Adenylation of maternally inherited MicroRNAs by wispy

Molecular Cell

Volumn 56, Issue 5, 2014, Pages 696-707

  Lee, Mihye ^a,b   Choi, Yeon ^a,b   Kim, Kijun ^a,b   Jin, Hua ^a,b   Lim, Jaechul ^a,b   Nguyen, Tuan Anh ^a,b   Yang, Jihye ^a,b   Jeong, Minsun ^c   Giraldez, Antonio J ^c   Yang, Hui ^d   Patel, Dinshaw J ^d   Kim, V Narry ^a,b  

^a Korea Basic Science Institute (KBSI)   (South Korea)

^b Seoul National University   (South Korea)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; MICRORNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; UNCLASSIFIED DRUG; WISPY; AGO1 PROTEIN, DROSOPHILA; ARGONAUTE PROTEIN; DROSOPHILA PROTEIN; POLYADENYLIC ACID; WISPY PROTEIN, DROSOPHILA;

ADENYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIPTERA; DROSOPHILA; EMBRYO; FEMALE; GENE OVEREXPRESSION; MOUSE; NONHUMAN; OOCYTE; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE; SEA URCHIN; ANIMAL; ANIMAL EMBRYO; CELL LINE; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS;

ECHINOIDEA;

ANIMALS; ARGONAUTE PROTEINS; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; MICRORNAS; MOLECULAR SEQUENCE DATA; OOCYTES; POLY A; POLYNUCLEOTIDE ADENYLYLTRANSFERASE;

EID: 84919482843     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.10.011     Document Type: Article

References (64)

1. Ameres S.L., Horwich M.D., Hung J.H., Xu J., Ghildiyal M., Weng Z., Zamore P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328:1534-1539.
2. Backes S., Shapiro J.S., Sabin L.R., Pham A.M., Reyes I., Moss B., Cherry S., tenOever B.R. Degradation of host microRNAs by poxvirus poly(A) polymerase reveals terminal RNA methylation as a protective antiviral mechanism. Cell Host Microbe 2012, 12:200-210.
3. Barckmann B., Simonelig M. Control of maternal mRNA stability in germ cells and early embryos. Biochim. Biophys. Acta 2013, 1829:714-724.
4. Baroux C., Autran D., Gillmor C.S., Grimanelli D., Grossniklaus U. The maternal to zygotic transition in animals and plants. Cold Spring Harb. Symp. Quant. Biol. 2008, 73:89-100.
5. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
6. Bashirullah A., Halsell S.R., Cooperstock R.L., Kloc M., Karaiskakis A., Fisher W.W., Fu W., Hamilton J.K., Etkin L.D., Lipshitz H.D. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 1999, 18:2610-2620.
7. Benoit P., Papin C., Kwak J.E., Wickens M., Simonelig M. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 2008, 135:1969-1979.
8. 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.
9. Brent A.E., MacQueen A., Hazelrigg T. The Drosophila wispy gene is required for RNA localization and other microtubule-based events of meiosis and early embryogenesis. Genetics 2000, 154:1649-1662.
10. Burns D.M., D'Ambrogio A., Nottrott S., Richter J.D. CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 2011, 473:105-108.
11. Burroughs A.M., Ando Y., de Hoon M.J., Tomaru Y., Nishibu T., Ukekawa R., Funakoshi T., Kurokawa T., Suzuki H., Hayashizaki Y., Daub C.O. A comprehensive survey of 3' animal miRNA modification events and a possible role for 3' adenylation in modulating miRNA targeting effectiveness. Genome Res. 2010, 20:1398-1410.
12. Bushati N., Cohen S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
13. Chang H.M., Triboulet R., Thornton J.E., Gregory R.I. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 2013, 497:244-248.
14. Cui J., Sackton K.L., Horner V.L., Kumar K.E., Wolfner M.F. Wispy, the Drosophila homolog of GLD-2, is required during oogenesis and egg activation. Genetics 2008, 178:2017-2029.
15. Cui J., Sartain C.V., Pleiss J.A., Wolfner M.F. Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila. Dev. Biol. 2013, 383:121-131.
16. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 2011, 12:19-31.
17. 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.
18. D'Ambrogio A., Gu W., Udagawa T., Mello C.C., Richter J.D. Specific miRNA stabilization by Gld2-catalyzed monoadenylation. Cell Rep. 2012, 2:1537-1545.
19. Fernandez-Valverde S.L., Taft R.J., Mattick J.S. Dynamic isomiR regulation in Drosophila development. RNA 2010, 16:1881-1888.
20. Gantier M.P., McCoy C.E., Rusinova I., Saulep D., Wang D., Xu D., Irving A.T., Behlke M.A., Hertzog P.J., Mackay F., Williams B.R. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res. 2011, 39:5692-5703.
21. Ha M., Kim V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15:509-524.
22. Hagan J.P., Piskounova E., Gregory R.I. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 2009, 16:1021-1025.
23. Harding J.L., Horswell S., Heliot C., Armisen J., Zimmerman L.B., Luscombe N.M., Miska E.A., Hill C.S. Small RNA profiling of Xenopus embryos reveals novel miRNAs and a new class of small RNAs derived from intronic transposable elements. Genome Res. 2014, 24:96-106.
24. Heifetz Y., Yu J., Wolfner M.F. Ovulation triggers activation of Drosophila oocytes. Dev. Biol. 2001, 234:416-424.
25. Heo I., Joo C., Cho J., Ha M., Han J., Kim V.N. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell 2008, 32:276-284.
26. Heo I., Joo C., Kim Y.K., Ha M., Yoon M.J., Cho J., Yeom K.H., Han J., Kim V.N. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009, 138:696-708.
27. Heo I., Ha M., Lim J., Yoon M.J., Park J.E., Kwon S.C., Chang H., Kim V.N. Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell 2012, 151:521-532.
28. Ibrahim F., Rymarquis L.A., Kim E.J., Becker J., Balassa E., Green P.J., Cerutti H. Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl. Acad. Sci. USA 2010, 107:3906-3911.
29. Katoh T., Sakaguchi Y., Miyauchi K., Suzuki T., Kashiwabara S., Baba T., Suzuki T. Selective stabilization of mammalian microRNAs by 3' adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 2009, 23:433-438.
30. Kawamata T., Tomari Y. Making RISC. Trends Biochem. Sci. 2010, 35:368-376.
31. 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.
32. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 2009, 10:126-139.
33. Kim Y.K., Heo I., Kim V.N. Modifications of small RNAs and their associated proteins. Cell 2010, 143:703-709.
34. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610.
35. Kwak J.E., Drier E., Barbee S.A., Ramaswami M., Yin J.C., Wickens M. GLD2 poly(A) polymerase is required for long-term memory. Proc. Natl. Acad. Sci. USA 2008, 105:14644-14649.
36. Liu N., Abe M., Sabin L.R., Hendriks G.J., Naqvi A.S., Yu Z., Cherry S., Bonini N.M. The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr. Biol. 2011, 21:1888-1893.
37. 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.
38. Martin G., Keller W. Mutational analysis of mammalian poly(A) polymerase identifies a region for primer binding and catalytic domain, homologous to the family X polymerases, and to other nucleotidyltransferases. EMBO J. 1996, 15:2593-2603.
39. Mendez R., Richter J.D. Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2001, 2:521-529.
40. Nakanishi T., Kubota H., Ishibashi N., Kumagai S., Watanabe H., Yamashita M., Kashiwabara S., Miyado K., Baba T. Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev. Biol. 2006, 289:115-126.
41. Neilsen C.T., Goodall G.J., Bracken C.P. IsomiRs the overlooked repertoire in the dynamic microRNAome. Trends Genet. 2012, 28:544-549.
42. Newman M.A., Thomson J.M., Hammond S.M. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 2008, 14:1539-1549.
43. Ohnishi Y., Totoki Y., Toyoda A., Watanabe T., Yamamoto Y., Tokunaga K., Sakaki Y., Sasaki H., Hohjoh H. Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development. Nucleic Acids Res. 2010, 38:5141-5151.
44. Pall G.S., Hamilton A.J. Improved northern blot method for enhanced detection of small RNA. Nat. Protoc. 2008, 3:1077-1084.
45. Ramachandran V., Chen X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 2008, 321:1490-1492.
46. Richter J.D. Cytoplasmic polyadenylation in development and beyond. Microbiol. Mol. Biol. Rev. 1999, 63:446-456.
47. Rouhana L., Wang L., Buter N., Kwak J.E., Schiltz C.A., Gonzalez T., Kelley A.E., Landry C.F., Wickens M. Vertebrate GLD2 poly(A) polymerases in the germline and the brain. RNA 2005, 11:1117-1130.
48. Rybak A., Fuchs H., Smirnova L., Brandt C., Pohl E.E., Nitsch R., Wulczyn F.G. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 2008, 10:987-993.
49. Schmidt M.J., Norbury C.J. Polyadenylation and beyond: emerging roles for noncanonical poly(A) polymerases. Wiley Interdiscip Rev RNA 2010, 1:142-151.
50. Semotok J.L., Luo H., Cooperstock R.L., Karaiskakis A., Vari H.K., Smibert C.A., Lipshitz H.D. Drosophila maternal Hsp83 mRNA destabilization is directed by multiple SMAUG recognition elements in the open reading frame. Mol. Cell. Biol. 2008, 28:6757-6772.
51. Song J.L., Stoeckius M., Maaskola J., Friedländer M., Stepicheva N., Juliano C., Lebedeva S., Thompson W., Rajewsky N., Wessel G.M. Select microRNAs are essential for early development in the sea urchin. Dev. Biol. 2012, 362:104-113.
52. Sotiropoulou G., Pampalakis G., Lianidou E., Mourelatos Z. Emerging roles of microRNAs as molecular switches in the integrated circuit of the cancer cell. RNA 2009, 15:1443-1461.
53. 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.
54. Svoboda P. Why mouse oocytes and early embryos ignore miRNAs?. RNA Biol. 2010, 7:559-563.
55. Tadros W., Lipshitz H.D. Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Dev. Dyn. 2005, 232:593-608.
56. Tadros W., Lipshitz H.D. The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042.
57. Thornton J.E., Chang H.M., Piskounova E., Gregory R.I. Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA 2012, 18:1875-1885.
58. Udagawa T., Swanger S.A., Takeuchi K., Kim J.H., Nalavadi V., Shin J., Lorenz L.J., Zukin R.S., Bassell G.J., Richter J.D. Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol. Cell 2012, 47:253-266.
59. Viswanathan S.R., Daley G.Q., Gregory R.I. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
60. Walser C.B., Lipshitz H.D. Transcript clearance during the maternal-to-zygotic transition. Curr. Opin. Genet. Dev. 2011, 21:431-443.
61. Wang Y., Juranek S., Li H., Sheng G., Wardle G.S., Tuschl T., Patel D.J. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 2009, 461:754-761.
62. Wyman S.K., Knouf E.C., Parkin R.K., Fritz B.R., Lin D.W., Dennis L.M., Krouse M.A., Webster P.J., Tewari M. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res. 2011, 21:1450-1461.
63. Yeom K.H., Heo I., Lee J., Hohng S., Kim V.N., Joo C. Single-molecule approach to immunoprecipitated protein complexes: insights into miRNA uridylation. EMBO Rep. 2011, 12:690-696.
64. Zhao Y., Yu Y., Zhai J., Ramachandran V., Dinh T.T., Meyers B.C., Mo B., Chen X. The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr. Biol. 2012, 22:689-694.