Histone acetyltransferase enok regulates oocyte polarization by promoting expression of the actin nucleation factor spire

Genes and Development

Volumn 28, Issue 24, 2014, Pages 2750-2763

  Huang, F ^a   Paulson, Ariel ^a   Dutta, Arnob ^a   Venkatesh, Swaminathan ^a   Smolle, Michaela ^a   Susan, M ^b   Workman, Jerry L ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Germ plasm; H3K23 acetylation; Oskar localization

Indexed keywords

ACTIN; ENOK PROTEIN; HISTONE ACETYLTRANSFERASE; MAELSTROM PROTEIN; PROTEIN; SPIRE PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; DROSOPHILA PROTEIN; ENOK PROTEIN, DROSOPHILA; HISTONE; ISOPROTEIN; MAELSTROM PROTEIN, DROSOPHILA; OSKAR PROTEIN, DROSOPHILA; SPIRE PROTEIN, DROSOPHILA;

ANTIBODY PRODUCTION; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME SPECIFICITY; FEMALE; GERMLINE STEM CELL; HISTONE ACETYLATION; HISTONE MODIFICATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OOCYTE; POLARIZATION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION; RNA SEQUENCE; UPREGULATION; ACETYLATION; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; OVARY;

EUKARYOTA;

ACETYLATION; ANIMALS; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE ACETYLTRANSFERASES; HISTONES; MICROFILAMENT PROTEINS; MUTATION; OOCYTES; OVARY; PROTEIN ISOFORMS;

EID: 84918546515     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.249730.114     Document Type: Article

References (56)

1. Ambrosio L, Mahowald AP, Perrimon N. 1989. l(1)pole hole is required maternally for pattern formation in the terminal regions of the embryo. Development 106: 145–158.
2. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37: W202–W208.
3. Bodai L, Zsindely N, Gaspar R, Kristo I, Komonyi O, Boros IM. 2012. Ecdysone induced gene expression is associated with acetylation of histone H3 lysine 23 in Drosophila melanogaster. PLoS ONE 7: e40565.
4. Boutros M, Agaisse H, Perrimon N. 2002. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 3: 711–722.
5. Brendza RP, Serbus LR, Duffy JB, Saxton WM. 2000. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289: 2120–2122.
6. Calvi BR, Lilly MA. 2004. Fluorescent BrdU labeling and nuclear flow sorting of the Drosophila ovary. Methods Mol Biol 247: 203–213.
7. Chou TB, Perrimon N. 1996. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144: 1673–1679.
8. Clegg NJ, Frost DM, Larkin MK, Subrahmanyan L, Bryant Z, Ruohola-Baker H. 1997. maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA. Development 124: 4661–4671.
9. Dahlgaard K, Raposo AA, Niccoli T, St Johnston D. 2007. Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev Cell 13: 539–553.
10. Dutta A, Gogol M, Kim JH, Smolle M, Venkatesh S, Gilmore J, Florens L, Washburn MP, Workman JL. 2014. Swi/Snf dynamics on stress-responsive genes is governed by competitive bromodomain interactions. Genes Dev 28: 2314–2330.
11. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
12. Emmons S, Phan H, Calley J, Chen W, James B, Manseau L. 1995. Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus. Genes Dev 9: 2482–2494.
13. Ephrussi A, Lehmann R. 1992. Induction of germ cell formation by oskar. Nature 358: 387–392.
14. Ephrussi A, Dickinson LK, Lehmann R. 1991. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66: 37–50.
15. Extavour CG, Akam M. 2003. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130: 5869–5884.
16. Filardo P, Ephrussi A. 2003. Bruno regulates gurken during Drosophila oogenesis. Mech Dev 120: 289–297.
17. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870–1881.
18. Fogarty P, Kalpin RF, Sullivan W. 1994. The Drosophila maternal-effect mutation grapes causes a metaphase arrest at nuclear cycle 13. Development 120: 2131–2142.
19. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, et al. 2011. The developmental transcriptome of Drosophila melanogaster. Nature 471: 473–479.
20. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. 2007. Quantifying similarity between motifs. Genome Biol 8: R24.
21. Hoch M, Gerwin N, Taubert H, Jackle H. 1992. Competition for overlapping sites in the regulatory region of the Drosophila gene Kruppel. Science 256: 94–97.
22. Howe L, Auston D, Grant P, John S, Cook RG, Workman JL, Pillus L. 2001. Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev 15: 3144– 3154.
23. Iida T, Kobayashi S. 1998. Essential role of mitochondrially encoded large rRNA for germ-line formation in Drosophila embryos. Proc Natl Acad Sci 95: 11274–11278.
24. Khurana JS, Theurkauf W. 2010. piRNAs, transposon silencing, and Drosophila germline development. J Cell Biol 191: 905– 913.
25. Kim-Ha J, Kerr K, Macdonald PM. 1995. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81: 403–412.
26. Kosman D, Small S, Reinitz J. 1998. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208: 290–294.
27. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.
28. Lin CH, Li B, Swanson S, Zhang Y, Florens L, Washburn MP, Abmayr SM, Workman JL. 2008. Heterochromatin protein 1a stimulates histone H3 lysine 36 demethylation by the Drosophila KDM4A demethylase. Mol Cell 32: 696–706.
29. Manseau L., Schupbach T. 1989. cappuccino and spire: two unique maternal-effect loci required for both the anteroposterior and dorsoventral patterns of the Drosophila embryo. Genes Dev 3: 1437–1452.
30. Nakamura A, Sato K, Hanyu-Nakamura K. 2004. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev Cell 6: 69–78.
31. Neumuller RA, Gross T, Samsonova AA, Vinayagam A, Buckner M, Founk K, Hu Y, Sharifpoor S, Rosebrock AP, Andrews B, et al. 2013. Conserved regulators of nucleolar size revealed by global phenotypic analyses. Sci Signal 6: ra70.
32. Nibu Y, Zhang H, Levine M. 1998. Interaction of short-range repressors with Drosophila CtBP in the embryo. Science 280: 101–104.
33. Perez-Campo FM, Costa G, Lie-a-Ling M, Kouskoff V, Lacaud G. 2013. The MYSTerious MOZ, a histone acetyltransferase with a key role in haematopoiesis. Immunology 139: 161– 165.
34. Quinlan ME. 2013. Direct interaction between two actin nucle-ators is required in Drosophila oogenesis. Development 140: 4417–4425.
35. Rongo C, Gavis ER, Lehmann R. 1995. Localization of oskar RNA regulates oskar translation and requires Oskar protein. Development 121: 2737–2746.
36. Rosales-Nieves AE, Johndrow JE, Keller LC, Magie CR, Pinto-Santini DM, Parkhurst SM. 2006. Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat Cell Biol 8: 367–376.
37. Sato K, Nishida KM, Shibuya A, Siomi MC, Siomi H. 2011. Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev 25: 2361–2373.
38. Schumacher N, Borawski JM, Leberfinger CB, Gessler M, Kerkhoff E. 2004. Overlapping expression pattern of the actin organizers Spir-1 and formin-2 in the developing mouse nervous system and the adult brain. Gene Expr Patterns 4: 249–255.
39. Scott EK, Lee T, Luo L. 2001. enok encodes a Drosophila putative histone acetyltransferase required for mushroom body neuroblast proliferation. Curr Biol 11: 99–104.
40. Shcherbata HR, Althauser C, Findley SD, Ruohola-Baker H. 2004. The mitotic-to-endocycle switch in Drosophila follicle cells is executed by Notch-dependent regulation of G1/S, G2/M and M/G1 cell-cycle transitions. Development 131: 3169–3181.
41. Sienski G, Donertas D, Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964–980.
42. St Pierre SE, Ponting L, Stefancsik R, McQuilton P. 2014. FlyBase 102—advanced approaches to interrogating FlyBase. Nucleic Acids Res 42: D780–D788.
43. Sugimura I, Lilly MA. 2006. Bruno inhibits the expression of mitotic cyclins during the prophase I meiotic arrest of Drosophila oocytes. Dev Cell 10: 127–135.
44. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ. 2009. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136: 3131– 3141.
45. Tsai WW, Wang Z, Yiu TT, Akdemir KC, Xia W, Winter S, Tsai CY, Shi X, Schwarzer D, Plunkett W, et al. 2010. TRIM24 links a non-canonical histone signature to breast cancer. Nature 468: 927–932.
46. Ullah M, Pelletier N, Xiao L, Zhao SP, Wang K, Degerny C, Tahmasebi S, Cayrou C, Doyon Y, Goh SL, et al. 2008. Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol Cell Biol 28: 6828–6843.
47. Voss AK, Collin C, Dixon MP, Thomas T. 2009. Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev Cell 17: 674– 686.
48. Weake VM, Swanson SK, Mushegian A, Florens L, Washburn MP, Abmayr SM, Workman JL. 2009. A novel histone fold domain-containing protein that replaces TAF6 in Drosophila SAGA is required for SAGA-dependent gene expression. Genes Dev 23: 2818–2823.
49. Wilkie GS, Dickson KS, Gray NK. 2003. Regulation of mRNA translation by 59- and 39-UTR-binding factors. Trends Biochem Sci 28: 182–188.
50. Williamson A, Lehmann R. 1996. Germ cell development in Drosophila. Annu Rev Cell Dev Biol 12: 365–391.
51. Wu LH, Lengyel JA. 1998. Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125: 2433–2442.
52. Xin T, Xuan T, Tan J, Li M, Zhao G. 2013. The Drosophila putative histone acetyltransferase Enok maintains female germline stem cells through regulating Bruno and the niche. Dev Biol 384: 1–12.
53. Xu P, Johnson TL, Stoller-Conrad JR, Schulz RA. 2012. Spire, an actin nucleation factor, regulates cell division during Drosophila heart development. PLoS ONE 7: e30565.
54. Yang XJ. 2004. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res 32: 959–976.
55. Yoshida S, Muller HA, Wodarz A, Ephrussi A. 2004. PKA-R1 spatially restricts Oskar expression for Drosophila embryonic patterning. Development 131: 1401–1410.
56. Yun M, Ruan C, Huh JW, Li B. 2012. Reconstitution of modified chromatin templates for in vitro functional assays. Methods Mol Biol 833: 237–253.