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

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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

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  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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Communicated by Michael Polymenis.

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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 67, 347–357 (2021). https://doi.org/10.1007/s00294-021-01154-7

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