Coordinately Co-opted Multiple Transposable Elements Constitute an Enhancer for wnt5a Expression in the Mammalian Secondary Palate

PLoS Genetics

Volumn 12, Issue 10, 2016, Pages

  Nishihara, Hidenori ^a   Kobayashi, Naoki ^a,i   Kimura Yoshida, Chiharu ^b   Yan, Kuo ^c   Bormuth, Olga ^c   Ding, Qiong ^a,j   Nakanishi, Akiko ^a,k   Sasaki, Takeshi ^a,l   Hirakawa, Mika ^d,m   Sumiyama, Kenta ^e,f   Furuta, Yasuhide ^f   Tarabykin, Victor ^c   Matsuo, Isao ^b   Okada, Norihiro ^a,g,h  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b OSAKA GENERAL MEDICAL CENTER   (Japan)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d KYOTO UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE OF GENETICS   (Japan)

^f RIKEN   (Japan)

^g NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^h Foundation for Advancement of International Science   (Japan)

ⁱ AZABU UNIVERSITY   (Japan)

^j UNIVERSITY OF TOKYO   (Japan)

^k NAGOYA UNIVERSITY   (Japan)

^l TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^m JT Biohistory Research Hall   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR MSX1; WNT5A PROTEIN; DNA BINDING PROTEIN; MSX1 PROTEIN, MOUSE; TRANSPOSON; WNT5A PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA TRANSPOSITION; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; FEMALE; GENE EXPRESSION; GENE LOCUS; MORPHOGENESIS; MOUSE; NONHUMAN; SECONDARY PALATE; TRANSPOSON; WNT5A GENE; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; KNOCKOUT MOUSE; MAMMAL; METABOLISM; MOLECULAR EVOLUTION; PALATE; REGULATORY SEQUENCE; TRANSGENE;

ANIMALS; BINDING SITES; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; MAMMALS; MICE; MICE, KNOCKOUT; MSX1 TRANSCRIPTION FACTOR; PALATE; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSGENES; WNT-5A PROTEIN;

EID: 84994357257     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006380     Document Type: Article

References (53)

1. Davidson EH, The Regulatory Genome: Gene Regulatory Networks In Development And Evolution: Elsevier; 2006.
2. Wray GA, The evolutionary significance of cis-regulatory mutations. Nat Rev Genet2007; 8(3):206–16. doi: 10.1038/nrg206317304246
3. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res2005; 15(8):1034–50. doi: 10.1101/gr.371500516024819
4. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature2006; 444(7118):499–502. doi: 10.1038/nature0529517086198
5. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, et al. Ultraconserved elements in the human genome. Science2004; 304(5675):1321–5. doi: 10.1126/science.109811915131266
6. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, et al. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet2008; 40(2):158–60. doi: 10.1038/ng.2007.5518176564
7. Nishihara H, Smit AF, Okada N, Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res2006; 16(7):864–74. doi: 10.1101/gr.525550616717141
8. Okada N, Sasaki T, Shimogori T, Nishihara H, Emergence of mammals by emergency: exaptation. Genes Cells2010; 15(8):801–12. doi: 10.1111/j.1365-2443.2010.01429.x20633052
9. Ferguson MW, Palate development. Development1988, 103Suppl:41–60. 3074914
10. Bush JO, Jiang R, Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development2012; 139(2):231–43. doi: 10.1242/dev.06708222186724
11. Dixon MJ, Marazita ML, Beaty TH, Murray JC, Cleft lip and palate: understanding genetic and environmental influences. Nat Rev Genet2011; 12(3):167–78. doi: 10.1038/nrg293321331089
12. Smith TM, Lozanoff S, Iyyanar PP, Nazarali AJ, Molecular signaling along the anterior-posterior axis of early palate development. Front Physiol2013; 3:488. doi: 10.3389/fphys.2012.0048823316168
13. Chiquet BT, Blanton SH, Burt A, Ma D, Stal S, Mulliken JB, et al. Variation in WNT genes is associated with non-syndromic cleft lip with or without cleft palate. Hum Mol Genet2008; 17(14):2212–8. doi: 10.1093/hmg/ddn12118413325
14. Yamaguchi TP, Bradley A, McMahon AP, Jones S, A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development1999; 126(6):1211–23. 10021340
15. He F, Xiong W, Yu X, Espinoza-Lewis R, Liu C, Gu S, et al. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development2008; 135(23):3871–9. doi: 10.1242/dev.02576718948417
16. Okada N, SINEs: Short interspersed repeated elements of the eukaryotic genome. Trends Ecol Evol1991; 6(11):358–61. doi: 10.1016/0169-5347(91)90226-N21232509
17. Prak ET, Kazazian HH, Jr.Mobile elements and the human genome. Nat Rev Genet2000; 1(2):134–44. doi: 10.1038/3503857211253653
18. Kramerov DA, Vassetzky NS, Short retroposons in eukaryotic genomes. Int Rev Cytol2005; 247:165–221. doi: 10.1016/S0074-7696(05)47004-716344113
19. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A, Salama SR, et al. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature2006; 441(7089):87–90. doi: 10.1038/nature0469616625209
20. 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 A2007; 104(19):8005–10. doi: 10.1073/pnas.061122310417463089
21. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature2007; 447(7141):167–77. doi: 10.1038/nature0580517495919
22. Brosius J, Gould SJ, On "genomenclature": a comprehensive (and respectful) taxonomy for pseudogenes and other "junk DNA". Proc Natl Acad Sci U S A1992; 89(22):10706–10. doi: 10.1073/pnas.89.22.107061279691
23. Sasaki T, Nishihara H, Hirakawa M, Fujimura K, Tanaka M, Kokubo N, Kimura-Yoshida C, Matsuo I, Sumiyama K, Saitou N, et al. Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci U S A2008; 105(11):4220–5. doi: 10.1073/pnas.070939810518334644
24. Hirakawa M, Nishihara H, Kanehisa M, Okada N, Characterization and evolutionary landscape of AmnSINE1 in Amniota genomes. Gene2009; 441(1–2):100–10. doi: 10.1016/j.gene.2008.12.00919166919
25. Tashiro K, Teissier A, Kobayashi N, Nakanishi A, Sasaki T, Yan K, et al. A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons. PLoS One2011; 6(12):e28497. doi: 10.1371/journal.pone.002849722174821
26. Nakanishi A, Kobayashi N, Suzuki-Hirano A, Nishihara H, Sasaki T, Hirakawa M, et al. A SINE-derived element constitutes a unique modular enhancer for mammalian diencephalic Fgf8. PLoS One2012; 7(8):e43785. doi: 10.1371/journal.pone.004378522937095
27. 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 Genet2007; 3(10):1813–26. doi: 10.1371/journal.pgen.003016617922573
28. Franchini LF, Lopez-Leal R, Nasif S, Beati P, Gelman DM, Low MJ, et al. Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons. Proc Natl Acad Sci U S A2011; 108(37):15270–5. doi: 10.1073/pnas.110499710821876128
29. Feschotte C, Transposable elements and the evolution of regulatory networks. Nat Rev Genet2008; 9(5):397–405. doi: 10.1038/nrg233718368054
30. Emera D, Wagner GP, Transformation of a transposon into a derived prolactin promoter with function during human pregnancy. Proc Natl Acad Sci USA2012; 109(28):11246–51. doi: 10.1073/pnas.111856610922733751
31. Alappat S, Zhang ZY, Chen YP, Msx homeobox gene family and craniofacial development. Cell Res2003; 13(6):429–42. doi: 10.1038/sj.cr.729018514728799
32. Tassabehji M, Hammond P, Karmiloff-Smith A, Thompson P, Thorgeirsson SS, Durkin ME, et al. GTF2IRD1 in craniofacial development of humans and mice. Science2005; 310(5751):1184–7. doi: 10.1126/science.111614216293761
33. van den Boogaard MJ, Dorland M, Beemer FA, van Amstel HK, MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans. Nat Genet2000; 24(4):342–3. doi: 10.1038/7415510742093
34. Satokata I, Maas R, Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet1994; 6(4):348–56. doi: 10.1038/ng0494-3487914451
35. Zhang Z, Song Y, Zhao X, Zhang X, Fermin C, Chen Y, Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development2002; 129(17):4135–46. 12163415
36. Catron KM, Iler N, Abate C, Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of three murine homeodomain proteins. Mol Cell Biol1993; 13(4):2354–65. doi: 10.1128/mcb.13.4.23548096059
37. dos Reis M, Zhu T, Yang Z, The impact of the rate prior on Bayesian estimation of divergence times with multiple Loci. Syst Biol2014; 63(4):555–65. doi: 10.1093/sysbio/syu02024658316
38. Lagha M, Bothma JP, Levine M, Mechanisms of transcriptional precision in animal development. Trends Genet2012; 28(8):409–16. doi: 10.1016/j.tig.2012.03.00622513408
39. Spitz F, Furlong EE, Transcription factors: from enhancer binding to developmental control. Nat Rev Genet2012; 13(9):613–26. doi: 10.1038/nrg320722868264
40. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, Pennacchio LA, et al. Deletion of ultraconserved elements yields viable mice. PLoS Biol2007; 5(9):e234. doi: 10.1371/journal.pbio.005023417803355
41. Cretekos CJ, Wang Y, Green ED, Martin JF, Rasweiler IV JJ, Behringer RR, Regulatory divergence modifies limb length between mammals. Genes Dev2008; 22(2):141–51. doi: 10.1101/gad.162040818198333
42. Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L, Splinter E, et al. A regulatory archipelago controls Hox genes transcription in digits. Cell2011; 147(5):1132–45. doi: 10.1016/j.cell.2011.10.02322118467
43. Kemp TS, Mammal-like Reptiles and the Origin of Mammals. London: Academic Press; 1982.
44. Nikaido M, Noguchi H, Nishihara H, Toyoda A, Suzuki Y, Kajitani R, et al. Coelacanth genomes reveal signatures for evolutionary transition from water to land. Genome Res2013; 23(10):1740–48. doi: 10.1101/gr.158105.11323878157
45. Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res2008; 18(11):1752–62. doi: 10.1101/gr.080663.10818682548
46. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Goncalves A, Kutter C, et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell2012; 148(1–2):335–48. doi: 10.1016/j.cell.2011.11.05822244452
47. Lynch VJ, Leclerc RD, May G, Wagner GP, Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet2011; 43(11):1154–9. doi: 10.1038/ng.91721946353
48. Notwell JH, Chung T, Heavner W, Bejerano G, A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat Commun2015; 6:6644. doi: 10.1038/ncomms764425806706
49. Lu X, Sachs F, Ramsay L, Jacques PE, Goke J, Bourque G, et al. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol2014; 21(4):423–5. doi: 10.1038/nsmb.279924681886
50. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, et al. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet2010; 42(7):631–4. doi: 10.1038/ng.60020526341
51. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW, The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development1998; 125(12):2315–25. 9584130
52. Yoshida M, Assimacopoulos S, Jones KR, Grove EA, Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development2006; 133(3):537–45. doi: 10.1242/dev.0220916410414
53. Yagi T, Tokunaga T, Furuta Y, Nada S, Yoshida M, Tsukada T, et al. A novel ES cell line, TT2, with high germline-differentiating potency. Anal Biochem1993; 214(1):70–6. doi: 10.1006/abio.1993.14588250257