Adaptive regulation of testis gene expression and control of male fertility by the drosophila harpin RNA pathway

Molecular Cell

Volumn 57, Issue 1, 2015, Pages 165-178

  Wen, Jiayu ^a   Duan, Hong ^a   Bejarano, Fernando ^a   Okamura, Katsutomo ^a,e   Fabian, Lacramioara ^b   Brill, Julie A ^b,c   Bortolamiol Becet, Diane ^a   Martin, Raquel ^a,f   Ruby, J Graham ^d,g   Lai, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^g Calico Life Sciences LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; INSECT PROTEIN; PROTEIN SUBUNIT;

ADULT; ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EVOLUTION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE TARGETING; GENETIC CODE; GERM CELL; MALE; MALE FERTILITY; NONHUMAN; ORGANISMAL INTERACTION; PHENOTYPE; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS; ADAPTATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CONFORMATION; DROSOPHILA MELANOGASTER; FERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SUBUNIT; SPERMATOZOON;

METAZOA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; FERTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSECT PROTEINS; MALE; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN SUBUNITS; RNA, SMALL INTERFERING; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 84920565409     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.11.025     Document Type: Article

References (60)

1. Allen E., Xie Z., Gustafson A.M., Sung G.H., Spatafora J.W., Carrington J.C. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 2004, 36:1282-1290.
2. Axtell M.J., Westholm J.O., Lai E.C. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 2011, 12. 10.1186/gb-2011-12-4-221.
3. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
4. Bartel D.P., Chen C.Z. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 2004, 5:396-400.
5. Bastide H., Cazemajor M., Ogereau D., Derome N., Hospital F., Montchamp-Moreau C. Rapid rise and fall of selfish sex-ratio X chromosomes in Drosophila simulans: spatiotemporal analysis of phenotypic and molecular data. Mol. Biol. Evol. 2011, 28:2461-2470.
6. 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.
7. Brennecke J., Stark A., Russell R.B., Cohen S.M. Principles of microRNA-target recognition. PLoS Biol. 2005, 3:e85.
8. Brown J.B., Boley N., Eisman R., May G.E., Stoiber M.H., Duff M.O., Booth B.W., Wen J., Park S., Suzuki A.M., et al. Diversity and dynamics of the Drosophila transcriptome. Nature 2014, 512:393-399.
9. Chen K., Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet. 2007, 8:93-103.
10. Chen S., Krinsky B.H., Long M. New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 2013, 14:645-660.
11. Chintapalli V.R., Wang J., Dow J.A. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 2007, 39:715-720.
12. 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.
13. 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.
14. Dai H., Chen Y., Chen S., Mao Q., Kennedy D., Landback P., Eyre-Walker A., Du W., Long M. The evolution of courtship behaviors through the origination of a new gene in Drosophila. Proc. Natl. Acad. Sci. USA 2008, 105:7478-7483.
15. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
16. Elde N.C., Child S.J., Eickbush M.T., Kitzman J.O., Rogers K.S., Shendure J., Geballe A.P., Malik H.S. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 2012, 150:831-841.
17. Fabian L., Brill J.A. Drosophila spermiogenesis: Big things come from little packages. Spermatogenesis 2012, 2:197-212.
18. Fabrizio J.J., Hime G., Lemmon S.K., Bazinet C. Genetic dissection of sperm individualization in Drosophila melanogaster. Development 1998, 125:1833-1843.
19. Fahlgren N., Howell M.D., Kasschau K.D., Chapman E.J., Sullivan C.M., Cumbie J.S., Givan S.A., Law T.F., Grant S.R., Dangl J.L., Carrington J.C. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2007, 2:e219.
20. Floyd S.K., Bowman J.L. Gene regulation: ancient microRNA target sequences in plants. Nature 2004, 428:485-486.
21. Förstemann 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.
22. Ghildiyal M., Seitz H., Horwich M.D., Li C., Du T., Lee S., Xu J., Kittler E.L., Zapp M.L., Weng Z., Zamore P.D. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008, 320:1077-1081.
23. Hain D., Bettencourt B.R., Okamura K., Csorba T., Meyer W., Jin Z., Biggerstaff J., Siomi H., Hutvagner G., Lai E.C., et al. Natural variation of the amino-terminal glutamine-rich domain in Drosophila argonaute2 is not associated with developmental defects. PLoS ONE 2010, 5:e15264.
24. Halic M., Moazed D. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 2010, 140:504-516.
25. Hartig J.V., Esslinger S., Böttcher R., Saito K., Förstemann K. Endo-siRNAs depend on a new isoform of loquacious and target artificially introduced, high-copy sequences. EMBO J. 2009, 28:2932-2944.
26. Horwich M.D., Li C., Matranga C., Vagin V., Farley G., Wang P., Zamore P.D. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 2007, 17:1265-1272.
27. 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.
28. Kemp C., Mueller S., Goto A., Barbier V., Paro S., Bonnay F., Dostert C., Troxler L., Hetru C., Meignin C., et al. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J.Immunol. 2013, 190:650-658.
29. Lai E.C. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 2002, 30:363-364.
30. 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.
31. Lee H.C., Li L., Gu W., Xue Z., Crosthwaite S.K., Pertsemlidis A., Lewis Z.A., Freitag M., Selker E.U., Mello C.C., Liu Y. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 2010, 38:803-814.
32. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
33. 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. MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat. Genet. 2004, 36:1079-1083.
34. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011, 39(Database issue):D225-D229.
35. Maurin T., Cazalla D., Yang S., Bortolamiol-Becet D., Lai E.C. RNase III-independent microRNA biogenesis in mammalian cells. RNA 2012, 18:2166-2173.
36. Mohammed J., Bortolamiol-Becet D., Flynt A.S., Gronau I., Siepel A., Lai E.C. Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila. RNA 2014, 20:1195-1209.
37. Moran Y., Fredman D., Praher D., Li X.Z., Wee L.M., Rentzsch F., Zamore P.D., Technau U., Seitz H. Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res. 2014, 24:651-663.
38. Okamura K., Lai E.C. Endogenous small interfering RNAs in animals. Nat. Rev. Mol. Cell Biol. 2008, 9:673-678.
39. 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.
40. Okamura K., Balla S., Martin R., Liu N., Lai E.C. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat. Struct. Mol. Biol. 2008, 15:581-590.
41. 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.
42. Okamura K., Chung W.J., Lai E.C. The long and short of inverted repeat genes in animals: microRNAs, mirtrons and hairpin RNAs. Cell Cycle 2008, 7:2840-2845.
43. * species has substantial influence on microRNA and 3' UTR evolution. Nat. Struct. Mol. Biol. 2008, 15:354-363.
44. Parker B.J., Moltke I., Roth A., Washietl S., Wen J., Kellis M., Breaker R., Pedersen J.S. New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes. Genome Res. 2011, 21:1929-1943.
45. Rajagopalan R., Vaucheret H., Trejo J., Bartel D.P. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 2006, 20:3407-3425.
46. Rhoades M.W., Reinhart B.J., Lim L.P., Burge C.B., Bartel B., Bartel D.P. Prediction of plant microRNA targets. Cell 2002, 110:513-520.
47. 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.
48. 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.
49. Seitz H., Youngson N., Lin S.P., Dalbert S., Paulsen M., Bachellerie J.P., Ferguson-Smith A.C., Cavaillé J. Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat. Genet. 2003, 34:261-262.
50. Smibert P., Yang J.S., Azzam G., Liu J.L., Lai E.C. Homeostatic control of Argonaute stability by microRNA availability. Nat. Struct. Mol. Biol. 2013, 20:789-795.
51. Tao Y., Araripe L., Kingan S.B., Ke Y., Xiao H., Hartl D.L. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biol. 2007, 5:e293.
52. Tao Y., Masly J.P., Araripe L., Ke Y., Hartl D.L. A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor. PLoS Biol. 2007, 5:e292.
53. Wang W., Brunet F.G., Nevo E., Long M. Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2002, 99:4448-4453.
54. Wen J., Mohammed J., Bortolamiol-Becet D., Tsai H., Robine N., Westholm J.O., Ladewig E., Dai Q., Okamura K., Flynt A.S., et al. Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines. Genome Res. 2014, 24:1236-1250.
55. White-Cooper H. Tissue, cell type and stage-specific ectopic gene expression and RNAi induction in the Drosophila testis. Spermatogenesis 2012, 2:11-22.
56. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 2007, 24:1586-1591.
57. Yang J.S., Lai E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 2011, 43:892-903.
58. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
59. Zhao L., Saelao P., Jones C.D., Begun D.J. Origin and spread of de novo genes in Drosophila melanogaster populations. Science 2014, 343:769-772.
60. Zhou R., Czech B., Brennecke J., Sachidanandam R., Wohlschlegel J.A., Perrimon N., Hannon G.J. Processing of Drosophila endo-siRNAs depends on a specific Loquacious isoform. RNA 2009, 15:1886-1895.