The role of Transposable Elements in shaping the combinatorial interaction of Transcription Factors

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Testori, Alessandro ^a   Caizzi, Livia ^a,b   Cutrupi, Santina ^a   Friard, Olivier ^a   De Bortoli, Michele ^a   Cora', Davide ^a,c   Caselle, Michele ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b Bioindustry Park Silvano Fumero   (Italy)

^c CANDIOLO CANCER INSTITUTE   (Italy)

Author keywords

ChIP seq; Combinatorial interaction; ER ; Transcription factors; Transposable elements

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; TRANSCRIPTION FACTOR;

ARTICLE; CELL STRAIN MCF 7; EUKARYOTE; GENE CONTROL; GENE REGULATORY NETWORK; HUMAN; NONHUMAN; RECEPTOR BINDING; SCORING SYSTEM; TRANSPOSON;

BASE SEQUENCE; BINDING SITES; DNA TRANSPOSABLE ELEMENTS; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; MCF-7 CELLS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; TRANSCRIPTION FACTORS;

EUKARYOTA; MAMMALIA;

EID: 84864938012     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-400     Document Type: Article

References (70)

1. Gann A, Ptashne M. Genes & Signals 2002, Cold Spring Harbor Laboratory Press.
2. Wunderlich Z, Mirny LA. Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 2009, 25(10):434-440. 10.1016/j.tig.2009.08.003, 19815308.
3. Ross-Innes CS, Stark R, Holmes KA, Schmidt D, Spyrou C, Russell R, Massie CE, Vowler SL, Eldridge M, Carroll JS. Cooperative interaction between retinoic acid receptor-alpha and estrogen receptor in breast cancer. Genes Dev 2010, 24(2):171-182. 10.1101/gad.552910, 2807352, 20080953.
4. King Jordan I, et al. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends in Genetics 2003, 19(2):68-72. 10.1016/S0168-9525(02)00006-9, 12547512.
5. Thornburg BG, Gotea V, Makalowski W. Transposable elements as a significant source of transcription regulating signals. Gene 2006, 365:104-110.
6. Mariño-Ramírez L, Lewis KC, Landsman D, Jordan IK. Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res. 2005, 110(1-4):333-341. 1803082, 16093685.
7. Huda A, Tyagi E, Mariño-Ramírez L, Bowen NJ, Jjingo D, Jordan IK. Prediction of transposable element derived enhancers using chromatin modification profiles. PLoS One 2011, 6(11):e27513. 10.1371/journal.pone.0027513, 3210180, 22087331.
8. Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler D. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci U S A 2007, 104(47):18613-18618. 10.1073/pnas.0703637104, 2141825, 18003932.
9. Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, Chew JL, Ruan Y, Wei CL, Ng HH, Liu ET. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 2008, 18(11):1752-1762. 10.1101/gr.080663.108, 2577865, 18682548.
10. Bourque G. Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev 2009, 19(6):607-612. 10.1016/j.gde.2009.10.013, 19914058.
11. Wang J, Bowen NJ, Mariño-Ramírez L, Jordan IK. A c-Myc regulatory subnetwork from human transposable element sequences. Mol Biosyst 2009, 5(12):1831-1839. 10.1039/b908494k, 2850603, 19763338.
12. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 2010, 42(7):631-634. 10.1038/ng.600, 20526341.
13. Schmid CD, Bucher P. MER41 repeat sequences contain inducible STAT1 binding sites. PLoS One 2010, 5(7):e11425. 10.1371/journal.pone.0011425, 2897888, 20625510.
14. Molineris I, Grassi E, Ala U, Di Cunto F, Provero P. Evolution of promoter affinity for transcription factors in the human lineage. Mol Biol Evol 2011, 28(8):2173-2183. 10.1093/molbev/msr027, 21335606.
15. Gould S, Vrba E. Exaptation: a missing term in the science of form. Paleobiology 1983, 8:4-15.
16. Kamal M, Xie X, Lander ES. A large family of ancient repeat elements in the human genome is under strong selection. Proc Natl Acad Sci U S A 2006, 103:2740-2745. 10.1073/pnas.0511238103, 1413850, 16477033.
17. Lowe CB, Bejerano G, Haussler D. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci U S A 2007, 104:8005-8010. 10.1073/pnas.0611223104, 1876562, 17463089.
18. Gentles AJ, Wakefield MJ, Kohany O, Gu W, Batzer MA, Pollock DD, Jurka J. Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 2007, 17:992-1004. 10.1101/gr.6070707, 1899126, 17495012.
19. Herpin A, Braasch I, Kraeussling M, Schmidt C, Thoma EC, Nakamura S, Tanaka M, Schartl M. Transcriptional rewiring of the sex determining dmrt1 gene duplicate by transposable elements. PLoS Genet 2010, 6(2):e1000844. 10.1371/journal.pgen.1000844, 2820524, 20169179.
20. Xie D, Chen CC, Ptaszek LM, Xiao S, Cao X, Fang F, Ng HH, Lewin HA, Cowan C, Zhong S. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res 2010, 20(6):804-815. 10.1101/gr.100594.109, 2877577, 20219939.
21. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M. Genome-wide analysis of estrogen receptor binding sites. Nat Genet 2006, 38(11):1289-1297. 10.1038/ng1901, 17013392.
22. Cicatiello L, Mutarelli M, Grober OM, Paris O, Ferraro L, Ravo M, Tarallo R, Luo S, Schroth GP, Seifert M, Zinser C, Chiusano ML, Traini A, De Bortoli M, Weisz A. Estrogen receptor alpha controls a gene network in luminal-like breast cancer cells comprising multiple transcription factors and microRNAs. Am J Pathol 2010, 176(5):2113-2130. 10.2353/ajpath.2010.090837, 2861078, 20348243.
23. Fullwood MJ, Liu MH, Pan YF, Liu J, Han X, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009, 462(7269):58-64. 10.1038/nature08497, 2774924, 19890323.
24. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, Brown GD, Gojis O, Ellis IO, Green AR, Ali S, Chin SF, Palmieri C, Caldas C, Carroll JS. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 2012, 481(7381):389-393. 3272464, 22217937.
25. Joseph R, Orlov YL, Huss M, Sun W, Kong SL, Ukil L, Pan YF, Li G, Lim M, Thomsen JS, Ruan Y, Clarke ND, Prabhakar S, Cheung E, Liu ET. Integrative model of genomic factors for determining binding site selection by estrogen receptor-α. Mol Syst Biol 2010, 6:456. 3018168, 21179027.
26. Smit AF, Riggs AD. (1995) MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation. Nucl. Acids Res 1995, 23(1):98-102. 10.1093/nar/23.1.98, 306635, 7870595.
27. Smit AF. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev 1999, 9(6):657-663. 10.1016/S0959-437X(99)00031-3, 10607616.
28. Romano CM, Ramalho CF, de A Zanotto PM. Tempo and mode of ERV-K evolution in human and chimpanzee genomes. Arch Virol 2006, 151:2215-2228. 10.1007/s00705-006-0792-1, 16830071.
29. Romano CM, de Melo FL, Corsini MAB, Holmes EC, de A Zanotto PM. Demographic histories of ERV-K in Humans, Chimpanzees and Rhesus Monkeys. PLoS One 2007, 2(10):e1026. 10.1371/journal.pone.0001026, 2001186, 17925874.
30. Martins H, Villesen P. Improved integration Time Estimation of endogenous retroviruses with phylogenetic data. PLoS One 2011, 6(3):e14745. 10.1371/journal.pone.0014745, 3048862, 21394200.
31. Stabenau A, McVicker G, Melsopp C, Proctor G, Clamp, Birney E. The Ensembl core software libraries. Genome Res 2004, 14(5):929-933. 10.1101/gr.1857204, 479122, 15123588.
32. Ghosh MG, Thompson DA, Weigel RJ. PDZK1 and GREB1 are estrogen-regulated genes expressed in hormone-responsive breast cancer. Cancer Res 2000, 60(22):6367-6375.
33. Johnykutty S, Tang P, Zhao H, Hicks DG, Yeh S, Wang X. Dual expression of alpha-tocopherol-associated protein and estrogen receptor in normal/benign human breast luminal cells and the downregulation of alpha-tocopherol-associated protein in estrogen-receptor-positive breast carcinomas. Mod Pathol 2009, 22(6):770-775.
34. Kim ST, Moley KH. Regulation of facilitative glucose transporters and AKT/MAPK/PRKAA signaling via estradiol and progesterone in the mouse uterine epithelium. Biol Reprod 2009, 81(1):188-198. 10.1095/biolreprod.108.072629, 3093992, 19208550.
35. Koda M, Kanczuga-Koda L, Sulkowska M, Surmacz E, Sulkowski S. Relationships between hypoxia markers and the leptin system, estrogen receptors in human primary and metastatic breast cancer: effects of preoperative chemotherapy. BMC Cancer 2010, 10:320. 10.1186/1471-2407-10-320, 2898699, 20569445.
36. Trépos-Pouplard M, Lardenois A, Staub C, Guitton N, Dorval-Coiffec I, Pineau C, Primig M, Jégou B. Proteome analysis and genome-wide regulatory motif prediction identify novel potentially sex hormone regulated proteins in rat efferent ducts. Int J Androl 2009, 33(5):661-674.
37. Hao S, Li P, Zhao J, Hu Y, Hou Y. 17beta-estradiol suppresses cytotoxicity and proliferative capacity of murine splenic NK1.1+ cells. Cell Mol Immunol 2008, 5(5):357-364. 10.1038/cmi.2008.44, 18954559.
38. Barnett DH, Sheng S, Charn TH, Waheed A, Sly WS, Lin CY, Liu ET, Katzenellenbogen BS. Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res 2008, 68(9):3505-3515. 10.1158/0008-5472.CAN-07-6151, 18451179.
39. Lin S, Lin CJ, Hsieh DP. Li LA ERα phenotype, estrogen level, and benzo[a]pyrene exposure modulate tumor growth and metabolism of lung adenocarcinoma cells. Lung Cancer 2012, 75(3):285-292. 10.1016/j.lungcan.2011.08.010, 21920623.
40. Zhu ZY, Mu YQ, Fu XM, Li SM, Zhao FX. Association of CYP1B1 gene polymorphisms and the positive expression of estrogen alpha and estrogen beta with endometrial cancer risk. Eur J Gynaecol Oncol 2011, 32(2):188-191.
41. Sheng S, Barnett DH, Katzenellenbogen BS. Differential estradiol and selective estrogen receptor modulator (SERM) regulation of Keratin 13 gene expression and its underlying mechanism in breast cancer cells. Mol Cell Endocrinol 2008, 296(1-2):1-9. 2654210, 18951949.
42. Zhang Y, Zhao H, Asztalos S, Chisamore M, Sitabkhan Y, Tonetti DA. Estradiol-induced regression in T47D:A18/PKCalpha tumors requires the estrogen receptor and interaction with the extracellular matrix. Mol Cancer Res 2009, 7(4):498-510. 10.1158/1541-7786.MCR-08-0415, 2743931, 19372579.
43. Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M. Positive cross-regulatory loop ties GATA-3 to estrogen receptor a expression in breast cancer. Cancer Res 2007, 67:6477-6483. 10.1158/0008-5472.CAN-07-0746, 17616709.
44. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122:33-43. 10.1016/j.cell.2005.05.008, 16009131.
45. Kim K, Barhoumi R, Burghardt R. Safe S analysis of estrogen receptor alpha-Sp1 interactions in breast cancer cells by fluorescence resonance energy transfer. Mol Endocrinol 2005, 19(4):843-854. 10.1210/me.2004-0326, 15637147.
46. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970. 10.1016/j.cell.2008.01.018, 2323438, 18358809.
47. Laganiere J, Deblois G, Lefebvre C, Bataille AR, Robert F, Giguere V. Location analysis of estrogen receptor-α target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci U S A 2005, 102:11651-11656. 10.1073/pnas.0505575102, 1183449, 16087863.
48. Whitington T, Frith MC, Johnson J, Bailey TL. Inferring transcription factor complexes from ChIP-seq data. Nucl Acids Res 2011, 39(15):e98. 10.1093/nar/gkr341, 3159476, 21602262.
49. Villadsen R, Fridriksdottir AJ, Rønnov-Jessen L, Gudjonsson T, Rank F, LaBarge MA, Bissell MJ, Petersen OW. Evidence for a stem cell hierarchy in the adult human breast. J Cell Biol 2007, 177(1):87-101. 10.1083/jcb.200611114, 2064114, 17420292.
50. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A, Salama SR, Rubin EM, Kent WJ, Haussler D. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 2006, 441:87-90. 10.1038/nature04696, 16625209.
51. Santangelo AM, de Souza FS, Franchini LF, Bumaschny VF, Low MJ, Rubinstein M. Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene. PLoS Genet 2007, 3(10):1813-1826. 2000970, 17922573.
52. Sasaki T, Nishihara H, Hirakawa M, Fujimura K, Tanaka M, Kokubo N, Kimura-Yoshida C, Matsuo I, Sumiyama K, Saitou N, Shimogori T, Okada N. Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci U S A 2008, 105:4220-4225. 10.1073/pnas.0709398105, 2393765, 18334644.
53. Gombart AF, Saito T, Koeffler HP. Exaptation of an ancient Alu short interspersed element provides a highly conserved vitamin D-mediated innate immune response in humans and primates. BMC Genomics 2009, 10:321. 10.1186/1471-2164-10-321, 2716374, 19607716.
54. Johnson R, Gamblin RJ, Ooi L, Bruce AW, Donaldson IJ, Westhead DR, Wood IC, Jackson RM, Buckley NJ. Identification of the REST regulon reveals extensive transposable element- mediated binding site duplication. Nucl Acids Res 2006, 34:3862-3877. 10.1093/nar/gkl525, 1557810, 16899447.
55. Polak P, Domany E. Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics 2006, 7:133. 10.1186/1471-2164-7-133, 1513395, 16740159.
56. Laperriere D, Wang TT, White JH, Mader S. Widespread Alu repeat-driven expansion of consensus DR2 retinoic acid response elements during primate evolution. BMC Genomics 2007, 8:23. 10.1186/1471-2164-8-23, 1785376, 17239240.
57. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, Waki K, Hornig N, Arakawa T, Takahashi H, Kawai J, Forrest AR, Suzuki H, Hayashizaki Y, Hume DA, Orlando V, Grimmond SM, Carninci P. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 2009, 41:563-571. 10.1038/ng.368, 19377475.
58. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonçalves A, Kutter C, Brown GD, Marshall A, Flicek P, Odom DT. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 2012, 148(1-2):335-348. 3368268, 22244452.
59. Lynch VJ, Leclerc RD, May G, Wagner GP. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 2011, 43(11):1154-1159. 10.1038/ng.917, 21946353.
60. Sironi M, Menozzi G, Comi GP, Cereda M, Cagliani R, Bresolin N, Pozzoli U. Gene function and expression level influence the insertion/fixation dynamics of distinct transposon families in mammalian introns. Genome Biol 2006, 7(12):R120. 10.1186/gb-2006-7-12-r120, 1794433, 17181857.
61. Jurka J, Zietkiewicz E, Labuda D. Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the mesozoic era. Nucleic Acids Res 1995, 23(1):170-5. 10.1093/nar/23.1.170, 306646, 7870583.
62. Cohen CJ, Lock WM, Mager DL. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 2009, 448(2):105-114. 10.1016/j.gene.2009.06.020, 19577618.
63. Mayer J, Meese E. Human endogenous retroviruses in the primate lineage and their influence on host genomes. Cytogenet Genome Res 2005, 110:448-456. 10.1159/000084977, 16093697.
64. Emera D, Casola C, Lynch VJ, Wildman DE, Agnew D, Wagner GP. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol Biol Evol 2011, 29(1):239-247.
65. Thornton JW, Need E, Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 2003, 301(5640):1714-1717. 10.1126/science.1086185, 14500980.
66. Schwabe JW, Teichmann SA. Nuclear receptors: the evolution of diversity. Sci STKE 2004 2004, (217). pe4.
67. Markov GV, Laudet V. Origin and evolution of the ligand-binding ability of nuclear receptors. Mol Cell Endocrinol 2011, 334(1-2):21-30.
68. Smit AFA, Hubley R. RepeatModeler Open-1.0 2008-2010 http://www.repeatmasker.org.
69. Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0 1996-2010 http://www.repeatmasker.org.
70. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protoc 2009, 4(1):44-57.