Whole-genome analysis of muscle founder cells implicates the chromatin regulator Sin3A in muscle identity

Cell Reports

Volumn 8, Issue 3, 2014, Pages 858-870

  Dobi, Krista C ^a   Halfon, Marc S ^b   Baylies, Mary K ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SIN3A;

ALH GENE; ANIMAL CELL; ARTICLE; CELL TRANSFORMATION; CHN GENE; CONTROLLED STUDY; CRP GENE; DEVELOPMENTAL GENE; DROSOPHILA; ELO B GENE; EMBRYO; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOME ANALYSIS; GUG GENE; KDM2 GENE; LID GENE; LOLA GENE; MED13 GENE; MICROARRAY ANALYSIS; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE DISEASE; NOM GENE; NONHUMAN; PRIORITY JOURNAL; SIN3A GENE; SKELETAL MUSCLE; SOMATIC CELL; UPREGULATION;

EID: 84924574417     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.005     Document Type: Article

References (64)

1. Artero, R.D., Castanon, I., and Baylies, M.K. (2001). The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. Development 21, 4251-4264.
2. Artero, R., Furlong, E.E., Beckett, K., Scott, M.P., and Baylies, M. (2003). Notch and Ras signaling pathway effector genes expressed in fusion competent and founder cells during Drosophila myogenesis. Development 130, 6257-6272.
3. Aso, T., and Conrad, M.N. (1997). Molecular cloning of DNAs encoding the regulatory subunits of elongin from Saccharomyces cerevisiae and Drosophila melanogaster. Biochem. Biophys. Res. Commun. 241, 334-340.
4. Baylies, M.K., and Bate, M. (1996). twist: a myogenic switch in Drosophila. Science 272, 1481-1484.
5. Baylies, M.K., and Michelson, A.M. (2001). Invertebrate myogenesis: looking back to the future of muscle development. Curr. Opin. Genet. Dev. 11, 431-439.
6. Baylies, M.K., Bate, M., and Ruiz Gomez, M. (1998). Myogenesis: a view from Drosophila. Cell 93, 921-927.
7. Beckett, K., and Baylies, M.K. (2006). The development of the Drosophila larval body wall muscles. Int. Rev. Neurobiol. 75, 55-70.
8. Boube, M., Faucher, C., Joulia, L., Cribbs, D.L., and Bourbon, H.M. (2000). Drosophila homologs of transcriptional mediator complex subunits are required for adult cell and segment identity specification. Genes Dev. 14, 2906-2917.
9. Bourgouin, C., Lundgren, S.E., and Thomas, J.B. (1992). Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549-561.
10. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
11. Busser, B.W., Shokri, L., Jaeger, S.A., Gisselbrecht, S.S., Singhania, A., Berger, M.F., Zhou, B., Bulyk, M.L., and Michelson, A.M. (2012). Molecular mechanism underlying the regulatory specificity of a Drosophila homeodomain protein that specifies myoblast identity. Development 139, 1164-1174.
12. Campos-Ortega, J.A., and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster (New York: Springer-Verlag).
13. Cardamone, M., Darras, B.T., and Ryan, M.M. (2008). Inherited myopathies and muscular dystrophies. Semin. Neurol. 28, 250-259.
14. Carrasco-Rando, M., Tutor, A.S., Prieto-Sánchez, S., González-Pérez, E., Barrios, N., Letizia, A., Martín, P., Campuzano, S., and Ruiz-Gómez, M. (2011). Drosophila araucan and caupolican integrate intrinsic and signalling inputs for the acquisition by muscle progenitors of the lateral transverse fate. PLoS Genet. 7, e1002186.
15. Cunliffe, V.T. (2008). Eloquent silence: developmental functions of Class I histone deacetylases. Curr. Opin. Genet. Dev. 18, 404-410.
16. Dobi, K.C., Metzger, T., and Baylies, M.K. (2011). Characterization of early steps in muscle morphogenesis in a Drosophila primary culture system. Fly (Austin) 5, 68-75.
17. Dohrmann, C., Azpiazu, N., and Frasch, M. (1990). A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev. 4 (12A), 2098-2111.
18. Doitsidou, M., Flames, N., Topalidou, I., Abe, N., Felton, T., Remesal, L., Popovitchenko, T., Mann, R., Chalfie, M., and Hobert, O. (2013). A combinatorial regulatory signature controls terminal differentiation of the dopaminergic nervous system in C. elegans. Genes Dev. 27, 1391-1405.
19. Duan, H., Zhang, C., Chen, J., Sink, H., Frei, E., and Noll, M. (2007). A key role of Pox meso in somatic myogenesis of Drosophila. Development 134, 3985-3997.
20. Erkner, A., Roure, A., Charroux, B., Delaage, M., Holway, N., Coré, N., Vola, C., Angelats, C., Pagès, F., Fasano, L., and Kerridge, S. (2002). Grunge, related to human Atrophin-like proteins, has multiple functions in Drosophila development. Development 129, 1119-1129.
21. Escudero, L.M., Caminero, E., Schulze, K.L., Bellen, H.J., and Modolell, J. (2005). Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila. Development 132, 1211-1222.
22. Estrada, B., and Michelson, A.M. (2008). A genomic approach to myoblast fusion in Drosophila. Methods Mol. Biol. 475, 299-314.
23. Estrada, B., Choe, S.E., Gisselbrecht, S.S., Michaud, S., Raj, L., Busser, B.W., Halfon, M.S., Church, G.M., and Michelson, A.M. (2006). An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet. 2, e16.
24. Fong, A.P., Yao, Z., Zhong, J.W., Cao, Y., Ruzzo, W.L., Gentleman, R.C., and Tapscott, S.J. (2012). Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev. Cell 22, 721-735.
25. Gildea, J.J., Lopez, R., and Shearn, A. (2000). A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics 156, 645-663.
26. Grzenda, A., Lomberk, G., Zhang, J.-S., and Urrutia, R. (2009). Sin3: master scaffoldandtranscriptional corepressor.Biochim.Biophys. Acta 1789, 443-450.
27. Huang, W., Sherman, B.T., and Lempicki, R.A. (2009a). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13.
28. Huang, W., Sherman, B.T., and Lempicki, R.A. (2009b). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
29. King-Jones, K., Korge, G., and Lehmann, M. (1999). The helix-loop-helix proteins dAP-4 and daughterless bind both in vitro and in vivo to SEBP3 sites required for transcriptional activation of the Drosophila gene Sgs-4. J. Mol. Biol. 291, 71-82.
30. Lagarou, A., Mohd-Sarip, A., Moshkin, Y.M., Chalkley, G.E., Bezstarosti, K., Demmers, J.A.A., and Verrijzer, C.P. (2008). dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev. 22, 2799-2810.
31. Leatherbarrow, J.R., and Halfon, M.S. (2009). Identification of receptor-tyrosinekinase-signaling target genes reveals receptor-specific activities and pathway branchpoints during Drosophila development. Genetics 181, 1335-1345.
32. Lilly, B., Galewsky, S., Firulli, A.B., Schulz, R.A., and Olson, E.N. (1994). D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc. Natl. Acad. Sci. USA 91, 5662-5666.
33. Linder, B., Gerlach, N., and Jäckle, H. (2001). The Drosophila homolog of the human AF10 is an HP1-interacting suppressor of position effect variegation. EMBO Rep. 2, 211-216.
34. Metzger, T., Gache, V., Xu, M., Cadot, B., Folker, E.S., Richardson, B.E., Gomes, E.R., and Baylies, M.K. (2012). MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 484, 120-124.
35. Nguyen, H.T., Bodmer, R., Abmayr, S.M., McDermott, J.C., and Spoerel, N.A. (1994). D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. USA 91, 7520-7524.
36. Nien, C.-Y., Liang, H.-L., Butcher, S., Sun, Y., Fu, S., Gocha, T., Kirov, N., Manak, J.R., and Rushlow, C. (2011). Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLoS Genet. 7, e1002339.
37. Pennetta, G., and Pauli, D. (1998). The Drosophila Sin3 gene encodes a widely distributed transcription factor essential for embryonic viability. Dev. Genes Evol. 208, 531-536.
38. Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
39. Poole, R.J., Bashllari, E., Cochella, L., Flowers, E.B., and Hobert, O. (2011). A Genome-Wide RNAi Screen for Factors Involved in Neuronal Specification in Caenorhabditis elegans. PLoS Genet. 7, e1002109.
40. Puri, P.L., and Sartorelli, V. (2010). HDACs and sirtuins: targets for new pharmacological interventions in human diseases. Pharmacol. Res. 62, 1-2.
41. Richardson, B.E., Beckett, K., Nowak, S.J., and Baylies, M.K. (2007). SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 134, 4357-4367.
42. Rochlin, K., Yu, S., Roy, S., and Baylies, M.K. (2010). Myoblast fusion: when it takes more to make one. Dev. Biol. 341, 66-83.
43. Ruiz-Gómez, M., Romani, S., Hartmann, C., Jäckle, H., and Bate, M. (1997). Specific muscle identities are regulated by Krüppel during Drosophila embryogenesis. Development 124, 3407-3414.
44. Rushton, E., Drysdale, R., Abmayr, S.M., Michelson, A.M., and Bate, M. (1995). Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121, 1979-1988.
45. Sartorelli, V., and Juan, A.H. (2011). Sculpting chromatin beyond the double helix: epigenetic control of skeletal myogenesis. Curr. Top. Dev. Biol. 96, 57-83.
46. Schnorrer, F., Kalchhauser, I., and Dickson, B.J. (2007). The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev. Cell 12, 751-766.
47. Schnorrer, F., Schönbauer, C., Langer, C.C.H., Dietzl, G., Novatchkova, M., Schernhuber, K., Fellner, M., Azaryan, A., Radolf, M., Stark, A., et al. (2010). Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464, 287-291.
48. Seeger, M., Tear, G., Ferres-Marco, D., and Goodman, C.S. (1993). Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
49. Sharma, V., Swaminathan, A., Bao, R., and Pile, L.A. (2008). Drosophila SIN3 is required at multiple stages of development. Dev. Dyn. 237, 3040-3050.
50. Sheeba, C.J., Palmeirim, I., and Andrade, R.P. (2007). Chick Hairy1 protein interacts with Sap18, a component of the Sin3/HDAC transcriptional repressor complex. BMC Dev. Biol. 7, 83.
51. Shi, X., and Garry, D.J. (2012). Sin3 interacts with Foxk1 and regulates myogenic progenitors. Mol. Cell. Biochem. 366, 251-258.
52. Silverstein, R.A., and Ekwall, K. (2005). Sin3: a flexible regulator of global gene expression and genome stability. Curr. Genet. 47, 1-17.
53. Spain, M.M., Caruso, J.A., Swaminathan, A., and Pile, L.A. (2010). Drosophila SIN3 isoforms interact with distinct proteins and have unique biological functions. J. Biol. Chem. 285, 27457-27467.
54. Stapleton, M., Liao, G., Brokstein, P., Hong, L., Carninci, P., Shiraki, T., Hayashizaki, Y., Champe, M., Pacleb, J., Wan, K., et al. (2002). The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res. 12, 1294-1300.
55. Taylor, M.V., Beatty, K.E., Hunter, H.K., and Baylies, M.K. (1995). Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral and heart musculature. Mech. Dev. 50, 29-41.
56. Tixier, V., Bataillé, L., and Jagla, K. (2010). Diversification of muscle types: recent insights from Drosophila. Exp. Cell Res. 316, 3019-3027.
57. Tomancak, P., Beaton, A., Weiszmann, R., Kwan, E., Shu, S., Lewis, S.E., Richards, S., Ashburner, M., Hartenstein, V., Celniker, S.E., and Rubin, G.M. (2002). Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 3, H0088.
58. Tursun, B., Patel, T., Kratsios, P., and Hobert, O. (2011). Direct conversion of C. elegans germ cells into specific neuron types. Science 331, 304-308.
59. van Oevelen, C., Wang, J., Asp, P., Yan, Q., Kaelin, W.G., Jr., Kluger, Y., and Dynlacht, B.D. (2008). A role for mammalian Sin3 in permanent gene silencing. Mol. Cell 32, 359-370.
60. van Oevelen, C., Bowman, C., Pellegrino, J., Asp, P., Cheng, J., Parisi, F., Micsinai, M., Kluger, Y., Chu, A., Blais, A., et al. (2010). The mammalian Sin3 proteins are required for muscle development and sarcomere specification. Mol. Cell. Biol. 30, 5686-5697.
61. Volk, T. (1999). Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet. 15, 448-453.
62. Weake, V.M., Dyer, J.O., Seidel, C., Box, A., Swanson, S.K., Peak, A., Florens, L., Washburn, M.P., Abmayr, S.M., and Workman, J.L. (2011). Post-transcription initiation function of the ubiquitous SAGA complex in tissue-specific gene activation. Genes Dev. 25, 1499-1509.
63. Weinberg, P., Flames, N., Sawa, H., Garriga, G., and Hobert, O. (2013). The SWI/SNF chromatin remodeling complex selectively affects multiple aspects of serotonergic neuron differentiation. Genetics 194, 189-198.
64. Zinzen, R.P., Girardot, C., Gagneur, J., Braun, M., and Furlong, E.E.M. (2009). Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462, 65-70.