1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Ty3, a Position-specific Retrotransposon in Budding Yeast

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    246.04 Kb
  • HTML
    249.32 Kb
  • PDF
    762.64 Kb
  • Authors: Suzanne Sandmeyer1, Kurt Patterson3, Virginia Bilanchone4
  • Editors: Suzanne Sandmeyer5, Nancy Craig6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Chemistry; 2: Department of Microbiology and Molecular Genetics, University of California, Irvine, CA; 3: Department of Biological Chemistry; 4: Department of Biological Chemistry; 5: University of California, Irvine, CA; 6: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
  • Received 22 January 2015 Accepted 30 January 2015 Published 19 March 2015
  • Suzanne Sandmeyer, sbsandme@uci.edu
image of Ty3, a Position-specific Retrotransposon in Budding Yeast
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Ty3, a Position-specific Retrotransposon in Budding Yeast, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0057-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0057-2014-2.gif
  • Abstract:

    Long terminal repeat (LTR) retrotransposons constitute significant fractions of many eukaryotic genomes. Two ancient families are Ty1/Copia () and Ty3/Gypsy (). The Ty3/Gypsy family probably gave rise to retroviruses based on the domain order, similarity of sequences, and the envelopes encoded by some members. The Ty3 element of is one of the most completely characterized elements at the molecular level. Ty3 is induced in mating cells by pheromone stimulation of the mitogen-activated protein kinase pathway as cells accumulate in G1. The two Ty3 open reading frames are translated into Gag3 and Gag3–Pol3 polyprotein precursors. In haploid mating cells Gag3 and Gag3–Pol3 are assembled together with Ty3 genomic RNA into immature virus-like particles in cellular foci containing RNA processing body proteins. Virus-like particle Gag3 is then processed by Ty3 protease into capsid, spacer, and nucleocapsid, and Gag3–Pol3 into those proteins and additionally, protease, reverse transcriptase, and integrase. After haploid cells mate and become diploid, genomic RNA is reverse transcribed into cDNA. Ty3 integration complexes interact with components of the RNA polymerase III transcription complex resulting in Ty3 integration precisely at the transcription start site. Ty3 activation during mating enables proliferation of Ty3 between genomes and has intriguing parallels with metazoan retrotransposon activation in germ cell lineages. Identification of nuclear pore, DNA replication, transcription, and repair host factors that affect retrotransposition has provided insights into how hosts and retrotransposons interact to balance genome stability and plasticity.

  • Citation: Sandmeyer S, Patterson K, Bilanchone V. 2015. Ty3, a Position-specific Retrotransposon in Budding Yeast. Microbiol Spectrum 3(2):MDNA3-0057-2014. doi:10.1128/microbiolspec.MDNA3-0057-2014.

Key Concept Ranking

Gene Expression and Regulation
0.5196819
Mouse mammary tumor virus
0.48691165
Human immunodeficiency virus 1
0.4717633
Mitogen-Activated Protein Kinase Pathway
0.4530119
0.5196819

References

1. Llorens C, Fares MA, Moya A. 2008. Relationships of gag–pol diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis. BMC Evol Biol 8:276. [PubMed][CrossRef]
2. Havecker, ER, Gao X, Voytas DF. 2004. The diversity of LTR retrotransposons. Genome Biol 5:225. [PubMed][CrossRef]
3. Eickbush TH, Jamburuthugoda VK. 2009. The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res 134:221–234. [PubMed][CrossRef]
4. Carr M, Bensasson D, Bergman CM. 2012. Evolutionary genomics of transposable elements in Saccharomyces cerevisiae. PLoS One 7:e50978. [PubMed][CrossRef]
5. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG. 1996. Life with 6000 genes. Science 274:546, 563–547. [PubMed][CrossRef]
6. 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. [PubMed]
7. del Rey FJ, Donahue TF, Fink GR. 1982. sigma, a repetitive element found adjacent to tRNA genes of yeast. Proc Natl Acad Sci U S A 79:4138–4142. [PubMed][CrossRef]
8. Sandmeyer SB, Olson MV. 1982. Insertion of a repetitive element at the same position in the 5′-flanking regions of two dissimilar yeast tRNA genes. Proc Natl Acad Sci U S A 79:7674–7678. [PubMed][CrossRef]
9. Hansen LJ, Chalker DL, Sandmeyer SB. 1988. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol 8:5245–5256. [PubMed]
10. Jordan IK, McDonald JF. 1999. Tempo and mode of Ty element evolution in Saccharomyces cerevisiae. Genetics 151:1341–1351. [PubMed]
11. Sandmeyer SB, Clemens KA. 2010. Function of a retrotransposon nucleocapsid protein. RNA Biol 7:642–654. [CrossRef]
12. Hansen LJ, Sandmeyer SB. 1990. Characterization of a transpositionally active Ty3 element and identification of the Ty3 integrase protein. J Virol 64:2599–2607. [PubMed]
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. [PubMed]
14. Clark DJ, Bilanchone VW, Haywood LJ, Dildine SL, Sandmeyer SB. 1988. A yeast sigma composite element, TY3, has properties of a retrotransposon. J Biol Chem 263:1413–1423. [PubMed]
15. Van Arsdell SW, Stetler GL, Thorner J. 1987. The yeast repeated element sigma contains a hormone-inducible promoter. Mol Cell Biol 7:749–759. [PubMed]
16. Bardwell, L. 2005. A walk-through of the yeast mating pheromone response pathway. Peptides 26:339–350. [PubMed][CrossRef]
17. Menees TM, Sandmeyer SB. 1994. Transposition of the yeast retroviruslike element Ty3 is dependent on the cell cycle. Mol Cell Biol 14:8229–8240. [PubMed]
18. Kinsey PT, Sandmeyer SB. 1995. Ty3 transposes in mating populations of yeast: a novel transposition assay for Ty3. Genetics 139:81–94. [PubMed]
19. Mieczkowski PA, Dominska M, Buck MJ, Gerton JL, Lieb JD, Petes TD. 2006. Global analysis of the relationship between the binding of the Bas1p transcription factor and meiosis-specific double-strand DNA breaks in Saccharomyces cerevisiae. Mol Cell Biol 26:1014–1027. [PubMed][CrossRef]
20. Daignan-Fornier B, Fink GR. 1992. Coregulation of purine and histidine biosynthesis by the transcriptional activators BAS1 and BAS2. Proc Natl Acad Sci U S A 89:6746–6750. [PubMed][CrossRef]
21. Arndt KT, Styles C, Fink GR. 1987. Multiple global regulators control HIS4 transcription in yeast. Science 237:874–880. [PubMed][CrossRef]
22. Servant G, Pinson B, Tchalikian-Cosson A, Coulpier F, Lemoine S, Pennetier C, Bridier-Nahmias A, Todeschini AL, Fayol H, Daignan-Fornier B, Lesage P. 2012. Tye7 regulates yeast Ty1 retrotransposon sense and antisense transcription in response to adenylic nucleotides stress. Nucleic Acids Res 40:5271–5282. [PubMed][CrossRef]
23. 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. [PubMed][CrossRef]
24. Hull MW, Erickson J, Johnston M, Engelke DR. 1994. tRNA genes as transcriptional repressor elements. Mol Cell Biol 14:1266–1277. [PubMed]
25. Wang L, Haeusler RA, Good PD, Thompson M, Nagar S, Engelke DR. 2005. Silencing near tRNA genes requires nucleolar localization. J Biol Chem 280:8637–8639. [PubMed][CrossRef]
26. Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR. 2008. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 22:2204–2214. [PubMed][CrossRef]
27. Bolton EC, Boeke JD. 2003. Transcriptional interactions between yeast tRNA genes, flanking genes and Ty elements: a genomic point of view. Genome Res 13:254–263. [PubMed][CrossRef]
28. Kirchner J, Sandmeyer SB, Forrest DB. 1992. Transposition of a Ty3 GAG3–POL3 fusion mutant is limited by availability of capsid protein. J Virol 66:6081–6092. [PubMed]
29. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA. 2004. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117:427–439. [PubMed][CrossRef]
30. Chen M, Gartenberg MR. 2014. Coordination of tRNA transcription with export at nuclear pore complexes in budding yeast. Genes Dev 28:959–970. [PubMed][CrossRef]
31. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendure J, Fields S, Blau CA, Noble WS. 2010. A three-dimensional model of the yeast genome. Nature 465:363–367. [PubMed][CrossRef]
32. Morillon A, Springer M, Lesage P. 2000. Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 20:5766–5776. [PubMed][CrossRef]
33. Saito H. 2010. Regulation of cross-talk in yeast MAPK signaling pathways. Curr Opin Microbiol 13:677–683. [PubMed][CrossRef]
34. Elder RT, St John TP, Stinchcomb DT, Davis RW, Scherer S. 1981. Studies on the transposable element Ty1 of yeast. I. RNA homologous to Ty1. II. Recombination and expression of Ty1 and adjacent sequences. Cold Spring Harb Symp Quant Biol 45(Pt 2):581–591. [PubMed][CrossRef]
35. Xu H, Boeke JD. 1991. Inhibition of Ty1 transposition by mating pheromones in Saccharomyces cerevisiae. Mol Cell Biol 11:2736–2743. [PubMed]
36. Conte D, Jr, Barber E, Banerjee M, Garfinkel DJ, Curcio MJ. 1998. Posttranslational regulation of Ty1 retrotransposition by mitogen-activated protein kinase Fus3. Mol Cell Biol 18:2502–2513. [PubMed]
37. Conte D, Jr, Curcio MJ. 2000. Fus3 controls Ty1 transpositional dormancy through the invasive growth MAPK pathway. Mol Microbiol 35:415–427. [PubMed][CrossRef]
38. Qi X, Daily K, Nguyen K, Wang H, Mayhew D, Rigor P, Forouzan S, Johnston M, Mitra RD, Baldi P, Sandmeyer S. 2012. Retrotransposon profiling of RNA polymerase III initiation sites. Genome Res 22:681–692. [PubMed][CrossRef]
39. Boeke JD, Trueheart J, Natsoulis G, Fink GR. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154:164–175. [PubMed][CrossRef]
40. Curcio MJ, Garfinkel DJ. 1991. Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci U S A 88:936–940. [PubMed][CrossRef]
41. Aye M, Sandmeyer SB. 2003. Ty3 requires yeast La homologous protein for wild-type frequencies of transposition. Mol Microbiol 49:501–515. [PubMed][CrossRef]
42. Farabaugh PJ, Zhao H, Vimaladithan A. 1993. A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell 74:93–103. [PubMed][CrossRef]
43. Kirchner J, Sandmeyer S. 1993. Proteolytic processing of Ty3 proteins is required for transposition. J Virol 67:19–28. [PubMed]
44. Kuznetsov YG, Zhang M, Menees TM, McPherson A, Sandmeyer S. 2005. Investigation by atomic force microscopy of the structure of Ty3 retrotransposon particles. J Virol 79:8032–8045. [PubMed][CrossRef]
45. Zhang M, Larsen LS, Irwin B, Bilanchone V, Sandmeyer S. 2010. Two-hybrid analysis of Ty3 capsid subdomain interactions. Mob DNA 1:14. [PubMed][CrossRef]
46. Kirchner J, Sandmeyer SB. 1996. Ty3 integrase mutants defective in reverse transcription or 3′-end processing of extrachromosomal Ty3 DNA. J Virol 70:4737–4747. [PubMed]
47. Qi X, Sandmeyer SB. 2012. In vitro targeting of strand transfer by the Ty3 retroelement integrase. J Biol Chem 287:18589–18595. [PubMed][CrossRef]
48. Claypool JA, Malik HS, Eickbush TH, Sandmeyer SB. 2001. Ten-kilodalton domain in Ty3 Gag3–Pol3p between PR and RT is dispensable for Ty3 transposition. J Virol 75:1557–1560. [PubMed][CrossRef]
49. Beliakova-Bethell N, Beckham C, Giddings TH, Jr, Winey M, Parker R, Sandmeyer S. 2006. Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components. RNA 12:94–101. [PubMed][CrossRef]
50. Orlinsky KJ, Sandmeyer SB.1994. The Cys-His motif of Ty3 NC can be contributed by Gag3 or Gag3–Pol3 polyproteins. J Virol 68:4152–4166. [PubMed]
51. Turkel S, Kaplan G, Farabaugh PJ. 2011. Glucose signalling pathway controls the programmed ribosomal frameshift efficiency in retroviral-like element Ty3 in Saccharomyces cerevisiae. Yeast 28:799–808. [PubMed][CrossRef]
52. Nymark-McMahon MH, Beliakova-Bethell NS, Darlix JL, Le Grice SF, Sandmeyer SB. 2002. Ty3 integrase is required for initiation of reverse transcription. J Virol 76:2804–2816. [PubMed][CrossRef]
53. Keeney JB, Chapman KB, Lauermann V, Voytas DF, Astrom SU, von Pawel-Rammingen U, Bystrom A, Boeke JD. 1995. Multiple molecular determinants for retrotransposition in a primer tRNA. Mol Cell Biol 15:217–226. [PubMed]
54. Hansen LJ, Chalker DL, Orlinsky KJ, Sandmeyer SB. 1992. Ty3 GAG3 and POL3 genes encode the components of intracellular particles. J Virol 66:1414–1424. [PubMed]
55. Larsen LS, Kuznetsov Y, McPherson A, Hatfield GW, Sandmeyer S. 2008. TY3 GAG3 protein forms ordered particles in Escherichia coli. Virology 370:223–227. [PubMed][CrossRef]
56. Clemens K, Larsen L, Zhang M, Kuznetsov Y, Bilanchone V, Randall A, Harned A, Dasilva R, Nagashima K, McPherson A, Baldi P, Sandmeyer S. 2011. The Ty3 Gag3 spacer controls intracellular condensation and uncoating. J Virol 85:3055–3066. [PubMed][CrossRef]
57. Larsen LS, Beliakova-Bethell N, Bilanchone V, Zhang M, Lamsa A, Dasilva R, Hatfield GW, Nagashima K, Sandmeyer S. 2008. Ty3 nucleocapsid controls localization of particle assembly. J Virol 82:2501–2514. [PubMed][CrossRef]
58. Larsen LS, Zhang M, Beliakova-Bethell N, Bilanchone V, Lamsa A, Nagashima K, Najdi R, Kosaka K, Kovacevic V, Cheng J, Baldi P, Hatfield GW, Sandmeyer S. 2007. Ty3 capsid mutations reveal early and late functions of the amino-terminal domain. J Virol 81:6957–6972. [PubMed][CrossRef]
59. Martin-Rendon E, Marfany G, Wilson S, Ferguson DJ, Kingsman SM, Kingsman AJ. 1996. Structural determinants within the subunit protein of Ty1 virus-like particles. Mol Microbiol 22:667–679. [PubMed][CrossRef]
60. Forshey BM, von Schwedler U, Sundquist WI, Aiken C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J Virol 76:5667–5677. [PubMed][CrossRef]
61. Briggs JA, Krausslich HG. 2011. The molecular architecture of HIV. J Mol Biol 410:491–500. [PubMed][CrossRef]
62. Ganser-Pornillos BK, Yeager M, Sundquist WI. 2008. The structural biology of HIV assembly. Curr Opin Struct Biol 18:203–217. [PubMed][CrossRef]
63. Sundquist WI, Hill CP. 2007. How to assemble a capsid. Cell 131:17–19. [PubMed][CrossRef]
64. 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. [PubMed][CrossRef]
65. Orlinsky KJ, Gu J, Hoyt M, Sandmeyer S, Menees TM. 1996. Mutations in the Ty3 major homology region affect multiple steps in Ty3 retrotransposition. J Virol 70:3440–3448. [PubMed]
66. Garbitt-Hirst R, Kenney SP, Parent LJ. 2009. Genetic evidence for a connection between Rous sarcoma virus gag nuclear trafficking and genomic RNA packaging. J Virol 83:6790–6797. [PubMed][CrossRef]
67. Parent LJ. 2011. New insights into the nuclear localization of retroviral Gag proteins. Nucleus 2:92–97. [PubMed][CrossRef]
68. Grigorov B, Decimo D, Smagulova F, Pechoux C, Mougel M, Muriaux D, Darlix JL. 2007. Intracellular HIV-1 Gag localization is impaired by mutations in the nucleocapsid zinc fingers. Retrovirology 4:54. [PubMed][CrossRef]
69. Levesque K, Halvorsen M, Abrahamyan L, Chatel-Chaix L, Poupon V, Gordon H, DesGroseillers L, Gatignol A, Mouland AJ. 2006. Trafficking of HIV-1 RNA is mediated by heterogeneous nuclear ribonucleoprotein A2 expression and impacts on viral assembly. Traffic 7:1177–1193. [PubMed][CrossRef]
70. Checkley MA, Mitchell JA, Eizenstat LD, Lockett SJ, Garfinkel DJ. 2013. Ty1 gag enhances the stability and nuclear export of Ty1 mRNA. Traffic 14:57–69. [PubMed]
71. Keller PW, Johnson MC, Vogt VM. 2008. Mutations in the spacer peptide and adjoining sequences in Rous sarcoma virus Gag lead to tubular budding. J Virol 82:6788–6797. [PubMed][CrossRef]
72. Yeager M. 2011. Design of in vitro symmetric complexes and analysis by hybrid methods reveal mechanisms of HIV capsid assembly. J Mol Biol 410:534–552. [PubMed][CrossRef]
73. Qualley DF, Stewart-Maynard KM, Wang F, Mitra M, Gorelick RJ, Rouzina I, Williams MC, Musier-Forsyth K. 2010. C-terminal domain modulates the nucleic acid chaperone activity of human T-cell leukemia virus type 1 nucleocapsid protein via an electrostatic mechanism. J Biol Chem 285:295–307. [PubMed][CrossRef]
74. Pettit SC, Moody MD, Wehbie RS, Kaplan AH, Nantermet PV, Klein CA, Swanstrom R. 1994. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J Virol 68:8017–8027. [PubMed]
75. Gabus C, Ficheux D, Rau M, Keith G, Sandmeyer S, Darlix JL. 1998. The yeast Ty3 retrotransposon contains a 5′–3′ bipartite primer-binding site and encodes nucleocapsid protein NCp9 functionally homologous to HIV-1 NCp7. EMBO J 17:4873–4880. [PubMed][CrossRef]
76. Clemens K, Bilanchone V, Beliakova-Bethell N, Larsen LS, Nguyen K, Sandmeyer S. 2013. Sequence requirements for localization and packaging of Ty3 retroelement RNA. Virus Res 171:319–331. [PubMed][CrossRef]
77. D'Souza V, Summers MF. 2005. How retroviruses select their genomes. Nat Rev Microbiol 3:643–655. [PubMed][CrossRef]
78. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. 1998. Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445. [PubMed][CrossRef]
79. Lecher P, Bucheton A, Pelisson A. 1997. Expression of the Drosophila retrovirus gypsy as ultrastructurally detectable particles in the ovaries of flies carrying a permissive flamenco allele. J Gen Virol 78(Pt 9):2379–2388. [PubMed]
80. Garfinkel DJ, Boeke JD, Fink GR. 1985. Ty element transposition: reverse transcriptase and virus-like particles. Cell 42:507–517. [PubMed][CrossRef]
81. 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. [PubMed]
82. Sheth U, Parker R. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805–808. [PubMed][CrossRef]
83. Brengues M, Teixeira D, Parker R. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310:486–489. [PubMed][CrossRef]
84. Hu W, Sweet TJ, Chamnongpol S, Baker KE, Coller J. 2009. Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461:225–229. [PubMed][CrossRef]
85. Thomas MG, Loschi M, Desbats MA, Boccaccio GL. 2011. RNA granules: the good, the bad and the ugly. Cell Signal 23:324–334. [PubMed][CrossRef]
86. Buchan JR, Nissan T, Parker R. 2010. Analyzing P-bodies and stress granules in Saccharomyces cerevisiae. Methods Enzymol 470:619–640. [CrossRef]
87. Mitchell SF, Jain S, She M, Parker R. 2013. Global analysis of yeast mRNPs. Nat Struct Mol Biol 20:127–133. [PubMed][CrossRef]
88. Nissan T, Rajyaguru P, She M, Song H, Parker R. 2010. Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol Cell 39:773–783. [PubMed][CrossRef]
89. Coller J, Parker R. 2005. General translational repression by activators of mRNA decapping. Cell 122:875–886. [PubMed][CrossRef]
90. Rajyaguru P, Parker R. 2009. CGH-1 and the control of maternal mRNAs. Trends Cell Biol 19:24–28. [PubMed][CrossRef]
91. Tharun S, Parker R. 2001. Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p–7p complex on deadenylated yeast mRNAs. Mol Cell 8:1075–1083. [PubMed][CrossRef]
92. Fillman C, Lykke-Andersen J. 2005. RNA decapping inside and outside of processing bodies. Curr Opin Cell Biol 17:326–331. [PubMed][CrossRef]
93. Nagarajan VK, Jones CI, Newbury SF, Green PJ. 2013. XRN 5′––>3′ exoribonucleases: structure, mechanisms and functions. Biochim Biophys Acta 1829:590–603. [PubMed][CrossRef]
94. Parker R. 2012. RNA degradation in Saccharomyces cerevisae. Genetics 191:671–702. [PubMed][CrossRef]
95. Anderson P, Kedersha N. 2009. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10:430–436. [PubMed][CrossRef]
96. Jain S, Parker R. 2013. The discovery and analysis of P Bodies. Adv Exp Med Biol 768:23–43. [PubMed][CrossRef]
97. Ka M, Park YU, Kim J. 2008. The DEAD-box RNA helicase, Dhh1, functions in mating by regulating Ste12 translation in Saccharomyces cerevisiae. Biochem Biophys Res Commun 367:680–686. [PubMed][CrossRef]
98. Dutko JA, Kenny AE, Gamache ER, Curcio MJ. 2010. 5′ to 3′ mRNA decay factors colocalize with Ty1 gag and human APOBEC3G and promote Ty1 retrotransposition. J Virol 84:5052–5066. [PubMed][CrossRef]
99. Checkley MA, Nagashima K, Lockett SJ, Nyswaner KM, Garfinkel DJ. 2010. P-body components are required for Ty1 retrotransposition during assembly of retrotransposition-competent virus-like particles. Mol Cell Biol 30:382–398. [PubMed][CrossRef]
100. Le Grice SFJ, Nowotny M. 2014. Nucleic acid polymerases: reverse transcriptases. Nucleic Acids Mol Biol 30:189–214. [CrossRef]
101. Rausch JW, Le Grice SF. 2004. ‘Binding, bending and bonding’: polypurine tract-primed initiation of plus-strand DNA synthesis in human immunodeficiency virus. Int J Biochem Cell Biol 36:1752–1766. [PubMed][CrossRef]
102. Malik HS, Eickbush TH. 2001. Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11:1187–1197. [PubMed][CrossRef]
103. Cristofari G, Gabus C, Ficheux D, Bona M, Le Grice SF, Darlix JL. 1999. Characterization of active reverse transcriptase and nucleoprotein complexes of the yeast retrotransposon Ty3 in vitro. J Biol Chem 274:36643–36648. [PubMed][CrossRef]
104. Rausch JW, Grice MK, Henrietta M, Nymark M, Miller JT, Le Grice SF. 2000. Interaction of p55 reverse transcriptase from the Saccharomyces cerevisiae retrotransposon Ty3 with conformationally distinct nucleic acid duplexes. J Biol Chem 275:13879–13887. [PubMed][CrossRef]
105. Lener D, Budihas SR, Le Grice SF. 2002. Mutating conserved residues in the ribonuclease H domain of Ty3 reverse transcriptase affects specialized cleavage events. J Biol Chem 277:26486–26495. [PubMed][CrossRef]
106. Nowak E, Miller JT, Bona MK, Studnicka J, Szczepanowski RH, Jurkowski J, Le Grice SF, Nowotny M. 2014. Ty3 reverse transcriptase complexed with an RNA–DNA hybrid shows structural and functional asymmetry. Nat Struct Mol Biol 21:389–396. [PubMed][CrossRef]
107. Friant S, Heyman T, Wilhelm ML, Wilhelm FX. 1996. Extended interactions between the primer tRNAi(Met) and genomic RNA of the yeast Ty1 retrotransposon. Nucleic Acids Res 24:441–449. [PubMed][CrossRef]
108. Le Grice SF. 2003. “In the beginning”: initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42:14349–14355. [PubMed][CrossRef]
109. Heyman T, Agoutin B, Friant S, Wilhelm FX, Wilhelm ML. 1995. Plus-strand DNA synthesis of the yeast retrotransposon Ty1 is initiated at two sites, PPT1 next to the 3′ LTR and PPT2 within the pol gene. PPT1 is sufficient for Ty1 transposition. J Mol Biol 253:291–303. [PubMed][CrossRef]
110. Bibillo A, Lener D, Tewari A, Le Grice SF. 2005. Interaction of the Ty3 reverse transcriptase thumb subdomain with template-primer. J Biol Chem 280:30282–30290. [PubMed][CrossRef]
111. Yi-Brunozzi HY, Brabazon DM, Lener D, Le Grice SF, Marino JP. 2005. A ribose sugar conformational switch in the LTR-retrotransposon Ty3 polypurine tract-containing RNA/DNA hybrid. J Am Chem Soc 127:16344–16345. [PubMed][CrossRef]
112. Dash C, Marino JP, Le Grice SF. 2006. Examining Ty3 polypurine tract structure and function by nucleoside analog interference. J Biol Chem 281:2773–2783. [PubMed][CrossRef]
113. Lener D, Kvaratskhelia M, Le Grice SF. 2003. Nonpolar thymine isosteres in the Ty3 polypurine tract DNA template modulate processing and provide a model for its recognition by Ty3 reverse transcriptase. J Biol Chem 278:26526–26532. [PubMed][CrossRef]
114. Nair GR, Dash C, Le Grice SF, DeStefano JJ. 2012. Viral reverse transcriptases show selective high affinity binding to DNA–DNA primer-templates that resemble the polypurine tract. PLoS One 7:e41712. [PubMed][CrossRef]
115. Ke N, Gao X, Keeney JB, Boeke JD, Voytas DF. 1999. The yeast retrotransposon Ty5 uses the anticodon stem–loop of the initiator methionine tRNA as a primer for reverse transcription. RNA 5:929–938. [PubMed][CrossRef]
116. Chapman KB, Boeke JD. 1991. Isolation and characterization of the gene encoding yeast debranching enzyme. Cell 65:483–492. [PubMed][CrossRef]
117. Cheng Z, Menees TM. 2004. RNA branching and debranching in the yeast retrovirus-like element Ty1. Science 303:240–243. [PubMed][CrossRef]
118. Coombes CE, Boeke JD. 2005. An evaluation of detection methods for large lariat RNAs. RNA 11:323–331. [PubMed][CrossRef]
119. Galvis AE, Fisher HE, Nitta T, Fan H, Camerini D. 2014. Impairment of HIV-1 cDNA Synthesis by DBR1 Knockdown. J Virol 88:7054–7069. [PubMed][CrossRef]
120. Moore MD, Hu WS. 2009. HIV-1 RNA dimerization: It takes two to tango. AIDS Rev 11:91–102. [PubMed]
121. Purzycka KJ, Legiewicz M, Matsuda E, Eizentstat LD, Lusvarghi S, Saha A, Le Grice SF, Garfinkel DJ. 2013. Exploring Ty1 retrotransposon RNA structure within virus-like particles. Nucleic Acids Res 41:463–473. [PubMed][CrossRef]
122. Wente SR, Rout MP. 2010. The nuclear pore complex and nuclear transport. Cold Spring Harbor Persp Biol 2:a000562. [PubMed][CrossRef]
123. Hoelz A, Debler EW, Blobel G. 2011. The structure of the nuclear pore complex. Annu Rev Biochem 80:613–643. [PubMed][CrossRef]
124. Taddei A, Gasser SM. 2012. Structure and function in the budding yeast nucleus. Genetics 192:107–129. [PubMed][CrossRef]
125. Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, Varela E, Hediger F, Gasser SM, Krogan NJ. 2008. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322:597–602. [PubMed][CrossRef]
126. Pante N, Kann M. 2002. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell 13:425–434. [PubMed][CrossRef]
127. 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. [PubMed]
128. Moore SP, Rinckel LA, Garfinkel DJ. 1998. A Ty1 integrase nuclear localization signal required for retrotransposition. Mol Cell Biol 18:1105–1114. [PubMed]
129. Dang VD, Levin HL. 2000. Nuclear import of the retrotransposon Tf1 is governed by a nuclear localization signal that possesses a unique requirement for the FXFG nuclear pore factor Nup124p. Mol Cell Biol 20:7798–7812. [PubMed][CrossRef]
130. Levin A, Loyter A, Bukrinsky M. 2011. Strategies to inhibit viral protein nuclear import: HIV-1 as a target. Biochim Biophys Acta 1813:1646–1653. [PubMed][CrossRef]
131. Katz RA, Greger JG, Darby K, Boimel P, Rall GF, Skalka AM. 2002. Transduction of interphase cells by avian sarcoma virus. J Virol 76:5422–5434. [PubMed][CrossRef]
132. 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. [PubMed][CrossRef]
133. Beliakova-Bethell N, Terry LJ, Bilanchone V, DaSilva R, Nagashima K, Wente SR, Sandmeyer S. 2009. Ty3 nuclear entry is initiated by viruslike particle docking on GLFG nucleoporins. J Virol 83:11914–11925. [PubMed][CrossRef]
134. Heath CV, Copeland CS, Amberg DC, Del Priore V, Snyder M, Cole CN. 1995. Nuclear pore complex clustering and nuclear accumulation of poly(A)+ RNA associated with mutation of the Saccharomyces cerevisiae RAT2/NUP120 gene. J Cell Biol 131:1677–1697. [PubMed][CrossRef]
135. Li O, Heath CV, Amberg DC, Dockendorff TC, Copeland CS, Snyder M, Cole CN. 1995. Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes. Mol Biol Cell 6:401–417. [PubMed][CrossRef]
136. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR. 2004. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 6:197–206. [PubMed][CrossRef]
137. Fassati A. 2012. Multiple roles of the capsid protein in the early steps of HIV-1 infection. Virus Res 170:15–24. [PubMed][CrossRef]
138. Matreyek KA, Engelman A. 2011. The requirement for nucleoporin NUP153 during human immunodeficiency virus type 1 infection is determined by the viral capsid. J Virol 85:7818–7827. [PubMed][CrossRef]
139. Krishnan L, Matreyek KA, Oztop I, Lee K, Tipper CH, Li X, Dar MJ, Kewalramani VN, Engelman A. 2010. The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase. J Virol 84:397–406. [PubMed][CrossRef]
140. Lin SS, Nymark-McMahon MH, Yieh L, Sandmeyer SB. 2001. Integrase mediates nuclear localization of Ty3. Mol Cell Biol 21:7826–7838. [PubMed][CrossRef]
141. Chalker DL, Sandmeyer SB. 1990. Transfer RNA genes are genomic targets for de novo transposition of the yeast retrotransposon Ty3. Genetics 126:837–850. [PubMed]
142. Sandmeyer SB, Hansen LJ, Chalker DL. 1990. Integration specificity of retrotransposons and retroviruses. Annu Rev Genet 24:491–518. [PubMed][CrossRef]
143. Hani J, Feldmann H. 1998. tRNA genes and retroelements in the yeast genome. Nucleic Acids Res 26:689–696. [PubMed][CrossRef]
144. Natsoulis G, Thomas W, Roghmann MC, Winston F, Boeke JD. 1989. Ty1 transposition in Saccharomyces cerevisiae is nonrandom. Genetics123:269–279. [PubMed]
145. Hofmann J, Schumann G, Borschet G, Gosseringer R, Bach M, Bertling WM, Marschalek R, Dingermann T. 1991. Transfer RNA genes from Dictyostelium discoideum are frequently associated with repetitive elements and contain consensus boxes in their 5′ and 3′-flanking regions. J Mol Biol 222:537–552. [CrossRef]
146. Zou S, Voytas DF. 1997. Silent chromatin determines target preference of the Saccharomyces retrotransposon Ty5. Proc Natl Acad Sci U S A 94:7412–7416. [PubMed][CrossRef]
147. Gao X, Hou Y, Ebina H, Levin HL, Voytas DF. 2008. Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res 18:359–369. [PubMed][CrossRef]
148. Hare S, Gupta SS, Valkov E, Engelman A, Cherepanov P. 2010. Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464:232–236. [PubMed][CrossRef]
149. Maertens GN, Hare S, Cherepanov P. 2010. The mechanism of retroviral integration from X-ray structures of its key intermediates. Nature 468:326–329. [PubMed][CrossRef]
150. Li X, Krishnan L, Cherepanov P, Engelman A. 2011. Structural biology of retroviral DNA integration. Virology 411:194–205. [PubMed][CrossRef]
151. Rice P, Craigie R, Davies DR. 1996. Retroviral integrases and their cousins. Curr Opin Struct Biol 6:76–83. [PubMed][CrossRef]
152. Kulkosky J, Jones KS, Katz RA, Mack JP, Skalka AM. 1992. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol Cell Biol 12:2331–2338. [PubMed]
153. Qi X, Vargas E, Larsen L, Knapp W, Hatfield GW, Lathrop R, Sandmeyer S. 2013. Directed DNA shuffling of retrovirus and retrotransposon integrase protein domains. PLoS One 8:e63957. [PubMed][CrossRef]
154. Malik HS, Eickbush TH. 1999. Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol 73:5186–5190. [PubMed]
155. Ebina H, Chatterjee AG, Judson RL, Levin HL. 2008. The GP(Y/F) domain of TF1 integrase multimerizes when present in a fragment, and substitutions in this domain reduce enzymatic activity of the full-length protein. J Biol Chem 283:15965–15974. [PubMed][CrossRef]
156. Nymark-McMahon MH, Sandmeyer SB. 1999. Mutations in nonconserved domains of Ty3 integrase affect multiple stages of the Ty3 life cycle. J Virol 73:453–465. [PubMed]
157. Engelman A, Englund G, Orenstein JM, Martin MA, Craigie R. 1995. Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J Virol 69:2729–2736. [PubMed]
158. Briggs JA, Grunewald K, Glass B, Forster F, Krausslich HG, Fuller SD. 2006. The mechanism of HIV-1 core assembly: insights from three-dimensional reconstructions of authentic virions. Structure 14:15–20. [PubMed][CrossRef]
159. Jurado KA, Wang H, Slaughter A, Feng L, Kessl JJ, Koh Y, Wang W, Ballandras-Colas A, Patel PA, Fuchs JR, Kvaratskhelia M, Engelman A. 2013. Allosteric integrase inhibitor potency is determined through the inhibition of HIV-1 particle maturation. Proc Natl Acad Sci U S A 110:8690–8695. [PubMed][CrossRef]
160. Millar CB, Grunstein M. 2006. Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol 7:657–666. [PubMed][CrossRef]
161. Brodeur GM, Sandmeyer SB, Olson MV. 1983. Consistent association between sigma elements and tRNA genes in yeast. Proc Natl Acad Sci U S A 80:3292–3296. [PubMed][CrossRef]
162. Chalker DL, Sandmeyer SB. 1992. Ty3 integrates within the region of RNA polymerase III transcription initiation. Genes Dev 6:117–128. [PubMed][CrossRef]
163. Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A. 2007. The expanding RNA polymerase III transcriptome. Trends Genet 23:614–622. [PubMed][CrossRef]
164. Geiduschek EP, Kassavetis GA. 2001. The RNA polymerase III transcription apparatus. J Mol Biol 310:1–26. [PubMed][CrossRef]
165. Kassavetis GA, Geiduschek EP. 2006. Transcription factor TFIIIB and transcription by RNA polymerase III. Biochem Soc Trans 34:1082–1087. [PubMed][CrossRef]
166. Kassavetis GA, Letts GA, Geiduschek EP. 2001. The RNA polymerase III transcription initiation factor TFIIIB participates in two steps of promoter opening. EMBO J 20:2823–2834. [PubMed][CrossRef]
167. Giuliodori S, Percudani R, Braglia P, Ferrari R, Guffanti E, Ottonello S, Dieci G. 2003. A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J Mol Biol 333:1–20. [PubMed][CrossRef]
168. Eschenlauer JB, Kaiser MW, Gerlach VL, Brow DA. 1993. Architecture of a yeast U6 RNA gene promoter. Mol Cell Biol 13:3015–3026. [PubMed]
169. Kassavetis GA, Braun BR, Nguyen LH, Geiduschek EP. 1990. S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell 60:235–245. [PubMed][CrossRef]
170. Roberts DN, Stewart AJ, Huff JT, Cairns BR. 2003. The RNA polymerase III transcriptome revealed by genome-wide localization and activity-occupancy relationships. Proc Natl Acad Sci U S A 100:14695–14700. [PubMed][CrossRef]
171. Moqtaderi Z, Struhl K. 2004. Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol Cell Biol 24:4118–4127. [PubMed][CrossRef]
172. Harismendy O, Gendrel CG, Soularue P, Gidrol X, Sentenac A, Werner M, Lefebvre O. 2003. Genome-wide location of yeast RNA polymerase III transcription machinery. EMBO J 22:4738–4747. [PubMed][CrossRef]
173. Chalker DL, Sandmeyer SB. 1993. Sites of RNA polymerase III transcription initiation and Ty3 integration at the U6 gene are positioned by the TATA box. Proc Natl Acad Sci U S A 90:4927–4931. [PubMed][CrossRef]
174. Kirchner J, Connolly CM, Sandmeyer SB. 1995. Requirement of RNA polymerase III transcription factors for in vitro position-specific integration of a retroviruslike element. Science 267:1488–1491. [PubMed][CrossRef]
175. 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. [PubMed][CrossRef]
176. 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. [PubMed][CrossRef]
177. Connolly CM, Sandmeyer SB. 1997. RNA polymerase III interferes with Ty3 integration. FEBS Lett 405:305–311. [PubMed][CrossRef]
178. Kassavetis GA, Soragni E, Driscoll R, Geiduschek EP. 2005. Reconfiguring the connectivity of a multiprotein complex: fusions of yeast TATA-binding protein with Brf1, and the function of transcription factor IIIB. Proc Natl Acad Sci U S A 102:15406–15411. [PubMed][CrossRef]
179. Parnell TJ, Huff JT, Cairns BR. 2008. RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J 27:100–110. [PubMed][CrossRef]
180. Orioli A, Pascali C, Pagano A, Teichmann M, Dieci G. 2012. RNA polymerase III transcription control elements: themes and variations. Gene 493:185–194. [PubMed][CrossRef]
181. Good PD, Kendall A, Ignatz-Hoover J, Miller EL, Pai DA, Rivera SR, Carrick B, Engelke DR. 2013. Silencing near tRNA genes is nucleosome-mediated and distinct from boundary element function. Gene 526:7–15. [PubMed][CrossRef]
182. Kirkland JG, Raab JR, Kamakaka RT. 2013. TFIIIC bound DNA elements in nuclear organization and insulation. Biochim Biophys Acta 1829:418–424. [PubMed][CrossRef]
183. Acker J, Conesa C, Lefebvre O. 2013. Yeast RNA polymerase III transcription factors and effectors. Biochim Biophys Acta 1829:283–295. [PubMed][CrossRef]
184. Mahapatra S, Dewari PS, Bhardwaj A, Bhargava P. 2011. Yeast H2A.Z, FACT complex and RSC regulate transcription of tRNA gene through differential dynamics of flanking nucleosomes. Nucleic Acids Res 39:4023–4034. [PubMed][CrossRef]
185. Nagarajavel V, Iben JR, Howard BH, Maraia RJ, Clark DJ. 2013. Global ‘bootprinting’ reveals the elastic architecture of the yeast TFIIIB-TFIIIC transcription complex in vivo. Nucleic Acids Res 41:8135–8143. [PubMed][CrossRef]
186. Van Bortle K, Corces VG. 2012. tDNA insulators and the emerging role of TFIIIC in genome organization. Transcription 3:277–284. [PubMed][CrossRef]
187. Kumar Y, Bhargava P. 2013. A unique nucleosome arrangement, maintained actively by chromatin remodelers facilitates transcription of yeast tRNA genes. BMC Genomics 14:402. [PubMed][CrossRef]
188. Mou Z, Kenny AE, Curcio MJ. 2006. Hos2 and Set3 promote integration of Ty1 retrotransposons at tRNA genes in Saccharomyces cerevisiae. Genetics 172:2157–2167. [PubMed][CrossRef]
189. Morse RH, Roth SY, Simpson RT. 1992. A transcriptionally active tRNA gene interferes with nucleosome positioning in vivo. Mol Cell Biol 12:4015–4025. [PubMed]
190. 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][CrossRef]
191. Deshpande AM, Newlon CS. 1996. DNA replication fork pause sites dependent on transcription. Science 272:1030–1033. [PubMed][CrossRef]
192. Thompson M, Haeusler RA, Good PD, Engelke DR. 2003. Nucleolar clustering of dispersed tRNA genes. Science 302:1399–1401. [PubMed][CrossRef]
193. 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. [PubMed][CrossRef]
194. Rinke J, Steitz JA. 1982. Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La lupus antibodies. Cell 29:149–159. [PubMed][CrossRef]
195. Wang GP, Ciuffi A, Leipzig J, Berry CC, Bushman FD. 2007. HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res 17:1186–1194. [PubMed][CrossRef]
196. Eidahl JO, Crowe BL, North JA, McKee CJ, Shkriabai N, Feng L, Plumb M, Graham RL, Gorelick RJ, Hess S, Poirier MG, Foster MP, Kvaratskhelia M. 2013. Structural basis for high-affinity binding of LEDGF PWWP to mononucleosomes. Nucleic Acids Res 41:3924–3936. [PubMed][CrossRef]
197. Sharma A, Larue RC, Plumb MR, Malani N, Male F, Slaughter A, Kessl JJ, Shkriabai N, Coward E, Aiyer SS, Green PL, Wu L, Roth MJ, Bushman FD, Kvaratskhelia M. 2013. BET proteins promote efficient murine leukemia virus integration at transcription start sites. Proc Natl Acad Sci U S A 110:12036–12041. [PubMed][CrossRef]
198. Risler JK, Kenny AE, Palumbo RJ, Gamache ER, Curcio MJ. 2012. Host co-factors of the retrovirus-like transposon Ty1. Mob DNA 3:12. [PubMed][CrossRef]
199. Scholes DT, Banerjee M, Bowen B, Curcio MJ. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449–1465. [PubMed]
200. Nyswaner KM, Checkley MA, Yi M, Stephens RM, Garfinkel DJ. 2008. Chromatin-associated genes protect the yeast genome from Ty1 insertional mutagenesis. Genetics 178:197–214. [PubMed][CrossRef]
201. Curcio MJ, Kenny AE, Moore S, Garfinkel DJ, Weintraub M, Gamache ER, Scholes DT. 2007. S-phase checkpoint pathways stimulate the mobility of the retrovirus-like transposon Ty1. Mol Cell Biol 27:8874–8885. [PubMed][CrossRef]
202. Saksena S, Sun J, Chu T, Emr SD. 2007. ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 32:561–573. [PubMed][CrossRef]
203. Webster BM, Colombi P, Jager J, Lusk CP. 2014. Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159:388–401. [PubMed][CrossRef]
204. Bushman FD, Malani N, Fernandes J, D'Orso I, Cagney G, Diamond TL, Zhou H, Hazuda DJ, Espeseth AS, Konig R, Bandyopadhyay S, Ideker T, Goff SP, Krogan NJ, Frankel AD, Young JA, Chanda SK. 2009. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog 5:e1000437. [PubMed][CrossRef]
205. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, Lieberman J, Elledge SJ. 2008. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319:921–926. [PubMed][CrossRef]
206. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, Irelan JT, Chiang CY, Tu BP, De Jesus PD, Lilley CE, Seidel S, Opaluch AM, Caldwell JS, Weitzman MD, Kuhen KL, Bandyopadhyay S, Ideker T, Orth AP, Miraglia LJ, Bushman FD, Young JA, Chanda SK. 2008. Global analysis of host–pathogen interactions that regulate early-stage HIV-1 replication. Cell 135:49–60. [PubMed][CrossRef]
207. Yeung ML, Houzet L, Yedavalli VS, Jeang KT. 2009. A genome-wide short hairpin RNA screening of jurkat T-cells for human proteins contributing to productive HIV-1 replication. J Biol Chem 284:19463–19473. [PubMed][CrossRef]
208. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, Castle JC, Stec E, Ferrer M, Strulovici B, Hazuda DJ, Espeseth AS. 2008. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 4:495–504. [PubMed][CrossRef]
209. Wolf D, Goff SP. 2008. Host restriction factors blocking retroviral replication. Annu Rev Genet 42:143–163. [PubMed][CrossRef]
210. Goff SP. 2007. Host factors exploited by retroviruses. Nat Rev Microbiol 5:253–263. [PubMed][CrossRef]
211. Freed EO, Mouland AJ. 2006. The cell biology of HIV-1 and other retroviruses. Retrovirology 3:77. [PubMed][CrossRef]
212. Ebina H, Aoki J, Hatta S, Yoshida T, Koyanagi Y. 2004. Role of Nup98 in nuclear entry of human immunodeficiency virus type 1 cDNA. Microbes Infect / Inst Pasteur 6:715–724. [PubMed][CrossRef]
213. Di Nunzio F, Fricke T, Miccio A, Valle-Casuso JC, Perez P, Souque P, Rizzi E, Severgnini M, Mavilio F, Charneau P, Diaz-Griffero F. 2013. Nup153 and Nup98 bind the HIV-1 core and contribute to the early steps of HIV-1 replication. Virology 440:8–18. [PubMed][CrossRef]
214. Koh Y, Wu X, Ferris AL, Matreyek KA, Smith SJ, Lee K, KewalRamani VN, Hughes SH, Engelman A. 2013. Differential effects of human immunodeficiency virus type 1 capsid and cellular factors nucleoporin 153 and LEDGF/p75 on the efficiency and specificity of viral DNA integration. J Virol 87:648–658. [PubMed][CrossRef]
215. Goodier JL, Mandal PK, Zhang L, Kazazian HH, Jr. 2010. Discrete subcellular partitioning of human retrotransposon RNAs despite a common mechanism of genome insertion. Hum Mol Genet 19:1712–1725. [PubMed][CrossRef]
216. Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, Kopera HC, Athanikar JN, Hasnaoui M, Bucheton A, Moran JV, Gilbert N. 2010. Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet 6(10):pii: e1001150. [PubMed][CrossRef]
217. Bann DV, Beyer AR, Parent LJ. 2014. A murine retrovirus co-Opts YB-1, a translational regulator and stress granule-associated protein, to facilitate virus assembly. J Virol 88:4434–4450. [PubMed][CrossRef]
218. Abrahamyan LG, Chatel-Chaix L, Ajamian L, Milev MP, Monette A, Clement JF, Song R, Lehmann M, DesGroseillers L, Laughrea M, Boccaccio G, Mouland AJ. 2010. Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J Cell Sci 123:369–383. [PubMed][CrossRef]
219. Goodier JL, Cheung LE, Kazazian HH, Jr. 2012. MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet 8:e1002941. [PubMed][CrossRef]
220. Furtak V, Mulky A, Rawlings SA, Kozhaya L, Lee K, Kewalramani VN, Unutmaz D. 2010. Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PLoS One 5:e9081. [PubMed][CrossRef]
221. Arjan-Odedra S, Swanson CM, Sherer NM, Wolinsky SM, Malim MH. 2012. Endogenous MOV10 inhibits the retrotransposition of endogenous retroelements but not the replication of exogenous retroviruses. Retrovirology 9:53. [PubMed][CrossRef]
222. Malim MH, Bieniasz PD. 2012. HIV Restriction Factors and Mechanisms of Evasion. Cold Spring Harbor Persp Med 2:a006940. [PubMed][CrossRef]
223. Lu C, Contreras X, Peterlin BM. 2011. P bodies inhibit retrotransposition of endogenous intracisternal a particles. J Virol 85:6244–6251. [PubMed][CrossRef]
224. Phalora PK, Sherer NM, Wolinsky SM, Swanson CM, Malim MH. 2012. HIV-1 replication and APOBEC3 antiviral activity are not regulated by P bodies. J Virol 86:11712–11724. [PubMed][CrossRef]
225. Reed JC, Molter B, Geary CD, McNevin J, McElrath J, Giri S, Klein KC, Lingappa JR. 2012. HIV-1 Gag co-opts a cellular complex containing DDX6, a helicase that facilitates capsid assembly. J Cell Biol 198:439–456. [PubMed][CrossRef]
226. Saito K, Siomi MC. 2010. Small RNA-mediated quiescence of transposable elements in animals. Dev Cell 19:687–697. [PubMed][CrossRef]
227. Aravin AA, Hannon GJ, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761–764. [PubMed][CrossRef]
228. Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I. 2011. RNA granules in germ cells. Cold Spring Harbor Perspectives in Biology 3:a002774. [PubMed][CrossRef]
microbiolspec.MDNA3-0057-2014.citations
cm/3/2
content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0057-2014
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0057-2014
2015-03-19
2017-02-25

Abstract:

Long terminal repeat (LTR) retrotransposons constitute significant fractions of many eukaryotic genomes. Two ancient families are Ty1/Copia () and Ty3/Gypsy (). The Ty3/Gypsy family probably gave rise to retroviruses based on the domain order, similarity of sequences, and the envelopes encoded by some members. The Ty3 element of is one of the most completely characterized elements at the molecular level. Ty3 is induced in mating cells by pheromone stimulation of the mitogen-activated protein kinase pathway as cells accumulate in G1. The two Ty3 open reading frames are translated into Gag3 and Gag3–Pol3 polyprotein precursors. In haploid mating cells Gag3 and Gag3–Pol3 are assembled together with Ty3 genomic RNA into immature virus-like particles in cellular foci containing RNA processing body proteins. Virus-like particle Gag3 is then processed by Ty3 protease into capsid, spacer, and nucleocapsid, and Gag3–Pol3 into those proteins and additionally, protease, reverse transcriptase, and integrase. After haploid cells mate and become diploid, genomic RNA is reverse transcribed into cDNA. Ty3 integration complexes interact with components of the RNA polymerase III transcription complex resulting in Ty3 integration precisely at the transcription start site. Ty3 activation during mating enables proliferation of Ty3 between genomes and has intriguing parallels with metazoan retrotransposon activation in germ cell lineages. Identification of nuclear pore, DNA replication, transcription, and repair host factors that affect retrotransposition has provided insights into how hosts and retrotransposons interact to balance genome stability and plasticity.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/2/MDNA3-0057-2014.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0057-2014&mimeType=html&fmt=ahah

Figures

Image of FIGURE 1

Click to view

FIGURE 1

Ty3 retrotransposition. (A) Ty3 replication cycle. Pheromone binding to or pheromone receptors activates G protein-coupled mating signal transduction via mitogen-activated protein (MAP) kinase kinase kinase Ste7, MAP kinase kinase Ste11 and MAP kinase Fus3 (rose). Scaffold protein Ste5 (blue) supports specificity of their interaction preventing crosstalk with the filamentous growth pathway. Fus3 phosphorylates Dig1 and Dig2 negative regulators (gold) of Ste12 (dark blue), which then dissociate allowing Ste12 activation of RNA Pol II transcription of Ty3. Ty3 poly(A) RNA (maroon) is exported and translated into Gag3 and Gag3–Pol3 (tan), which then associate, together with the gRNA and RNA processing body (PB) factors, forming retrosomes within which Ty3 VLPs assemble. These foci become perinuclear over time. Assembly activates protease (PR) processing and maturation of the virus-like particles (VLPs). After cells mate (not shown) reverse transcription of the gRNA into cDNA occurs. Uncoating (dissociation of Gag3) presumably accompanies nuclear entry of the PIC. (A, B) Ty3 cDNA associates with RNAP III transcription initiation complexes composed of TFIIIB (yellow) and TFIIIC (green). TATA binding protein and Brf1 constitute the minimum target, but evidence suggests that TFIIIC can also be present. doi:10.1128/microbiolspec.MDNA3-0057-2014.f1

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2a

Click to view

FIGURE 2a

Ty3 DNA, RNA, and protein. (A) DNA and RNA. The 5.4-kbp Ty3 element is transcribed into a 5.2-kb RNA. The major 5′ end of Ty3 RNA maps to 118 nucleotides (nt) inside the upstream long terminal repeat (LTR), and the 3′ end to heterogeneous positions between 243 and 273 nt inside the downstream LTR, as well as beyond the downstream LTR ( 14 ). The overlap resulting from termination downstream of the position of initiation results in a sequence that is repeated (“R”) and defines 5′ U5 and 3′ U3 sequences. The initiator AUG of the open reading frame (ORF) occurs at nucleotides 76 to 78 inside the Ty3 internal domain for a total 5′ untranslated region (UTR) of 193 nt; extends into the downstream LTR to define a 3′ UTR of ∼227 nt ( 12 , 14 ). Candidate upstream TATA and downstream polyadenylation sites are identified, but not experimentally verified. The RNA contains a bipartite primer binding site (PBS), which anneals to initiator tRNA in the upstream untranslated region and the downstream LTR (gold boxes). The and ORFs encode Gag3 and Gag3–Pol3. (B) Protein. Gag3 is 290 amino acids (aa) and contains domains that mature via Ty3 PR processing into 207-aa capsid (CA), 27-aa spacer (SP), and 57-aa nucleocapsid (NC). Gag3–Pol3 contains those and additionally, protease (PR); reverse transcriptase (RT) starting at amino acids 536; and two forms of integrase (IN) domains (starting at amino acids 1012 and 1038) produced via a programmed frameshift. The ORF terminates within the downstream LTR so that the polypurine tract (PPT) plus strand primer is actually within the IN-coding region. (C) Reverse transcription of Ty3 genomic RNA. The tRNA primes synthesis of a minus-strand strong stop containing U5 and R segments, which then transfers to the 3′ end and primes extension of the minus strand. The plus-strand strong stop intermediate is initiated with cleavage by RNaseH at the downstream end of the PPT just outside the downstream LTR and is extended through U3, R, and U5 and likely copied into the 3′ end of the tRNA then transferred to the 5′ end of the RNA and extended to form the plus strand of the cDNA. Although as described in the text minus- and plus-strand strong-stop intermediates have been identified, the overall flow described is based on the retrovirus model. An additional possibility (not shown) is that the 5′ and 3′ ends are transiently joined in a lariat RNA (see text). Bottom, the full-length cDNA has two extra base pairs on each end derived from a 2-nt offset between the priming sites and the LTR ends of the integrated element. Integrase (IN) processes 2 nt from each 3′ end and mediates the nucleophilic attacks of the resulting hydroxyls at 5-bp staggered positions flanking the RNA polymerase III (RNAPIII) transcription initiation sites. The integration site is repaired, resulting in 5-bp direct repeats flanking the ends of the Ty3 element. doi:10.1128/microbiolspec.MDNA3-0057-2014.f2a

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2b

Click to view

FIGURE 2b

Ty3 DNA, RNA, and protein. (A) DNA and RNA. The 5.4-kbp Ty3 element is transcribed into a 5.2-kb RNA. The major 5′ end of Ty3 RNA maps to 118 nucleotides (nt) inside the upstream long terminal repeat (LTR), and the 3′ end to heterogeneous positions between 243 and 273 nt inside the downstream LTR, as well as beyond the downstream LTR ( 14 ). The overlap resulting from termination downstream of the position of initiation results in a sequence that is repeated (“R”) and defines 5′ U5 and 3′ U3 sequences. The initiator AUG of the open reading frame (ORF) occurs at nucleotides 76 to 78 inside the Ty3 internal domain for a total 5′ untranslated region (UTR) of 193 nt; extends into the downstream LTR to define a 3′ UTR of ∼227 nt ( 12 , 14 ). Candidate upstream TATA and downstream polyadenylation sites are identified, but not experimentally verified. The RNA contains a bipartite primer binding site (PBS), which anneals to initiator tRNA in the upstream untranslated region and the downstream LTR (gold boxes). The and ORFs encode Gag3 and Gag3–Pol3. (B) Protein. Gag3 is 290 amino acids (aa) and contains domains that mature via Ty3 PR processing into 207-aa capsid (CA), 27-aa spacer (SP), and 57-aa nucleocapsid (NC). Gag3–Pol3 contains those and additionally, protease (PR); reverse transcriptase (RT) starting at amino acids 536; and two forms of integrase (IN) domains (starting at amino acids 1012 and 1038) produced via a programmed frameshift. The ORF terminates within the downstream LTR so that the polypurine tract (PPT) plus strand primer is actually within the IN-coding region. (C) Reverse transcription of Ty3 genomic RNA. The tRNA primes synthesis of a minus-strand strong stop containing U5 and R segments, which then transfers to the 3′ end and primes extension of the minus strand. The plus-strand strong stop intermediate is initiated with cleavage by RNaseH at the downstream end of the PPT just outside the downstream LTR and is extended through U3, R, and U5 and likely copied into the 3′ end of the tRNA then transferred to the 5′ end of the RNA and extended to form the plus strand of the cDNA. Although as described in the text minus- and plus-strand strong-stop intermediates have been identified, the overall flow described is based on the retrovirus model. An additional possibility (not shown) is that the 5′ and 3′ ends are transiently joined in a lariat RNA (see text). Bottom, the full-length cDNA has two extra base pairs on each end derived from a 2-nt offset between the priming sites and the LTR ends of the integrated element. Integrase (IN) processes 2 nt from each 3′ end and mediates the nucleophilic attacks of the resulting hydroxyls at 5-bp staggered positions flanking the RNA polymerase III (RNAPIII) transcription initiation sites. The integration site is repaired, resulting in 5-bp direct repeats flanking the ends of the Ty3 element. doi:10.1128/microbiolspec.MDNA3-0057-2014.f2b

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view

FIGURE 3

Retrotransposition assays. Ty3 retrotransposition can be assayed using the reporter embedded in the mobilized Ty3 (genetic) or by PCR. In the case of the Genetic Assay (left panel), Ty3 transcription is accompanied by splicing of a synthetic intron which is antisense to the marker, preventing from being productively expressed. After Ty3 transcription, splicing and reverse transcription, the intronless gene is expressed and cells in which transposition has occurred are selected on medium lacking histidine. Alternatively, retrotransposition of a tagged Ty3 element can be monitored by PCR assay (right panel) using one primer complementary to the Ty3 tag and one complementary to a sequence present in a tDNA family or in the unique sequence downstream of any tDNA target. doi:10.1128/microbiolspec.MDNA3-0057-2014.f3

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view

FIGURE 4

Hierarchical clustering of Ty3 cofactors and restriction factors by gene ontology groups. Gene ontology (GO) analysis was performed using the GO SLIM Biological Process mapping tool available through Genome Database (http://www.yeastgenome.org). Knockout mutants identified as having either increased “Up” or decreased “Down” Ty3 retrotransposition phenotypes were analyzed for GO: Biological Process terms. Enriched categories were determined using chi-squared test. GO categories were considered enriched if two criteria were met: (i) the -value was <0.05 and (ii) the number of genes in the enriched category exceeded 10% of the total number of genes in the Up or Down list. Enriched categories were converted to a heat map with hierarchical clustering using R; values represent the [–Log(-value)] scaled from 0 (no significance) to 1, blue coloring reflects the intensity of significance. doi:10.1128/microbiolspec.MDNA3-0057-2014.f4

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table

Click to view

TABLE 1

Host factors in common between Ty3 and HIV-1

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0057-2014

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error