Transposable Elements Re-Wire and Fine-Tune the Transcriptome

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What good are transposable elements (TEs)? Although their activity can be harmful to host genomes and can cause disease, they nevertheless represent an important source of genetic variation that has helped shape genomes. In this review, we examine the impact of TEs, collectively referred to as the mobilome, on the transcriptome. We explore how TEs—particularly retrotransposons—contribute to transcript diversity and consider their potential significance as a source of small RNAs that regulate host gene transcription. We also discuss a critical role for the mobilome in engineering transcriptional networks, permitting coordinated gene expression, and facilitating the evolution of novel physiological processes.

Vyšlo v časopise: Transposable Elements Re-Wire and Fine-Tune the Transcriptome. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003234
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003234

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Zdroje

1. FedoroffN (2001) How jumping genes were discovered. Nat Struct Biol 8: 300–301.

2. LanderES, LintonLM, BirrenB, NusbaumC, ZodyMC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.

3. de KoningAP, GuW, CastoeTA, BatzerMA, PollockDD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384 doi:10.1371/journal.pgen.1002384.

4. HuangCR, SchneiderAM, LuY, NiranjanT, ShenP, et al. (2010) Mobile interspersed repeats are major structural variants in the human genome. Cell 141: 1171–1182.

5. BeckCR, CollierP, MacfarlaneC, MaligM, KiddJM, et al. (2010) LINE-1 retrotransposition activity in human genomes. Cell 141: 1159–1170.

6. EwingAD, KazazianHHJr (2010) High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20: 1262–1270.

7. IskowRC, McCabeMT, MillsRE, ToreneS, PittardWS, et al. (2010) Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141: 1253–1261.

8. KazazianHHJr, WongC, YoussoufianH, ScottAF, PhillipsDG, et al. (1988) Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 332: 164–166.

9. ChenJM, StensonPD, CooperDN, FerecC (2005) A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease. Hum Genet 117: 411–427.

10. GraveleyBR (2001) Alternative splicing: increasing diversity in the proteomic world. Trends Genet 17: 100–107.

11. NilsenTW, GraveleyBR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457–463.

12. BourqueG, LeongB, VegaVB, ChenX, LeeYL, et al. (2008) Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18: 1752–1762.

13. SchmidtD, SchwaliePC, WilsonMD, BallesterB, GoncalvesA, et al. (2012) Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148: 335–348.

14. HodgkinJ (2001) What does a worm want with 20,000 genes? Genome Biol 2: COMMENT2008.

15. PanQ, ShaiO, LeeLJ, FreyBJ, BlencoweBJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413–1415.

16. RamaniAK, CalarcoJA, PanQ, MavandadiS, WangY, et al. (2011) Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res 21: 342–348.

17. LiWH, GuZ, WangH, NekrutenkoA (2001) Evolutionary analyses of the human genome. Nature 409: 847–849.

18. NekrutenkoA, LiWH (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17: 619–621.

19. Lev-MaorG, SorekR, ShomronN, AstG (2003) The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science 300: 1288–1291.

20. SelaN, MerschB, Gal-MarkN, Lev-MaorG, Hotz-WagenblattA, et al. (2007) Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome. Genome Biol 8: R127.

21. SorekR, AstG, GraurD (2002) Alu-containing exons are alternatively spliced. Genome Res 12: 1060–1067.

22. ShenS, LinL, CaiJJ, JiangP, KenkelEJ, et al. (2011) Widespread establishment and regulatory impact of Alu exons in human genes. Proc Natl Acad Sci U S A 108: 2837–2842.

23. LinL, ShenS, TyeA, CaiJJ, JiangP, et al. (2008) Diverse splicing patterns of exonized Alu elements in human tissues. PLoS Genet 4: e1000225 doi:10.1371/journal.pgen.1000225.

24. FaulknerGJ, KimuraY, DaubCO, WaniS, PlessyC, et al. (2009) The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563–571.

25. DjebaliS, DavisCA, MerkelA, DobinA, LassmannT, et al. (2012) Landscape of transcription in human cells. Nature 489: 101–108.

26. DertiA, Garrett-EngeleP, MacisaacKD, StevensRC, SriramS, et al. (2012) A quantitative atlas of polyadenylation in five mammals. Genome Res 22: 1173–1183.

27. LeeJY, JiZ, TianB (2008) Phylogenetic analysis of mRNA polyadenylation sites reveals a role of transposable elements in evolution of the 3′-end of genes. Nucleic Acids Res 36: 5581–5590.

28. TangW, GunnTM, McLaughlinDF, BarshGS, SchlossmanSF, et al. (2000) Secreted and membrane attractin result from alternative splicing of the human ATRN gene. Proc Natl Acad Sci U S A 97: 6025–6030.

29. Duke-CohanJS, GuJ, McLaughlinDF, XuY, FreemanGJ, et al. (1998) Attractin (DPPT-L), a member of the CUB family of cell adhesion and guidance proteins, is secreted by activated human T lymphocytes and modulates immune cell interactions. Proc Natl Acad Sci U S A 95: 11336–11341.

30. NagleDL, McGrailSH, VitaleJ, WoolfEA, DussaultBJJr, et al. (1999) The mahogany protein is a receptor involved in suppression of obesity. Nature 398: 148–152.

31. GunnTM, MillerKA, HeL, HymanRW, DavisRW, et al. (1999) The mouse mahogany locus encodes a transmembrane form of human attractin. Nature 398: 152–156.

32. EsnaultC, MaestreJ, HeidmannT (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24: 363–367.

33. VinckenboschN, DupanloupI, KaessmannH (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci U S A 103: 3220–3225.

34. WoodAJ, SchulzR, WoodfineK, KoltowskaK, BeecheyCV, et al. (2008) Regulation of alternative polyadenylation by genomic imprinting. Genes Dev 22: 1141–1146.

35. CowleyM, WoodAJ, BohmS, SchulzR, OakeyRJ (2012) Epigenetic control of alternative mRNA processing at the imprinted Herc3/Nap1l5 locus. Nucleic Acids Res 40: 8917–8926.

36. ShearwinKE, CallenBP, EganJB (2005) Transcriptional interference–a crash course. Trends Genet 21: 339–345.

37. LiJ, AkagiK, HuY, TrivettAL, HlynialukCJ, et al. (2012) Mouse endogenous retroviruses can trigger premature transcriptional termination at a distance. Genome Res 22: 870–884.

38. DrukerR, BruxnerTJ, LehrbachNJ, WhitelawE (2004) Complex patterns of transcription at the insertion site of a retrotransposon in the mouse. Nucleic Acids Res 32: 5800–5808.

39. MorganHD, SutherlandHG, MartinDI, WhitelawE (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23: 314–318.

40. PeastonAE, EvsikovAV, GraberJH, de VriesWN, HolbrookAE, et al. (2004) Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597–606.

41. WolffEM, ByunHM, HanHF, SharmaS, NicholsPW, et al. (2010) Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet 6: e1000917 doi:10.1371/journal.pgen.1000917.

42. MuotriAR, ChuVT, MarchettoMC, DengW, MoranJV, et al. (2005) Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435: 903–910.

43. ThomasCA, PaquolaAC, MuotriAR (2012) LINE-1 Retrotransposition in the Nervous System. Annu Rev Cell Dev Biol 28: 555–573.

44. CoufalNG, Garcia-PerezJL, PengGE, YeoGW, MuY, et al. (2009) L1 retrotransposition in human neural progenitor cells. Nature 460: 1127–1131.

45. EvronyGD, CaiX, LeeE, HillsLB, ElhosaryPC, et al. (2012) Single-neuron sequencing analysis of l1 retrotransposition and somatic mutation in the human brain. Cell 151: 483–496.

46. Bourc'hisD, BestorTH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96–99.

47. SuzukiS, OnoR, NaritaT, PaskAJ, ShawG, et al. (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3: e55 doi:10.1371/journal.pgen.0030055.

48. BarlowDP (1993) Methylation and imprinting: from host defense to gene regulation? Science 260: 309–310.

49. HaigD (2012) Retroviruses and the placenta. Curr Biol 22: R609–613.

50. RougetC, PapinC, BoureuxA, MeunierAC, FrancoB, et al. (2010) Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467: 1128–1132.

51. WatanabeT, TomizawaS, MitsuyaK, TotokiY, YamamotoY, et al. (2011) Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332: 848–852.

52. DrakeNM, ParkYJ, ShiraliAS, ClelandTA, SolowayPD (2009) Imprint switch mutations at Rasgrf1 support conflict hypothesis of imprinting and define a growth control mechanism upstream of IGF1. Mamm Genome 20: 654–663.

53. YanY, ZhangY, YangK, SunZ, FuY, et al. (2011) Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J 65: 820–828.

54. WongS, WolfeKH (2005) Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat Genet 37: 777–782.

55. LeeJM, SonnhammerEL (2003) Genomic gene clustering analysis of pathways in eukaryotes. Genome Res 13: 875–882.

56. CohenBA, MitraRD, HughesJD, ChurchGM (2000) A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26: 183–186.

57. KunarsoG, ChiaNY, JeyakaniJ, HwangC, LuX, et al. (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: 631–634.

58. JordanIK, RogozinIB, GlazkoGV, KooninEV (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19: 68–72.

59. PolavarapuN, Marino-RamirezL, LandsmanD, McDonaldJF, JordanIK (2008) Evolutionary rates and patterns for human transcription factor binding sites derived from repetitive DNA. BMC Genomics 9: 226.

60. MacfarlanTS, GiffordWD, DriscollS, LettieriK, RoweHM, et al. (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487: 57–63.

61. MacfarlanTS, GiffordWD, AgarwalS, DriscollS, LettieriK, et al. (2011) Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev 25: 594–607.

62. RoweHM, JakobssonJ, MesnardD, RougemontJ, ReynardS, et al. (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237–240.

63. SchultzDC, AyyanathanK, NegorevD, MaulGG, RauscherFJ3rd (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16: 919–932.

64. GellersenB, BrosensIA, BrosensJJ (2007) Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med 25: 445–453.

65. LynchVJ, LeclercRD, MayG, WagnerGP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43: 1154–1159.

66. GerloS, DavisJR, MagerDL, KooijmanR (2006) Prolactin in man: a tale of two promoters. Bioessays 28: 1051–1055.

67. EmeraD, CasolaC, LynchVJ, WildmanDE, AgnewD, et al. (2012) Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol Biol Evol 29: 239–247.

68. DupressoirA, VernochetC, HarperF, GueganJ, DessenP, et al. (2011) A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc Natl Acad Sci U S A 108: E1164–1173.

69. SamsteinRM, JosefowiczSZ, ArveyA, TreutingPM, RudenskyAY (2012) Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 150: 29–38.

70. NaitoK, ZhangF, TsukiyamaT, SaitoH, HancockCN, et al. (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461: 1130–1134.

71. LeeE, IskowR, YangL, GokcumenO, HaseleyP, et al. (2012) Landscape of somatic retrotransposition in human cancers. Science 337: 967–971.

72. Fiston-LavierAS, CarriganM, PetrovDA, GonzalezJ (2011) T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data. Nucleic Acids Res 39: e36.

73. StewartC, KuralD, StrombergMP, WalkerJA, KonkelMK, et al. (2011) A comprehensive map of mobile element insertion polymorphisms in humans. PLoS Genet 7: e1002236 doi:10.1371/journal.pgen.1002236.

74. PoppC, DeanW, FengS, CokusSJ, AndrewsS, et al. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463: 1101–1105.

75. LaneN, DeanW, ErhardtS, HajkovaP, SuraniA, et al. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88–93.

76. RakyanVK, ChongS, ChampME, CuthbertPC, MorganHD, et al. (2003) Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100: 2538–2543.

77. StoyeJP (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nature reviews Microbiology 10: 395–406.

78. CopelandNG, HutchisonKW, JenkinsNA (1983) Excision of the DBA ecotropic provirus in dilute coat-color revertants of mice occurs by homologous recombination involving the viral LTRs. Cell 33: 379–387.

79. CordauxR, HedgesDJ, HerkeSW, BatzerMA (2006) Estimating the retrotransposition rate of human Alu elements. Gene 373: 134–137.

80. XingJ, ZhangY, HanK, SalemAH, SenSK, et al. (2009) Mobile elements create structural variation: analysis of a complete human genome. Genome Res 19: 1516–1526.

81. MoyesD, GriffithsDJ, VenablesPJ (2007) Insertional polymorphisms: a new lease of life for endogenous retroviruses in human disease. Trends Genet 23: 326–333.

82. BurnsKH, BoekeJD (2012) Human transposon tectonics. Cell 149: 740–752.

83. FinneganDJ (2012) Retrotransposons. Curr Biol 22: R432–437.