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Ty3 Retrotransposon Hijacks Mating Yeast RNA Processing Bodies to Infect New Genomes


Cells undergoing changes in gene expression programs such as nutritional deprivation and other stresses exhibit formation of ribonucleoprotein (RNP) complexes. In Saccharomyces cerevisiae, the majority of investigations to date involve analysis of P-body (PB) and stress-granule RNP formation following nutritional stress. Few studies have investigated RNP formation induced by the mating-MAP-kinase pathway. In this study, we examined how this process influences genome stability via control of retrotransposon activation. During the mating response, expression of the retrotransposon Ty3 is induced and Ty3 virus-like particles form in RNP clusters called retrosomes. We show that mating retrosomes contain PB components that are essential for Ty3 expression, re-localization of Ty3 RNA and protein from polysomes into foci, and retrotransposition. In animal germ cell lineages, PB components are found in perinuclear complexes with RNA interference suppressors of retrotransposition. We speculate that when RNA interference is relaxed and retrotransposition is observed, some members of these complexes play positive roles as we observe in budding yeast.


Vyšlo v časopise: Ty3 Retrotransposon Hijacks Mating Yeast RNA Processing Bodies to Infect New Genomes. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005528
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005528

Souhrn

Cells undergoing changes in gene expression programs such as nutritional deprivation and other stresses exhibit formation of ribonucleoprotein (RNP) complexes. In Saccharomyces cerevisiae, the majority of investigations to date involve analysis of P-body (PB) and stress-granule RNP formation following nutritional stress. Few studies have investigated RNP formation induced by the mating-MAP-kinase pathway. In this study, we examined how this process influences genome stability via control of retrotransposon activation. During the mating response, expression of the retrotransposon Ty3 is induced and Ty3 virus-like particles form in RNP clusters called retrosomes. We show that mating retrosomes contain PB components that are essential for Ty3 expression, re-localization of Ty3 RNA and protein from polysomes into foci, and retrotransposition. In animal germ cell lineages, PB components are found in perinuclear complexes with RNA interference suppressors of retrotransposition. We speculate that when RNA interference is relaxed and retrotransposition is observed, some members of these complexes play positive roles as we observe in budding yeast.


Zdroje

1. Decker CJ, Parker R. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harbor perspectives in biology. 2012;4(9):a012286. Epub 2012/07/06. doi: 10.1101/cshperspect.a012286 22763747.

2. Anderson P, Kedersha N, Ivanov P. Stress granules, P-bodies and cancer. Biochim Biophys Acta. 2014. Epub 2014/12/09. doi: 10.1016/j.bbagrm.2014.11.009 25482014.

3. Huch S, Nissan T. Interrelations between translation and general mRNA degradation in yeast. Wiley interdisciplinary reviews RNA. 2014;5(6):747–63. Epub 2014/06/20. doi: 10.1002/wrna.1244 24944158.

4. Kulkarni M, Ozgur S, Stoecklin G. On track with P-bodies. Biochem Soc Trans. 2010;38(Pt 1):242–51. Epub 2010/01/16. doi: 10.1042/BST0380242 20074068.

5. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol. 2007;8(1):9–22. Epub 2006/12/22. nrm2080 [pii] 0.1038/nrm2080. 17183357.

6. Beliakova-Bethell N, Beckham C, Giddings TH Jr., Winey M, Parker R, Sandmeyer S. Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components. RNA. 2006;12(1):94–101. Epub 2005/12/24. 12/1/94 [pii]doi: 10.1261/rna.2264806 16373495.

7. Irwin B, Aye M, Baldi P, Beliakova-Bethell N, Cheng H, Dou Y, et al. Retroviruses and yeast retrotransposons use overlapping sets of host genes. Genome Res. 2005;15(5):641–54. Epub 2005/04/20. gr.3739005 [pii]doi: 10.1101/gr.3739005 15837808.

8. Sandmeyer S, Patterson K, Bilanchone V. Ty3, a Position-specific Retrotransposon in Budding Yeast. Microbiol Spectr. 2015;3(2). Epub 2015/06/25. doi: 10.1128/microbiolspec.MDNA3-0057-2014 26104707.

9. Clemens K, Bilanchone V, Beliakova-Bethell N, Larsen LS, Nguyen K, Sandmeyer S. Sequence requirements for localization and packaging of Ty3 retroelement RNA. Virus Res. 2013;171:319–31. Epub 2012/10/18. doi: 10.1016/j.virusres.2012.10.008 23073180.

10. Clemens K, Larsen L, Zhang M, Kuznetsov Y, Bilanchone V, Randall A, et al. The Ty3 Gag3 Spacer Controls Intracellular Condensation and Uncoating. J Virol. 2011;85:3055–66. Epub 2011/01/29. JVI.01055-10 [pii] doi: 10.1128/JVI.01055-10 21270167.

11. Larsen LS, Beliakova-Bethell N, Bilanchone V, Zhang M, Lamsa A, Dasilva R, et al. Ty3 nucleocapsid controls localization of particle assembly. J Virol. 2008;82(5):2501–14. Epub 2007/12/21. JVI.01814-07 [pii]doi: 10.1128/JVI.01814-07 18094177.

12. Larsen LS, Zhang M, Beliakova-Bethell N, Bilanchone V, Lamsa A, Nagashima K, et al. Ty3 capsid mutations reveal early and late functions of the amino-terminal domain. J Virol. 2007;81(13):6957–72. Epub 2007/04/20. JVI.02207-06 [pii]doi: 10.1128/JVI.02207-06 17442718.

13. Sandmeyer SB, Clemens KA. Function of a retrotransposon nucleocapsid protein. RNA Biol. 2010;7(6). Epub 2010/12/30. 14117 [pii]. 21189452.

14. Bilanchone VW, Claypool JA, Kinsey PT, Sandmeyer SB. Positive and negative regulatory elements control expression of the yeast retrotransposon Ty3. Genetics. 1993;134(3):685–700. Epub 1993/07/01. 8394262.

15. Kinsey PT, Sandmeyer SB. Ty3 transposes in mating populations of yeast: a novel transposition assay for Ty3. Genetics. 1995;139(1):81–94. Epub 1995/01/01. 7705653.

16. Ka M, Park YU, Kim J. The DEAD-box RNA helicase, Dhh1, functions in mating by regulating Ste12 translation in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 2008;367(3):680–6. Epub 2008/01/10. S0006-291X(07)02809-4 [pii] doi: 10.1016/j.bbrc.2007.12.169 18182159.

17. Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 2003;300(5620):805–8. Epub 2003/05/06. 12730603.

18. Campbell SG, Hoyle NP, Ashe MP. Dynamic cycling of eIF2 through a large eIF2B-containing cytoplasmic body: implications for translation control. J Cell Biol. 2005;170(6):925–34. Epub 2005/09/15. jcb.200503162 [pii] doi: 10.1083/jcb.200503162 16157703.

19. Buchan JR, Yoon JH, Parker R. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J Cell Sci. 2011;124(Pt 2):228–39. Epub 2010/12/22. jcs.078444 [pii] doi: 10.1242/jcs.078444 21172806.

20. Romero-Santacreu L, Moreno J, Perez-Ortin JE, Alepuz P. Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA. 2009;15(6):1110–20. Epub 2009/04/17. doi: 10.1261/rna.1435709 19369426.

21. Presnyak V, Coller J. The DHH1/RCKp54 family of helicases: An ancient family of proteins that promote translational silencing. Biochim Biophys Acta. 2013;1829(8):817–23. Epub 2013/03/27. doi: 10.1016/j.bbagrm.2013.03.006 23528737.

22. Beckham C, Hilliker A, Cziko AM, Noueiry A, Ramaswami M, Parker R. The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol Biol Cell. 2008;19(3):984–93. Epub 2007/12/29. E07-09-0954 [pii] doi: 10.1091/mbc.E07-09-0954 18162578.

23. Kshirsagar M, Parker R. Identification of Edc3p as an enhancer of mRNA decapping in Saccharomyces cerevisiae. Genetics. 2004;166(2):729–39. Epub 2004/03/17. 166/2/729 [pii]. 15020463.

24. Nagarajan VK, Jones CI, Newbury SF, Green PJ. XRN 5'—>3' exoribonucleases: Structure, mechanisms and functions. Biochim Biophys Acta. 2013;1829(6–7):590–603. Epub 2013/03/23. doi: 10.1016/j.bbagrm.2013.03.005 23517755.

25. Brengues M, Teixeira D, Parker R. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science. 2005;310(5747):486–9. Epub 2005/09/06. 1115791 [pii] doi: 10.1126/science.1115791 16141371.

26. Aizer A, Kalo A, Kafri P, Shraga A, Ben-Yishay R, Jacob A, et al. Quantifying mRNA targeting to P-bodies in living human cells reveals their dual role in mRNA decay and storage. J Cell Sci. 2014;127(Pt 20):4443–56. Epub 2014/08/17. doi: 10.1242/jcs.152975 25128566.

27. Grousl T, Ivanov P, Frydlova I, Vasicova P, Janda F, Vojtova J, et al. Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J Cell Sci. 2009;122(Pt 12):2078–88. Epub 2009/05/28. jcs.045104 [pii] doi: 10.1242/jcs.045104 19470581.

28. Hoyle NP, Castelli LM, Campbell SG, Holmes LE, Ashe MP. Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J Cell Biol. 2007;179(1):65–74. Epub 2007/10/03. jcb.200707010 [pii]doi: 10.1083/jcb.200707010 17908917.

29. Buchan JR, Nissan T, Parker R. Analyzing P-bodies and stress granules in Saccharomyces cerevisiae. Methods Enzymol. 2010;470:619–40. Epub 2010/10/16. S0076-6879(10)70025-2 [pii]doi: 10.1016/S0076-6879(10)70025-2 20946828.

30. Mitchell SF, Jain S, She M, Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol. 2013;20(1):127–33. Epub 2012/12/12. doi: 10.1038/nsmb.2468 23222640.

31. Saito K, Siomi MC. Small RNA-mediated quiescence of transposable elements in animals. Dev Cell. 2010;19(5):687–97. Epub 2010/11/16. doi: 10.1016/j.devcel.2010.10.011 21074719.

32. Khurana JS, Theurkauf W. piRNAs, transposon silencing, and Drosophila germline development. J Cell Biol. 2010;191(5):905–13. Epub 2010/12/01. doi: 10.1083/jcb.201006034 21115802.

33. Crichton JH, Dunican DS, Maclennan M, Meehan RR, Adams IR. Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline. Cell Mol Life Sci. 2014;71(9):1581–605. Epub 2013/09/21. doi: 10.1007/s00018-013-1468-0 24045705.

34. Gallois-Montbrun S, Kramer B, Swanson CM, Byers H, Lynham S, Ward M, et al. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol. 2007;81(5):2165–78. Epub 2006/12/15. JVI.02287-06 [pii]doi: 10.1128/JVI.02287-06 17166910.

35. Phalora PK, Sherer NM, Wolinsky SM, Swanson CM, Malim MH. HIV-1 replication and APOBEC3 antiviral activity are not regulated by P bodies. J Virol. 2012;86(21):11712–24. Epub 2012/08/24. doi: 10.1128/JVI.00595-12 22915799.

36. Chiu YL, Greene WC. APOBEC3G: an intracellular centurion. Philos Trans R Soc Lond B Biol Sci. 2009;364(1517):689–703. Epub 2008/11/15. X561868G4K8208TV [pii] doi: 10.1098/rstb.2008.0193 19008196.

37. Lu C, Contreras X, Peterlin BM. P bodies inhibit retrotransposition of endogenous intracisternal a particles. J Virol. 2011;85(13):6244–51. Epub 2011/04/29. JVI.02517-10 [pii]doi: 10.1128/JVI.02517-10 21525359.

38. Goodier JL, Cheung LE, Kazazian HH Jr. MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet. 2012;8(10):e1002941. Epub 2012/10/25. doi: 10.1371/journal.pgen.1002941 23093941.

39. Furtak V, Mulky A, Rawlings SA, Kozhaya L, Lee K, Kewalramani VN, et al. Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PLoS One. 2010;5(2):e9081. Epub 2010/02/09. doi: 10.1371/journal.pone.0009081 20140200.

40. Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol. 2011;12(4):246–58. Epub 2011/03/24. doi: 10.1038/nrm3089 21427766.

41. Liu J, Rivas FV, Wohlschlegel J, Yates JR 3rd, Parker R, Hannon GJ. A role for the P-body component GW182 in microRNA function. Nat Cell Biol. 2005;7(12):1261–6. Epub 2005/11/15. ncb1333 [pii] doi: 10.1038/ncb1333 16284623.

42. Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I. RNA granules in germ cells. Cold Spring Harbor perspectives in biology. 2011;3(12). Epub 2011/07/20. doi: 10.1101/cshperspect.a002774 21768607.

43. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, et al. RNAi in budding yeast. Science. 2009;326(5952):544–50. Epub 2009/09/12. doi: 10.1126/science.1176945 19745116.

44. Teixeira D, Parker R. Analysis of P-body assembly in Saccharomyces cerevisiae. Mol Biol Cell. 2007;18(6):2274–87. Epub 2007/04/13. E07-03-0199 [pii] doi: 10.1091/mbc.E07-03-0199 17429074.

45. Decker CJ, Teixeira D, Parker R. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol. 2007;179(3):437–49. Epub 2007/11/07. jcb.200704147 [pii] doi: 10.1083/jcb.200704147 17984320.

46. Pilkington GR, Parker R. Pat1 contains distinct functional domains that promote P-body assembly and activation of decapping. Mol Cell Biol. 2008;28(4):1298–312. Epub 2007/12/19. MCB.00936-07 [pii] doi: 10.1128/MCB.00936-07 18086885.

47. Reijns MA, Alexander RD, Spiller MP, Beggs JD. A role for Q/N-rich aggregation-prone regions in P-body localization. J Cell Sci. 2008;121(Pt 15):2463–72. Epub 2008/07/10. jcs.024976 [pii] doi: 10.1242/jcs.024976 18611963.

48. Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol. 2008;10(10):1224–31. Epub 2008/09/17. ncb1783 [pii] doi: 10.1038/ncb1783 18794846.

49. Chen C, Nott TJ, Jin J, Pawson T. Deciphering arginine methylation: Tudor tells the tale. Nat Rev Mol Cell Biol. 2011;12(10):629–42. Epub 2011/09/15. doi: 10.1038/nrm3185 21915143.

50. Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014;505(7481):117–20. Epub 2013/11/29. doi: 10.1038/nature12730 24284625.

51. Pek JW, Anand A, Kai T. Tudor domain proteins in development. Development. 2012;139(13):2255–66. Epub 2012/06/07. doi: 10.1242/dev.073304 22669818.

52. Ramachandran V, Shah KH, Herman PK. The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation. Mol Cell. 2011;43(6):973–81. Epub 2011/09/20. doi: 10.1016/j.molcel.2011.06.032 21925385.

53. Yoon JH, Choi EJ, Parker R. Dcp2 phosphorylation by Ste20 modulates stress granule assembly and mRNA decay in Saccharomyces cerevisiae. J Cell Biol. 2010;189(5):813–27. Epub 2010/06/02. jcb.200912019 [pii]doi: 10.1083/jcb.200912019 20513766.

54. Griffith JL, Coleman LE, Raymond AS, Goodson SG, Pittard WS, Tsui C, et al. Functional genomics reveals relationships between the retrovirus-like Ty1 element and its host Saccharomyces cerevisiae. Genetics. 2003;164(3):867–79. Epub 2003/07/23. 12871900.

55. Saito H. Regulation of cross-talk in yeast MAPK signaling pathways. Curr Opin Microbiol. 2010;13(6):677–83. Epub 2010/10/01. doi: 10.1016/j.mib.2010.09.001 20880736.

56. Van Arsdell SW, Stetler GL, Thorner J. The yeast repeated element sigma contains a hormone-inducible promoter. Mol Cell Biol. 1987;7(2):749–59. Epub 1987/02/01. 3547081.

57. Hansen LJ, Chalker DL, Orlinsky KJ, Sandmeyer SB. Ty3 GAG3 and POL3 genes encode the components of intracellular particles. J Virol. 1992;66(3):1414–24. Epub 1992/03/01. 1371165.

58. Zhang M, Larsen LS, Irwin B, Bilanchone V, Sandmeyer S. Two-hybrid analysis of Ty3 capsid subdomain interactions. Mob DNA. 2010;1(1):14. Epub 2010/05/07. 1759-8753-1-14 [pii]doi: 10.1186/1759-8753-1-14 20444245.

59. Kirchner J, Sandmeyer S. Proteolytic processing of Ty3 proteins is required for transposition. J Virol. 1993;67(1):19–28. Epub 1993/01/01. 7677953.

60. Menees TM, Sandmeyer SB. Transposition of the yeast retroviruslike element Ty3 is dependent on the cell cycle. Mol Cell Biol. 1994;14(12):8229–40. Epub 1994/12/01. 7969160.

61. Kaake RM, Wang X, Huang L. Profiling of protein interaction networks of protein complexes using affinity purification and quantitative mass spectrometry. Mol Cell Proteomics. 9(8):1650–65. Epub 2010/05/07. R110.000265 [pii]doi: 10.1074/mcp.R110.000265 20445003.

62. Sadeghi N, Rutz ML, Menees TM. Thermal blockage of viruslike particle formation for the yeast retrotransposon Ty3 reveals differences in the cellular stress response. Arch Virol. 2001;146(10):1919–34. Epub 2001/11/28. 11722014.

63. Kirchner J, Sandmeyer SB, Forrest DB. Transposition of a Ty3 GAG3-POL3 fusion mutant is limited by availability of capsid protein. J Virol. 1992;66(10):6081–92. Epub 1992/10/01. 1326658.

64. Hansen LJ, Sandmeyer SB. Characterization of a transpositionally active Ty3 element and identification of the Ty3 integrase protein. J Virol. 1990;64(6):2599–607. Epub 1990/06/01. 2159534.

65. Balagopal V, Parker R. Stm1 modulates mRNA decay and Dhh1 function in Saccharomyces cerevisiae. Genetics. 2009;181(1):93–103. Epub 2008/11/19. genetics.108.092601 [pii] doi: 10.1534/genetics.108.092601 19015546;.

66. Kuznetsov YG, Zhang M, Menees TM, McPherson A, Sandmeyer S. Investigation by atomic force microscopy of the structure of Ty3 retrotransposon particles. J Virol. 2005;79(13):8032–45. Epub 2005/06/16. 79/13/8032 [pii] doi: 10.1128/JVI.79.13.8032-8045.2005 15956549.

67. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, et al. Life with 6000 genes. Science. 1996;274(5287):546, 63–7. Epub 1996/10/25. 8849441.

68. Chang F, Herskowitz I. Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell. 1990;63(5):999–1011. Epub 1990/11/30. 2147873.

69. Garmendia-Torres C, Skupin A, Michael SA, Ruusuvuori P, Kuwada NJ, Falconnet D, et al. Unidirectional P-body transport during the yeast cell cycle. PLoS One. 2014;9(6):e99428. Epub 2014/06/12. doi: 10.1371/journal.pone.0099428 24918601.

70. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JE, et al. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell. 2003;115(6):739–50. Epub 2003/12/17. 14675538.

71. Karst SM, Sadeghi N, Menees TM. Cell cycle control of reverse transcriptase activity for the yeast retrotransposon Ty3. Biochem Biophys Res Commun. 1999;254(3):679–84. Epub 1999/01/28. S0006-291X(98)90128-0 [pii]doi: 10.1006/bbrc.1998.0128 9920800.

72. Parker R. RNA degradation in Saccharomyces cerevisae. Genetics. 2012;191(3):671–702. Epub 2012/07/13. doi: 10.1534/genetics.111.137265 22785621.

73. Kedersha N, Ivanov P, Anderson P. Stress granules and cell signaling: more than just a passing phase? Trends Biochem Sci. 2013;38(10):494–506. Epub 2013/09/14. doi: 10.1016/j.tibs.2013.07.004 24029419.

74. Sweet T, Kovalak C, Coller J. The DEAD-box protein Dhh1 promotes decapping by slowing ribosome movement. PLoS Biol. 2012;10(6):e1001342. Epub 2012/06/22. doi: 10.1371/journal.pbio.1001342 22719226.

75. Hurto RL, Hopper AK. P-body components, Dhh1 and Pat1, are involved in tRNA nuclear-cytoplasmic dynamics. RNA. 2011;17(5):912–24. Epub 2011/03/15. doi: 10.1261/rna.2558511 21398402.

76. Nissan T, Rajyaguru P, She M, Song H, Parker R. Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol Cell. 2010;39(5):773–83. Epub 2010/09/14. S1097-2765(10)00635-0 [pii]doi: 10.1016/j.molcel.2010.08.025 20832728.

77. Rajyaguru P, Parker R. CGH-1 and the control of maternal mRNAs. Trends Cell Biol. 2009;19(1):24–8. Epub 2008/12/09. S0962-8924(08)00280-8 [pii] doi: 10.1016/j.tcb.2008.11.001 19062290.

78. Kruk JA, Dutta A, Fu J, Gilmour DS, Reese JC. The multifunctional Ccr4-Not complex directly promotes transcription elongation. Genes Dev. 2011;25(6):581–93. Epub 2011/03/17. doi: 10.1101/gad.2020911 21406554.

79. Hu W, Sweet TJ, Chamnongpol S, Baker KE, Coller J. Co-translational mRNA decay in Saccharomyces cerevisiae. Nature. 2009;461(7261):225–9. Epub 2009/08/25. nature08265 [pii]doi: 10.1038/nature08265 19701183.

80. Bashkirov VI, Solinger JA, Heyer WD. Identification of functional domains in the Sep1 protein (= Kem1, Xrn1), which is required for transition through meiotic prophase in Saccharomyces cerevisiae. Chromosoma. 1995;104(3):215–22. Epub 1995/11/01. 8529461.

81. MacKay VL, Li X, Flory MR, Turcott E, Law GL, Serikawa KA, et al. Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteomics. 2004;3(5):478–89. Epub 2004/02/10. doi: 10.1074/mcp.M300129-MCP200 14766929.

82. Serikawa KA, Xu XL, MacKay VL, Law GL, Zong Q, Zhao LP, et al. The transcriptome and its translation during recovery from cell cycle arrest in Saccharomyces cerevisiae. Mol Cell Proteomics. 2003;2(3):191–204. Epub 2003/04/10. doi: 10.1074/mcp.D200002-MCP200 12684541.

83. Kim J, Ljungdahl PO, Fink GR. kem mutations affect nuclear fusion in Saccharomyces cerevisiae. Genetics. 1990;126(4):799–812. Epub 1990/12/01. 2076815.

84. Checkley MA, Nagashima K, Lockett SJ, Nyswaner KM, Garfinkel DJ. P-body components are required for Ty1 retrotransposition during assembly of retrotransposition-competent virus-like particles. Mol Cell Biol. 2010;30(2):382–98. Epub 2009/11/11. MCB.00251-09 [pii] doi: 10.1128/MCB.00251-09 19901074.

85. Dutko JA, Kenny AE, Gamache ER, Curcio MJ. 5' to 3' mRNA decay factors colocalize with Ty1 gag and human APOBEC3G and promote Ty1 retrotransposition. J Virol. 2010;84(10):5052–66. Epub 2010/03/12. JVI.02477-09 [pii] doi: 10.1128/JVI.02477-09 20219921.

86. Malagon F, Jensen TH. The T body, a new cytoplasmic RNA granule in Saccharomyces cerevisiae. Mol Cell Biol. 2008;28(19):6022–32. Epub 2008/08/06. MCB.00684-08 [pii] doi: 10.1128/MCB.00684-08 18678648.

87. Garfinkel DJ, Nyswaner KM, Stefanisko KM, Chang C, Moore SP. Ty1 copy number dynamics in Saccharomyces. Genetics. 2005;169(4):1845–57. Epub 2005/02/03. genetics.104.037317 [pii] doi: 10.1534/genetics.104.037317 15687270.

88. Matsuda E, Garfinkel DJ. Posttranslational interference of Ty1 retrotransposition by antisense RNAs. Proc Natl Acad Sci U S A. 2009;106(37):15657–62. Epub 2009/09/02. 0908305106 [pii] doi: 10.1073/pnas.0908305106 19721006.

89. Saha A, Mitchell JA, Nishida Y, Hildreth JE, Ariberre JA, Gilbert WV, et al. A trans-dominant form of Gag restricts Ty1 retrotransposition and mediates copy number control. J Virol. 2015. Epub 2015/01/23. doi: 10.1128/JVI.03060-14 25609815.

90. Berretta J, Pinskaya M, Morillon A. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev. 2008;22(5):615–26. Epub 2008/03/05. 22/5/615 [pii] doi: 10.1101/gad.458008 18316478.

91. Orlinsky KJ, Sandmeyer SB. The Cys-His motif of Ty3 NC can be contributed by Gag3 or Gag3-Pol3 polyproteins. J Virol. 1994;68(7):4152–66. Epub 1994/07/01. 7515969.

92. Doh JH, Lutz S, Curcio MJ. Co-translational localization of an LTR-retrotransposon RNA to the endoplasmic reticulum nucleates virus-like particle assembly sites. PLoS Genet. 2014;10(3):e1004219. Epub 2014/03/08. doi: 10.1371/journal.pgen.1004219 24603646.

93. Risler JK, Kenny AE, Palumbo RJ, Gamache ER, Curcio MJ. Host co-factors of the retrovirus-like transposon Ty1. Mob DNA. 2012;3(1):12. Epub 2012/08/04. doi: 10.1186/1759-8753-3-12 22856544.

94. Xu H, Boeke JD. Inhibition of Ty1 transposition by mating pheromones in Saccharomyces cerevisiae. Mol Cell Biol. 1991;11(5):2736–43. Epub 1991/05/01. 1850102.

95. Curcio MJ, Garfinkel DJ. New lines of host defense: inhibition of Ty1 retrotransposition by Fus3p and NER/TFIIH. Trends Genet. 1999;15(2):43–5. Epub 1999/03/31. S0168-9525(98)01643-6 [pii]. 10098404.

96. Company M, Errede B. A Ty1 cell-type-specific regulatory sequence is a recognition element for a constitutive binding factor. Mol Cell Biol. 1988;8(12):5299–309. Epub 1988/12/01. 2854195.

97. Morillon A, Springer M, Lesage P. Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol. 2000;20(15):5766–76. Epub 2000/07/13. 10891512.

98. Noueiry AO, Diez J, Falk SP, Chen J, Ahlquist P. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol Cell Biol. 2003;23(12):4094–106. Epub 2003/05/30. 12773554.

99. Reed JC, Molter B, Geary CD, McNevin J, McElrath J, Giri S, et al. HIV-1 Gag co-opts a cellular complex containing DDX6, a helicase that facilitates capsid assembly. J Cell Biol. 2012;198(3):439–56. Epub 2012/08/02. doi: 10.1083/jcb.201111012 22851315.

100. Yu SF, Lujan P, Jackson DL, Emerman M, Linial ML. The DEAD-box RNA helicase DDX6 is required for efficient encapsidation of a retroviral genome. PLoS Pathog. 2011;7(10):e1002303. Epub 2011/10/25. doi: 10.1371/journal.ppat.1002303 PPATHOGENS-D-11-01147 [pii]. 22022269.

101. Yedavalli VS, Neuveut C, Chi YH, Kleiman L, Jeang KT. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell. 2004;119(3):381–92. Epub 2004/10/28. S0092867404008360 [pii] doi: 10.1016/j.cell.2004.09.029 15507209.

102. Beliakova-Bethell N, Terry LJ, Bilanchone V, DaSilva R, Nagashima K, Wente SR, et al. Ty3 nuclear entry is initiated by viruslike particle docking on GLFG nucleoporins. J Virol. 2009;83(22):11914–25. Epub 2009/09/18. JVI.01192-09 [pii] doi: 10.1128/JVI.01192-09 19759143.

103. Checkley MA, Mitchell JA, Eizenstat LD, Lockett SJ, Garfinkel DJ. Ty1 gag enhances the stability and nuclear export of Ty1 mRNA. Traffic. 2013;14(1):57–69. Epub 2012/09/25. doi: 10.1111/tra.12013 22998189.

104. Zaitseva L, Myers R, Fassati A. tRNAs promote nuclear import of HIV-1 intracellular reverse transcription complexes. PLoS Biol. 2006;4(10):e332. Epub 2006/10/06. doi: 10.1371/journal.pbio.0040332 17020411.

105. Castaneda J, Genzor P, Bortvin A. piRNAs, transposon silencing, and germline genome integrity. Mutat Res. 2011;714(1–2):95–104. Epub 2011/05/24. doi: 10.1016/j.mrfmmm.2011.05.002 21600904.

106. Amberg DC, Burke DJ, Strathern JN. Methods in Yeast Genetics. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2005.

107. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, et al. Current Protocols in Molecular Biology: John Wiley and Sons, Inc.; 2007.

108. Kaake RM, Milenkovic T, Przulj N, Kaiser P, Huang L. Characterization of cell cycle specific protein interaction networks of the yeast 26S proteasome complex by the QTAX strategy. J Proteome Res. 2010;9(4):2016–29. Epub 2010/02/23. doi: 10.1021/pr1000175 20170199.

109. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, et al. A travel guide to Cytoscape plugins. Nat Methods. 2012;9(11):1069–76. Epub 2012/11/08. doi: 10.1038/nmeth.2212 23132118.

110. Curcio MJ, Garfinkel DJ. Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci U S A. 1991;88(3):936–40. Epub 1991/02/01. 1846969.

111. Sarkar S, Hopper AK. tRNA nuclear export in saccharomyces cerevisiae: in situ hybridization analysis. Mol Biol Cell. 1998;9(11):3041–55. Epub 1998/11/05. 9802895.

112. Lin SS, Nymark-McMahon MH, Yieh L, Sandmeyer SB. Integrase mediates nuclear localization of Ty3. Mol Cell Biol. 2001;21(22):7826–38. Epub 2001/10/18. doi: 10.1128/MCB.21.22.7826-7838.2001 11604517.

113. Grote E. Cell fusion assays for yeast mating pairs. Methods Mol Biol. 2008;475:165–96. Epub 2008/11/04. doi: 10.1007/978-1-59745-250-2_10 18979244.

114. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.

115. Masek T, Valasek L, Pospisek M. Polysome analysis and RNA purification from sucrose gradients. Methods Mol Biol. 2011;703:293–309. Epub 2010/12/03. doi: 10.1007/978-1-59745-248-9_20 21125498.

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