Conservation and regulatory associations of a wide affinity range of mouse transcription factor binding sites

Genomics

Volumn 95, Issue 4, 2010, Pages 185-195

  Jaeger, Savina A ^a   Chan, Esther T ^c   Berger, Michael F ^a,d   Stottmann, Rolf ^a   Hughes, Timothy R ^b,c   Bulyk, Martha L ^a,d,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d HARVARD UNIVERSITY   (United States)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Conservation; DNA binding site affinities; Transcription factors, Transcription factor binding sites, Protein binding microarrays

Indexed keywords

TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CPG ISLAND; DNA BINDING; DNA SEQUENCE; GENE EXPRESSION; GENETIC CONSERVATION; GENOME; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CPG ISLANDS; GENE EXPRESSION REGULATION; HUMANS; MICE; PROMOTER REGIONS, GENETIC; PROTEIN ARRAY ANALYSIS; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

METAZOA;

EID: 77950339177     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2010.01.002     Document Type: Article

References (62)

1. Tanay A. Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res. 2006, 16:962-972.
2. Segal E., Raveh-Sadka T., Schroeder M., Unnerstall U., Gaul U. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 2008, 451:535-540.
3. Benos P.V., Bulyk M.L., Stormo G.D. Additivity in protein-DNA interactions: how good an approximation is it. Nucleic Acids Res. 2002, 30:4442-4451.
4. Bulyk M.L., Johnson P.L., Church G.M. Nucleotides of transcription factor binding sites exert interdependent effects on the binding affinities of transcription factors. Nucleic Acids Res. 2002, 30:1255-1261.
5. Man T.K., Stormo G.D. Non-independence of Mnt repressor-operator interaction determined by a new quantitative multiple fluorescence relative affinity (QuMFRA) assay. Nucleic Acids Res. 2001, 29:2471-2478.
6. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., Kuznetsov H., Wang C.F., Coburn D., Newburger D.E., Morris Q., Hughes T.R., Bulyk M.L. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
7. Berger M.F., Philippakis A.A., Qureshi A.M., He F.S., Estep P.W., Bulyk M.L. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat. Biotechnol. 2006, 24:1429-1435.
8. Bulyk M.L., Huang X., Choo Y., Church G.M. Exploring the DNA-binding specificities of zinc fingers with DNA microarrays. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7158-7163.
9. Mukherjee S., Berger M.F., Jona G., Wang X.S., Muzzey D., Snyder M., Young R.A., Bulyk M.L. Rapid analysis of the DNA-binding specificities of transcription factors with DNA microarrays. Nat. Genet. 2004, 36:1331-1339.
10. Maerkl S.J., Quake S.R. A systems approach to measuring the binding energy landscapes of transcription factors. Science 2007, 315:233-237.
11. Berger M.F., Bulyk M.L. Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat. Protoc. 2009, 4:393-411.
12. Bulyk M.L. Computational prediction of transcription-factor binding site locations. Genome Biol. 2003, 5:201.
13. Zhu C., Byers K., McCord R., Shi Z., Berger M., Newburger D., Saulrieta K., Smith Z., Shah M., Radhakrishnan M., Philippakis A., Hu Y., De Masi F., Pacek M., Rolfs A., Murthy T., Labaer J., Bulyk M.L. High-resolution DNA binding specificity analysis of yeast transcription factors. Genome Res. 2009, 19:556-566.
14. Bejerano G., Pheasant M., Makunin I., Stephen S., Kent W.J., Mattick J.S., Haussler D. Ultraconserved elements in the human genome. Science 2004, 304:1321-1325.
15. Xu X., Bieda M., Jin V.X., Rabinovich A., Oberley M.J., Green R., Farnham P.J. A comprehensive ChIP-chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals interchangeable roles of E2F family members. Genome Res. 2007, 17:1550-1561.
16. Saxonov S., Berg P., Brutlag D.L. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1412-1417.
17. Campanero M.R., Armstrong M.I., Flemington E.K. CpG methylation as a mechanism for the regulation of E2F activity. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6481-6486.
18. Bailey P.J., Klos J.M., Andersson E., Karlen M., Kallstrom M., Ponjavic J., Muhr J., Lenhard B., Sandelin A., Ericson J. A global genomic transcriptional code associated with CNS-expressed genes. Exp. Cell Res. 2006, 312:3108-3119.
19. Chiang C.W., Derti A., Schwartz D., Chou M.F., Hirschhorn J.N., Wu C.T. Ultraconserved elements: analyses of dosage sensitivity, motifs and boundaries. Genetics 2008, 180:2277-2293.
20. Pennacchio L.A., Ahituv N., Moses A.M., Prabhakar S., Nobrega M.A., Shoukry M., Minovitsky S., Dubchak I., Holt A., Lewis K.D., Plajzer-Frick I., Akiyama J., De Val S., Afzal V., Black B.L., Couronne O., Eisen M.B., Visel A., Rubin E.M. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
21. Visel A., Prabhakar S., Akiyama J.A., Shoukry M., Lewis K.D., Holt A., Plajzer-Frick I., Afzal V., Rubin E.M., Pennacchio L.A. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 2008, 40:158-160.
22. Guthrie S. Patterning and axon guidance of cranial motor neurons. Nat. Rev. Neurosci. 2007, 8:859-871.
23. Gray P.A., Fu H., Luo P., Zhao Q., Yu J., Ferrari A., Tenzen T., Yuk D.I., Tsung E.F., Cai Z., Alberta J.A., Cheng L.P., Liu Y., Stenman J.M., Valerius M.T., Billings N., Kim H.A., Greenberg M.E., McMahon A.P., Rowitch D.H., Stiles C.D., Ma Q. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 2004, 306:2255-2257.
24. Allen Developing Mouse Brain Atlas., Allen Institute for Brain Science, Seattle, WA., 2009. http://evelopingmouse.brain-map.org.z
25. Jonk L.J., de Jonge M.E., Pals C.E., Wissink S., Vervaart J.M., Schoorlemmer J., Kruijer W. Cloning and expression during development of three murine members of the COUP family of nuclear orphan receptors. Mech. Dev. 1994, 47:81-97.
26. Kurokawa D., Kiyonari H., Nakayama R., Kimura-Yoshida C., Matsuo I., Aizawa S. Regulation of Otx2 expression and its functions in mouse forebrain and midbrain. Development 2004, 131:3319-3331.
27. Suda Y., Hossain Z.M., Kobayashi C., Hatano O., Yoshida M., Matsuo I., Aizawa S. Emx2 directs the development of diencephalon in cooperation with Otx2. Development 2001, 128:2433-2450.
28. George K.M., Leonard M.W., Roth M.E., Lieuw K.H., Kioussis D., Grosveld F., Engel J.D. Embryonic expression and cloning of the murine GATA-3 gene. Development 1994, 120:2673-2686.
29. Nardelli J., Thiesson D., Fujiwara Y., Tsai F.Y., Orkin S.H. Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 1999, 210:305-321.
30. Aubert J., Stavridis M.P., Tweedie S., O'Reilly M., Vierlinger K., Li M., Ghazal P., Pratt T., Mason J.O., Roy D., Smith A. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(Suppl. 1):11836-11841.
31. Purandare S.M., Ware S.M., Kwan K.M., Gebbia M., Bassi M.T., Deng J.M., Vogel H., Behringer R.R., Belmont J.W., Casey B. A complex syndrome of left-right axis, central nervous system and axial skeleton defects in Zic3 mutant mice. Development 2002, 129:2293-2302.
32. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425:917-925.
33. Norton W.H., Mangoli M., Lele Z., Pogoda H.M., Diamond B., Mercurio S., Russell C., Teraoka H., Stickney H.L., Rauch G.J., Heisenberg C.P., Houart C., Schilling T.F., Frohnhoefer H.G., Rastegar S., Neumann C.J., Gardiner R.M., Strahle U., Geisler R., Rees M., Talbot W.S., Wilson S.W. Monorail/Foxa2 regulates floorplate differentiation and specification of oligodendrocytes, serotonergic raphe neurones and cranial motoneurones. Development 2005, 132:645-658.
34. Ferri A.L., Lin W., Mavromatakis Y.E., Wang J.C., Sasaki H., Whitsett J.A., Ang S.L. Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner. Development 2007, 134:2761-2769.
35. Giudicelli F., Gilardi-Hebenstreit P., Mechta-Grigoriou F., Poquet C., Charnay P. Novel activities of Mafb underlie its dual role in hindbrain segmentation and regional specification. Dev. Biol. 2003, 253:150-162.
36. Zhang J., Hagopian-Donaldson S., Serbedzija G., Elsemore J., Plehn-Dujowich D., McMahon A.P., Flavell R.A., Williams T. Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 1996, 381:238-241.
37. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., Lee W., Mendenhall E., O'Donovan A., Presser A., Russ C., Xie X., Meissner A., Wernig M., Jaenisch R., Nusbaum C., Lander E.S., Bernstein B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
38. Asthana S., Roytberg M., Stamatoyannopoulos J.A., Sunyaev S. Analysis of sequence conservation at nucleotide resolution. PLoS Comput. Biol. 2007, 3:e254.
39. Nachman M.W., Crowell S.L. Estimate of the mutation rate per nucleotide in humans. Genetics 2000, 156:297-304.
40. Warner J.B., Philippakis A.A., Jaeger S.A., He F.S., Lin J., Bulyk M.L. Systematic identification of mammalian regulatory motifs' target genes and their functions. Nat. Methods 2008, 5:347-353.
41. Zhang W., Morris Q.D., Chang R., Shai O., Bakowski M.A., Mitsakakis N., Mohammad N., Robinson M.D., Zirngibl R., Somogyi E., Laurin N., Eftekharpour E., Sat E., Grigull J., Pan Q., Peng W.T., Krogan N., Greenblatt J., Fehlings M., van der Kooy D., Aubin J., Bruneau B.G., Rossant J., Blencowe B.J., Frey B.J., Hughes T.R. The functional landscape of mouse gene expression. J. Biol. 2004, 3:21.
42. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000, 25:25-29.
43. Mamane Y., Heylbroeck C., Genin P., Algarte M., Servant M.J., LePage C., DeLuca C., Kwon H., Lin R., Hiscott J. Interferon regulatory factors: the next generation. Gene 1999, 237:1-14.
44. Zhou X., Long J.M., Geyer M.A., Masliah E., Kelsoe J.R., Wynshaw-Boris A., Chien K.R. Reduced expression of the Sp4 gene in mice causes deficits in sensorimotor gating and memory associated with hippocampal vacuolization. Mol. Psychiatry 2005, 10:393-406.
45. Korswagen H.C., Clevers H.C. Activation and repression of wingless/Wnt target genes by the TCF/LEF-1 family of transcription factors. Cold Spring Harb. Symp. Quant. Biol. 1999, 64:141-147.
46. Merrill B.J., Pasolli H.A., Polak L., Rendl M., Garcia-Garcia M.J., Anderson K.V., Fuchs E. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 2004, 131:263-274.
47. Orlov S.V., Kuteykin-Teplyakov K.B., Ignatovich I.A., Dizhe E.B., Mirgorodskaya O.A., Grishin A.V., Guzhova O.B., Prokhortchouk E.B., Guliy P.V., Perevozchikov A.P. Novel repressor of the human FMR1 gene-identification of p56 human (GCC)(n)-binding protein as a Kruppel-like transcription factor ZF5. FEBS J. 2007, 274:4848-4862.
48. Ge W., He F., Kim K.J., Blanchi B., Coskun V., Nguyen L., Wu X., Zhao J., Heng J.I., Martinowich K., Tao J., Wu H., Castro D., Sobeih M.M., Corfas G., Gleeson J.G., Greenberg M.E., Guillemot F., Sun Y.E. Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1319-1324.
49. Odom D.T., Dowell R.D., Jacobsen E.S., Gordon W., Danford T.W., MacIsaac K.D., Rolfe P.A., Conboy C.M., Gifford D.K., Fraenkel E. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat. Genet. 2007, 39:730-732.
50. Berger M.F., Badis G., Gehrke A.R., Talukder S., Philippakis A.A., Pena-Castillo L., Alleyne T.M., Mnaimneh S., Botvinnik O.B., Chan E.T., Khalid F., Zhang W., Newburger D., Jaeger S.A., Morris Q.D., Bulyk M.L., Hughes T.R. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008, 133:1266-1276.
51. C.A. Grove, F. De Masi, I. Barrasa, D.E. Newburger, M.J. Alkema, M.L. Bulyk, and A.J.M. Walhout, A multi-parameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell Cell 138 (2009) 314-327.
52. Cawley S., Bekiranov S., Ng H.H., Kapranov P., Sekinger E.A., Kampa D., Piccolboni A., Sementchenko V., Cheng J., Williams A.J., Wheeler R., Wong B., Drenkow J., Yamanaka M., Patel S., Brubaker S., Tammana H., Helt G., Struhl K., Gingeras T.R. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004, 116:499-509.
53. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigo R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E., Kuehn M.S., Taylor C.M., Neph S., Koch C.M., Asthana S., Malhotra A., Adzhubei I., Greenbaum J.A., Andrews R.M., Flicek P., Boyle P.J., Cao H., Carter N.P., Clelland G.K., Davis S., Day N., Dhami P., Dillon S.C., Dorschner M.O., Fiegler H., Giresi P.G., Goldy J., Hawrylycz M., Haydock A., Humbert R., James K.D., Johnson B.E., Johnson E.M., Frum T.T., Rosenzweig E.R., Karnani N., Lee K., Lefebvre G.C., Navas P.A., Neri F., Parker S.C., Sabo P.J., Sandstrom R., Shafer A., Vetrie D., Weaver M., Wilcox S., Yu M., Collins F.S., Dekker J., Lieb J.D., Tullius T.D., Crawford G.E., Sunyaev S., Noble W.S., Dunham I., Denoeud F., Reymond A., Kapranov P., Rozowsky J., Zheng D., Castelo R., Frankish A., Harrow J., Ghosh S., Sandelin A., Hofacker I.L., Baertsch R., Keefe D., Dike S., Cheng J., Hirsch H.A., Sekinger E.A., Lagarde J., Abril J.F., Shahab A., Flamm C., Fried C., Hackermuller J., Hertel J., Lindemeyer M., Missal K., Tanzer A., Washietl S., Korbel J., Emanuelsson O., Pedersen J.S., Holroyd N., Taylor R., Swarbreck D., Matthews N., Dickson M.C., Thomas D.J., Weirauch M.T., Gilbert J., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816.
54. West A.G., Fraser P. Remote control of gene transcription. Hum. Mol. Genet. 2005, 14(Spec No 1):R101-R111.
55. Ludwig M.Z., Bergman C., Patel N.H., Kreitman M. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 2000, 403:564-567.
56. Philippakis A.A., Busser B.W., Gisselbrecht S.S., He F.S., Estrada B., Michelson A.M., ML B. Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput. Biol. 2006, 2.
57. Siepel A., Bejerano G., Pedersen J.S., Hinrichs A.S., Hou M., Rosenbloom K., Clawson H., Spieth J., Hillier L.W., Richards S., Weinstock G.M., Wilson R.K., Gibbs R.A., Kent W.J., Miller W., Haussler D. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome. Res. 2005, 15:1034-1050.
58. Karolchik E., Baertsch R., Diekhans M., Furey T., Hinrichs A., YT Y.L., Roskin K., Schwartz M., Sugnet C., Thomas D., Weber R., Haussler D., Kent W., Cruz U.o.C.S. The UCSC Genome Browser Database. Nucleic Acids Res. 2003, 31:51-54.
59. Ponty Y., Termier M., Denise A. GenRGenS: software for generating random genomic sequences and structures. Bioinformatics 2006, 22:1534-1535.
60. Margulies E.H., Cooper G.M., Asimenos G., Thomas D.J., Dewey C.N., Siepel A., Birney E., Keefe D., Schwartz A.S., Hou M., Taylor J., Nikolaev S., Montoya-Burgos J.I., Loytynoja A., Whelan S., Pardi F., Massingham T., Brown J.B., Bickel P., Holmes I., Mullikin J.C., Ureta-Vidal A., Paten B., Stone E.A., Rosenbloom K.R., Kent W.J., Bouffard G.G., Guan X., Hansen N.F., Idol J.R., Maduro V.V., Maskeri B., McDowell J.C., Park M., Thomas P.J., Young A.C., Blakesley R.W., Muzny D.M., Sodergren E., Wheeler D.A., Worley K.C., Jiang H., Weinstock G.M., Gibbs R.A., Graves T., Fulton R., Mardis E.R., Wilson R.K., Clamp M., Cuff J., Gnerre S., Jaffe D.B., Chang J.L., Lindblad-Toh K., Lander E.S., Hinrichs A., Trumbower H., Clawson H., Zweig A., Kuhn R.M., Barber G., Harte R., Karolchik D., Field M.A., Moore R.A., Matthewson C.A., Schein J.E., Marra M.A., Antonarakis S.E., Batzoglou S., Goldman N., Hardison R., Haussler D., Miller W., Pachter L., Green E.D., Sidow A. Analyses of deep mammalian sequence alignments and constraint predictions for 1% of the human genome. Genome Res. 2007, 17:760-774.
61. Su A.I., Wiltshire T., Batalov S., Lapp H., Ching K.A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., Cooke M.P., Walker J.R., Hogenesch J.B. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6062-6067.
62. Frey B.J., Dueck D. Clustering by passing messages between data points. Science 2007, 315:972-976.