A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Tashiro, Kensuke ^a   Teissier, Anne ^b   Kobayashi, Naoki ^a   Nakanishi, Akiko ^a   Sasaki, Takeshi ^a,f   Yan, Kuo ^c   Tarabykin, Victor ^c,h   Vigier, Lisa ^b   Sumiyama, Kenta ^d   Hirakawa, Mika ^e,g   Nishihara, Hidenori ^a   Pierani, Alessandra ^b   Okada, Norihiro ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b CNRS   (France)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^g JT Biohistory Research Hall   (Japan)

^h CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROTEIN SAT2B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BETA GALACTOSIDASE; MATRIX ATTACHMENT REGION BINDING PROTEIN; MESSENGER RNA; SATB2 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CONTROLLED STUDY; CORPUS CALLOSUM; DEVELOPMENTAL STAGE; DNA SEQUENCE; EMBRYO; EMBRYO DEVELOPMENT; GENE LOCUS; MOLECULAR CLONING; MOUSE; NERVE FIBER; NONHUMAN; PERINATAL PERIOD; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHORT INTERSPERSED REPEAT; TELENCEPHALON; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETICS; MAMMAL; METABOLISM; MOLECULAR GENETICS; NERVE CELL; NEWBORN; NUCLEOTIDE SEQUENCE; SYNTENY; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; BASE SEQUENCE; BETA-GALACTOSIDASE; BINDING SITES; CONSERVED SEQUENCE; CORPUS CALLOSUM; EMBRYONIC DEVELOPMENT; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; MAMMALS; MATRIX ATTACHMENT REGION BINDING PROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEURONS; ORGAN SPECIFICITY; RNA, MESSENGER; SHORT INTERSPERSED NUCLEOTIDE ELEMENTS; SYNTENY; TRANSCRIPTION FACTORS;

EID: 82955188747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028497     Document Type: Article

References (73)

1. Singer MF, (1982) SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell 28: 433-434.
2. Okada N, (1991) SINEs. Curr Opin Genet Dev 1: 498-504.
3. Okada N, (1991) SINEs: short interspersed repeated elements of the eucaryotic genome. Trends Ecol Evol 6: 358-361.
4. Deininger PL, Batzer MA, (1993) Evolution of retroposons. In: Heckht MK, editors. Evolutionary biology New York Plenum Publishing. vol. 27 pp. 157-196.
5. Kazazian HH, (2004) Mobile elements: drivers of genome evolution. Science 303: 1626-1632.
6. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
7. Gould SJ, Vrba ES, (1982) Exaptation; a missing term in the science of form. Paleobiology 8: 4-15.
8. Brosius J, Gould SJ, (1992) On "genomenclature": a comprehensive (and respectful) taxonomy for pseudogenes and other "junk DNA". Proc Natl Acad Sci U S A 89: 10706-10710.
9. Ferrigno O, Virolle T, Djabari Z, Ortonne JP, White RJ, et al. (2001) Transposable B2 SINE elements can provide mobile RNA polymerase II promoters. Nat Genet 28: 77-81.
10. Saffer JD, Thurston SJ, (1989) A negative regulatory element with properties similar to those of enhancers is contained within an Alu sequence. Mol Cell Biol 9: 355-364.
11. Hambor JE, Mennone J, Coon ME, Hanke JH, Kavathas P, (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.
12. Norris J, Fan D, Aleman C, Marks JR, Futreal PA, et al. (1995) Identification of a new subclass of Alu DNA repeats which can function as estrogen receptor-dependent transcriptional enhancers. J Biol Chem 270: 22777-22782.
13. Shimamura M, Nikaido M, Ohshima K, Okada N, (1998) A SINE that acquired a role in signal transduction during evolution. Mol Biol Evol 15: 923-925.
14. Lev-Maor G, Sorek R, Shomron N, Ast G, (2003) The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science 300: 1288-1291.
15. Lunyak VV, Prefontaine GG, Nunez E, Cramer T, Ju BG, et al. (2007) Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317: 248-251.
16. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
17. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
18. Boffelli D, McAuliffe J, Ovcharenko D, Lewis KD, Ovcharenko I, et al. (2003) Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299: 1391-1394.
19. Dermitzakis ET, Reymond A, Scamuffa N, Ucla C, Kirkness E, et al. (2003) Evolutionary discrimination of mammalian conserved non-genic sequences (CNGs). Science 302: 1033-1035.
20. Margulies EH, Blanchette M, Haussler D, Green ED, (2003) Identification and characterization of multi-species conserved sequences. Genome Res 13: 2507-2518.
21. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, et al. (2004) Ultraconserved elements in the human genome. Science 304: 1321-1325.
22. Dermitzakis ET, Reymond A, Antonarakis SE, (2005) Conserved non-genic sequences- an unexpected feature of mammalian genomes. Nat Rev Genet 6: 151-157.
23. Thomas JW, Touchman JW, Blakesley RW, Bouffard GG, Beckstrom-Sternberg SM, et al. (2003) Comparative analyses of multi-species sequences from targeted genomic regions. Nature 424: 788-793.
24. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3: e7.
25. Prabhakar S, Poulin F, Shoukry M, Afzal V, Rubin EM, et al. (2006) Close sequence comparisons are sufficient to identify human cis-regulatory elements. Genome Res 16: 855-863.
26. Okada N, Sasaki T, Shimogori T, Nishihara H, (2010) Emergence of mammals by emergency: exaptation. Genes Cells 15: 801-812.
27. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, et al. (2006) In vivo enhancer analysis of human conserved non-coding sequences. Nature 444: 499-502.
28. Visel A, Minovitsky S, Dubchak I, Pennacchio LA, (2007) VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res 35: D88-92.
29. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, et al. (2008) Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet 40: 158-160.
30. Sasaki T, Nishihara H, Hirakawa M, Fujimura K, Tanaka M, et al. (2008) Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci U S A 105: 4220-4225.
31. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A, et al. (2006) A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441: 87-90.
32. Kamal M, Xie X, Lander ES, (2006) A large family of ancient repeat elements in the human genome is under strong selection. Proc Natl Acad Sci U S A 103: 2740-2745.
33. Nishihara H, Smit AF, Okada N, (2006) Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res 16: 864-874.
34. Gentles AJ, Wakefield MJ, Kohany O, Gu W, Batzer MA, et al. (2007) Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 17: 992-1004.
35. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, et al. (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447: 167-177.
36. Lowe CB, Bejerano G, Haussler D, (2007) Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci U S A 104: 8005-8010.
37. Santangelo AM, de Souza FS, Franchini LF, Bumaschny VF, Low MJ, et al. (2007) Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene. PLoS Genet 3: 1813-1826.
38. Biemont C, Vieira C, (2006) Genetics: junk DNA as an evolutionary force. Nature 443: 521-524.
39. Feschotte C, (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9: 397-405.
40. Hirakawa M, Nishihara H, Kanehisa M, Okada N, (2009) Characterization and evolutionary landscape of AmnSINE1 in Amniota genomes. Gene 441: 100-110.
41. Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V, (2005) Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 21: 658-668.
42. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, et al. (2008) Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57: 378-392.
43. Britanova O, Alifragis P, Junek S, Jones K, Gruss P, et al. (2006) A novel mode of tangential migration of cortical projection neurons. Dev Biol 298: 299-311.
44. Dobreva G, Chahrour M, Dautzenberg M, Chirivella L, Kanzler B, et al. (2006) SATB2 is a multifunctional determinant of craniofacial patterning and osteoblast differentiation. Cell 125: 971-986.
45. Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Farinas I, et al. (2008) Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57: 364-377.
46. Bystron I, Blakemore C, Rakic P, (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9: 110-122.
47. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK, (2008) The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18: 28-35.
48. Rakic P, (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10: 724-735.
49. Rattenborg N, Martinez-Gonzalez D, Lesku JA, (2009) Avian sleep homeostasis: Convergent evolution of complex brains, cognition and sleep functions in mammals and birds. Neurosci Biobehav Rev 33: 253-270.
50. Merry DE, Veis DJ, Hickey WF, Korsmeyer SJ, (1994) bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120: 301-311.
51. Price D, Lotto RB, (1996) Influences of the thalamus on the survival of subplate and cortical plate cells. J Neurosci 16: 3247-3255.
52. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, et al. (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45: 207-221.
53. Niquille M, Garel S, Mann F, Hornung JP, Otsmane B, et al. (2009) Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol 7: e1000230.
54. Aboitiz F, Montiel J, (2003) One hundred million years of interhemispheric communication: the history of the corpus callosum. Braz J Med Biol Res 36: 409-420.
55. Granger EM, Masterton RB, Glendenning KK, (1985) Origin of interhemispheric fibers in acallosal opossum (with a comparison to callosal origins in rat). J Comp Neurol 241: 82-98.
56. Donahoo AL, Richards LJ, (2009) Understanding the mechanisms of callosal development through the use of transgenic mouse models. Semin Pediatr Neurol 16: 127-142.
57. Fame RM, MacDonald JL, Macklis JD, (2011) Development, specification, and diversity of callosal projection neurons. Trends Neurosci 34: 41-50.
58. Richards LJ, Plachez C, Ren T, (2004) Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet 66: 276-289.
59. Kamnasaran D, (2005) Agenesis of the corpus callosum: lessons from humans and mice. Clin Invest Med 28: 267-282.
60. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, et al. (2007) Deletion of ultraconserved elements yields viable mice. PLoS Biol 5: e234.
61. Hong JW, Hendrix DA, Levine MS, (2008) Shadow enhancers as a source of evolutionary novelty. Science 321: 1314.
62. Frankel N, Davis GK, Vargas D, Wang S, Payre F, et al. (2010) Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466: 490-493.
63. Ghiasvand NM, Rudolph DD, Mashayekhi M, Brzezinski JA IV, Goldman D, et al. (2011) Deletion of a remote enhancer near ATOH7 disrupts retinal neurogenesis, causing NCRNA disease. Nat Neurosci 14: 578-586.
64. Britten RJ, Davidson EH, (1969) Gene regulation for higher cells: a theory. Science 165: 349-357.
65. Britten RJ, (1996) DNA sequence insertion and evolutionary variation in gene regulation. Proc Natl Acad Sci U S A 93: 9374-9377.
66. Bejerano G, Haussler D, Blanchette M, (2004) Into the heart of darkness: large-scale clustering of human non-coding DNA. Bioinformatics 20: i40-i48.
67. Xie X, Mikkelsen TS, Gnirke A, Lindblad-Toh K, Kellis M, et al. (2007) Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc Natl Acad Sci U S A 104: 7145-7150.
68. McEvilly RJ, de Diaz MO, Schonemann MD, Hooshmand F, Rosenfeld MG, (2002) Transcriptional regulation of cortical neuron migration by POU domain factors. Science 295: 1528-1532.
69. Cook AL, Sturm RA, (2008) POU domain transcription factors: BRN2 as a regulator of melanocytic growth and tumourigenesis. Pigment Cell Melanoma Res 21: 611-626.
70. Sebastiano V, Dalvai M, Gentile L, Schubart K, Sutter J, et al. (2010) Oct1 regulates trophoblast development during early mouse embryogenesis. Development 137: 3551-3560.
71. Kothary R, Clapoff S, Darling S, Perry MD, Moran LA, et al. (1989) Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105: 707-714.
72. Sumiyama K, Irvine SQ, Stock DW, Weiss KM, Kawasaki K, et al. (2002) Genomic structure and functional control of the Dlx3-7 bigene cluster. Proc Natl Acad Sci U S A 99: 780-785.
73. Bielle F, Griveau A, Narboux-Nême N, Vigneau S, Sigrist M, et al. (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8: 1002-1012.