Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division

Developmental Biology

Volumn 365, Issue 2, 2012, Pages 384-394

  Azzam, Ghows ^a   Smibert, Peter ^b   Lai, Eric C ^b   Liu, Ji Long ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; DROSHA PROTEIN; DROSOPHILA PROTEIN; FODRIN; MICRORNA; PASHA PROTEIN; PROTEIN DCR 1; SPECTRIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL DIVISION; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; GENE INSERTION; IMMUNOREACTIVITY; INTRON; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

EID: 84860009222     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.005     Document Type: Article

References (61)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
3. 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.
4. Berdnik D., Fan A.P., Potter C.J., Luo L. MicroRNA processing pathway regulates olfactory neuron morphogenesis. Curr. Biol. 2008, 18:1754-1759.
5. Bohnsack M.T., Czaplinski K., Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 2004, 10:185-191.
6. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007, 128:1089-1103.
7. Buszczak M., Paterno S., Lighthouse D., Bachman J., Planck J., Owen S., Skora A.D., Nystul T.G., Ohlstein B., Allen A., Wilhelm J.E., Murphy T.D., Levis R.W., Matunis E., Srivali N., Hoskins R.A., Spradling A.C. The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 2007, 175:1505-1531.
8. Carrington J.C., Ambros V. Role of microRNAs in plant and animal development. Science 2003, 301:336-338.
9. Christerson L.B., Mckearin D.M. Orb Is Required for Anteroposterior and Dorsoventral Patterning during Drosophila Oogenesis. Genes Dev. 1994, 8:614-628.
10. Cox D.N., Lu B., Sun T.Q., Williams L.T., Jan Y.N. Drosophila par-1 is required for oocyte differentiation and microtubule organization. Curr. Biol. 2001, 11:75-87.
11. Czech B., Zhou R., Erlich Y., Brennecke J., Binari R., Villalta C., Gordon A., Perrimon N., Hannon G.J. Hierarchical rules for Argonaute loading in Drosophila. Mol. Cell 2009, 36:445-456.
12. de Cuevas M., Lee J.K., Spradling A.C. alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 1996, 122:3959-3968.
13. Denli A.M., Tops B.B., Plasterk R.H., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
14. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
15. Djuranovic S., Zinchenko M.K., Hur J.K., Nahvi A., Brunelle J.L., Rogers E.J., Green R. Allosteric regulation of Argonaute proteins by miRNAs. Nat. Struct. Mol. Biol. 2010, 17:144-150.
16. Flynt A.S., Lai E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 2008, 9:831-842.
17. Forstemann K., Horwich M.D., Wee L., Tomari Y., Zamore P.D. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 2007, 130:287-297.
18. Forstemann K., Tomari Y., Du T., Vagin V.V., Denli A.M., Bratu D.P., Klattenhoff C., Theurkauf W.E., Zamore P.D. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 2005, 3:e236.
19. Ghildiyal M., Xu J., Seitz H., Weng Z., Zamore P.D. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 2010, 16:43-56.
20. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
21. Gregory R.I., Yan K.P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
22. Han J., Lee Y., Yeom K.H., Kim Y.K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004, 18:3016-3027.
23. Hatfield S.D., Shcherbata H.R., Fischer K.A., Nakahara K., Carthew R.W., Ruohola-Baker H. Stem cell division is regulated by the microRNA pathway. Nature 2005, 435:974-978.
24. Hong A., Lee-Kong S., Iida T., Sugimura I., Lilly M.A. The p27cip/kip ortholog dacapo maintains the Drosophila oocyte in prophase of meiosis I. Development 2003, 130:1235-1242.
25. Huynh J.R., St Johnston D. The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 2000, 127:2785-2794.
26. Huynh J.R., St Johnston D. The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr. Biol. 2004, 14:R438-R449.
27. Iovino N., Pane A., Gaul U. miR-184 has multiple roles in Drosophila female germline development. Dev. Cell 2009, 17:123-133.
28. Jin Z., Xie T. Dcr-1 maintains Drosophila ovarian stem cells. Curr. Biol. 2007, 17:539-544.
29. 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.
30. Kim K., Lee Y.S., Harris D., Nakahara K., Carthew R.W. The RNAi pathway initiated by Dicer-2 in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:39-44.
31. Kim V.N., Nam J.W. Genomics of microRNA. Trends Genet. 2006, 22:165-173.
32. Lai E.C. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 2002, 30:363-364.
33. Lantz V., Chang J.S., Horabin J.I., Bopp D., Schedl P. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 1994, 8:598-613.
34. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., Carthew R.W. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
35. Lilly M.A., Spradling A.C. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 1996, 10:2514-2526.
36. Lin H., Yue L., Spradling A.C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 1994, 120:947-956.
37. Lund E., Guttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303:95-98.
38. Martin R., Smibert P., Yalcin A., Tyler D.M., Schafer U., Tuschl T., Lai E.C. A Drosophila pasha mutant distinguishes the canonical microRNA and mirtron pathways. Mol. Cell. Biol. 2009, 29:861-870.
39. Mata J., Curado S., Ephrussi A., Rorth P. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 2000, 101:511-522.
40. Megosh H.B., Cox D.N., Campbell C., Lin H. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr. Biol. 2006, 16:1884-1894.
41. Nakahara K., Kim K., Sciulli C., Dowd S.R., Minden J.S., Carthew R.W. Targets of microRNA regulation in the Drosophila oocyte proteome. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12023-12028.
42. Nakamura A., Sato K., Hanyu-Nakamura K. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 2004, 6:69-78.
43. 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.
44. 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.
45. Okamura K., Liu N., Lai E.C. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol. Cell 2009, 36:431-444.
46. Piccioni F., Zappavigna V., Verrotti A.C. A cup full of functions. RNA Biol. 2005, 2:125-128.
47. Reich J., Snee M.J., Macdonald P.M. miRNA-dependent translational repression in the Drosophila ovary. PLoS One 2009, 4:e4669.
48. Ruby J.G., Jan C.H., Bartel D.P. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86.
49. Saito K., Ishizuka A., Siomi H., Siomi M.C. Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 2005, 3:e235.
50. Senger S., Csokmay J., Akbar T., Jones T.I., Sengupta P., Lilly M.A. The nucleoporin Seh1 forms a complex with Mio and serves an essential tissue-specific function in Drosophila oogenesis. Development 2011, 138:2133-2142.
51. 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.
52. Smibert P., Bejarano F., Wang D., Garaulet D.L., Yang J.S., Martin R., Bortolamiol-Becet D., Robine N., Hiesinger P.R., Lai E.C. A Drosophila genetic screen yields allelic series of core microRNA biogenesis factors and reveals post-developmental roles for microRNAs. RNA 2011, 17:1997-2010.
53. Spradling A.C. Developmental genetics of oogenesis. The development of Drosophila melanogaster 1993, 1:1-70.
54. Stark A., Bushati N., Jan C.H., Kheradpour P., Hodges E., Brennecke J., Bartel D.P., Cohen S.M., Kellis M. A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev. 2008, 22:8-13.
55. Tomari Y., Du T., Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130:299-308.
56. Xie T., Spradling A.C. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 1998, 94:251-260.
57. Yang L., Chen D., Duan R., Xia L., Wang J., Qurashi A., Jin P., Chen D. Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development 2007, 134:4265-4272.
58. 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. 2003, 17:3011-3016.
59. Yu J.Y., Reynolds S.H., Hatfield S.D., Shcherbata H.R., Fischer K.A., Ward E.J., Long D., Ding Y., Ruohola-Baker H. Dicer-1-dependent Dacapo suppression acts downstream of Insulin receptor in regulating cell division of Drosophila germline stem cells. Development 2009, 136:1497-1507.
60. Zappavigna V., Piccioni F., Villaescusa J.C., Verrotti A.C. Cup is a nucleocytoplasmic shuttling protein that interacts with the eukaryotic translation initiation factor 4E to modulate Drosophila ovary development. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:14800-14805.
61. Zecca M., Struhl G. Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development 2002, 129:1357-1368.