Microfluidic affinity and ChIP-seq analyses converge on a conserved FOXP2-binding motif in chimp and human, which enables the detection of evolutionarily novel targets

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 5991-6004

  Nelson, Christopher S ^a   Fuller, Chris K ^a   Fordyce, Polly M ^a,b   Greninger, Alexander L ^a   Li, Hao ^a   DeRisi, Joseph L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR FOXP2;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE IDENTIFICATION; MICROFLUIDIC ANALYSIS; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CONSERVED SEQUENCE; DNA; EVOLUTION, MOLECULAR; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MUTATION; NUCLEOTIDE MOTIFS; PAN TROGLODYTES; SEQUENCE ANALYSIS, DNA;

EID: 84880213877     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt259     Document Type: Article

References (57)

1. Scharff, C. and Petri, J. (2011) Evo-devo, deep homology and FoxP2: implications for the evolution of speech and language. Philos. Trans. R Soc. Lond. B Biol. Sci., 366, 2124-2140.
2. Lai, C.S., Fisher, S.E., Hurst, J.A., Vargha-Khadem, F. and Monaco, A.P. (2001) A forkhead-domain gene is mutated in a severe speech and language disorder. Nature, 413, 519-523.
3. Fisher, S.E., Vargha-Khadem, F., Watkins, K.E., Monaco, A.P. and Pembrey, M.E. (1998) Localisation of a gene implicated in a severe speech and language disorder. Nat. Genet., 18, 168-170.
4. Stroud, J.C., Wu, Y., Bates, D.L., Han, A., Nowick, K., Paabo, S., Tong, H. and Chen, L. (2006) Structure of the forkhead domain of FOXP2 bound to DNA. Structure, 14, 159-166.
5. Wu, Y., Borde, M., Heissmeyer, V., Feuerer, M., Lapan, A.D., Stroud, J.C., Bates, D.L., Guo, L., Han, A., Ziegler, S.F. et al. (2006) FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell, 126, 375-387.
6. Shu, W., Yang, H., Zhang, L., Lu, M.M. and Morrisey, E.E. (2001) Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors. J. Biol. Chem., 276, 27488-27497.
7. MacDermot, K.D., Bonora, E., Sykes, N., Coupe, A.M., Lai, C.S.L., Vernes, S.C., Vargha-Khadem, F., McKenzie, F., Smith, R.L., Monaco, A.P. et al. (2005) Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am. J. Hum. Genet., 76, 1074-1080.
8. Hurst, J.A., Baraitser, M., Auger, E., Graham, F. and Norell, S. (1990) An extended family with a dominantly inherited speech disorder. Dev. Med. Child. Neurol., 32, 352-355.
9. Zhang, J., Webb, D.M. and Podlaha, O. (2002) Accelerated protein evolution and origins of human-specific features: Foxp2 as an example. Genetics, 162, 1825-1835.
10. Enard, W., Przeworski, M., Fisher, S.E., Lai, C.S.L., Wiebe, V., Kitano, T., Monaco, A.P. and Paabo, S. (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature, 418, 869-872.
11. Yu, F., Keinan, A., Chen, H., Ferland, R.J., Hill, R.S., Mignault, A.A., Walsh, C.A. and Reich, D. (2009) Detecting natural selection by empirical comparison to random regions of the genome. Hum. Mol. Genet., 18, 4853-4867.
12. Shu, W., Cho, J.Y., Jiang, Y., Zhang, M., Weisz, D., Elder, G.A., Schmeidler, J., De Gasperi, R., Sosa, M.A.G., Rabidou, D. et al. (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc. Natl Acad. Sci. USA, 102, 9643-9648.
13. Haesler, S., Rochefort, C., Georgi, B., Licznerski, P., Osten, P. and Scharff, C. (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol., 5, e321.
14. Enard, W., Gehre, S., Hammerschmidt, K., Holter, S.M., Blass, T., Somel, M., Bruckner, M.K., Schreiweis, C., Winter, C., Sohr, R. et al. (2009) A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell, 137, 961-971.
15. Schubert, L.A., Jeffery, E., Zhang, Y., Ramsdell, F. and Ziegler, S.F. (2001) Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation. J. Biol. Chem., 276, 37672-37679.
16. Wang, B., Lin, D., Li, C. and Tucker, P. (2003) Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J. Biol. Chem., 278, 24259-24268.
17. Vernes, S.C., Spiteri, E., Nicod, J., Groszer, M., Taylor, J.M., Davies, K.E., Geschwind, D.H. and Fisher, S.E. (2007) High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am. J. Hum. Genet., 81, 1232-1250.
18. Maerkl, S.J. and Quake, S.R. (2007) A systems approach to measuring the binding energy landscapes of transcription factors. Science, 315, 233-237.
19. Fordyce, P.M., Gerber, D., Tran, D., Zheng, J., Li, H., DeRisi, J.L. and Quake, S.R. (2010) De novo identification and biophysical characterization of transcription-factor binding sites with microfluidic affinity analysis. Nat. Biotechnol., 28, 970-975.
20. Edelheit, O., Hanukoglu, A. and Hanukoglu, I. (2009) Simple and efficient site-directed mutagenesis using two single-primer reactions in parallel to generate mutants for protein structure-function studies. BMC Biotechnol., 9, 61.
21. Vernes, S.C., Nicod, J., Elahi, F.M., Coventry, J.A., Kenny, N., Coupe, A.M., Bird, L.E., Davies, K.E. and Fisher, S.E. (2006) Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum. Mol. Genet., 15, 3154-3167.
22. Khare, S.D., Ding, F., Gwanmesia, K.N. and Dokholyan, N.V. (2005) Molecular origin of polyglutamine aggregation in neurodegenerative diseases. PLoS Comput. Biol., 1, 230-235.
23. Ross, C.A. (2002) Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron, 35, 819-822.
24. Fordyce, P.M., Pincus, D., Kimmig, P., Nelson, C.S., El-Samad, H., Walter, P. and DeRisi, J.L. (2012) Basic leucine zipper transcription factor Hac1 binds DNA in two distinct modes as revealed by microfluidic analyses. Proc. Natl Acad. Sci. USA, 109, E3084-E3093.
25. Mintseris, J. and Eisen, M.B. (2006) Design of a combinatorial DNA microarray for protein-DNA interaction studies. BMC Bioinformatics, 7, 429.
26. Wu, R.Z., Chaivorapol, C., Zheng, J., Li, H. and Liang, S. (2007) fREDUCE: detection of degenerate regulatory elements using correlation with expression. BMC Bioinformatics, 8, 399.
27. Foat, B.C., Morozov, A.V. and Bussemaker, H.J. (2006) Statistical mechanical modeling of genome-wide transcription factor occupancy data by MatrixREDUCE. Bioinformatics, 22, e141-e149.
28. Marticke, S. (2008) Ultra-high Throughput Sequencing Analysis of Foxp2 Occupancy In the Human Genome, Doctoral Thesis. Stanford University. Retrieved from Proquest. http://proquest. umi.com/pqdweb?RQT=305&attempt=1&skip= 1&SQ= STYPE%28dissertation%29+AND+ISBN%289780549847847% 29&cfc=1 (2 April 2013, date last accessed).
29. Valouev, A., Johnson, D.S., Sundquist, A., Medina, C., Anton, E., Batzoglou, S., Myers, R.M. and Sidow, A. (2008) Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods, 5, 829-834.
30. Hochberg, Y. and Benjamini, Y. (1990) More powerful procedures for multiple significance testing. Stat. Med., 9, 811-818.
31. Bailey, T.L. and Elkan, C. (1995) The value of prior knowledge in discovering motifs with MEME. Proc. Int. Conf. Intell. Syst. Mol. Biol., 3, 21-29.
32. Gordon, D.B., Nekludova, L., McCallum, S. and Fraenkel, E. (2005) TAMO: a flexible, object-oriented framework for analyzing transcriptional regulation using DNA-sequence motifs. Bioinformatics, 21, 3164-3165.
33. Schroeder, D.I. and Myers, R.M. (2008) Multiple transcription start sites for FOXP2 with varying cellular specificities. Gene, 413, 42-48.
34. Schneider, T.D., Stormo, G.D., Gold, L. and Ehrenfeucht, A. (1986) Information content of binding sites on nucleotide sequences. J. Mol. Biol., 188, 415-431.
35. Chokas, A.L., Trivedi, C.M., Lu, M.M., Tucker, P.W., Li, S., Epstein, J.A. and Morrisey, E.E. (2010) Foxp1/2/4-NuRD interactions regulate gene expression and epithelial injury response in the lung via regulation of interleukin-6. J. Biol. Chem., 285, 13304-13313.
36. Li, S., Weidenfeld, J. and Morrisey, E.E. (2004) Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions. Mol. Cell. Biol., 24, 809-822.
37. Yang, Z., Hikosaka, K., Sharkar, M.T.K., Tamakoshi, T., Chandra, A., Wang, B., Itakura, T., Xue, X., Uezato, T., Kimura, W. et al. (2010) The mouse forkhead gene Foxp2 modulates expression of the lung genes. Life Sci., 87, 17-25.
38. Pollard, K.S., Hubisz, M.J., Rosenbloom, K.R. and Siepel, A. (2009) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res., 20, 110-121.
39. Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S. et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res., 15, 1034-1050.
40. Yoshima, T., Yura, T. and Yanagi, H. (1998) Novel testis-specific protein that interacts with heat shock factor 2. Gene, 214, 139-146.
41. Kallio, M., Chang, Y., Manuel, M., Alastalo, T.-P., Rallu, M., Gitton, Y., Pirkkala, L., Loones, M.-T., Paslaru, L., Larney, S. et al. (2002) Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice. EMBO J., 21, 2591-2601.
42. Kim, E., Lowenson, J.D., MacLaren, D.C., Clarke, S. and Young, S.G. (1997) Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc. Natl Acad. Sci USA, 94, 6132-6137.
43. Yamamoto, A., Takagi, H., Kitamura, D., Tatsuoka, H., Nakano, H., Kawano, H., Kuroyanagi, H., Yahagi, Y., Kobayashi, S., Koizumi, K. et al. (1998) Deficiency in protein L-isoaspartyl methyltransferase results in a fatal progressive epilepsy. J. Neurosci., 18, 2063-2074.
44. Bennett, M.V.L. and Zukin, R.S. (2004) Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron, 41, 495-511.
45. Blankenship, A.G., Hamby, A.M., Firl, A., Vyas, S., Maxeiner, S., Willecke, K. and Feller, M.B. (2011) The role of neuronal connexins 36 and 45 in shaping spontaneous firing patterns in the developing retina. J. Neurosci., 31, 9998-10008.
46. Del Castillo, F.J., Cohen-Salmon, M., Charollais, A., Caille, D., Lampe, P.D., Chavrier, P., Meda, P. and Petit, C. (2009) Consortin, a trans-Golgi network cargo receptor for the plasma membrane targeting and recycling of connexins. Hum. Mol. Genet., 19, 262-275.
47. Saab, B.J., Georgiou, J., Nath, A., Lee, F.J.S., Wang, M., Michalon, A., Liu, F., Mansuy, I.M. and Roder, J.C. (2009) NCS-1 in the dentate gyrus promotes exploration, synaptic plasticity, and rapid acquisition of spatial memory. Neuron, 63, 643-656.
48. Yip, P.K., Wong, L.F., Sears, T.A., Yanez-Munoz, R.J. and McMahon, S.B. (2010) Cortical overexpression of neuronal calcium sensor-1 induces functional plasticity in spinal cord following unilateral pyramidal tract injury in rat. PLoS Biol., 8, e1000399.
49. Pierrou, S., Hellqvist, M., Samuelsson, L., Enerback, S. and Carlsson, P. (1994) Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J., 13, 5002-5012.
50. Nirula, A., Moore, D.J. and Gaynor, R.B. (1997) Constitutive binding of the transcription factor interleukin-2 (IL-2) enhancer binding factor to the IL-2 promoter. J. Biol. Chem., 272, 7736-7745.
51. Gardiner-Garden, M. and Frommer, M. (1987) CpG islands in vertebrate genomes. J. Mol. Biol., 196, 261-282.
52. Vernes, S.C., Oliver, P.L., Spiteri, E., Lockstone, H.E., Puliyadi, R., Taylor, J.M., Ho, J., Mombereau, C., Brewer, A., Lowy, E. et al. (2011) Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS Genet., 7, e1002145.
53. Bhattacharya, S., Michels, C.L., Leung, M.K., Arany, Z.P., Kung, A.L. and Livingston, D.M. (1999) Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev., 13, 64-75.
54. Barthel, A., Schmoll, D. and Unterman, T.G. (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab., 16, 183-189.
55. Bacon, C. and Rappold, G.A. (2012) The distinct and overlapping phenotypic spectra of FOXP1 and FOXP2 in cognitive disorders. Hum. Genet., 131, 1687-1698.
56. Shu, W., Lu, M.M., Zhang, Y., Tucker, P.W., Zhou, D. and Morrisey, E.E. (2007) Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development, 134, 1991-2000.
57. Konopka, G., Friedrich, T., Davis-Turak, J., Winden, K., Oldham, M.C., Gao, F., Chen, L., Wang, G.-Z., Luo, R., Preuss, T.M. et al. (2012) Human-specific transcriptional networks in the brain. Neuron, 75, 601-617.