-1277.
56. 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.
57. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew R.W. A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137:273-282.
58. Li W., Cressy M., Qin H., Fulga T., Van Vactor D., Dubnau J. MicroRNA-276a functions in ellipsoid body and mushroom body neurons for naive and conditioned olfactory avoidance in Drosophila. J Neurosci. 2013, 33:5821-5833.
59. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
60. Liu N., Landreh M., Cao K., Abe M., Hendriks G.J., Kennerdell J.R., Zhu Y., Wang L.S., Bonini N.M. The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 2012, 482:519-523.
61. Loya C.M., Lu C.S., Van Vactor D., Fulga T.A. Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat. Methods 2009, 6:897-903.
62. Luo W., Sehgal A. Regulation of circadian behavioral output via a MicroRNA-JAK/STAT circuit. Cell 2012, 148:765-779.
63. Mahowald A.P. Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 2001, 203:187-213.
64. Miska E.A., Alvarez-Saavedra E., Abbott A.L., Lau N.C., Hellman A.B., McGonagle S.M., Bartel D.P., Ambros V.R., Horvitz H.R. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 2007, 3:e215.
65. Morante J., Vallejo D.M., Desplan C., Dominguez M. Conserved miR-8/miR-200 defines a glial niche that controls neuroepithelial expansion and neuroblast transition. Dev. Cell 2013, 27:174-187.
66. 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.
67. Park C.Y., Jeker L.T., Carver-Moore K., Oh A., Liu H.J., Cameron R., Richards H., Li Z., Adler D., Yoshinaga Y., et al. A resource for the conditional ablation of microRNAs in the mouse. Cell Reports 2012, 1:385-391.
68. Prosser H.M., Koike-Yusa H., Cooper J.D., Law F.C., Bradley A. A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat. Biotechnol. 2011, 29:840-845.
69. Ruby J.G., Stark A., Johnston W.K., Kellis M., Bartel D.P., Lai E.C. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 2007, 17:1850-1864.
70. Schertel C., Rutishauser T., Förstemann K., Basler K. Functional characterization of Drosophila microRNAs by a novel invivo library. Genetics 2012, 192:1543-1552.
71. Selbach M., Schwanhäusser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63.
72. Shcherbata H.R., Ward E.J., Fischer K.A., Yu J.Y., Reynolds S.H., Chen C.H., Xu P., Hay B.A., Ruohola-Baker H. Stage-specific differences in the requirements for germline stem cell maintenance in the Drosophila ovary. Cell Stem Cell 2007, 1:698-709.
73. Sokol N.S., Ambros V. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev. 2005, 19:2343-2354.
74. Sokol N.S., Xu P., Jan Y.N., Ambros V. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev. 2008, 22:1591-1596.
75. Song Y., Ori-McKenney K.M., Zheng Y., Han C., Jan L.Y., Jan Y.N. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev. 2012, 26:1612-1625.
76. Stark A., Brennecke J., Bushati N., Russell R.B., Cohen S.M. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005, 123:1133-1146.
77. Szuplewski S., Kugler J.M., Lim S.F., Verma P., Chen Y.W., Cohen S.M. MicroRNA transgene overexpression complements deficiency-based modifier screens in Drosophila. Genetics 2012, 190:617-626.
78. Teleman A.A., Maitra S., Cohen S.M. Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev. 2006, 20:417-422.
79. Thompson B.J., Cohen S.M. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006, 126:767-774.
80. Varghese J., Cohen S.M. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev. 2007, 21:2277-2282.
81. Varghese J., Lim S.F., Cohen S.M. Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev. 2010, 24:2748-2753.
82. Vodala S., Pescatore S., Rodriguez J., Buescher M., Chen Y.W., Weng R., Cohen S.M., Rosbash M. The oscillating miRNA 959-964 cluster impacts Drosophila feeding time and other circadian outputs. Cell Metab. 2012, 16:601-612.
83. Weng R., Cohen S.M. Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. Development 2012, 139:1427-1434.
84. Weng R., Chen Y.W., Bushati N., Cliffe A., Cohen S.M. Recombinase-mediated cassette exchange provides a versatile platform for gene targeting: knockout of miR-31b. Genetics 2009, 183:399-402.
85. Weng R., Chin J.S., Yew J.Y., Bushati N., Cohen S.M. miR-124 controls male reproductive success in Drosophila. eLife 2013, 2:e00640.
86. 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 1993, 75:855-862.
87. Wu Y.C., Chen C.H., Mercer A., Sokol N.S. Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev. Cell 2012, 23:202-209.
88. 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. 2003, 13:790-795.
89. Yang Y., Xu S., Xia L., Wang J., Wen S., Jin P., Chen D. The bantam microRNA is associated with Drosophila fragile X mental retardation protein and regulates the fate of germline stem cells. PLoS Genet. 2009, 5:e1000444.
90. Zhang W., Cohen S.M. The Hippo pathway acts via p53 and microRNAs to control proliferation and proapoptotic gene expression during tissue growth. Biol. Open 2013, 2:822-828.