A 3' Poly(A) Tract Is Required for LINE-1 Retrotransposition

Molecular Cell

Volumn 60, Issue 5, 2015, Pages 728-741

  Doucet, Aurélien J ^a,c   Wilusz, Jeremy E ^b   Miyoshi, Tomoichiro ^a   Liu, Ying ^a   Moran, John V ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; MESSENGER RNA; METASTASIS ASSOCIATED LUNG ADENOCARCINOMA TRANSCRIPT 1; POLYADENYLIC ACID; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; ENDONUCLEASE; MALAT1 LONG NON-CODING RNA, HUMAN; ORF2 PROTEIN, HUMAN; RNA DIRECTED DNA POLYMERASE;

3' UNTRANSLATED REGION; ALU SEQUENCE; ARTICLE; BASE PAIRING; BIOACCUMULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR STABILITY; OPEN READING FRAME; POLYADENYLATION; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RETROPOSON; RNA BINDING; RNA SEQUENCE; SIGNAL TRANSDUCTION; CHEMISTRY; GENETICS; HELA CELL LINE; LONG INTERSPERSED REPEAT; METABOLISM;

ENDONUCLEASES; HELA CELLS; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; POLY A; RNA, LONG NONCODING; RNA, MESSENGER; RNA-DIRECTED DNA POLYMERASE;

EID: 84951275519     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.012     Document Type: Article

References (69)

1. Ahl V., Keller H., Schmidt S., Weichenrieder O. Retrotransposition and crystal structure of an Alu RNP in the ribosome stalling conformation. Mol Cell 2015, 60:715-727. this issue.
2. Alisch R.S., Garcia-Perez J.L., Muotri A.R., Gage F.H., Moran J.V. Unconventional translation of mammalian LINE-1 retrotransposons. Genes Dev. 2006, 20:210-224.
3. Athanikar J.N., Badge R.M., Moran J.V. A YY1-binding site is required for accurate human LINE-1 transcription initiation. Nucleic Acids Res. 2004, 32:3846-3855.
4. Bao W., Jurka J. Origin and evolution of LINE-1 derived "half-L1" retrotransposons (HAL1). Gene 2010, 465:9-16.
5. Beck C.R., Collier P., Macfarlane C., Malig M., Kidd J.M., Eichler E.E., Badge R.M., Moran J.V. LINE-1 retrotransposition activity in human genomes. Cell 2010, 141:1159-1170.
6. Beck C.R., Garcia-Perez J.L., Badge R.M., Moran J.V. LINE-1 elements in structural variation and disease. Annu. Rev. Genomics Hum. Genet. 2011, 12:187-215.
7. Becker K.G., Swergold G.D., Ozato K., Thayer R.E. Binding of the ubiquitous nuclear transcription factor YY1 to a cis regulatory sequence in the human LINE-1 transposable element. Hum. Mol. Genet. 1993, 2:1697-1702.
8. Belancio V.P., Whelton M., Deininger P. Requirements for polyadenylation at the 3' end of LINE-1 elements. Gene 2007, 390:98-107.
9. Bennett E.A., Keller H., Mills R.E., Schmidt S., Moran J.V., Weichenrieder O., Devine S.E. Active Alu retrotransposons in the human genome. Genome Res. 2008, 18:1875-1883.
10. Boeke J.D. LINEs and Alus--the polyA connection. Nat. Genet. 1997, 16:6-7.
11. Brouha B., Schustak J., Badge R.M., Lutz-Prigge S., Farley A.H., Moran J.V., Kazazian H.H. Hot L1s account for the bulk of retrotransposition in the human population. Proc. Natl. Acad. Sci. USA 2003, 100:5280-5285.
12. Brown J.A., Valenstein M.L., Yario T.A., Tycowski K.T., Steitz J.A. Formation of triple-helical structures by the 3'-end sequences of MALAT1 and MENβ noncoding RNAs. Proc. Natl. Acad. Sci. USA 2012, 109:19202-19207.
13. Brown J.A., Bulkley D., Wang J., Valenstein M.L., Yario T.A., Steitz T.A., Steitz J.A. Structural insights into the stabilization of MALAT1 noncoding RNA by a bipartite triple helix. Nat. Struct. Mol. Biol. 2014, 21:633-640.
14. Cost G.J., Boeke J.D. Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry 1998, 37:18081-18093.
15. Cost G.J., Feng Q., Jacquier A., Boeke J.D. Human L1 element target-primed reverse transcription in vitro. EMBO J. 2002, 21:5899-5910.
16. Dewannieux M., Heidmann T. Role of poly(A) tail length in Alu retrotransposition. Genomics 2005, 86:378-381.
17. Dewannieux M., Esnault C., Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. 2003, 35:41-48.
18. Dmitriev S.E., Andreev D.E., Terenin I.M., Olovnikov I.A., Prassolov V.S., Merrick W.C., Shatsky I.N. Efficient translation initiation directed by the 900-nucleotide-long and GC-rich 5' untranslated region of the human retrotransposon LINE-1 mRNA is strictly cap dependent rather than internal ribosome entry site mediated. Mol. Cell. Biol. 2007, 27:4685-4697.
19. Dombroski B.A., Mathias S.L., Nanthakumar E., Scott A.F., Kazazian H.H. Isolation of an active human transposable element. Science 1991, 254:1805-1808.
20. Doucet A.J., Hulme A.E., Sahinovic E., Kulpa D.A., Moldovan J.B., Kopera H.C., Athanikar J.N., Hasnaoui M., Bucheton A., Moran J.V., Gilbert N. Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet. 2010, 6:e1001150.
21. Ergün S., Buschmann C., Heukeshoven J., Dammann K., Schnieders F., Lauke H., Chalajour F., Kilic N., Strätling W.H., Schumann G.G. Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J. Biol. Chem. 2004, 279:27753-27763.
22. Esnault C., Maestre J., Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 2000, 24:363-367.
23. Feng Q., Moran J.V., Kazazian H.H., Boeke J.D. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996, 87:905-916.
24. Grimaldi G., Skowronski J., Singer M.F. Defining the beginning and end of KpnI family segments. EMBO J. 1984, 3:1753-1759.
25. Hancks D.C., Kazazian H.H. Active human retrotransposons: variation and disease. Curr. Opin. Genet. Dev. 2012, 22:191-203.
26. Hancks D.C., Goodier J.L., Mandal P.K., Cheung L.E., Kazazian H.H. Retrotransposition of marked SVA elements by human L1s in cultured cells. Hum. Mol. Genet. 2011, 20:3386-3400.
27. Hayashi Y., Kajikawa M., Matsumoto T., Okada N. Mechanism by which a LINE protein recognizes its 3' tail RNA. Nucleic Acids Res. 2014, 42:10605-10617.
28. Hohjoh H., Singer M.F. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 1996, 15:630-639.
29. Holmes S.E., Singer M.F., Swergold G.D. Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J. Biol. Chem. 1992, 267:19765-19768.
30. Holmes S.E., Dombroski B.A., Krebs C.M., Boehm C.D., Kazazian H.H. A new retrotransposable human L1 element from the LRE2 locus on chromosome 1q produces a chimaeric insertion. Nat. Genet. 1994, 7:143-148.
31. Houseley J., LaCava J., Tollervey D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
32. Hulme A.E., Bogerd H.P., Cullen B.R., Moran J.V. Selective inhibition of Alu retrotransposition by APOBEC3G. Gene 2007, 390:199-205.
33. Jurka J., Kapitonov V.V., Pavlicek A., Klonowski P., Kohany O., Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 2005, 110:462-467.
34. Kajikawa M., Okada N. LINEs mobilize SINEs in the eel through a shared 3' sequence. Cell 2002, 111:433-444.
35. Kazazian H.H., Wong C., Youssoufian H., Scott A.F., Phillips D.G., Antonarakis S.E. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 1988, 332:164-166.
36. Khazina E., Truffault V., Büttner R., Schmidt S., Coles M., Weichenrieder O. Trimeric structure and flexibility of the L1ORF1 protein in human L1 retrotransposition. Nat. Struct. Mol. Biol. 2011, 18:1006-1014.
37. Kulpa D.A., Moran J.V. Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum. Mol. Genet. 2005, 14:3237-3248.
38. Kulpa D.A., Moran J.V. Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat. Struct. Mol. Biol. 2006, 13:655-660.
39. Labuda D., Striker G. Sequence conservation in Alu evolution. Nucleic Acids Res. 1989, 17:2477-2491.
40. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921. International Human Genome Sequencing Consortium.
41. Lee M., Kim B., Kim V.N. Emerging roles of RNA modification: m(6)A and U-tail. Cell 2014, 158:980-987.
42. Leibold D.M., Swergold G.D., Singer M.F., Thayer R.E., Dombroski B.A., Fanning T.G. Translation of LINE-1 DNA elements in vitro and in human cells. Proc. Natl. Acad. Sci. USA 1990, 87:6990-6994.
43. Luan D.D., Korman M.H., Jakubczak J.L., Eickbush T.H. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 1993, 72:595-605.
44. Malik H.S., Burke W.D., Eickbush T.H. The age and evolution of non-LTR retrotransposable elements. Mol. Biol. Evol. 1999, 16:793-805.
45. Martin S.L. Ribonucleoprotein particles with LINE-1 RNA in mouse embryonal carcinoma cells. Mol. Cell. Biol. 1991, 11:4804-4807.
46. Martin S.L., Bushman F.D. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol. Cell. Biol. 2001, 21:467-475.
47. Mathias S.L., Scott A.F., Kazazian H.H., Boeke J.D., Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 1991, 254:1808-1810.
48. McMillan J.P., Singer M.F. Translation of the human LINE-1 element, L1Hs. Proc. Natl. Acad. Sci. USA 1993, 90:11533-11537.
49. Monot C., Kuciak M., Viollet S., Mir A.A., Gabus C., Darlix J.L., Cristofari G. The specificity and flexibility of l1 reverse transcription priming at imperfect T-tracts. PLoS Genet. 2013, 9:e1003499.
50. Moran J.V., Holmes S.E., Naas T.P., DeBerardinis R.J., Boeke J.D., Kazazian H.H. High frequency retrotransposition in cultured mammalian cells. Cell 1996, 87:917-927.
51. Moran J.V., DeBerardinis R.J., Kazazian H.H. Exon shuffling by L1 retrotransposition. Science 1999, 283:1530-1534.
52. Morrish T.A., Gilbert N., Myers J.S., Vincent B.J., Stamato T.D., Taccioli G.E., Batzer M.A., Moran J.V. DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat. Genet. 2002, 31:159-165.
53. Moser B.A., Subramanian L., Khair L., Chang Y.T., Nakamura T.M. Fission yeast Tel1(ATM) and Rad3(ATR) promote telomere protection and telomerase recruitment. PLoS Genet. 2009, 5:e1000622.
54. Ohshima K. Parallel relaxation of stringent RNA recognition in plant and mammalian L1 retrotransposons. Mol. Biol. Evol. 2012, 29:3255-3259.
55. Ohshima K., Hamada M., Terai Y., Okada N. The 3' ends of tRNA-derived short interspersed repetitive elements are derived from the 3' ends of long interspersed repetitive elements. Mol. Cell. Biol. 1996, 16:3756-3764.
56. Raiz J., Damert A., Chira S., Held U., Klawitter S., Hamdorf M., Löwer J., Strätling W.H., Löwer R., Schumann G.G. The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery. Nucleic Acids Res. 2012, 40:1666-1683.
57. Richardson S.R., Doucet A.J., Kopera H.C., Moldovan J.B., Garcia-Perez J.L., Moran J.V. The influence of LINE-1 and SINE retrotransposons on mammalian genomes. Microbiol. Spectr. 2015, 3. MDNA3-0061-2014.
58. Sassaman D.M., Dombroski B.A., Moran J.V., Kimberland M.L., Naas T.P., DeBerardinis R.J., Gabriel A., Swergold G.D., Kazazian H.H. Many human L1 elements are capable of retrotransposition. Nat. Genet. 1997, 16:37-43.
59. Scott A.F., Schmeckpeper B.J., Abdelrazik M., Comey C.T., O'Hara B., Rossiter J.P., Cooley T., Heath P., Smith K.D., Margolet L. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1987, 1:113-125.
60. Sinnett D., Richer C., Deragon J.M., Labuda D. Alu RNA secondary structure consists of two independent 7 SL RNA-like folding units. J. Biol. Chem. 1991, 266:8675-8678.
61. Smit A.F. The origin of interspersed repeats in the human genome. Curr. Opin. Genet. Dev. 1996, 6:743-748.
62. Smit A.F. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 1999, 9:657-663.
63. Swergold G.D. Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol. Cell. Biol. 1990, 10:6718-6729.
64. Taylor M.S., LaCava J., Mita P., Molloy K.R., Huang C.R., Li D., Adney E.M., Jiang H., Burns K.H., Chait B.T., et al. Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 2013, 155:1034-1048.
65. Wei W., Gilbert N., Ooi S.L., Lawler J.F., Ostertag E.M., Kazazian H.H., Boeke J.D., Moran J.V. Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 2001, 21:1429-1439.
66. West N., Roy-Engel A.M., Imataka H., Sonenberg N., Deininger P. Shared protein components of SINE RNPs. J. Mol. Biol. 2002, 321:423-432.
67. Wilusz J.E., Freier S.M., Spector D.L. 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 2008, 135:919-932.
68. Wilusz J.E., JnBaptiste C.K., Lu L.Y., Kuhn C.D., Joshua-Tor L., Sharp P.A. A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 2012, 26:2392-2407.
69. Zhang Z., Harrison P.M., Liu Y., Gerstein M. Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res. 2003, 13:2541-2558.