Linear decay of retrotransposon antisense bias across genes is contingent upon tissue specificity

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Linker, Sara ^a   Hedges, Dale ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' UNTRANSLATED REGION; ALU SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE INSERTION; HOUSEKEEPING GENE; NATURAL SELECTION; QUANTITATIVE TRAIT LOCUS; RETROPOSON; TISSUE SPECIFICITY; 5' UNTRANSLATED REGION; ANTIBODY SPECIFICITY; EXON; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETICS; HUMAN; LONG INTERSPERSED REPEAT; MOLECULAR EVOLUTION; NUCLEOTIDE MOTIF;

5' UNTRANSLATED REGION; COMPLEMENTARY RNA; RETROPOSON;

5' UNTRANSLATED REGIONS; ALU ELEMENTS; EVOLUTION, MOLECULAR; EXONS; GENE FREQUENCY; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; NUCLEOTIDE MOTIFS; ORGAN SPECIFICITY; POLYMORPHISM, GENETIC; QUANTITATIVE TRAIT LOCI; RETROELEMENTS; RNA, ANTISENSE;

EID: 84896706322     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079402     Document Type: Article

References (57)

1. Lander E, Linton L, Birren B, Nusbaum C, Zody M, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921. (Pubitemid 32165345)
2. Liu WM, Maraia RJ, Rubin CM, Schmid CW (1994) Alu transcripts: cytoplasmic localisation and regulation by DNA methylation. Nucleic Acids Res 22: 1087-1095. (Pubitemid 24162174)
3. Muckenfuss H, Hamdorf M, Held U, Perkovic M, Löwer J, et al. (2006) APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 281: 22161-22172. (Pubitemid 44181920)
4. Vagin V V, Sigova A, Li C, Seitz H, Gvozdev V, et al. (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science (80-) 313: 320-324.
5. Cordaux R, Hedges DJ, Herke SW, Batzer MA (2006) Estimating the retrotransposition rate of human Alu elements. Gene 373: 134-137.
6. Ewing AD, Kazazian HH (2010) High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res 20: 1262-1270.
7. Deininger PL, Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab 67: 183-193. (Pubitemid 29390169)
8. Kines KJ, Belancio VP (2012) Expressing genes do not forget their LINEs: transposable elements and gene expression. Front Biosci a J virtual Libr 17: 1329-1344.
9. Zhang Y, Romanish MT, Mager DL (2011) Distributions of Transposable Elements Reveal Hazardous Zones in Mammalian Introns. PLoS Comput Biol 7: 13.
10. Graham T, Boissinot S (2006) The Genomic Distribution of L1 Elements: The Role of Insertion Bias and Natural Selection. J Biomed Biotechnol 2006: 75327.
11. Grover D, Majumder PP, B Rao C, Brahmachari SK, Mukerji M (2003) Nonrandom distribution of alu elements in genes of various functional categories: insight from analysis of human chromosomes 21 and 22. Mol Biol Evol 20: 1420-1424. (Pubitemid 37082577)
12. Pavlícek A, Jabbari K, Paces J, Paces V, Hejnar J V, et al. (2001) Similar integration but different stability of Alus and LINEs in the human genome. Gene 276: 39-45. (Pubitemid 32925258)
13. Soriano P, Meunier-Rotival M, Bernardi G (1983) The distribution of interspersed repeats is nonuniform and conserved in the mouse and human genomes. Proc Natl Acad Sci U S A 80: 1816-1820. (Pubitemid 13079187)
14. Fuhrman SA, Deininger PL, LaPorte P, Friedmann T, Geiduschek EP (1981) Analysis of transcription of the human Alu family ubiquitous repeating element by eukaryotic RNA polymerase III. Nucleic Acids Res 9: 6439-6456.
15. Minakami R, Kurose K, Etoh K, Furuhata Y, Hattori M, et al. (1992) Identification of an internal cis-element essential for the human L1 transcription and a nuclear factor(s) binding to the element. Nucleic Acids Res 20: 3139-3145.
16. Swergold GD (1990) Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol 10: 6718-6729.
17. Kaer K, Branovets J, Hallikma A, Nigumann P, Speek M (2011) Intronic L1 retrotransposons and nested genes cause transcriptional interference by inducing intron retention, exonization and cryptic polyadenylation. PLoS One 6: e26099.
18. Polak P, Domany E (2006) Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics 7: 133.
19. Speek M (2001) Antisense Promoter of Human L1 Retrotransposon Drives Transcription of Adjacent Cellular Genes. Mol Cell Biol 21: 1973-1985.
20. Mätlik K, Redik K, Speek M (2006) L1 Antisense Promoter Drives Tissue-Specific Transcription of Human Genes. J Biomed Biotechnol 2006: 71753.
21. Englander EW, Howard BH (1995) Nucleosome positioning by human Alu elements in chromatin. J Biol Chem 270: 10091-10096.
22. Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, et al. (2011) Retrotransposon-Induced Heterochromatin Spreading in the Mouse Revealed by Insertional Polymorphisms. PLoS Genet 7: e1002301.
23. Wang X-F, Jin X, Wang X, Liu J, Feng J, et al. (2009) Effects of L1-ORF2 fragments on green fluorescent protein gene expression. Genet Mol Biol 32: 688-696.
24. Shephard E, Chandan P, Stevanovic-Walker M, Edwards M, Phillips I (2007) Alternative promoters and repetitive DNA elements define the speciesdependent tissue-specific expression of the FMO1 genes of human and mouse. Biochem J 406: 491-499. (Pubitemid 47425455)
25. Hayakawa T, Satta Y, Gagneux P, Varki A, Takahata N (2001) Alu-mediated inactivation of the human CMP- N-acetylneuraminic acid hydroxylase gene. Proc Natl Acad Sci U S A 98: 11399-11404. (Pubitemid 32928740)
26. Yu Z, Morais D, Ivanga M, Harrison PM (2007) Analysis of the role of retrotransposition in gene evolution in vertebrates. BMC Bioinformatics 8: 308.
27. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonçalves Â, et al. (2012) Waves of Retrotransposon Expansion Remodel Genome Organization and CTCF Binding in Multiple Mammalian Lineages. Cell 148: 335-348.
28. Robins DM, Samuelson LC (1992) Retrotransposons and the evolution of mammalian gene expression. Genetica 86: 191-201.
29. Van De Lagemaat LN, Medstrand P, Mager DL (2006) Multiple effects govern endogenous retrovirus survival patterns in human gene introns. Genome Biol 7: R86.
30. Chen C, Ara T, Gautheret D (2009) Using Alu elements as polyadenylation sites: A case of retroposon exaptation. Mol Biol Evol 26: 327-334.
31. Medstrand P, Van De Lagemaat LN, Mager DL (2002) Retroelement Distributions in the Human Genome: Variations Associated With Age and Proximity to Genes. Genome Res 12: 1483-1495. (Pubitemid 35175086)
32. Han JS, Szak ST, Boeke JD (2004) Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 429: 268-274. (Pubitemid 38684807)
33. Moyzis RK, Torney DC, Meyne J, Buckingham JM, Wu JR, et al. (1989) The distribution of interspersed repetitive DNA sequences in the human genome. Genomics 4: 273-289.
34. Ovchinnikov I, Troxel AB, Swergold GD (2001) Genomic Characterization of Recent Human LINE-1 Insertions: Evidence Supporting Random Insertion. Genome Res 11: 2050-2058. (Pubitemid 33138802)
35. Stewart C, Kural D, Strömberg MP, Walker JA, Konkel MK, et al. (2011) A Comprehensive Map of Mobile Element Insertion Polymorphisms in Humans. PLoS Genet 7: 1. Available: http://dx.plos.org/10.1371/journal.pgen.1002236.
36. Bennett EA, Keller H, Mills RE, Schmidt S, Moran J V, et al. (2008) Active Alu retrotransposons in the human genome. Genome Res 18: 1875-1883.
37. Eller CD, Regelson M, Merriman B, Nelson S, Horvath S, et al. (2007) Repetitive sequence environment distinguishes housekeeping genes. Gene 390: 153-165. (Pubitemid 46241747)
38. Lev-Maor G, Ram O, Kim E, Sela N, Goren A, et al. (2008) Intronic Alus Influence Alternative Splicing. PLoS Genet 4: 12.
39. Perez-Stable C, Ayres TM, Shen CK (1984) Distinctive sequence organization and functional programming of an Alu repeat promoter. Proc Natl Acad Sci U S A 81: 5291-5295. (Pubitemid 14048733)
40. Athanikar JN, Badge RM, Moran J V (2004) A YY1-binding site is required for accurate human LINE-1 transcription initiation. Nucleic Acids Res 32: 3846-3855. (Pubitemid 39199077)
41. Yang W-M, Inouye C, Zeng Y, Bearss D, Seto E (1996) Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc Natl Acad Sci U S A 93: 12845-12850. (Pubitemid 26382731)
42. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492.
43. Sved J, Bird A (1990) The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proc Natl Acad Sci U S A 87: 4692-4696.
44. Shakhmuradov IA, Kapitonov V V, Kolchanov NA, Omel'ianchuk L V (1989) Evolution of Alu repeats: dynamics of distribution in genome. Genetika 25: 1682-1689. (Pubitemid 19243936)
45. Tchénio T, Casella J-F, Heidmann T (2000) Members of the SRY family regulate the human LINE retrotransposons. Nucleic Acids Res 28: 411-415. (Pubitemid 30057978)
46. Omar MFM, Ito K, Nga ME, Soo R, Peh BK, et al. (2012) RUNX3 downregulation in human lung adenocarcinoma is independent of p53, EGFR or KRAS status. Pathol Oncol Res POR 18: 783-792.
47. Ostertag EM, Kazazian HH (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet 35: 501-538. (Pubitemid 34032985)
48. Zingler N, Willhoeft U, Brose H-P, Schoder V, Jahns T, et al. (2005) Analysis of 59 junctions of human LINE-1 and Alu retrotransposons suggests an alternative model for 59-end attachment requiring microhomology-mediated end-joining. Genome Res 15: 780-789. (Pubitemid 41003101)
49. Putku M, Kepp K, Org E, Sõber S, Comas D, et al. (2011) Novel polymorphic AluYb8 insertion in the WNK1 gene is associated with blood pressure variation in Europeans. Hum Mutat 32: 806-814.
50. Montgomery SB, Sammeth M, Gutierrez-Arcelus M, Lach RP, Ingle C, et al. (2010) Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773-777.
51. Wagstaff BJ, Hedges DJ, Derbes RS, Campos Sanchez R, Chiaromonte F, et al. (2012) Rescuing Alu: Recovery of New Inserts Shows LINE-1 Preserves Alu Activity through A-Tail Expansion. PLoS Genet 8: e1002842.
52. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
53. Belancio VP, Roy-Engel AM, Deininger P (2008) The impact of multiple splice sites in human L1 elements. Gene 411: 38-45.
54. Sorek R, Ast G, Graur D (2002) Alu-Containing Exons are Alternatively Spliced. Genome Res 12: 1060-1067. (Pubitemid 34785198)
55. Smit AF, Tóth G, Riggs AD, Jurka J (1995) Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. J Mol Biol 246: 401-417.
56. Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39: 175-191.
57. Chang CW, Cheng WC, Chen CR, Shu WY, Tsai ML, et al. (2011) Identification of Human Housekeeping Genes and Tissue-Selective Genes by Microarray Meta-Analysis. PLoS One 6: 10.