Homology-dependent silencing by an exogenous sequence in the drosophila germline

G3: Genes, Genomes, Genetics

Volumn 2, Issue 3, 2012, Pages 331-338

  Pöyhönen, Maria ^a   de Vanssay, Augustin ^a   Delmarre, Valérie ^a   Hermant, Catherine ^a   Todeschini, Anne Laure ^a,b   Teysset, Laure ^a   Ronsseray, Stéphane ^a  

^a Université René Descartes   (France)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

Drosophila; Elements; Epigenetics; Germline; RNA silencing; Transposable

Indexed keywords

EID: 84874251943     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.111.001925     Document Type: Article

References (73)

1. Ajioka, J. W., and W. F. Eanes, 1989 The accumulation of P-elements on the tip of the X chromosome in populations of Drosophila melanogaster. Genet. Res. 53: 1-6.
2. Anxolabehere, D., M. G. Kidwell, and G. Periquet, 1988 Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol. Biol. Evol. 5: 252-269.
3. Blackman, R. K., R. Grimaila, M. M. Koehler, andW. M. Gelbart, 1987 Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell 49: 497-505.
4. Blackman, R. K., and W.M. Gelbart, 1989 The transposable hobo of Drosophila melanogaster, pp. 523-529 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, DC.
5. Boivin, A., C. Gally, S. Netter, D. Anxolabehere, and S. Ronsseray, 2003 Telomeric associated sequences of Drosophila recruit polycomb-group proteins in vivo and can induce pairing-sensitive repression. Genetics 164: 195-208.
6. Brennecke, J., A. A. Aravin, A. Stark, M. Dus, M. Kellis et al., 2007 Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
7. Brennecke, J., C. D. Malone, A. A. Aravin, R. Sachidanandam, A. Stark et al., 2008 An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322: 1387-1392.
8. Bucheton, A., 1979 Non-Mendelian female sterility in Drosophila melanogaster: influence of aging and thermic treatments. III. Cumulative effects induced by these factors. Genetics 93: 131-142.
9. Bucheton, A., J. M. Lavige, G. Picard, and P. L'Heritier, 1976 Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity 36: 305-314.
10. Bucheton, A., I. Busseau, and D. Teninges, 2002 I Elements in Drosophila melanogaster, pp. 523-525 in Mobile DNA II, edited by N. L. Craig, R. Craigie, Gellert et al., American Society for Microbiology, Washington, DC.
11. Cam, H. P., K. Noma, H. Ebina, H. L. Levin, and S. I. Grewal, 2008 Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451: 431-436.
12. Cary, L. C., M. Goebel, B. G. Corsaro, H. G. Wang, E. Rosen et al., 1989 Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172: 156-169.
13. Chambeyron, S., and A. Bucheton, 2005 I elements in Drosophila: in vivo retrotransposition and regulation. Cytogenet. Genome Res. 110: 215-222.
14. Chambeyron, S., A. Popkova, G. Payen-Groschene, C. Brun, D. Laouini et al., 2008 piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc. Natl. Acad. Sci. USA 105: 14964-14969.
15. Coen, D., B. Lemaitre, M. Delattre, H. Quesneville, S. Ronsseray et al., 1994 Drosophila P element: transposition, regulation and evolution. Genetica 93: 61-78.
16. Desset, S., C. Meignin, B. Dastugue, and C. Vaury, 2003 COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164: 501-509.
17. Desset, S., N. Buchon, C. Meignin, M. Coiffet, and C. Vaury, 2008 In Drosophila melanogaster the COM locus directs the somatic silencing of two retrotransposons through both piwi-dependent and -independent pathways. PLoS ONE 3: e1526.
18. Dorer, D. R., and S. Henikoff, 1994 Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993-1002.
19. Dorer, D. R., and S. Henikoff, 1997 Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics 147: 1181-1190.
20. Dufourt, J., E. Brasset, S. Desset, P. Pouchin, and C. Vaury, 2011 Polycomb group-dependent, heterochromatin protein 1-independent, chromatin structures silence retrotransposons in somatic tissues outside ovaries. DNA Res. 18: 451-461.
21. Engels, W. R., 1979 Hybrid dysgenesis in Drosophila melanogaster: rules of inheritance of female sterility. Genet. Res. 33: 219-236.
22. Engels, W. R., 1989 P elements in Drosophila, pp. 437-484 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, DC.
23. Fanti, L., D. R. Dorer, M. Berloco, S. Henikoff, and S. Pimpinelli, 1998 Heterochromatin protein 1 binds transgene arrays. Chromosoma 107: 286-292.
24. Finnegan, D. J., 1989 The I factor and I-R hybrid dysgenesis in Drosophila melanogaster, pp. 503-518, in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, DC.
25. Fraser, M. J., L. Cary, K. Boonvisudhi, and H. G. Wang, 1995 Assay for movement of Lepidopteran transposon IFP2 in insect cells using a baculovirus genome as a target DNA. Virology 211: 397-407.
26. Girard, A., and G. J. Hannon, 2008 Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol. 18: 136-148.
27. Girton, J. R., and K. M. Johansen, 2008 Chromatin structure and the regulation of gene expression: the lessons of PEV in Drosophila. Adv. Genet. 61: 1-43.
28. Gunawardane, L. S., K. Saito, K. M. Nishida, K. Miyoshi, Y. Kawamura et al., 2007 A slicer-mediated mechanism for repeat-associated siRNA 59 end formation in Drosophila. Science 315: 1587-1590.
29. Harris, A. N., and P. M. Macdonald, 2001 Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
30. Hartig, J. V., and K. Forstemann, 2011 Loqs-PD and R2D2 define independent pathways for RISC generation in Drosophila. Nucleic Acids Res. 39: 3836-3851.
31. Horn, C., N. Offen, S. Nystedt, U. Hacker, and E. A. Wimmer, 2003 piggyBacbased insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 163: 647-661.
32. Jensen, S., M. P. Gassama, and T. Heidmann, 1999 Taming of transposable elements by homology-dependent gene silencing. Nat. Genet. 21: 209-212.
33. Jensen, S., M. P. Gassama, X. Dramard, and T. Heidmann, 2002 Regulation of I-transposon activity in Drosophila: evidence for cosuppression of nonhomologous transgenes and possible role of ancestral I-related pericentromeric elements. Genetics 162: 1197-1209.
34. Josse, T., L. Teysset, A. L. Todeschini, C. M. Sidor, D. Anxolabehere et al., 2007 Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genet. 3: 1633-1643.
35. Josse, T., C. Maurel-Zaffran, A. de Vanssay, L. Teysset, A. L. Todeschini et al., 2008 Telomeric trans-silencing in Drosophila melanogaster: tissue specificity, development and functional interactions between non-homologous telomeres. PLoS ONE 3: e3249.
36. Karpen, G. H., and A. C. Spradling, 1992 Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics 132: 737-753.
37. Kidwell, M. G., J. F. Kidwell, and J. A. Sved, 1977 Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility, and male recombination. Genetics 86: 813-833.
38. Klenov, M. S., S. A. Lavrov, A. D. Stolyarenko, S. S. Ryazansky, A. A. Aravin et al., 2007 Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. Nucleic Acids Res. 35: 5430-5438.
39. Laski, F. A., D. C. Rio, and G.M. Rubin, 1986 Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44: 7-19.
40. Li, X., N. Lobo, C. A. Bauser, andM. J. Fraser Jr., 2001 The minimum internal and external sequence requirements for transposition of the eukaryotic transformation vector piggyBac. Mol. Genet. Genomics 266: 190-198.
41. Li, X., R. A. Harrell, A. M. Handler, T. Beam, K. Hennessy et al., 2005 piggyBac internal sequences are necessary for efficient transformation of target genomes. Insect Mol. Biol. 14: 17-30.
42. Li, C.,V.V.Vagin, S. Lee, J. Xu, S. Ma et al., 2009 Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137: 509-521.
43. Malinsky, S., A. Bucheton, and I. Busseau, 2000 New insights on homologydependent silencing of I factor activity by transgenes containing ORF1 in Drosophila melanogaster. Genetics 156: 1147-1155.
44. Malone, C. D., J. Brennecke, M. Dus, A. Stark, W. R. McCombie et al., 2009 Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522-535.
45. Marin, L., M. Lehmann, D. Nouaud, H. Izaabel, D. Anxolabehere et al., 2000 P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics 155: 18411854.
46. Mevel-Ninio, M., A. Pelisson, J. Kinder, A. R. Campos, and A. Bucheton, 2007 The flamenco locus controls the gypsy and ZAM retroviruses and is required for Drosophila oogenesis. Genetics 175: 1615-1624.
47. Muerdter, F., I. Olovnikov, A. Molaro, N. V. Rozhkov, B. Czech et al., 2012 Production of artificial piRNAs in flies and mice. RNA 18: 42-52.
48. Niemi, J. B., J. D. Raymond, R. Patrek, andM. J. Simmons, 2004 Establishment and maintenance of the P cytotype associated with telomeric P elements in Drosophila melanogaster. Genetics 166: 255-264.
49. O'Kane, C. J., and W. J. Gehring, 1987 Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84: 9123-9127.
50. Pelisson, A., S. U. Song, N. Prud'homme, P. A. Smith, A. Bucheton et al., 1994 Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 13: 4401-4411.
51. Pelisson, A., L. Mejlumian, V. Robert, C. Terzian, and A. Bucheton, 2002 Drosophila germline invasion by the endogenous retrovirus gypsy: involvement of the viral env gene. Insect Biochem. Mol. Biol. 32: 1249-1256.
52. Picard, G., 1978 Non mendelian female sterility in Drosophila melanogaster: sterility in the daughter progeny of SF and RSF females. Biol. Cell. 31: 235-244.
53. Picard, G., J. C. Bregliano, A. Bucheton, J. M. Lavige, A. Pelisson et al., 1978 Non-mendelian female sterility and hybrid dysgenesis in Drosophila melanogaster. Genet. Res. 32: 275-287.
54. Prud'homme, N., M. Gans, M. Masson, C. Terzian, and A. Bucheton, 1995 Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139: 697-711.
55. Reiss, D., T. Josse, D. Anxolabehere, and S. Ronsseray, 2004 aubergine mutations in Drosophila melanogaster impair P cytotype determination by telomeric P elements inserted in heterochromatin. Mol. Genet. Genomics 272: 336-343.
56. Rio, D. C., 2002 in P transposable elements in Drosophila melanogaster, pp. 484-518 in Mobile DNA II, edited by N. L. Craig, R. Craigie, and Gellert et al., American Society for Microbiology, Washington, DC.
57. Robin, S., S. Chambeyron, A. Bucheton, and I. Busseau, 2003 Gene silencing triggered by non-LTR retrotransposons in the female germline of Drosophila melanogaster. Genetics 164: 521-531.
58. Roche, S. E., and D. C. Rio, 1998 Trans-silencing by P elements inserted in subtelomeric heterochromatin involves the Drosophila Polycomb group gene, Enhancer of zeste. Genetics 149: 1839-1855.
59. Ronsseray, S., M. Lehmann, and D. Anxolabehere, 1989 Copy number and distribution of P and I mobile elements in Drosophila melanogaster populations. Chromosoma 98: 207-214.
60. Ronsseray, S., M. Lehmann, and D. Anxolabehere, 1991 The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics 129: 501-512.
61. Ronsseray, S., B. Lemaitre, and D. Coen, 1993 Maternal inheritance of P cytotype in Drosophila melanogaster: a "pre-P cytotype" is strictly extra-chromosomally transmitted. Mol. Gen. Genet. 241: 115-123.
62. Ronsseray, S., M. Lehmann, D. Nouaud, and D. Anxolabehere, 1996 The regulatory properties of autonomous subtelomeric P elements are sensitive to a Suppressor of variegation in Drosophila melanogaster. Genetics 143: 1663-1674.
63. Ronsseray, S., L. Marin, M. Lehmann, and D. Anxolabehere, 1998 Repression of hybrid dysgenesis in Drosophila melanogaster by combinations of telomeric P-element reporters and naturally occurring P elements. Genetics 149: 1857-1866.
64. Ronsseray, S., A. Boivin, and D. Anxolabehere, 2001 P-Element repression in Drosophila melanogaster by variegating clusters of P-lacZ-white transgenes. Genetics 159: 1631-1642.
65. Ronsseray, S., T. Josse, A. Boivin, and D. Anxolabehere, 2003 Telomeric transgenes and trans-silencing in Drosophila. Genetica 117: 327-335.
66. Schupbach, T., and E. Wieschaus, 1991 Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129: 1119-1136.
67. Simmons, M. J., D. F. Ryzek, C. Lamour, J. W. Goodman, N. E. Kummer et al., 2007 Cytotype regulation by telomeric P elements in Drosophila melanogaster: evidence for involvement of an RNA interference gene. Genetics 176: 1945-1955.
68. Slotkin, R. K., and R. Martienssen, 2007 Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8: 272-285.
69. Stuart, J. R., K. J. Haley, D. Swedzinski, S. Lockner, P. E. Kocian et al., 2002 Telomeric P elements associated with cytotype regulation of the P transposon family in Drosophila melanogaster. Genetics 162: 1641-1654.
70. Sved, J. A., 1987 Hybrid dysgenesis in Drosophila melanogaster: evidence from sterility and southern hybridization tests that P cytotype is not maintained in the absence of chromosomal P factors. Genetics 115: 121-127.
71. Todeschini, A. L., L. Teysset, V. Delmarre, and S. Ronsseray, 2010 The epigenetic trans-silencing effect in Drosophila involves maternally-transmitted small RNAs whose production depends on the piRNA pathway and HP1. PLoS ONE 5: e11032.
72. Wicker, T., F. Sabot, A. Hua-Van, J. L. Bennetzen, P. Capy et al., 2007 A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8: 973-982.
73. Wilson, J. E., J. E. Connell, J. D. Schlenker, and P. M. Macdonald, 1996 Novel genetic screen for genes involved in posterior body patterning in Drosophila. Dev. Genet. 19: 199-209.