Akirin links twist-regulated transcription with the brahma chromatin remodeling complex during embryogenesis

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Nowak, Scott J ^a,d   Aihara, Hitoshi ^b,e   Gonzalez, Katie ^c,f   Nibu, Yutaka ^b,c   Baylies, Mary K ^a,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

^d KENNESAW STATE UNIVERSITY   (United States)

^e NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^f Molecular Diagnostic Services   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKIRIN; BRM PROTEIN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; AKIRIN1 PROTEIN, DROSOPHILA; BRM PROTEIN, DROSOPHILA; CELL CYCLE PROTEIN; DROSOPHILA PROTEIN; MEF2 PROTEIN, DROSOPHILA; MYOGENIC FACTOR; NONHISTONE PROTEIN; SWI SNF B CHROMATIN REMODELING COMPLEX; SWI-SNF-B CHROMATIN-REMODELING COMPLEX; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TWI PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; MALE; MESODERM; MUSCLE DEVELOPMENT; MUSCLE DISEASE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; ANIMAL; CONGENITAL MALFORMATION; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUSCLE; MUTATION; PHENOTYPE; PRENATAL DEVELOPMENT;

DROSOPHILA MELANOGASTER;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC DEVELOPMENT; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUSCLES; MUTATION; MYOGENIC REGULATORY FACTORS; PHENOTYPE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR;

EID: 84859242345     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002547     Document Type: Article

References (75)

1. Barnes RM, Firulli AB, (2009) A twist of insight- the role of Twist-family bHLH factors in development. The International Journal of Developmental Biology 53: 909-924.
2. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
3. Miraoui H, Marie PJ, (2010) Pivotal role of Twist in skeletal biology and pathology. Gene 468: 1-7.
4. Baylies MK, Bate M, (1996) twist: a myogenic switch in Drosophila. Science 272: 1481-1484.
5. Bernard F, Krejci A, Housden B, Adryan B, Bray SJ, (2010) Specificity of Notch pathway activation: Twist controls the transcriptional output in adult muscle progenitors. Development.
6. Castanon I, Baylies MK, (2002) A Twist in fate: evolutionary comparison of Twist structure and function. Gene 287: 11-22.
7. Leptin M, (1991) twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes & Development 5: 1568-1576.
8. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, et al. (2007) A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes & Development 21: 436-449.
9. Zeitlinger J, Zinzen RP, Stark A, Kellis M, Zhang H, et al. (2007) Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes & Development 21: 385-390.
10. Castanon I, von Stetina S, Kass J, Baylies MK, (2001) Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128: 3145-3159.
11. Wong M-C, Castanon I, Baylies MK, (2008) Daughterless dictates Twist activity in a context-dependent manner during somatic myogenesis. Developmental Biology 317: 417-429.
12. González-Crespo S, Levine M, (1993) Interactions between dorsal and helix-loop-helix proteins initiate the differentiation of the embryonic mesoderm and neuroectoderm in Drosophila. Genes & Development 7: 1703-1713.
13. Jiang J, Kosman D, Ip YT, Levine M, (1991) The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes & Development 5: 1881-1891.
14. Shirokawa JM, Courey AJ, (1997) A direct contact between the dorsal rel homology domain and Twist may mediate transcriptional synergy. Molecular and Cellular Biology 17: 3345-3355.
15. Clapier CR, Cairns BR, (2009) The Biology of Chromatin Remodeling Complexes. Annual Review of Biochemistry 78: 273-304.
16. Mohrmann L, Verrijzer CP, (2005) Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochimica et Biophysica Acta 1681: 59-73.
17. Brizuela BJ, Elfring L, Ballard J, Tamkun JW, Kennison JA, (1994) Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics 137: 803-813.
18. Brizuela BJ, Kennison JA, (1997) The Drosophila homeotic gene moira regulates expression of engrailed and HOM genes in imaginal tissues. Mechanisms of Development 65: 209-220.
19. Collins RT, Furukawa T, Tanese N, Treisman JE, (1999) Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. The EMBO journal 18: 7029-7040.
20. Crosby MA, Miller C, Alon T, Watson KL, Verrijzer CP, et al. (1999) The trithorax group gene moira encodes a brahma-associated putative chromatin-remodeling factor in Drosophila melanogaster. Molecular and Cellular Biology 19: 1159-1170.
21. Elfring LK, Daniel C, Papoulas O, Deuring R, Sarte M, et al. (1998) Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 148: 251-265.
22. Treisman JE, Luk A, Rubin GM, Heberlein U, (1997) eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins. Genes & Development 11: 1949-1962.
23. Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, et al. (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. The EMBO journal 21: 5245-5254.
24. Chalkley GE, Moshkin YM, Langenberg K, Bezstarosti K, Blastyak A, et al. (2008) The Transcriptional Coactivator SAYP Is a Trithorax Group Signature Subunit of the PBAP Chromatin Remodeling Complex. Molecular and Cellular Biology 28: 2920-2929.
25. Carrera I, Zavadil J, Treisman JE, (2008) Two subunits specific to the PBAP chromatin remodeling complex have distinct and redundant functions during drosophila development. Molecular and Cellular Biology 28: 5238-5250.
26. Collins RT, Treisman JE, (2000) Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes & Development 14: 3140-3152.
27. Rendina R, Strangi A, Avallone B, Giordano E, (2010) Bap170, a Subunit of the Drosophila PBAP Chromatin Remodeling Complex, Negatively Regulates the Egfr Signaling. Genetics.
28. Carrera I, Treisman JE, (2008) Message in a nucleus: signaling to the transcriptional machinery. Current Opinion in Genetics & Development 18: 397-403.
29. Goto A, Matsushita K, Gesellchen V, el Chamy L, Kuttenkeuler D, et al. (2008) Akirins are highly conserved nuclear proteins required for NF-kappaB-dependent gene expression in drosophila and mice. Nature Immunology 9: 97-104.
30. Marshall A, Salerno MS, Thomas M, Davies T, Berry C, et al. (2008) Mighty is a novel promyogenic factor in skeletal myogenesis. Experimental Cell Research 314: 1013-1029.
31. Yu Y, Yussa M, Song J, Hirsch J, Pick L, (1999) A double interaction screen identifies positive and negative ftz gene regulators and ftz-interacting proteins. Mechanisms of Development 83: 95-105.
32. Gonzalez K, Baylies M, (2005) bhringi: A novel Twist co-regulator. Program and Abstracts 46th Annual Drosophila Research Conference, San Diego, CA, 2005 pp. 320B.
33. Cripps RM, Black BL, Zhao B, Lien CL, Schulz RA, et al. (1998) The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by Twist during Drosophila myogenesis. Genes & Development 12: 422-434.
34. Yin Z, Xu XL, Frasch M, (1997) Regulation of the twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124: 4971-4982.
35. Macqueen DJ, Johnston IA, (2009) Evolution of the multifaceted eukaryotic akirin gene family. BMC Evolutionary Biology 9: 34.
36. Bate M, (1990) The embryonic development of larval muscles in Drosophila. Development 110: 791-804.
37. Chou TB, Perrimon N, (1996) The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144: 1673-1679.
38. Bulchand S, Menon SD, George SE, Chia W, (2010) Muscle wasted: a novel component of the Drosophila histone locus body required for muscle integrity. Journal of Cell Science 123: 2697-2707.
39. Simpson P, (1983) Maternal-Zygotic Gene Interactions during Formation of the Dorsoventral Pattern in Drosophila Embryos. Genetics 105: 615-632.
40. Bour BA, O'Brien MA, Lockwood WL, Goldstein ES, Bodmer R, et al. (1995) Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes & Development 9: 730-741.
41. Gunthorpe D, Beatty KE, Taylor MV, (1999) Different levels, but not different isoforms, of the Drosophila transcription factor DMEF2 affect distinct aspects of muscle differentiation. Developmental Biology 215: 130-145.
42. Ranganayakulu G, Zhao B, Dokidis A, Molkentin JD, Olson EN, et al. (1995) A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Developmental Biology 171: 169-181.
43. Elgar SJ, Han J, Taylor MV, (2008) mef2 activity levels differentially affect gene expression during Drosophila muscle development. Proceedings of the National Academy of Sciences of the United States of America 105: 918-923.
44. Junion G, Jagla T, Duplant S, Tapin R, Da Ponte J-P, et al. (2005) Mapping Dmef2-binding regulatory modules by using a ChIP-enriched in silico targets approach. Proceedings of the National Academy of Sciences of the United States of America 102: 18479-18484.
45. Lilly B, Galewsky S, Firulli AB, Schulz RA, Olson EN, (1994) D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proceedings of the National Academy of Sciences of the United States of America 91: 5662-5666.
46. Nguyen HT, Xu X, (1998) Drosophila mef2 expression during mesoderm development is controlled by a complex array of cis-acting regulatory modules. Developmental Biology 204: 550-566.
47. Sandmann T, Jensen LJ, Jakobsen JS, Karzynski MM, Eichenlaub MP, et al. (2006) A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Developmental Cell 10: 797-807.
48. Taylor MV, Beatty KE, Hunter HK, Baylies MK, (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. Mechanisms of Development 50: 29-41.
49. Salerno MS, Dyer K, Bracegirdle J, Platt L, Thomas M, et al. (2009) Akirin1 (Mighty), a novel promyogenic factor regulates muscle regeneration and cell chemotaxis. Experimental Cell Research 315: 2012-2021.
50. Spradling A, Penman S, Pardue ML, (1975) Analysis of drosophila mRNA by in situ hybridization: sequences transcribed in normal and heat shocked cultured cells. Cell 4: 395-404.
51. Buszczak M, Spradling AC, (2006) The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes & Development 20: 977-989.
52. Karam CS, Kellner WA, Takenaka N, Clemmons AW, Corces VG, (2010) 14-3-3 mediates histone cross-talk during transcription elongation in Drosophila. PLoS Genet 6: e1000975 doi:10.1371/journal.pgen.1000975.
53. Nowak SJ, Corces VG, (2000) Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes & Development 14: 3003-3013.
54. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, et al. (2007) Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318: 1780-1782.
55. Thisse C, Thisse B, (1992) Dorsoventral development of the Drosophila embryo is controlled by a cascade of transcriptional regulators. Dev Suppl pp. 173-181.
56. Zhimulev IF, Belyaeva ES, Semeshin VF, Shloma VV, Makunin IV, et al. (2003) Overexpression of the SuUR gene induces reversible modifications at pericentric, telomeric and intercalary heterochromatin of Drosophila melanogaster polytene chromosomes. Journal of Cell Science 116: 169-176.
57. Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727-1736.
58. Möller A, Avila FW, Erickson JW, Jäckle H, (2005) Drosophila BAP60 is an essential component of the Brahma complex, required for gene activation and repression. Journal of Molecular Biology 352: 329-337.
59. Halfon MS, Carmena A, Gisselbrecht S, Sackerson CM, Jiménez F, et al. (2000) Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103: 63-74.
60. Kim-Ha J, Webster PJ, Smith JL, Macdonald PM, (1993) Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. Development 119: 169-178.
61. Celniker SE, Dillon LAL, Gerstein MB, Gunsalus KC, Henikoff S, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927-930.
62. Peña-Rangel MT, Rodriguez I, Riesgo-Escovar JR, (2002) A misexpression study examining dorsal thorax formation in Drosophila melanogaster. Genetics 160: 1035-1050.
63. Escudero LM, Caminero E, Schulze KL, Bellen HJ, 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.
64. Vorobyeva NE, Soshnikova NV, Nikolenko JV, Kuzmina JL, Nabirochkina EN, et al. (2009) Transcription coactivator SAYP combines chromatin remodeler Brahma and transcription initiation factor TFIID into a single supercomplex. Proceedings of the National Academy of Sciences of the United States of America 106: 11049-11054.
65. Ohkawa Y, Yoshimura S, Higashi C, Marfella CGA, Dacwag CS, et al. (2007) Myogenin and the SWI/SNF ATPase Brg1 maintain myogenic gene expression at different stages of skeletal myogenesis. The Journal of Biological Chemistry 282: 6564-6570.
66. Martin SG, Dobi KC, St Johnston D, (2001) A rapid method to map mutations in Drosophila. Genome Biology 2: RESEARCH0036.
67. Halfon MS, Gisselbrecht S, Lu J, Estrada B, Keshishian H, et al. (2002) New fluorescent protein reporters for use with the Drosophila Gal4 expression system and for vital detection of balancer chromosomes. Genesis (New York, NY: 2000) 34: 135-138.
68. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
69. Cox VT, Baylies MK, (2005) Specification of individual Slouch muscle progenitors in Drosophila requires sequential Wingless signaling. Development 132: 713-724.
70. Richardson BE, Beckett K, Nowak SJ, Baylies MK, (2007) SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 134: 4357-4367.
71. Beckett K, Baylies MK, (2006) Parcas, a regulator of non-receptor tyrosine kinase signaling, acts during anterior-posterior patterning and somatic muscle development in Drosophila melanogaster. Developmental Biology 299: 176-192.
72. Nowak SJ, Nahirney PC, Hadjantonakis A-K, Baylies MK, (2009) Nap1-mediated actin remodeling is essential for mammalian myoblast fusion. Journal of Cell Science 122: 3282-3293.
73. Nowak SJ, Pai C-Y, Corces VG, (2003) Protein phosphatase 2A activity affects histone H3 phosphorylation and transcription in Drosophila melanogaster. Molecular and Cellular Biology 23: 6129-6138.
74. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
75. Lilja T, Aihara H, Stabell M, Nibu Y, Mannervik M, (2007) The acetyltransferase activity of Drosophila CBP is dispensable for regulation of the Dpp pathway in the early embryo. Developmental Biology 305: 650-658.