Light and shadow on the mechanisms of integration site selection in yeast Ty retrotransposon families

Abstract

Transposable elements are ubiquitous in genomes. Their successful expansion depends in part on their sites of integration in their host genome. In Saccharomyces cerevisiae, evolution has selected various strategies to target the five Ty LTR-retrotransposon families into gene-poor regions in a genome, where coding sequences occupy 70% of the DNA. The integration of Ty1/Ty2/Ty4 and Ty3 occurs upstream and at the transcription start site of the genes transcribed by RNA polymerase III, respectively. Ty5 has completely different integration site preferences, targeting heterochromatin regions. Here, we review the history that led to the identification of the cellular tethering factors that play a major role in anchoring Ty retrotransposons to their preferred sites. We also question the involvement of additional factors in the fine-tuning of the integration site selection, with several studies converging towards an importance of the structure and organization of the chromatin.

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References

  1. Abascal-Palacios G, Ramsay EP, Beuron F, Morris E, Vannini A (2018) Structural basis of RNA polymerase III transcription initiation. Nature 553:301–306

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. Achuthan V, Perreira JM, Sowd GA, Puray-Chavez M, McDougall WM, Paulucci-Holthauzen A, Wu X, Fadel HJ, Poeschla EM, Multani AS et al (2018) Capsid-CPSF6 interaction licenses nuclear HIV-1 trafficking to sites of viral DNA Integration. Cell Host Microbe 24:392-404.e8

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. Acker J, Conesa C, Lefebvre O (2013) Yeast RNA polymerase III transcription factors and effectors. Biochim Biophys Acta Gene Regul Mech 1829:283–295

    CAS  Article  Google Scholar 

  4. Asif-Laidin A, Conesa C, Bonnet A, Grison C, Adhya I, Menouni R, Fayol H, Palmic N, Acker J, Lesage P (2020) A small targeting domain in Ty1 integrase is sufficient to direct retrotransposon integration upstream of tRNA genes. EMBO J 39(17):e104337

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Aye M, Dildine SL, Claypool JA, Jourdain S, Sandmeyer SB (2001) A truncation mutant of the 95-kilodalton subunit of transcription factor IIIC reveals asymmetry in Ty3 integration. Mol Cell Biol 21:7839–7851

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Aye M, Irwin B, Beliakova-Bethell N, Chen E, Garrus J, Sandmeyer S (2004) Host factors that affect Ty3 retrotransposition in Saccharomyces cerevisiae. Genetics 168:1159–1176

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Bachman N, Eby Y, Boeke JD (2004) Local definition of Ty1 target preference by long terminal repeats and clustered tRNA genes. Genome Res 14:1232–1247

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Bachman N, Gelbart ME, Tsukiyama T, Boeke JD (2005) TFIIIB subunit Bdp1p is required for periodic integration of the Ty1 retrotransposon and targeting of Isw2p to S. cerevisiae tDNAs. Genes Dev 19:955–964

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Baller JA, Gao J, Voytas DF (2011) Access to DNA establishes a secondary target site bias for the yeast retrotransposon Ty5. Proc Natl Acad Sci USA 108:20351–20356

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  10. Baller JA, Gao J, Stamenova R, Curcio MJ, Voytas DF (2012) A nucleosomal surface defines an integration hotspot for the Saccharomyces cerevisiae Ty1 retrotransposon. Genome Res 22:704–713

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Bejarano DA, Peng K, Laketa V, Bo K, Lusic M, Mu B (2019) HIV-1 nuclear import in macrophages is regulated by CPSF6-capsid interactions at the nuclear pore complex. Elife 8:e41800

    PubMed  PubMed Central  Article  Google Scholar 

  12. Bhargava A, Lahaye X, Manel N (2018) Let me in: control of HIV nuclear entry at the nuclear envelope. Cytokine Growth Factor Rev 40:59–67

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Bilanchone VW, Claypool JA, Kinsey PT, Sandmeyer SB (1993) Positive and negative regulatory elements control expression of the yeast retrotransposon Ty3. Genetics 134:685–700

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. Bleykasten-Grosshans C, Neuvéglise C (2011) Transposable elements in yeasts. Comptes Rendus Biol 334:679–686

    CAS  Article  Google Scholar 

  15. Bridier-Nahmias A, Tchalikian-Cosson A, Baller JA, Menouni R, Fayol H, Flores A, Saïb A, Werner M, Voytas D, Lesage P (2015) An RNA polymerase III subunit determines sites of retrotransposon integration. Science 348:585–588

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. Britten RJ, Davidson EH (1969) Gene regulation for higher cells: a theory. Science 165:349–357

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. Brown CA, Murray AW, Verstrepen KJ (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20:895–903

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. Brun I, Sentenac A, Werner M (1997) Dual role of the C34 subunit of RNA polymerase III in transcription initiation. EMBO J 16:5730–5741

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Buffone C, Martinez-Lopez A, Fricke T, Opp S, Severgnini M, Cifola I, Frabetti S, Skorupka K, Zadrozny KK, Ganser-Pornillos BK et al (2018) Nup153 Unlocks the nuclear pore complex for HIV-1 nuclear import in non-dividing cells. J Virol 92:1–29

    Article  Google Scholar 

  20. Burns KH (2017) Transposable elements in cancer. Nat Rev Cancer 17:415–424

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. Bushman FD (2003) Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115:135–138

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  22. Canat A, Veillet A, Bonnet A, Therizols P (2020) Genome anchoring to nuclear landmarks drives functional compartmentalization of the nuclear space. Br Funct Genomics 19:101–110

    Article  CAS  Google Scholar 

  23. Carr M, Bensasson D, Bergman CM (2012) Evolutionary genomics of transposable elements in Saccharomyces cerevisiae. PLoS ONE 7:e50978

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Chalker DL, Sandmeyer SB (1992) Ty3 integrates within the region of RNA polymerase III transcription initiation. Genes Dev 6:117–128

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  25. Chen M, Gartenberg MR (2014) Coordination of tRNA transcription with export at nuclear pore complexes in budding yeast. Genes Dev 28:959–970

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Cherepanov P, Maertens G, Proost P, Devreese B, Van Beeumen J, Engelborghs Y, De Clercq E, Debyser Z (2003) HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J Biol Chem 278:372–381

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. Cheung S, Ma L, Chan PHW, Hu H-L, Mayor T, Chen H-T, Measday V (2016) Ty1-Integrase interacts with RNA Polymerase III specific subcomplexes to promote insertion of Ty1 elements upstream of Pol III-transcribed genes. J Biol Chem 291:6396–6411

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. Cheung S, Manhas S, Measday V (2018) Retrotransposon targeting to RNA polymerase III-transcribed genes. Mob DNA 9:1–15

    Article  CAS  Google Scholar 

  29. Chuong EB, Elde NC, Feschotte C (2016) Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet 18:71–86

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  30. Connolly CM, Sandmeyer SB (1997) RNA-Polymerase-III Interferes with Ty3 Integration. FEBS Lett 405:305–311

    CAS  PubMed  Article  Google Scholar 

  31. Cosby RL, Chang N, Feschotte C (2019) Host–transposon interactions: conflict, cooperation, and cooption. Genes Dev 33:1098–1116

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Costantino L, Hsieh T-H, Lamothe R, Darzacq X, Koshland D (2020) Cohesin residency determines chromatin loop patterns. Elife 9:e59889

    PubMed  PubMed Central  Article  Google Scholar 

  33. Curcio MJ, Garfinkel DJ (1992) Posttranslational control of Ty1 retrotransposition occurs at the level of protein posttranslational control of Tyl retrotransposition occurs at the level of protein processing. Molec Cell Biol 12:2813–2825

    CAS  PubMed  Article  Google Scholar 

  34. Curcio MJ, Hedge AM, Boeke JD, Garfinkel DJ (1990) Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet 220:213–221

    CAS  PubMed  Article  Google Scholar 

  35. Curcio MJ, Lesage P, Lutz S (2015) The Ty1 LTR-retrotransposon of budding yeast Saccharomyces cerevisiae. Mob DNA III:927–964

    Google Scholar 

  36. D’Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22:2215–2227

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. Dai J, Xie W, Brady TL, Gao J, Voytas DF (2007) Phosphorylation regulates integration of the yeast Ty5 retrotransposon into heterochromatin. Mol Cell 27:289–299

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. Dakshinamurthy A, Nyswaner KM, Farabaugh PJ, Garfinkel DJ (2010) BUD22 affects Ty1 retrotransposition and ribosome biogenesis in Saccharomyces cerevisiae. Genetics 185:1193–1205

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. De Rijck J, de Kogel C, Demeulemeester J, Vets S, El Ashkar S, Malani N, Bushman FD, Landuyt B, Husson SJ, Busschots K et al (2013) The BET family of proteins targets Moloney murine leukemia virus integration near transcription start sites. Cell Rep 5:886–894

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  40. Devine SE, Boeke JD (1996) Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III. Genes Dev 10:620–633

    CAS  PubMed  Article  Google Scholar 

  41. Downs JA, Lowndes NF, Jackson SP (2000) A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001–1004

    CAS  PubMed  Article  Google Scholar 

  42. Eigel A, Feldmann H (1982) Ty1 and delta elements occur adjacent to several tRNA genes in yeast. EMBO J 1:1245–1250

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. Elder RT, St. John TP, Stinchcomb DT, Davis RW, Scherer S (1981) Studies on the transposable element Ty1 of yeast. Cold Spring Harb Symp Quant Biol 45:581–591

    CAS  PubMed  Article  Google Scholar 

  44. Gai X, Voytas DF (1998) A single amino acid change in the yeast retrotransposon Ty5 abolishes targeting to silent chromatin. Mol Cell 1:1051–1055

    CAS  PubMed  Article  Google Scholar 

  45. Gelbart ME, Bachman N, Delrow J, Boeke JD, Tsukiyama T (2005) Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes Dev 19:942–954

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Gligoris TG, Scheinost JC, Bürmann F, Petela N, Chan KL, Uluocak P, Beckouët F, Gruber S, Nasmyth K, Löwe J (2014) Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science 346:963–967

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M et al (1996) Life with 6000 genes. Science 274:546–567

    CAS  PubMed  Article  Google Scholar 

  48. Griffith JL, Coleman LE, Raymond AS, Goodson SG, Pittard WS, Tsui C, Devine SE (2003) Functional genomics reveals relationships between the retrovirus-like Ty1 element and its host Saccharomyces cerevisiae. Genetics 164:867–879

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Gupta SS, Maetzig T, Maertens GN, Sharif A, Rothe M, Weidner-Glunde M, Galla M, Schambach A, Cherepanov P, Schulz TF (2013) Bromo- and extraterminal domain chromatin regulators serve as cofactors for murine leukemia virus integration. J Virol 87:12721–12736

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K (2008) The cohesin ring concatenates sister DNA molecules. Nature 454:297–301

    CAS  PubMed  Article  Google Scholar 

  51. Han Y, Yan C, Fishbain S, Ivanov I, He Y (2018) Structural visualization of RNA polymerase III transcription machineries. Cell Discov 4:1–15

    CAS  Article  Google Scholar 

  52. Hancks DC, Kazazian HH (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22:191–203

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Hickey A, Esnault C, Majumdar A, Chatterjee AG, Iben JR, McQueen PG, Yang AX, Mizuguchi T, Grewal SIS, Levin HL (2015) Single nucleotide specific targeting of the Tf1 retrotransposon promoted by the DNA-binding protein Sap1 of Schizosaccharomyces pombe. Genetics 201:905–924

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Ho KL, Ma L, Cheung S, Manhas S, Fang N, Wang K, Young B, Loewen C, Mayor T, Measday V (2015) A role for the budding yeast separase, Esp1, in Ty1 element retrotransposition. PLoS Genet 11:e1005109

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  55. Hocher A, Ruault M, Kaferle P, Descrimes M, Garnier M, Morillon A, Taddei A (2018) Expanding heterochromatin reveals discrete subtelomeric domains delimited by chromatin landscape transitions. Genome Res 28:1867–1881

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Hug AM, Feldmann H (1996) Yeast retrotransposon Ty4: the majority of the rare transcripts lack a U3-R sequence. Nucleic Acids Res 24:2338–2346

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. Hull MW, Erickson J, Johnston M, Engelke DR (1994) tRNA genes as transcriptional repressor elements. Mol Cell Biol 14:1266–1277

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Irwin B, Aye M, Baldi P, Beliakova-bethell N, Cheng H, Dou Y, Liou W, Sandmeyer S (2005) Retroviruses and yeast retrotransposons use overlapping sets of host genes. Genome Res 15:641–654

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Jacobs JZ, Rosado-Lugo JD, Cranz-Mileva S, Ciccaglione KM, Tournier V, Zaratiegui M (2015) Arrested replication forks guide retrotransposon integration. Science 349:1549–1553

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Ji H, Moore DP, Blomberg MA, Braiterman LT, Voytas DF, Natsoulis G, Boeke JD (1993) Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell 73:1007–1018

    CAS  PubMed  Article  Google Scholar 

  61. Ke N, Irwin PA, Voytas DF (1997) The pheromone response pathway activates transcription of Ty5 retrotransposons located within silent chromatin of Saccharomyces cerevisiae. EMBO J 16:6272–6280

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. Kenna MA, Brachmann CB, Devine SE, Boeke JD (1998) Invading the yeast nucleus: a nuclear localization signal at the C terminus of Ty1 integrase is required for transposition in vivo. Mol Cell Biol 18:1115–1124

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478

    CAS  PubMed  Article  Google Scholar 

  64. Kinsey PT, Sandmeyer SB (1991) Adjacent pol II and pol III promoters: transcription of the yeast retrotransposon Ty3 and a target tRNA gene. Nucleic Acids Res 19:1317–1324

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Kinsey PT, Sandmeyer SB (1995) Ty3 transposes in mating populations of yeast: a novel transposition assay for Ty3. Genetics 139:81–94

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Kirchner J, Connolly CM, Sandmeyer SB (1995) Requirement of RNA polymerase III transcription factors for in vitro position-specific integration of a retrovirus like element. Science 267:1488–1491

    CAS  PubMed  Article  Google Scholar 

  67. Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E, Tomita M, Yanagawa H (2009) Six classes of nuclear localization signals specific to different binding grooves of importinα. J Biol Chem 284:478–485

    CAS  PubMed  Article  Google Scholar 

  68. Kumar Y, Bhargava P (2013) A unique nucleosome arrangement, maintained actively by chromatin remodelers facilitates transcription of yeast tRNA genes. BMC Genomics 14:402

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. Kvaratskhelia M, Sharma A, Larue RC, Serrao E, Engelman A (2014) Molecular mechanisms of retroviral integration site selection. Nucleic Acids Res 42:10209–10225

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. Lange A, McLane LM, Mills RE, Devine SE, Corbett AH (2010) Expanding the definition of the classical bipartite nuclear localization signal. Traffic 11:311–323

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. Lelek M, Casartelli N, Pellin D, Rizzi E, Souque P, Severgnini M, Di Serio C, Fricke T, Diaz-Griffero F, Zimmer C et al (2015) Chromatin organization at the nuclear pore favours HIV replication. Nat Commun 6:6483–6494

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. Lengronne A, Katou Y, Mori S, Yokabayashi S, Kelly GP, Ito T, Watanabe Y, Shirahige K, Uhlmann F (2004) Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430:573–578

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Lesbats P, Engelman AN, Cherepanov P (2016) Retroviral DNA integration. Chem Rev 116:12730–12757

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Leśniewska E, Boguta M (2017) Novel layers of RNA polymerase III control affecting tRNA gene transcription in eukaryotes. Open Biol 7(2):170001

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  75. Levin HL, Moran JV (2011) Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12:615–627

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. Lin DH, Hoelz A (2019) The structure of the nuclear pore complex (an update). Annu Rev Biochem 88:725–783

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Lin SS, Nymark-McMahon MH, Yieh L, Sandmeyer SB (2001) Integrase mediates nuclear localization of Ty3. Mol Cell Biol 21:7826–7838

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. Llano M, Saenz DT, Meehan A, Wongthida P, Peretz M, Walker WH, Teo W, Poeschla EM (2006) An essential role for LEDGF/p75 in HIV integration. Science 314:461–464

    CAS  PubMed  Article  Google Scholar 

  79. Lusic M, Siliciano RF (2017) Nuclear landscape of HIV-1 infection and integration. Nat Rev Microbiol 15:69–82

    CAS  PubMed  Article  Google Scholar 

  80. Manhas S, Ma L, Measday V (2018) The yeast Ty1 retrotransposon requires components of the nuclear pore complex for transcription and genomic integration. Nucleic Acids Res 46:3552–3578

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  81. Marini B, Kertesz-Farkas A, Ali H, Lucic B, Lisek K, Manganaro L, Pongor S, Luzzati R, Recchia A, Mavilio F et al (2015) Nuclear architecture dictates HIV-1 integration site selection. Nature 521:227–231

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  82. Maskell DP, Renault L, Serrao E, Lesbats P, Matadeen R, Hare S, Lindemann D, Engelman AN, Costa A, Cherepanov P (2015) Structural basis for retroviral integration into nucleosomes. Nature 523:366–369

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  83. McLane LM, Pulliam KF, Devine SE, Corbett AH (2008) The Ty1 integrase protein can exploit the classical nuclear protein import machinery for entry into the nucleus. Nucleic Acids Res 36:4317–4326

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Michieletto D, Lusic M, Marenduzzo D, Orlandini E (2019) Physical principles of retroviral integration in the human genome. Nat Commun 10:575–587

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. Molenberghs F, Bogers JJ, De Vos WH (2020) Confined no more: viral mechanisms of nuclear entry and egress. Int J Biochem Cell Biol 129:105875

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  86. Moore SP, Rinckel LA, Garfinkel DJ (1998) A Ty1 Integrase nuclear localization signal required for retrotransposition. Mol Cell Biol 18:1105–1114

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. Morillon A, Bénard L, Springer M, Lesage P (2002) Differential effects of chromatin and Gcn4 on the 50-fold range of expression among individual yeast Ty1 retrotransposons. Mol Cell Biol 22:2078–2088

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  88. Mularoni L, Zhou Y, Bowen T, Gangadharan S, Wheelan SJ, Boeke JD (2012) Retrotransposon Ty1 integration targets specifically positioned asymmetric nucleosomal DNA segments in tRNA hotspots. Genome Res 22:693–703

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. Neuvéglise C, Feldmann H, Bon E, Gaillardin C, Casaregola S (2002) Genomic evolution of the long terminal repeat retrotransposons in hemiascomycetous yeasts. Genome Res 12:930–943

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  90. Ocampo-Hafalla MT, Uhlmann F (2011) Cohesin loading and sliding. J Cell Sci 124:685–691

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  91. Oficjalska-Pham D, Harismendy O, Smagowicz WJ, Gonzalez de Peredo A, Boguta M, Sentenac A, Lefebvre O (2006) General repression of RNA polymerase III transcription is triggered by protein phosphatase type 2A-mediated dephosphorylation of Maf1. Mol Cell 22:623–632

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  92. Patterson MN, Scannapieco AE, Au PH, Dorsey S, Royer CA, Maxwell PH (2015) Preferential retrotransposition in aging yeast mother cells is correlated with increased genome instability. DNA Repair (Amst) 34:18–27

    CAS  Article  Google Scholar 

  93. Patterson K, Shavarebi F, Magnan C, Chang I, Qi X, Baldi P, Bilanchone V, Sandmeyer SB (2019) Local features determine Ty3 targeting frequency at RNA polymerase III transcription start sites. Genome Res 29:1298–1309

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. Qi X, Sandmeyer S (2012) In vitro targeting of strand transfer by the Ty3 retroelement integrase. J Biol Chem 287:18589–18595

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Qi X, Daily K, Nguyen K, Wang H, Mayhew D, Rigor P, Forouzan S, Johnston M, Mitra RD, Baldi P et al (2012) Retrotransposon profiling of RNA polymerase III initiation sites. Genome Res 22:681–692

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. Quadrana L, Etcheverry M, Gilly A, Caillieux E, Madoui MA, Guy J, Bortolini Silveira A, Engelen S, Baillet V, Wincker P et al (2019) Transposition favors the generation of large effect mutations that may facilitate rapid adaption. Nat Commun 10:3421–3430

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  97. Risler JK, Kenny AE, Palumbo RJ, Gamache ER, Curcio MJ (2012) Host co-factors of the retrovirus-like transposon Ty1. Mob DNA 3:12

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Rothenbusch U, Sawatzki M, Chang Y, Caesar S, Schlenstedt G (2012) Sumoylation regulates Kap114-mediated nuclear transport. EMBO J 31:2461–2472

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Sharma A, Larue RC, Plumb MR, Malani N, Male F, Slaughter A, Kessl JJ, Shkriabai N, Coward E, Aiyer SS et al (2013) BET proteins promote efficient murine leukemia virus integration at transcription start sites. Proc Natl Acad Sci USA 110:12036–12041

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  100. Sharma D, De Falco L, Padavattan S, Rao C, Geifman-Shochat S, Liu CF, Davey CA (2019) PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome. Nat Commun 10:5751–5763

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. Souciet JL, Dujon B, Gaillardin C, Johnston M, Baret PV, Cliften P, Sherman DJ, Weissenbach J, Westhof E, Wincker P et al (2009) Comparative genomics of protoploid Saccharomycetaceae. Genome Res 19:1696–1709

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  102. Spaller T, Kling E, Glöckner G, Hillmann F, Winckler T (2016) Convergent evolution of tRNA gene targeting preferences in compact genomes. Mob DNA 7:17

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  103. Sultana T, Zamborlini A, Cristofari G, Lesage P (2017) Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet 18:292–308

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  104. Szilard RK, Jacques PE, Laramée L, Cheng B, Galicia S, Bataille AR, Yeung M, Mendez M, Bergeron M, Robert F et al (2011) Systematic identification of fragile sites via genome-wide location analysis of γ-H2AX. Nat Struct Mol Biol 17:299–305

    Article  CAS  Google Scholar 

  105. Vannini A, Cramer P (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45:439–446

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  106. Vorländer MK, Khatter H, Wetzel R, Hagen WJH, Müller CW (2018) Molecular mechanism of promoter opening by RNA polymerase III. Nature 553:295–300

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  107. Wilson MD, Renault L, Maskell DP, Ghoneim M, Pye VE, Nans A, Rueda DS, Cherepanov P, Costa A (2019) Retroviral integration into nucleosomes through DNA looping and sliding along the histone octamer. Nat Commun 10:4189–4198

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  108. Wu CC, Lin YC, Chen HT (2011) The TFIIF-like Rpc37/53 dimer lies at the center of a protein network to connect TFIIIC, Bdp1, and the RNA polymerase III active center. Mol Cell Biol 31:2715–2728

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. Xie W, Gai X, Zhu Y, Zappulla DC, Sternglanz R, Voytas DF (2001) Targeting of the yeast Ty5 retrotransposon to silent chromatin is mediated by interactions between integrase and Sir4p. Mol Cell Biol 21:6606–6614

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  110. Yieh L, Kassavetis G, Geiduschek EP, Sandmeyer SB (2000) The Brf and TATA-binding protein subunits of the RNA polymerase III transcription factor IIIB mediate position-specific integration of the gypsy-like element, Ty3. J Biol Chem 275:29800–29807

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  111. Yieh L, Hatzis H, Kassavetis G, Sandmeyer SB (2002) Mutational analysis of the transcription factor IIIB-DNA target of Ty3 retroelement integration. J Biol Chem 277:25920–25928

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  112. Zhu Y, Dai J, Fuerst PG, Voytas DF (2003) From the cover: controlling integration specificity of a yeast retrotransposon. Proc Natl Acad Sci USA 100:5891–5895

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  113. Zou S, Ke N, Kim JM, Voytas DF (1996) The saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes Dev 10:634–645

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We apologize to the many scientists that we may have omitted to mention in this review due to space limitations. The authors thank J. Acker, A. Asif-Laidin, J. Curcio and E. Fabre for the critical reading of the manuscript.

Funding

This work was supported by intramural funding from Centre National de la Recherche Scientifique (CNRS), the Université of Paris and the Institut National de la Santé et de la Recherche Médicale (INSERM), and from grants from the Fondation ARC pour la Recherche sur le Cancer (PJA 20151203412 and PJA 20191209703), the Agence Nationale de la Recherche through the generic call project ANR-17-CE11-0025. AB was supported by a post-doctoral fellowship from the ANR through the initiatives d’excellence (Idex ANR-11-IDEX-0005-02) and the Labex “Who am I?” (ANR11-LABX-0071).

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Amandine Bonnet and Pascale Lesage, equal contribution.

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Correspondence to Pascale Lesage.

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Bonnet, A., Lesage, P. Light and shadow on the mechanisms of integration site selection in yeast Ty retrotransposon families. Curr Genet (2021). https://doi.org/10.1007/s00294-021-01154-7

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Keywords

  • Ty1
  • Ty3
  • Ty5
  • LTR-retrotransposon
  • Integration targeting
  • S. cerevisiae