Distant cis-regulatory elements in human skeletal muscle differentiation

Genomics

Volumn 98, Issue 6, 2011, Pages 401-411

  McCord, Rachel Patton ^a,d   Zhou, Vicky W ^a,c   Yuh, Tiffany ^a,e   Bulyk, Martha L ^a,b,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

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

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD UNIVERSITY   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cis regulatory modules; DNA binding sites; DNA looping interactions; Transcription factors; Transcriptional regulation

Indexed keywords

ALPHA ACTIN; CYTOSKELETON PROTEIN; HISTONE; MYOD PROTEIN; MYOGENIN; PDLIM3 PROTEIN; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE CONTROL; HISTONE MODIFICATION; HUMAN; HUMAN CELL; MUSCLE DEVELOPMENT; MYOBLAST; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN INTERACTION; REGULATORY SEQUENCE; SKELETAL MUSCLE; TRANSCRIPTION INITIATION;

ALGORITHMS; CELL DIFFERENTIATION; CELLS, CULTURED; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; LIM DOMAIN PROTEINS; MICROFILAMENT PROTEINS; MICRORNAS; MUSCLE, SKELETAL; MYOBLASTS, SMOOTH MUSCLE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 81955160676     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2011.08.003     Document Type: Article

References (50)

1. Zhu C., Byers K.J., McCord R.P., Shi Z., Berger M.F., Newburger D.E., Saulrieta K., Smith Z., Shah M.V., Radhakrishnan M., Philippakis A.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.
2. Chua G., Robinson M.D., Morris Q., Hughes T.R. Transcriptional networks: reverse-engineering gene regulation on a global scale. Curr. Opin. Microbiol. 2004, 7:638-646.
3. Davidson E.H. Genomic Regulatory Systems: Development and Evolution 2001, Academic Press, San Diego.
4. Sexton T., Bantignies F., Cavalli G. Genomic interactions: chromatin loops and gene meeting points in transcriptional regulation. Semin. Cell Dev. Biol. 2009, 20:849-855.
5. Kumaran R.I., Thakar R., Spector D.L. Chromatin dynamics and gene positioning. Cell 2008, 132:929-934.
6. Dostie J., Richmond T.A., Arnaout R.A., Selzer R.R., Lee W.L., Honan T.A., Rubio E.D., Krumm A., Lamb J., Nusbaum C., Green R.D., Dekker J. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 2006, 16:1299-1309.
7. Lin Q., Lin L., Zhou J. Chromatin insulator and the promoter targeting sequence modulate the timing of long-range enhancer-promoter interactions in the Drosophila embryo. Dev. Biol. 2010, 339:329-337.
8. Tolhuis B., Palstra R.J., Splinter E., Grosveld F., de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 2002, 10:1453-1465.
9. Vakoc C.R., Letting D.L., Gheldof N., Sawado T., Bender M.A., Groudine M., Weiss M.J., Dekker J., Blobel G.A. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol. Cell 2005, 17:453-462.
10. Cao Y., Kumar R.M., Penn B.H., Berkes C.A., Kooperberg C., Boyer L.A., Young R.A., Tapscott S.J. Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J. 2006, 25:502-511.
11. Blais A., Tsikitis M., Acosta-Alvear D., Sharan R., Kluger Y., Dynlacht B.D. An initial blueprint for myogenic differentiation. Genes Dev. 2005, 19:553-569.
12. 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 functions. Nat. Methods 2008, 5:347-353.
13. Bergstrom D.A., Penn B.H., Strand A., Perry R.L., Rudnicki M.A., Tapscott S.J. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell 2002, 9:587-600.
14. Cao Y., Yao Z., Sarkar D., Lawrence M., Sanchez G.J., Parker M.H., MacQuarrie K.L., Davison J., Morgan M.T., Ruzzo W.L., Gentleman R.C., Tapscott S.J. Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev. Cell 2010, 18:662-674.
15. Berkes C.A., Tapscott S.J. MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol. 2005, 16:585-595.
16. Gianakopoulos P.J., Mehta V., Voronova A., Cao Y., Yao Z., Coutu J., Wang X., Waddington M.S., Tapscott S.J., Skerjanc I.S. MyoD directly up-regulates premyogenic mesoderm factors during induction of skeletal myogenesis in stem cells. J. Biol. Chem. 2011, 286:2517-2525.
17. Thompson W., Palumbo M.J., Wasserman W.W., Liu J.S., Lawrence C.E. Decoding human regulatory circuits. Genome Res. 2004, 14:1967-1974.
18. Sun Q., Chen G., Streb J.W., Long X., Yang Y., Stoeckert C.J., Miano J.M. Defining the mammalian CArGome. Genome Res. 2006, 16:197-207.
19. Frith M.C., Spouge J.L., Hansen U., Weng Z. Statistical significance of clusters of motifs represented by position specific scoring matrices in nucleotide sequences. Nucleic Acids Res. 2002, 30:3214-3224.
20. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., Wang W., Weng Z., Green R.D., Crawford G.E., Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
21. Berman B.P., Nibu Y., Pfeiffer B.D., Tomancak P., Celniker S.E., Levine M., Rubin G.M., Eisen M.B. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:757-762.
22. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., Afzal V., Ren B., Rubin E.M., Pennacchio L.A. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
23. Ernst J., Kheradpour P., Mikkelsen T.S., Shoresh N., Ward L.D., Epstein C.B., Zhang X., Wang L., Issner R., Coyne M., Ku M., Durham T., Kellis M., Bernstein B.E. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49.
24. Guenther M.G., Levine S.S., Boyer L.A., Jaenisch R., Young R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130:77-88.
25. Chickering D.M. The WinMine Toolkit, in, Microsoft 2002.
26. Heckerman D., Chickering D.M., Meek C., Rounthwaite R., Kadie C. Dependency networks for inference, collaborative filtering, and data visualization. J. Mach. Learn. Res. 2000, 1:49-75.
27. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:D152-157.
28. Chen J.F., Mandel E.M., Thomson J.M., Wu Q., Callis T.E., Hammond S.M., Conlon F.L., Wang D.Z. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 2006, 38:228-233.
29. Chen Y., Gelfond J., McManus L.M., Shireman P.K. Temporal microRNA expression during in vitro myogenic progenitor cell proliferation and differentiation: regulation of proliferation by miR-682. Physiol. Genomics 2010, 43:621-630.
30. Hosoda T., Zheng H., Cabral-da-Silva M., Sanada F., Ide-Iwata N., Ogorek B., Ferreira-Martins J., Arranto C., D'Amario D., Del Monte F., Urbanek K., D'Alessandro D.A., Michler R.E., Anversa P., Rota M., Kajstura J., Leri A. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 2011, 123:1287-1296.
31. van Rooij E., Quiat D., Johnson B.A., Sutherland L.B., Qi X., Richardson J.A., Kelm R.J., Olson E.N. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell 2009, 17:662-673.
32. Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311.
33. Hagege H., Klous P., Braem C., Splinter E., Dekker J., Cathala G., de Laat W., Forne T. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2007, 2:1722-1733.
34. Pomies P., Pashmforoush M., Vegezzi C., Chien K.R., Auffray C., Beckerle M.C. The cytoskeleton-associated PDZ-LIM protein, ALP, acts on serum response factor activity to regulate muscle differentiation. Mol. Biol. Cell 2007, 18:1723-1733.
35. Dean A. In the loop: long range chromatin interactions and gene regulation. Brief. Funct. Genomics 2011, 10:3-10.
36. Heintzman N.D., Hon G.C., Hawkins R.D., Kheradpour P., Stark A., Harp L.F., Ye Z., Lee L.K., Stuart R.K., Ching C.W., Ching K.A., Antosiewicz-Bourget J.E., Liu H., Zhang X., Green R.D., Lobanenkov V.V., Stewart R., Thomson J.A., Crawford G.E., Kellis M., Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
37. Gerstein M.B., Lu Z.J., Van Nostrand E.L., Cheng C., Arshinoff B.I., Liu T., Yip K.Y., Robilotto R., Rechtsteiner A., Ikegami K., Alves P., Chateigner A., Perry M., Morris M., Auerbach R.K., Feng X., Leng J., Vielle A., Niu W., Rhrissorrakrai K., Agarwal A., Alexander R.P., Barber G., Brdlik C.M., Brennan J., Brouillet J.J., Carr A., Cheung M.S., Clawson H., Contrino S., Dannenberg L.O., Dernburg A.F., Desai A., Dick L., Dose A.C., Du J., Egelhofer T., Ercan S., Euskirchen G., Ewing B., Feingold E.A., Gassmann R., Good P.J., Green P., Gullier F., Gutwein M., Guyer M.S., Habegger L., Han T., Henikoff J.G., Henz S.R., Hinrichs A., Holster H., Hyman T., Iniguez A.L., Janette J., Jensen M., Kato M., Kent W.J., Kephart E., Khivansara V., Khurana E., Kim J.K., Kolasinska-Zwierz P., Lai E.C., Latorre I., Leahey A., Lewis S., Lloyd P., Lochovsky L., Lowdon R.F., Lubling Y., Lyne R., MacCoss M., Mackowiak S.D., Mangone M., McKay S., Mecenas D., Merrihew G., Miller D.M., Muroyama A., Murray J.I., Ooi S.L., Pham H., Phippen T., Preston E.A., Rajewsky N., Ratsch G., Rosenbaum H., Rozowsky J., Rutherford K., Ruzanov P., Sarov M., Sasidharan R., Sboner A., Scheid P., Segal E., Shin H., Shou C., Slack F.J., Slightam C., Smith R., Spencer W.C., Stinson E.O., Taing S., Takasaki T., Vafeados D., Voronina K., Wang G., Washington N.L., Whittle C.M., Wu B., Yan K.K., Zeller G., Zha Z., Zhong M., Zhou X., Ahringer J., Strome S., Gunsalus K.C., Micklem G., Liu X.S., Reinke V., Kim S.K., Hillier L.W., Henikoff S., Piano F., Snyder M., Stein L., Lieb J.D., Waterston R.H. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2010, 330:1775-1787.
38. Moorman C., Sun L.V., Wang J., de Wit E., Talhout W., Ward L.D., Greil F., Lu X.J., White K.P., Bussemaker H.J., van Steensel B. Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12027-12032.
39. Phillips J.E., Corces V.G. CTCF: master weaver of the genome. Cell 2009, 137:1194-1211.
40. Hakim O., Sung M.H., Voss T.C., Splinter E., John S., Sabo P.J., Thurman R.E., Stamatoyannopoulos J.A., de Laat W., Hager G.L. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 2011, 21:697-706.
41. Heintzman N.D., Ren B. Finding distal regulatory elements in the human genome. Curr. Opin. Genet. Dev. 2009, 19:541-549.
42. Dejardin J., Kingston R.E. Purification of proteins associated with specific genomic Loci. Cell 2009, 136:175-186.
43. Ni Z., Abou El Hassan M., Xu Z., Yu T., Bremner R. The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers. Nat. Immunol. 2008, 9:785-793.
44. Rajapakse I., Perlman M.D., Scalzo D., Kooperberg C., Groudine M., Kosak S.T. The emergence of lineage-specific chromosomal topologies from coordinate gene regulation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6679-6684.
45. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
46. Harris M.A., Clark J., Ireland A., Lomax J., Ashburner M., Foulger R., Eilbeck K., Lewis S., Marshall B., Mungall C., Richter J., Rubin G.M., Blake J.A., Bult C., Dolan M., Drabkin H., Eppig J.T., Hill D.P., Ni L., Ringwald M., Balakrishnan R., Cherry J.M., Christie K.R., Costanzo M.C., Dwight S.S., Engel S., Fisk D.G., Hirschman J.E., Hong E.L., Nash R.S., Sethuraman A., Theesfeld C.L., Botstein D., Dolinski K., Feierbach B., Berardini T., Mundodi S., Rhee S.Y., Apweiler R., Barrell D., Camon E., Dimmer E., Lee V., Chisholm R., Gaudet P., Kibbe W., Kishore R., Schwarz E.M., Sternberg P., Gwinn M., Hannick L., Wortman J., Berriman M., Wood V., de la Cruz N., Tonellato P., Jaiswal P., Seigfried T., White R. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 2004, 32:D258-261.
47. Lee T.I., Johnstone S.E., Young R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 2006, 1:729-748.
48. Buck M.J., Nobel A.B., Lieb J.D. ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol. 2005, 6:R97.
49. Wasserman W.W., Palumbo M., Thompson W., Fickett J.W., Lawrence C.E. Human-mouse genome comparisons to locate regulatory sites. Nat. Genet. 2000, 26:225-228.
50. Dekker J. The three 'C' s of chromosome conformation capture: controls, controls, controls. Nat. Methods 2006, 3:17-21.