Chapter 43 : The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap43-1.gif /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap43-2.gif


The fission yeast , discovered in the late 1800s in East Africa and genetically characterized in the 1950s by Urs Leupold ( ), has became a central model for studies of cell cycle, gene expression, and the complex relationship between transposable elements (TEs) and their host. , also known as fission yeast, can be studied with a sophisticated toolbox of molecular and genetic techniques. The haploid genome is 12.57 Mbp and encodes 5,052 genes distributed among three chromosomes ( ). The complete genome sequence of the Leupold isolate revealed that TEs constitute 1.1% of the genome ( ) ( Table 1 ). All TE-related sequences in derive from long terminal repeat (LTR) retrotransposons. The intact elements present in the Leupold strain are 13 full-length copies of the Tf2 element ( ). Recombination that occurs between the LTRs of a full-length element results in solo LTRs that serve as a fossil record of TEs that are no longer present. The Leupold strain contains 249 solo LTRs or LTR fragments that are derived from nine clades of LTR retrotransposons. The youngest clades are the 35 LTR sequences from Tf2 and the 28 LTRs from Tf1, an element related to Tf2 but that is no longer present in the Leupold strain ( ). Full-length Tf1 elements are present in wild isolates of collected from different geographic regions ( ). The transposition activity of Tf1 and the function of its proteins is measured by expressing a plasmid-encoded copy of Tf1 that contains ( ). Levels of Tf1 transposition correspond to amounts of G418 resistance. are another form of repeat identified in the Leupold strain ( ). They are present in 25 copies and are generally 250 bp downstream of an LTR ( ). Their function is unknown, but they appear to encode protein and their transcription is strongly induced during meiosis ( ).

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Tf1 transposition in . Full-length Tf1 (blue rectangles) is transcribed and translated. The polyprotein assembles into particle precursors and PR processes the protein into Gag (pink), protease (PR), reverse transcriptase (RT) (orange), and integrase (IN) (orange). The mature virus-like particles (VLP) contain the processed proteins and two copies of mRNA (blue wavy lines). The RT reverse-transcribes the mRNA into double-stranded cDNA that associates with IN. Once transported into the nucleus (above dotted line), the IN integrates the cDNA at a new position in the genome. The long terminal repeats are symbolized by triangles. The protein coding sequences are represented by rectangles.

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Reverse transcription of Tf1 is initiated by a self-priming mechanism. (A) The 5′ end of the Tf1 mRNA anneals to the primer binding site (PBS). The first 11 nucleotides (red) are cleaved from the Tf1 mRNA (black) and prime reverse transcription towards the 5′ end of the mRNA. The scissors indicate the position of cleavage. The arrow indicates the direction of reverse transcription. (B) The 5′ end of the Tf1 mRNA folds into a complex duplex structure. The scissors indicate the position of the cleavage that liberates the self-primer (red). The position of the U5-IR stem-loop is indicated.

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Distribution of the distance from Tf1 integration to the nearest open reading frame (ORF). A collection of 800,723 independent integration events was positioned according to the distance to the nearest ORF (red) ( ). The -axis represents the distance from the 5′ end and 3′ end of ORFs in bins that are 100 bp wide; distances within ORFs are divided into 15 bins of equal proportion. The -axis represents the percentage of independent integration events positioned within the bins. The majority of integration events are located near the 5′ end of ORFs, 3.8% of all integration events targeted coding sequences. Figure reproduced with permission from ref. ( ).

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Impact of Tf elements on gene expression. Tf element integration can activate the expression of adjacent genes. (A) Tf2 long terminal repeat (LTR) (blue) possesses a motif ATCGTACCAT bound by the transcription factor Sre1 (green), which activates the transcription of oxygen-dependent genes such as . Pol II (pink); RNA polymerase II. (B) Sequences within the Tf1 LTR substitute for the elements in the promoter that are disrupted by Tf1 integration. Tf1 integration results in a 2.1- to 3.6-fold increase in expression. TF (grey): transcription factor. (C) Tf1 integration near the heat shock gene acts as an enhancer of transcription, through a mechanism that may involve the transcription activation factor Atf1 (red). A motif TGACGT similar to the sequence bound by Atf1 is within the Tf1 LTR (blue).

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Wood V,, Harris MA,, McDowall MD,, Rutherford K,, Vaughan BW,, Staines DM,, Aslett M,, Lock A,, Bahler J,, Kersey PJ,, Oliver SG . 2011. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40 : D695 D699.[PubMed] [CrossRef]
2. Bowen NJ,, Jordan I,, Epstein J,, Wood V,, Levin HL . 2003. Retrotransposons and their recognition of pol ii promoters: a comprehensive survey of the transposable elements derived from the complete genome sequence of Schizosaccharomyces pombe . Genome Res 13 : 1984 1997.[PubMed] [CrossRef]
3. Levin HL,, Weaver DC,, Boeke JD . 1990. Two related families of retrotransposons from Schizosaccharomyces pombe [published erratum appears in Mol Cell Biol 1991; 11(4) :2334]. Mol Cell Biol 10 : 6791 6798.[PubMed]
4. Levin HL . 1995. A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol Cell Biol 15 : 3310 3317.[PubMed]
5. Levin HL,, Boeke JD . 1992. Demonstration of retrotransposition of the Tf1 element in fission yeast. EMBO J 11 : 1145 1153.[PubMed]
6. Lespinet O,, Wolf YI,, Koonin EV,, Aravind L . 2002. The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12 : 1048 1059.[PubMed] [CrossRef]
7. Mata J,, Lyne R,, Burns G,, Bahler J . 2002. The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32 : 143 147.[PubMed] [CrossRef]
8. Watanabe T,, Miyashita K,, Saito TT,, Yoneki T,, Kakihara Y,, Nabeshima K,, Kishi YA,, Shimoda C,, Nojima H . 2001. Comprehensive isolation of meiosis-specific genes identifies novel proteins and unusual non-coding transcripts in Schizosaccharomyces pombe . Nucleic Acids Res 29 : 2327 2337.[PubMed] [CrossRef]
9. Weaver DC,, Shpakovski GV,, Caputo E,, Levin HL,, Boeke JD . 1993. Sequence analysis of closely related retrotransposon families from fission yeast. Gene 131 : 135 139.[PubMed] [CrossRef]
10. Song SU,, Kurkulos M,, Boeke JD,, Corces VG . 1997. Infection of the germ line by retroviral particles produced in the follicle cells: a possible mechanism for the mobilization of the gypsy retroelement of Drosophila . Development 124 : 2789 2798.[PubMed]
11. Song SU,, Gerasimova T,, Kurkulos M,, Boeke JD,, Corces VG . 1994. An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8 : 2046 2057.[PubMed] [CrossRef]
12. Teysset L,, Burns JC,, Shike H,, Sullivan BL,, Bucheton A,, Terzian C . 1998. A moloney murine leukemia virus-based retroviral vector pseudotyped by the insect retroviral gypsy envelope can infect Drosophila cells. J Virol 72 : 853 856.[PubMed]
13. 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]
14. Malik HS,, Henikoff S,, Eickbush TH . 2000. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10 : 1307 1318.[PubMed] [CrossRef]
15. Levin HL,, Weaver DC,, Boeke JD . 1993. Novel gene expression mechanism in a fission yeast retroelement: Tf1 proteins are derived from a single primary translation product [published erratum appears in EMBO J 1994;13:1494]. EMBO J 12 : 4885 4895.[PubMed]
16. Atwood A,, Lin JH,, Levin HL . 1996. The retrotransposon Tf1 assembles virus-like particles that contain excess Gag relative to integrase because of a regulated degradation process. Mol Cell Biol 16 : 338 346.[PubMed]
17. Haag AL,, Lin JH,, Levin HL . 2000. Evidence for the packaging of multiple copies of Tfl mRNA into particles and the trans priming of reverse transcription. J Virol 74 : 7164 7170.[PubMed] [CrossRef]
18. Teysset L,, Dang VD,, Kim MK,, Levin HL . 2003. A long terminal repeat-containing retrotransposon of Schizosaccharomyces pombe expresses a Gag-like protein that assembles into virus-like particles which mediate reverse transcription. J Virol 77 : 5451 5463.[PubMed] [CrossRef]
19. 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.[CrossRef]
20. Kim MK,, Claiborn KC,, Levin HL . 2005. The long terminal repeat-containing retrotransposon Tf1 possesses amino acids in Gag that regulate nuclear localization and particle formation. J Virol 79 : 9540 9555.[PubMed] [CrossRef]
21. Balasundaram D,, Benedik MJ,, Morphew M,, Dang VD,, Levin HL . 1999. Nup124p is a nuclear pore factor of Schizosaccharomyces pombe that is important for nuclear import and activity of retrotransposon Tf1. Mol Cell Biol 19 : 5768 5784.[PubMed]
22. Sistla S,, Pang JV,, Wang CX,, Balasundaram D . 2007. Multiple conserved domains of the nucleoporin Nup124p and its orthologs Nup1p and Nup153 are critical for nuclear import and activity of the fission yeast Tf1 retrotransposon. Mol Biol Cell 18 : 3692 3708.[PubMed] [CrossRef]
23. Varadarajan P,, Mahalingam S,, Liu P,, Ng SB,, Gandotra S,, Dorairajoo DS,, Balasundaram D . 2005. The functionally conserved nucleoporins Nup124p from fission yeast and the human Nup153 mediate nuclear import and activity of the Tf1 retrotransposon and HIV-1 Vpr. Mol Biol Cell 16 : 1823 1838.[PubMed] [CrossRef]
24. Matreyek KA,, Yucel SS,, Li X,, Engelman A . 2013. Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog 9 : e1003693. [PubMed] [CrossRef]
25. Matreyek KA,, Engelman A . 2013. Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes. Viruses 5 : 2483 2511.[PubMed] [CrossRef]
26. 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]
27. 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]
28. Dang VD,, Benedik MJ,, Ekwall K,, Choi J,, Allshire RC,, Levin HL . 1999. A new member of the sin3 family of corepressors is essential for cell viability and required for retroelement propagation in fission yeast. Mol Cell Biol 19 : 2351 2365.[PubMed]
29. Levin HL . 1997. It’s prime time for reverse transcriptase. Cell 88 : 5 8.[CrossRef]
30. Levin HL . 1996. An unusual mechanism of self-primed reverse transcription requires the RNase H domain of reverse transcriptase to cleave an RNA duplex. Mol Cell Biol 16 : 5645 5654.[PubMed]
31. Atwood-Moore A,, Ejebe K,, Levin HL . 2005. Specific recognition and cleavage of the plus-strand primer by reverse transcriptase. J Virol 79 : 14863 14875.[PubMed] [CrossRef]
32. Hizi A . 2008. The reverse transcriptase of the Tf1 retrotransposon has a specific novel activity for generating the RNA self-primer that is functional in cDNA synthesis. J Virol 82 : 10906 10910.[PubMed] [CrossRef]
33. Lin JH,, Levin HL . 1997. A complex structure in the mRNA of Tf1 is recognized and cleaved to generate the primer of reverse transcription. Genes Dev 11 : 270 285.[CrossRef]
34. Lin JH,, Levin HL . 1998. Reverse transcription of a self-primed retrotransposon requires an RNA structure similar to the U5-IR stem-loop of retroviruses. Mol Cell Biol 18 : 6859 6869.[PubMed]
35. Lin JH,, Levin HL . 1997. Self-primed reverse transcription is a mechanism shared by several LTR-containing retrotransposons [letter]. RNA 3 : 952 953.[PubMed]
36. Butler M,, Goodwin T,, Simpson M,, Singh M,, Poulter R . 2001. Vertebrate LTR retrotransposons of the Tf1/Sushi group. J Mol Evol 52 : 260 274.[PubMed]
37. SanMiguel P,, Tikhonov A,, Jin YK,, Motchoulskaia N,, Zakharov D,, Melake-Berhan A,, Springer PS,, Edwards KJ,, Lee M,, Avramova Z,, Bennetzen JL . 1996. Nested retrotransposons in the intergenic regions of the maize genome [see comments]. Science 274 : 765 768.[PubMed] [CrossRef]
38. Atwood-Moore A,, Yan K,, Judson RL,, Levin HL . 2006. The self primer of the long terminal repeat retrotransposon Tf1 is not removed during reverse transcription. J Virol 80 : 8267 8270.[PubMed] [CrossRef]
39. Hizi A,, Levin HL . 2005. The integrase of the long terminal repeat-retrotransposon tf1 has a chromodomain that modulates integrase activities. J Biol Chem 280 : 39086. [PubMed] [CrossRef]
40. Herzig E,, Voronin N,, Hizi A . 2012. The removal of RNA primers from DNA synthesized by the reverse transcriptase of the retrotransposon Tf1 is stimulated by Tf1 integrase. J Virol 86 : 6222 6230.[PubMed] [CrossRef]
41. Oz-Gleenberg I,, Herzig E,, Voronin N,, Hizi A . 2012. Substrate variations that affect the nucleic acid clamp activity of reverse transcriptases. FEBS J 279 : 1894 1903.[PubMed] [CrossRef]
42. Oz-Gleenberg I,, Herschhorn A,, Hizi A . 2011. Reverse transcriptases can clamp together nucleic acids strands with two complementary bases at their 3′-termini for initiating DNA synthesis. Nucleic Acids Res 39 : 1042 1053.[PubMed] [CrossRef]
43. Oz-Gleenberg I,, Herzig E,, Hizi A . 2012. Template-independent DNA synthesis activity associated with the reverse transcriptase of the long terminal repeat retrotransposon Tf1. FEBS J 279 : 142 153.[PubMed] [CrossRef]
44. Kirshenboim N,, Hayouka Z,, Friedler A,, Hizi A . 2007. Expression and characterization of a novel reverse transcriptase of the LTR retrotransposon Tf1. Virology 366 : 263 276.[PubMed] [CrossRef]
45. 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]
46. Leem YE,, Ripmaster TL,, Kelly FD,, Ebina H,, Heincelman ME,, Zhang K,, Grewal SIS,, Hoffman CS,, Levin HL . 2008. Retrotransposon Tf1 is targeted to pol II promoters by transcription activators. Mol Cell 30 : 98 107.[PubMed] [CrossRef]
47. 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]
48. Chatterjee AG,, Leem YE,, Kelly FD,, Levin HL . 2009. The chromodomain of Tf1 integrase promotes binding to cDNA and mediates target site selection. J Virol 83 : 2675 2685.[PubMed] [CrossRef]
49. Qi X,, Sandmeyer S . 2012. In vitro targeting of strand transfer by the Ty3 retroelement integrase. J Biol Chem 287 : 18589 18595.[PubMed] [CrossRef]
50. Dai J,, Xie W,, Brady TL,, Gao J,, Voytas DF . 2007. Phosphorylation regulates integration of the yeast Ty5 retrotransposon into heterochromatin. Molecular Cell 27 : 289 299.[PubMed] [CrossRef]
51. Behrens R,, Hayles J,, Nurse P . 2000. Fission yeast retrotransposon Tf1 integration is targeted to 5′ ends of open reading frames. Nucleic Acids Res 28 : 4709 4716.[PubMed] [CrossRef]
52. Singleton TL,, Levin HL . 2002. A long terminal repeat retrotransposon of fission yeast has strong preferences for specific sites of insertion. Eukaryotic Cell 1 : 44 55.[CrossRef]
53. Cherry KE,, Hearn WE,, Seshie OY,, Singleton TL . 2014. Identification of Tf1 integration events in S. pombe under nonselective conditions. Gene 542 : 221 231.[PubMed] [CrossRef]
54. Hoff EF,, Levin HL,, Boeke JD . 1998. Schizosaccharomyces pombe retrotransposon Tf2 mobilizes primarily through homologous cDNA recombination. Mol Cell Biol 18 : 6839 6852.[PubMed]
55. Hoff EKF . 1997. Dissertation, Johns Hopkins University, Baltimore, MD.
56. Majumdar A,, Chatterjee AG,, Ripmaster TL,, Levin HL . 2011. The determinants that specify the integration pattern of retrotransposon Tf1 in the fbp1 promoter of Schizosaccharomyces pombe . J Virol 85 : 519 529.[PubMed] [CrossRef]
57. Chatterjee AG,, Esnault C,, Guo Y,, Hung S,, McQueen PG,, Levin HL . 2014. Serial number tagging reveals a prominent sequence preference of retrotransposon integration. Nucleic Acids Res 42 : 8449 8460.[PubMed] [CrossRef]
58. Guo Y,, Levin HL . 2010. High-throughput sequencing of retrotransposon integration provides a saturated profile of target activity in Schizosaccharomyces pombe . Genome Res 20 : 239 248.[PubMed] [CrossRef]
59. Arcangioli B,, Copeland TD,, Klar AJ . 1994. Sap1, a protein that binds to sequences required for mating-type switching, is essential for viability in Schizosaccharomyces pombe . Mol Cell Biol 14 : 2058 2065.[PubMed]
60. Arcangioli B,, Klar AJ . 1991. A novel switch-activating site (SAS1) and its cognate binding factor (SAP1) required for efficient mat1 switching in Schizosaccharomyces pombe . EMBO J 10 : 3025 3032.[PubMed]
61. de Lahondes R,, Ribes V,, Arcangioli B . 2003. Fission yeast Sap1 protein is essential for chromosome stability. Eukaryot Cell 2 : 910 921.[PubMed] [CrossRef]
62. Mejia-Ramirez E,, Sanchez-Gorostiaga A,, Krimer DB,, Schvartzman JB,, Hernandez P . 2005. The mating type switch-activating protein Sap1 Is required for replication fork arrest at the rRNA genes of fission yeast. Mol Cell Biol 25 : 8755 8761.[PubMed] [CrossRef]
63. Krings G,, Bastia D . 2005. Sap1p binds to Ter1 at the ribosomal DNA of Schizosaccharomyces pombe and causes polar replication fork arrest. J Biol Chem 280 : 39135 39142.[PubMed] [CrossRef]
64. Noguchi C,, Noguchi E . 2007. Sap1 promotes the association of the replication fork protection complex with chromatin and is involved in the replication checkpoint in Schizosaccharomyces pombe . Genetics 175 : 553 566.[PubMed] [CrossRef]
65. Zaratiegui M,, Vaughn MW,, Irvine DV,, Goto D,, Watt S,, Bahler J,, Arcangioli B,, Martienssen RA . 2011. CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469 : 112 115.[PubMed] [CrossRef]
66. Fedoroff NV . 2012. Presidential address. Transposable elements, epigenetics, and genome evolution. Science 338 : 758 767.[PubMed] [CrossRef]
67. Levin HL,, Moran JV . 2011. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12 : 615 627.[PubMed] [CrossRef]
68. Wilson RC,, Doudna JA . 2013. Molecular mechanisms of RNA interference. Annu Rev Biophys 42 : 217 239.[PubMed] [CrossRef]
69. Guzzardo PM,, Muerdter F,, Hannon GJ . 2013. The piRNA pathway in flies: highlights and future directions. Curr Opin Genet Dev 23 : 44 52.[PubMed] [CrossRef]
70. Lejeune E,, Allshire RC . 2011. Common ground: small RNA programming and chromatin modifications. Curr Opin Cell Biol 23 : 258 265.[PubMed] [CrossRef]
71. Reyes-Turcu FE,, Grewal SI . 2012. Different means, same end-heterochromatin formation by RNAi and RNAi-independent RNA processing factors in fission yeast. Curr Opin Genet Dev 22 : 156 163.[PubMed] [CrossRef]
72. Slotkin RK,, Martienssen R . 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8 : 272 285.[PubMed] [CrossRef]
73. Hansen KR,, Burns G,, Mata J,, Volpe TA,, Martienssen RA,, Bahler J,, Thon G . 2005. Global effects on gene expression in fission yeast by silencing and RNA interference machineries. Mol Cell Biol 25 : 590 601.[PubMed] [CrossRef]
74. Cam HP,, Sugiyama T,, Chen ES,, Chen X,, FitzGerald PC,, Grewal SI . 2005. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37 : 809 819.[PubMed] [CrossRef]
75. Halic M,, Moazed D . 2010. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140 : 504 516.[PubMed] [CrossRef]
76. Zaratiegui M,, Castel SE,, Irvine DV,, Kloc A,, Ren J,, Li F,, de Castro E,, Marin L,, Chang AY,, Goto D,, Cande WZ,, Antequera F,, Arcangioli B,, Martienssen RA . 2011. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479 : 135 138.[PubMed] [CrossRef]
77. Rhind N,, Chen Z,, Yassour M,, Thompson DA,, Haas BJ,, Habib N,, Wapinski I,, Roy S,, Lin MF,, Heiman DI,, Young SK,, Furuya K,, Guo Y,, Pidoux A,, Chen HM,, Robbertse B,, Goldberg JM,, Aoki K,, Bayne EH,, Berlin AM,, Desjardins CA,, Dobbs E,, Dukaj L,, Fan L,, FitzGerald MG,, French C,, Gujja S,, Hansen K,, Keifenheim D,, Levin JZ,, Mosher RA,, Müller CA,, Pfiffner J,, Priest M,, Russ C,, Smialowska A,, Swoboda P,, Sykes SM,, Vaughn M,, Vengrova S,, Yoder R,, Zeng Q,, Allshire R,, Baulcombe D,, Birren BW,, Brown W,, Ekwall K,, Kellis M,, Leatherwood J,, Levin H,, Margalit H,, Martienssen R,, Nieduszynski CA,, Spatafora JW,, Friedman N,, Dalgaard JZ,, Baumann P,, Niki H,, Regev A,, Nusbaum C . 2011. Comparative functional genomics of the fission yeasts. Science 332 : 930 936.[PubMed] [CrossRef]
78. Yamanaka S,, Mehta S,, Reyes-Turcu FE,, Zhuang F,, Fuchs RT,, Rong Y,, Robb GB,, Grewal SI . 2013. RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493 : 557 560.[PubMed] [CrossRef]
79. Lee NN,, Chalamcharla VR,, Reyes-Turcu F,, Mehta S,, Zofall M,, Balachandran V,, Dhakshnamoorthy J,, Taneja N,, Yamanaka S,, Zhou M,, Grewal SI . 2013. Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155 : 1061 1074.[PubMed] [CrossRef]
80. Anderson HE,, Wardle J,, Korkut SV,, Murton HE,, Lopez-Maury L,, Bahler J,, Whitehall SK . 2009. The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts. Mol Cell Biol 29 : 5158 5167.[PubMed] [CrossRef]
81. Greenall A,, Williams ES,, Martin KA,, Palmer JM,, Gray J,, Liu C,, Whitehall SK . 2006. Hip3 interacts with the HIRA proteins Hip1 and Slm9 and is required for transcriptional silencing and accurate chromosome segregation. J Biol Chem 281 : 8732 8739.[PubMed] [CrossRef]
82. Casola C,, Hucks D,, Feschotte C . 2008. Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals. Mol Biol Evol 25 : 29 41.[PubMed] [CrossRef]
83. Smit AF . 1996. The origin of interspersed repeats in the human genome. Curr Opin Genet Dev 6 : 743 748.[PubMed] [CrossRef]
84. Tudor M,, Lobocka M,, Goodell M,, Pettitt J,, O’Hare K . 1992. The pogo transposable element family of Drosophila melanogaster . Mol Gen Genet 232 : 126 134.[PubMed] [CrossRef]
85. Masumoto H,, Nakano M,, Ohzeki J . 2004. The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres. Chromosome Res 12 : 543 556.[PubMed] [CrossRef]
86. Cam HP,, Noma K,, Ebina H,, Levin HL,, Grewal SIS . 2008. Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451 : U431 U432.[PubMed] [CrossRef]
87. Lorenz DR,, Mikheyeva IV,, Johansen P,, Meyer L,, Berg A,, Grewal SI,, Cam HP . 2012. CENP-B cooperates with Set1 in bidirectional transcriptional silencing and genome organization of retrotransposons. Mol Cell Biol 32 : 4215 4225.[PubMed] [CrossRef]
88. Tanaka A,, Tanizawa H,, Sriswasdi S,, Iwasaki O,, Chatterjee AG,, Speicher DW,, Levin HL,, Noguchi E,, Noma K . 2012. Epigenetic regulation of condensin-mediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation. Mol Cell 48 : 532 546.[PubMed] [CrossRef]
89. Baum M,, Clarke L . 2000. Fission yeast homologs of human CENP-B have redundant functions affecting cell growth and chromosome segregation. Mol Cell Biol 20 : 2852 2864.[CrossRef]
90. McClintock B . 1984. The significance of responses of the genome to challenge. Science 226 : 792 801.[PubMed] [CrossRef]
91. 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]
92. 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.[CrossRef]
93. Sehgal A,, Lee CY,, Espenshade PJ . 2007. SREBP controls oxygen-dependent mobilization of retrotransposons in fission yeast. PLoS Genet 3 : e131. [PubMed] [CrossRef]
94. Feng G,, Leem YE,, Levin HL . 2013. Transposon integration enhances expression of stress response genes. Nucleic Acids Res 41 : 775 789.[PubMed] [CrossRef]
95. Wood V,, Gwilliam R,, Rajandream MA,, Lyne M,, Lyne R,, Stewart A,, Sgouros J,, Peat N,, Hayles J,, Baker S,, Basham D,, Bowman S,, Brooks K,, Brown D,, Brown S,, Chillingworth T,, Churcher C,, Collins M,, Connor R,, Cronin A,, Davis P,, Feltwell T,, Fraser A,, Gentles S,, Goble A,, Hamlin N,, Harris D,, Hidalgo J,, Hodgson G,, Holroyd S,, Hornsby T,, Howarth S,, Huckle EJ,, Hunt S,, Jagels K,, James K,, Jones L,, Jones M,, Leather S,, McDonald S,, McLean J,, Mooney P,, Moule S,, Mungall K,, Murphy L,, Niblett D,, Odell C,, Oliver K,, O’Neil S,, Pearson D,, Quail MA,, Rabbinowitsch E,, Rutherford K,, Rutter S,, Saunders D,, Seeger K,, Sharp S,, Skelton J,, Simmonds M,, Squares R . 2002. The genome sequence of Schizosaccharomyces pombe . Nature 415 : 871 880.[PubMed] [CrossRef]
96. Sugiyama T,, Sugioka-Sugiyama R . 2011. Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO J 30 : 1027 1039.[PubMed] [CrossRef]
97. Leupold U, . 1993. The origins of Schizosaccharomyces pombe genetics, p 125 128. In Hall MN,, Linder P (ed), The Early Days of Yeast Genetics. Cold Spring Harbor Laboratory Press, New York.


Generic image for table
Table 1

Features and content in transposable elements of the genome

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Generic image for table
Table 2

Sizes of transposable elements and the molecular weights of their components in

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014
Generic image for table
Table 3

Host factors that restrict transposable element activity

Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of , p 997-1010. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0040-2014

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