A recent evolutionary change affects a regulatory element in the human FOXP2 gene

Molecular Biology and Evolution

Volumn 30, Issue 4, 2013, Pages 844-852

  Maricic, Tomislav ^a   Günther, Viola ^b   Georgiev, Oleg ^b   Gehre, Sabine ^a   Ćurlin, Marija ^c   Schreiweis, Christiane ^a   Naumann, Ronald ^d   Burbano, Hernán A ^a,h   Meyer, Matthias ^a   Lalueza Fox, Carles ^e   De La Rasilla, Marco ^f   Rosas, Antonio ^g   Gajović, Srećko ^c   Kelso, Janet ^a   Enard, Wolfgang ^a   Schaffner, Walter ^b   Pääbo, Svante ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF ZAGREB   (Croatia)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^e CSIC   (Spain)

^f UNIVERSITY OF OVIEDO   (Spain)

^g MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^h MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

ancient DNA; FOXP2; gene regulation; Neandertals; speech and language

Indexed keywords

NUCLEASE S1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP2; TRANSCRIPTION FACTOR POU3F2; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BINDING SITE; DNA SEQUENCE; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FORKHEAD TRANSCRIPTION FACTORS; GENE FREQUENCY; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; INTRONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEANDERTHALS; POU DOMAIN FACTORS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SEQUENCE ANALYSIS, DNA; TRANSCRIPTIONAL ACTIVATION;

VERTEBRATA;

EID: 84875614116     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss271     Document Type: Article

References (48)

1. Bao L, Zhou M, Cui Y. 2008. CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators. Nucleic Acids Res. 36:D83-D87..
2. Blanchette M, Kent WJ, Riemer C, et al. (12 co-authors). 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14:708-715..
3. Briggs AW, Stenzel U, Johnson PL, et al. (11 co-authors). 2007. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci U S A. 104:14616-14621..
4. Briggs AW, Stenzel U, Meyer M, Krause J, Kircher M, Paabo S. 2010. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 38:e87..
5. Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R, Austin J, Cooper A. 2007. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Res. 35:5717-5728..
6. Burbano HA, Green RE,Maricic T, et al. (10 co-authors). 2012. Analysis of human accelerated DNA regions using archaic hominin genomes. PloS One 7:e32877..
7. Burbano HA, Hodges E, Green RE, et al. (20 co-authors). 2010. Targeted investigation of the Neandertal genome by array-based sequence capture. Science 328:723-725..
8. Cann HM, de Toma C, Cazes L, et al. (41 co-authors). 2002. A human genome diversity cell line panel. Science 296:261-262..
9. Coop G, Bullaughey K, Luca F, Przeworski M. 2008. The timing of selection at the human FOXP2 gene. Mol Biol Evol. 25:1257-1259..
10. de Torres T, Ortiz JE, Grün R, et al. (19 co-authors). 2009. Dating of the hominid (Homo Neanderthalensis) remains accumulation from El Sidrón cave (Pilona, Asturias, North Spain): an example of a multimethodological approach to the dating of upper Pleistocene sites. Archaeometry 52:680-705..
11. Enard W. 2011. FOXP2 and the role of cortico-basal ganglia circuits in speech and language evolution. Curr Opin Neurobiol. 21: 415-424..
12. Enard W, Gehre S, Hammerschmidt K, et al. (56 co-authors). 2009. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137:961-971..
13. Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V, Kitano T, Monaco AP, Paabo S. 2002. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869-872..
14. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol. 460:266-279..
15. Fisher SE, Scharff C. 2009. FOXP2 as a molecular window into speech and language. Trends Genet. 25:166-177..
16. Fortea J, de la Rasilla M, Garcia-Tabernero A, Gigli E, Rosas A, Lalueza-Fox C. 2008. Excavation protocol of bone remains for Neandertal DNA analysis in El Sidron Cave (Asturias, Spain). J HumEvol. 55:353-357..
17. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. 2004. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 32:W273-W279..
18. Gotea V, Visel A, Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I. 2010. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res. 20:565-577..
19. Green RE, Krause J, Briggs AW, et al. (56 co-authors). 2010. A draft sequence of the Neandertal genome. Science 328:710-722..
20. Hagino-Yamagishi K, Saijoh Y, Ikeda M, Ichikawa M, Minamikawa- Tachino R, Hamada H. 1997. Predominant expression of Brn-2 in the postmitotic neurons of the developing mouse neocortex. Brain Res. 752:261-268..
21. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res. 12:996-1006..
22. Kircher M, Stenzel U, Kelso J. 2009. Improved base calling for the Illumina Genome Analyzer using machine learning strategies. Genome Biol. 10:R83..
23. Krause J, Lalueza-Fox C, Orlando L, et al. (13 co-authors). 2007. The derived FOXP2 variant of modern humans was shared with Neandertals. Curr Biol. 17:1908-1912..
24. Kumar S, Hedges SB. 1998. A molecular timescale for vertebrate evolution. Nature 392:917-920..
25. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. 2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:519-523..
26. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760..
27. Li H, Handsaker B, Wysoker A, et al. (10 co-authors). 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079..
28. Meyer M, Kircher M, Gansauge MT, et al. (34 co-authors). 2012. A high-coverage genome sequence from an archaic Denisovan individual. Science 338:222-226..
29. Prabhakar S, Visel A, Akiyama JA, et al. (13 co-authors). 2008. Human-specific gain of function in a developmental enhancer. Science 321:1346-1350..
30. Ptak SE, Enard W, Wiebe V, Hellmann I, Krause J, Lachmann M, Paabo S. 2009. Linkage disequilibrium extends across putative selected sites in FOXP2. Mol Biol Evol. 26:2181-2184..
31. Raab JR, Kamakaka RT. 2010. Insulators and promoters: closer than we think. Nat Rev Genet. 11:439-446..
32. Radtke F, Heuchel R, Georgiev O, Hergersberg M, Gariglio M, Dembic Z, Schaffner W. 1993. Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12:1355-1362..
33. Reich D, Green RE, Kircher M, et al. (28 co-authors). 2010. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053-1060..
34. Reimers-Kipping S, Hevers W, Paabo S, Enard W. 2011. Humanized Foxp2 specifically affects cortico-basal ganglia circuits. Neuroscience 175:75-84..
35. Rhee JM, Gruber CA, Brodie TB, Trieu M, Turner EE. 1998. Highly cooperative homodimerization is a conserved property of neural POU proteins. J Biol Chem. 273:34196-34205..
36. Rohland N, Hofreiter M. 2007. Comparison and optimization of ancient DNA extraction. Biotechniques 42:343-352..
37. Rosas A, Martinez-Maza C, Bastir M, et al. (18 co-authors). 2006. Paleobiology and comparative morphology of a late Neandertal sample from El Sidron, Asturias, Spain. Proc Natl Acad Sci U S A. 103:19266-19271..
38. Schreiber E, Matthias P, Muller MM, Schaffner W. 1988. Identification of a novel lymphoid specific octamer binding protein (OTF-2B) by proteolytic clipping bandshift assay (PCBA). EMBO J. 7:4221-4229..
39. Schreiber E, Matthias P, Muller MM, SchaffnerW. 1989. Rapid detection of octamer binding proteins with "mini-extracts", prepared from a small number of cells. Nucleic Acids Res. 17:6419..
40. Schreiber E, Tobler A, Malipiero U, SchaffnerW, Fontana A. 1993. cDNA cloning of human N-Oct3, a nervous-system specific POU domain transcription factor binding to the octamer DNA motif. Nucleic Acids Res. 21:253-258..
41. Seipel K, Georgiev O, Schaffner W. 1992. Different activation domains stimulate transcription from remote ("enhancer") and proximal ('promoter") positions. EMBO J. 11:4961-4968..
42. Siepel A, Bejerano G, Pedersen JS, et al. (16 co-authors). 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15:1034-1050..
43. Vargha-Khadem F,Watkins K, Alcock K, Fletcher P, Passingham R. 1995. Praxic and nonverbal cognitive deficits in a large family with a genetically transmitted speech and language disorder. Proc Natl Acad Sci U S A. 92:930-933..
44. Visel A, Minovitsky S, Dubchak I, Pennacchio LA. 2007. VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 35:D88-D92..
45. Weaver RF, Weissmann C. 1979. Mapping of RNA by a modification of the Berk-Sharp procedure: the 50 termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 7: 1175-1193..
46. Westin G, Gerster T,Muller MM, Schaffner G, Schaffner W. 1987. OVEC, a versatile system to study transcription in mammalian cells and cell-free extracts. Nucleic Acids Res. 15:6787-6798..
47. Yu F, Keinan A, Chen H, Ferland RJ, Hill RS, Mignault AA, Walsh CA, Reich D. 2009. Detecting natural selection by empirical comparison to random regions of the genome. Hum Mol Genet. 18: 4853-4867..
48. Zhang J,Webb DM, Podlaha O. 2002. Accelerated protein evolution and origins of human-specific features: Foxp2 as an example. Genetics 162:1825-1835..