The transcript repeat element: The human Alu sequence as a component of gene networks influencing cancer

Functional and Integrative Genomics

Volumn 10, Issue 3, 2010, Pages 307-319

  Moolhuijzen, Paula ^a   Kulski, Jerzy K ^a,b,c   Dunn, David S ^a   Schibeci, David ^a   Barrero, Roberto ^a   Gojobori, Takashi ^d   Bellgard, Matthew ^a  

^a MURDOCH UNIVERSITY   (Australia)

^b TOKAI UNIVERSITY   (Japan)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Bioinformatics; Comparative genomics; Disease; Gene control

Indexed keywords

DOUBLE STRANDED RNA; MESSENGER RNA; SMALL INTERFERING RNA;

ALU SEQUENCE; CANCER CELL; DOWN REGULATION; EXON; GENE CONTROL; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN GENOME; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA EDITING; TRANSPOSON; UNTRANSLATED REGION; GENE REGULATORY NETWORK;

ALU ELEMENTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS;

EID: 77955851699     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-010-0168-1     Document Type: Review

References (78)

1. HJ An D Lee KH Lee J Bhak 2004 The association of Alu repeats with the generation of potential AU-rich elements (ARE) at 3′ untranslated regions BMC Genomics 5 97 102 10.1186/1471-2164-5-97 15610565 (Pubitemid 41357636)
2. R Apweiler TK Attwood A Bairoch 2001 The InterPro database, an integrated documentation resource for protein families, domains and functional sites Nucl Acids Res 29 37 40 10.1093/nar/29.1.37 1:CAS:528:DC%2BD3MXjtlWnsbw%3D 11125043
3. AA Aravin GJ Hannon J Brennecke 2007 The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race Science 318 761 764 10.1126/science.1146484 1:CAS:528:DC%2BD2sXht1els77M 17975059 (Pubitemid 351411762)
4. M Ashburner CA Ball JA Blake D Botstein H Butler JM Cherry AP Davis K Dolinski SS Dwight JT Eppig MA Harris DP Hill L Issel-Tarver A Kasarskis S Lewis JC Matese JE Richardson M Ringwald GM Rubin G Sherlock 2000 Gene ontology: tool for the unification of biology Nat Genet 25 25 29 10.1038/75556 1:CAS:528:DC%2BD3cXjtFSlsbc%3D 10802651 (Pubitemid 30257031)
5. AP Bird 1993 Functions for DNA methylation in vertebrates Cold Spring Harb Symp Quant Biol 58 281 285 1:CAS:528:DyaK2MXmtF2juw%3D%3D 7956040
6. V Bollati S Fabris V Pegoraro D Ronchetti L Mosca GL Deliliers V Motta PA Bertazzi A Baccarelli A Neri 2009 Differential repetitive DNA methylation in multiple myeloma molecular subgroups Carcinogenesis 30 1330 1335 10.1093/carcin/bgp149 1:CAS:528:DC%2BD1MXpsVaksbk%3D 19531770
7. GM Borchert W Lanier B Davidson 2006 RNA polymerase III transcribes human microRNAs Nat Struct Mol Biol 13 1097 1101 10.1038/nsmb1167 1:CAS:528:DC%2BD28Xht1KrurnO 17099701 (Pubitemid 44885920)
8. RJ Britten 1996 Cases of ancient mobile element DNA insertions that now affect gene regulation Mol Phylogenet Evol 5 13 17 10.1006/mpev.1996.0003 1:CAS:528:DyaK28XitVyrsLc%3D 8673282 (Pubitemid 126316994)
9. RJ Britten 2004 Coding sequences of functioning human genes derived entirely from mobile element sequences Proc Natl Acad Sci 101 16825 16830 10.1073/pnas.0406985101 1:CAS:528:DC%2BD2cXhtFansr3F 15546984 (Pubitemid 39601323)
10. RJ Britten EH Davidson 1969 Gene regulation for higher cells: a theory Science 165 349 357 10.1126/science.165.3891.349 1:CAS:528:DyaF1MXkslOnurw%3D 5789433
11. RJ Britten EH Davidson 1971 Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty Q Rev Biol 46 111 138 10.1086/406830 1:STN:280:DyaE387hsFSqsw%3D%3D 5160087
12. V Chandler M Alleman 2008 Paramutation: epigenetic instructions passed across generations Genetics 178 1839 1844 1:CAS:528:DC%2BD1cXmt1eltbw%3D 18430919
13. VL Chandler M Stam 2004 Chromatin conversations: mechanisms and implications of paramutation Nat Rev Genet 5 532 544 10.1038/nrg1378 1:CAS:528:DC%2BD2cXltVSmsb8%3D 15211355 (Pubitemid 38868509)
14. K Chen N Rajewsky 2007 The evolution of gene regulation by transcription factors and microRNAs Nat Rev Genet 8 93 103 10.1038/nrg1990 1:CAS:528:DC%2BD2sXmt1OmsQ%3D%3D 17230196 (Pubitemid 46122839)
15. WM Chu R Ballard BW Carpick BRG Williams CW Schmid 1998 Potential Alu function: regulation of the activity of double-stranded RNA-activated kinase PKR Mol Cell Biol 18 58 68 1:CAS:528:DyaK1cXivFWksQ%3D%3D 9418853
16. F Claverie-Martin C Flores M Anton-Gamero H Gonzalez-Acosta V GarcIa-Nieto 2005 The Alu insertion in the CLCN5 gene of a patient with Dent's disease leads to exon 11 skipping J Hum Genet 50 370 374 10.1007/s10038-005- 0265-5 1:CAS:528:DC%2BD2MXovVOitLk%3D 16041495 (Pubitemid 41206931)
17. T Dagan R Sorek E Sharon G Ast D Graur 2004 AluGene: a database of Alu elements incorporated within protein-coding genes Nucleic Acids Res 32 D489 D492 10.1093/nar/gkh132 1:CAS:528:DC%2BD3sXhtVSru7vF 14681464
18. A Daskalos G Nikolaidis G Xinarianos P Savvari A Cassidy R Zakopoulou A Kotsinas V Gorgoulis JK Field T Liloglou 2009 Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer Int J Cancer 124 81 87 10.1002/ijc.23849 1:CAS:528: DC%2BD1cXhsFahtrjF 18823011
19. SM De La Monte K Ghanbari WH Frey I Beheshti P Averback SL Hauser HA Ghanbari JR Wands 1997 Characterization of the AD7c-NTP cDNA expression in Alzheimer' disease and measurement of a 41-kD protein in cerebrospinal fluid J Clin Invest 100 3093 3104 10.1172/JCI119864 1:STN:280:DyaK1c%2FmsVSltQ%3D%3D 9399956
20. C Feschotte 2008 Transposable elements and the evolution of regulatory networks Nat Rev Genet 9 397 405 10.1038/nrg2337 1:CAS:528:DC%2BD1cXkvVOhs7k%3D 18368054 (Pubitemid 351556062)
21. V Gotea W Makalowski 2006 Do transposable elements really contribute to protease? Trends Genet 22 260 267 10.1016/j.tig.2006.03.006 1:CAS:528: DC%2BD28XksVCmtLs%3D 16569458
22. SI Grewal S Jia 2007 Heterochromatin revisited Nat Rev Genet 8 35 46 10.1038/nrg2008 1:CAS:528:DC%2BD28Xhtlakt7fO 17173056 (Pubitemid 46006048)
23. CR Hagan RF Sheffield CM Rudin 2003 Human Alu element retrotransposition induced by genotoxic stress Nat Genet 35 219 220 10.1038/ng1259 1:CAS:528:DC%2BD3sXosFWrt78%3D 14578886 (Pubitemid 37363174)
24. JE Hambor J Mennone ME Coon JH Hanke P Kavathas 1993 Identification and characterization of an Alu-containing, T-cell-specific enhancer located in the last intron of the human CD8 alpha gene Mol Cell Biol 13 7056 7070 1:CAS:528:DyaK2cXisV2hug%3D%3D 8413295
25. J Hasler K Strub 2006 Alu elements as regulators of gene expression Nucleic Acids Res 34 5491 5497 10.1093/nar/gkl706 17020921 (Pubitemid 44742437)
26. CM Houck FP Rinehart CW Schmid 1979 A ubiquitous family of repeated DNA sequences in the human genome J Mol Biol 132 289 306 10.1016/0022-2836(79)90261- 4 1:CAS:528:DyaE1MXlslantLk%3D 533893 (Pubitemid 10227802)
27. T Imanishi T Itoh Y Suzuki C O'Donovan S Fukuchi KO Koyanagi RA Barrero T Tamura Y Yamaguchi-Kabata M Tanino K Yura 2004 Integrative annotation of 21, 037 human genes validated by full-length cDNA clones PLoS Biol 2 856 875 10.1371/journal.pbio.0020162 1:CAS:528:DC%2BD2cXltVGrurg%3D (Pubitemid 39234451)
28. SA Jamalkandi A Masoudi-Nejad 2009 Reconstruction of Arabidopsis thaliana fully integrated small RNA pathway Funct Integr Genomics 9 419 432 10.1007/s10142-009-0141-z 1:CAS:528:DC%2BD1MXht1Cmtr%2FF 19802639
29. R Johnson RJ Gamblin L Ooi AW Bruce IJ Donaldson DR Westhead IC Wood RM Jackson NJ Buckley 2006 Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication Nucleic Acids Res 34 3862 3877 10.1093/nar/gkl525 1:CAS:528:DC%2BD28Xps1yis70%3D 16899447 (Pubitemid 44391002)
30. J Jurka P Klonowski V Dagman P Pelton 1996 CENSOR-a program for identification and elimination of repetitive elements from DNA sequences Comput Chem 20 119 121 10.1016/S0097-8485(96)80013-1 1:CAS:528:DyaK28XhslWnsLc%3D 8867843
31. V Kapitonov J Jurka 1996 The age of Alu subfamilies J Mol Evol 42 59 65 10.1007/BF00163212 1:CAS:528:DyaK28XntFOmtg%3D%3D 8576965 (Pubitemid 26030574)
32. VN Kim 2005 Small RNAs: classification, biogenesis, and function Mol Cells 19 1 15 10.1016/j.molcel.2005.05.026 1:CAS:528:DC%2BD2MXis1Wisr8%3D 15750334 (Pubitemid 40884653)
33. DDY Kim TTY Kim T Walsh Y Kobayashi TC Matise S Buyske A Gabriel 2004 Widespread RNA editing of embedded Alu elements in the human transcriptome Genome Res 14 1719 1725 10.1101/gr.2855504 1:CAS:528:DC%2BD2cXnsFGjsb8%3D 15342557 (Pubitemid 39276429)
34. DS Kim JW Huh HS Kim 2007 Transposable elements in human cancers by genome-wide EST alignment Genes Genet Syst 82 145 156 10.1266/ggs.82.145 1:CAS:528:DC%2BD2sXoslGktr4%3D 17507780 (Pubitemid 46743508)
35. Y Kondo JP Issa 2003 Enrichment for histone H3 lysine 9 methylation at Alu repeats in human cells J Biol Chem 278 30 27658 27662 10.1074/jbc.M304072200 1:CAS:528:DC%2BD3sXlsFKkt7g%3D 12724318 (Pubitemid 36899953)
36. JA Kriegs J Schmitz W Makalowski J Brosius 2005 Does the AD7c-NTP locus encode a protein? BBA Gene Struct Expr 1727 1 4
37. M Krull J Brosius J Schmitz 2005 Alu-SINE exonization: en route to protein-coding function Mol Biol Evol 22 1702 1711 10.1093/molbev/msi164 1:CAS:528:DC%2BD2MXmslGjsro%3D 15901843 (Pubitemid 41373581)
38. ES Lander LM Linton B Birren C Nusbaum MC Zody J Baldwin K Devon K Dewar M Doyle W FitzHugh R Funke 2001 Initial sequencing and analysis of the human genome Nature 409 860 921 10.1038/35057062 1:CAS:528:DC%2BD3MXhsFCjtLc%3D 11237011 (Pubitemid 32165345)
39. S Lehnert P Van Loo PJ Thilakarathne P Marynen G Verbeke FC Schuit 2009 Evidence for co-evolution between human microRNAs and Alu-repeats PLoS ONE 4 e4456 10.1371/journal.pone.0004456 19209240
40. H Lei I Vorechovsky 2005 Identification of splicing silencers and enhancers in sense Alus: a role for pseudoacceptors in splice site repression Mol Cell Biol 24 6912 6920 10.1128/MCB.25.16.6912-6920.2005 (Pubitemid 41105892)
41. H Lei INM Day I Vorechovsky 2005 Exonization of AluYa5 in the human ACE gene requires mutations in both 3′ and 5′ splice sites and is facilitated by a conserved splicing enhancer Nucleic Acids Res 33 3897 3906 10.1093/nar/gki707 1:CAS:528:DC%2BD2MXmsV2hsbk%3D 16027113 (Pubitemid 41418558)
42. EY Levanon E Eisenberg R Yelin S Nemzer M Hallengger R Shemesh ZY Fligelman A Shoshan SR Pollock D Sztybel M Olshansky G Rechavi MF Jantsch 2004 Systematic identification of abundant A-to-I editing sites in the human transcriptome Nat Biotechnol 22 1001 1005 10.1038/nbt996 1:CAS:528: DC%2BD2cXmtFWru7w%3D 15258596 (Pubitemid 39014477)
43. G Lev-Maor O Ram E Kim N Sela A Goren EY Levanon G Ast 2008 Intronic Alus influence alternative splicing PLoS Genet 4 e1000204 10.1371/journal.pgen. 1000204 18818740
44. WM Liu RJ Maraia CM Rubin CW Schmid 1994 Alu transcripts: cytoplasmic localisation and regulation by DNA methylation Nucleic Acids Res 22 1087 1095 10.1093/nar/22.6.1087 1:CAS:528:DyaK2cXktVags70%3D 7512262
45. S Maas S Patt M Schrey A Rich 2001 Underediting of glutamine receptor GluR-B mRNA in malignant gliomas Proc Natl Acad Sci 98 14687 14692 10.1073/pnas.251531398 1:CAS:528:DC%2BD3MXptFCksbk%3D 11717408 (Pubitemid 33121452)
46. S Maas A Rich K Nishikura 2003 A to I RNA editing: recent news and residual mysteries J Biol Chem 278 1391 1394 10.1074/jbc.R200025200 1:CAS:528:DC%2BD3sXisFyjsg%3D%3D 12446659 (Pubitemid 36801360)
47. W Makalowski 2000 Genomic scrap yard: how genomes utilize all that junk Gene 259 61 67 10.1016/S0378-1119(00)00436-4 1:CAS:528:DC%2BD3MXitV2msQ%3D%3D 11163962 (Pubitemid 32120150)
48. W Makalowski 2003 Not junk after all Science 300 1246 1247 10.1126/science.1085690 1:CAS:528:DC%2BD3sXlt1Sjsrw%3D 12764185 (Pubitemid 36618227)
49. JS Mattick 2007 A new paradigm for developmental biology J Exp Biol 210 1526 1547 10.1242/jeb.005017 17449818 (Pubitemid 46841958)
50. P Medstrand LN van de Lagemaat CA Dunn JR Landry D Svenback DL Mager 2005 Impact of transposable elements on the evolution of mammalian gene regulation Cytogenet Genome Res 110 342 352 10.1159/000084966 1:STN:280: DC%2BD2MvisleksA%3D%3D 16093686 (Pubitemid 41159911)
51. KV Morris SW Chan SE Jacobsen DJ Looney 2004 Small interfering RNA-induced transcriptional gene silencing in human cells Science 305 1289 1292 10.1126/science.1101372 1:CAS:528:DC%2BD2cXmvFCit78%3D 15297624 (Pubitemid 39129233)
52. O Novikova 2009 Chromodomains and LTR retrotransposons in plants Commun Integr Biol 2 2 158 162 1:CAS:528:DC%2BD1MXht1Ojs7zJ 19513271
53. N Paz EY Levanon N Amariglio AB Heimberger Z Ram S Constantini ZS Barbash K Adamsky M Safran A Hirschberg M Krupsky I Ben-Dov S Cazacu T Mikkelsen C Brodie E Eisenberg G Rechavi 2007 Altered adenosine-to-inosine RNA editing in human cancer Genome Res 17 1586 1595 10.1101/gr.6493107 1:CAS:528: DC%2BD2sXhtlSlu7nF 17908822 (Pubitemid 350074854)
54. AE Peaston AV Evsikov JH Graber WN de Vries AE Holbrook D Solter BB Knowles 2004 Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos Dev Cell 7 597 606 10.1016/j.devcel.2004.09.004 1:CAS:528:DC%2BD2cXptlGjur4%3D 15469847 (Pubitemid 39341844)
55. J Piriyapongsa L Marino-Ramirez IK Jordan 2007 Origin and evolution of human microRNAs from transposable elements Genetics 176 1323 1337 10.1534/genetics.107.072553 1:CAS:528:DC%2BD2sXovVOqs7k%3D 17435244 (Pubitemid 46961124)
56. AL Price E Eskin PA Pevzner 2004 Whole-genome analysis of Alu repeat elements reveals complex evolutionary history Genome Res 14 2245 2252 10.1101/gr.2693004 1:CAS:528:DC%2BD2cXpvVCitbg%3D 15520288 (Pubitemid 39517330)
57. Y Quentin 1992 Fusion of a free left Alu monomer and a free right Alu monomer at the origin of the Alu family in the primate genomes Nucleic Acids Res 20 487 493 10.1093/nar/20.3.487 1:CAS:528:DyaK38XhvVyqsbY%3D 1741283
58. Y Quentin 1992 Origin of the Alu family: a family of Alu-like monomers gave birth to the left and the right arms of the Alu elements Nucleic Acids Res 20 3397 3401 10.1093/nar/20.13.3397 1:CAS:528:DyaK3sXisVyrsro%3D 1378589
59. K Richards B Zhang K Baggerly S Colella J Lang D Schuller R Krahe 2009 Genome-wide hypomethylation in head and neck cancer is more pronounced in HPV-negative tumors and is associated with genomic instability PLoS ONE 4 e4941 10.1371/journal.pone.0004941 19293934
60. Y Saito H Suzuki H Tsugawa I Nakagawa J Matsuzaki Y Kanai T Hibi 2009 Chromatin remodeling at Alu repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells Oncogene 28 2738 2744 10.1038/onc.2009.140 1:CAS:528:DC%2BD1MXntVWisL8%3D 19503096
61. WA Schulz C Steinhoff AR Florl 2006 Methylation of endogenous human retroelements in health and disease Curr Top Microbiol Immunol 3 211 250 10.1007/3-540-31181-5-11
62. RK Slotkin R Martienssen 2007 Transposable elements and the epigenetic regulation of the genome Nat Rev Genet 8 272 285 10.1038/nrg2072 1:CAS:528:DC%2BD2sXivVGkurw%3D 17363976 (Pubitemid 46439291)
63. NR Smalheiser VI Torvik 2005 Mammalian microRNAs derived from genomic repeats Trends Genet 21 322 326 10.1016/j.tig.2005.04.008 1:CAS:528: DC%2BD2MXks1Cmsb4%3D 15922829 (Pubitemid 40726387)
64. NR Smalheiser VI Torvik 2006 Alu elements within human mRNAs are probable microRNA targets Trends Genet 22 532 536 10.1016/j.tig.2006.08.007 1:CAS:528:DC%2BD28Xps1WgsLk%3D 16914224 (Pubitemid 44374128)
65. Smit A, Hubley R, Green P (1996-2004) RepeatMasker Open-3.0. http://www.repeatmasker.org
66. K Sobczak WJ Krzyzosiak 2002 Structural determinants of BRCA1 translational regulation J Biol Chem 277 17349 17358 10.1074/jbc.M109162200 1:CAS:528:DC%2BD38XjslWgsb8%3D 11877386 (Pubitemid 34967771)
67. R Sorek G Ast D Graur 2002 Alu-containing exons are alternatively spliced Genome Res 12 1060 1067 10.1101/gr.229302 1:CAS:528:DC%2BD38XlsVWgsr8%3D 12097342 (Pubitemid 34785198)
68. JE Stajich D Block K Boulez SE Brenner SA Chervitz C Dagdigian G Fuellen JGR Gilbert I Korf H Lapp H Lehvaslaiho C Matsalla CJ Mungall BI Osborne MR Pocock P Schattner M Senger LD Stein ED Stupka M Wilkinson E Birney 2002 The Bioperl toolkit: Perl modules for the life sciences Genome Res 12 1611 1618 10.1101/gr.361602 1:CAS:528:DC%2BD38XotVKgtbY%3D 12368254 (Pubitemid 35175100)
69. M Stam C Belele JE Dorweiler VL Chandler 2002 Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation Genes Dev 16 1906 1918 10.1101/gad.1006702 1:CAS:528:DC%2BD38XmtFalu7g%3D 12154122 (Pubitemid 34832920)
70. E Ullu C Tschudi 1984 Alu sequences are processed 7SL RNA genes Nature 312 171 172 10.1038/312171a0 1:CAS:528:DyaL2MXktVymtw%3D%3D 6209580 (Pubitemid 14000085)
71. MR Vila C Gelpi A Nicolas J Morote SJ Schwartz S Schwartz A Meseguer 2003 Higher processing rates of Alu-containing sequences in kidney tumours and cell lines with overexpressed Alu-mRNAs Oncol Rep 10 1903 1909 1:CAS:528: DC%2BD3sXptlCkurk%3D 14534716
72. AS Wilson BE Power P Molloy 2007 DNA hypomethylation and human diseases Biochim Biophys Acta 1775 138 162 1:CAS:528:DC%2BD28Xhtlaltr7K 17045745
73. C Yamasaki KO Koyanagi Y Fujii T Itoh R Barrero T Tamura Y Yamaguchi-Kabata M Tanino J Takeda S Fukuchi S Miyazaki N Nomura S Sugano T Imanishi T Gojobori 2005 Investigation of protein functions through data-mining on integrated human transcriptome database, H-Invitational database (H-InvDB) Gene 364 99 107 10.1016/j.gene.2005.05.036 1:CAS:528:DC%2BD2MXht12ju7nI 16185827 (Pubitemid 41773239)
74. JA Yoder CP Walsh TH Bestor 1997 Cytosine methylation and the ecology of intragenomic parasites Trends Genet 13 335 340 10.1016/S0168-9525(97)01181-5 1:CAS:528:DyaK2sXlt1Ggu78%3D 9260521 (Pubitemid 27309911)
75. IG Yulug A Yulug EMC Fisher 1995 The frequency and position of Alu repeats in cDNAs, as determined by database searching Genomics 27 544 548 10.1006/geno.1995.1090 1:CAS:528:DyaK2MXmvVSntLw%3D 7558040
76. K Yura M Shionyu K Hagino A Hijikata Y Hirashima T Nakahara T Eguchi K Shinoda A Yamaguchi K Takahashi T Itoh T Imanishi T Gojobori M Go 2006 Alternative splicing in human transcriptome: functional and structural influence on proteins Gene 380 63 71 10.1016/j.gene.2006.05.015 1:CAS:528: DC%2BD28XpsFygu78%3D 16872759 (Pubitemid 44349162)
77. YH Zhou JB Zheng X Gu GF Saunders WK Yung 2002 Novel PAX6 binding sites in the human genome and the role of repetitive elements in the evolution of gene regulation Genome Res 12 1716 1722 10.1101/gr.188302 1:CAS:528: DC%2BD38XovVarsLY%3D 12421758 (Pubitemid 35363675)
78. Zilberman DE, Safran M, Paz N, Amariglio N, Simon A, Fridman E, Kleinmann N, Ramon J, Rechavi G (2009) Does RNA editing play a role in the development of urinary bladder cancer? Urol Oncol (in press)