Role of elongator subunit Elp3 in Drosophila melanogaster larval development and immunity

Genetics

Volumn 187, Issue 4, 2011, Pages 1067-1075

  Walker, Jane ^a   Kwon, So Yeon ^b   Badenhorst, Paul ^b   East, Phil ^c   McNeill, Helen ^c,d   Svejstrup, Jesper Q ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ECDYSONE; ELONGATION FACTOR; ELONGATOR COMPLEX; PROTEIN DERIVATIVE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA MELANOGASTER; EGG LAYING; GENE DELETION; GENE EXPRESSION; IMMUNITY; LARVAL DEVELOPMENT; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PUPA (LIFE CYCLE STAGE); PUPATION;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ECDYSONE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, LETHAL; HISTONE ACETYLTRANSFERASES; LARVA; LINEAR MODELS; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PUPA; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER;

EID: 79955380420     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.123893     Document Type: Article

References (56)

1. Anderson S.L, R. Coli, I.W. Daly, E.A. Kichula, M.J. Rork et al., 2001 Familial dysautonomia is caused by mutations of the IKAP gene. Am. J. Hum. Genet. 68: 753-758.
2. Badenhorst P., H. Xiao, L. Cherbas, S.Y. Kwon, M. Voas et al., 2005 The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev. 19: 2540-2545.
3. Brand A.H., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
4. Braun A., B. Lemaitre, R. Lanot, D. Zachary and M. Meister, 1997 Drosophila immunity: analysis of larval hemocytes by P-element-mediated enhancer trap. Genetics 147: 623-634.
5. Braun A., J.A. Hoffmann and M. Meister, 1998 Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc. Natl. Acad. Sci. USA 95: 14337-14342.
6. Brun S., S. Vidal, P. Spellman, K. Takahashi, H. Tricoire et al., 2006 The MAPKKK Mekk1 regulates the expression of Turandot stress genes in response to septic injury in Drosophila. Genes Cells 11: 397-407.
7. Chen Y.T., M.M. Hims, R.S. Shetty, J. Mull, L. Liu et al., 2009 Loss of mouse Ikbkap, a subunit of elongator, leads to transcriptional deficits and embryonic lethality that can be rescued by human IKBKAP. Mol. Cell. Biol. 29: 736-744.
8. Chinenov, Y., 2002 A second catalytic domain in the Elp3 histone acetyltransferases: A candidate for histone demethylase activity? Trends Biochem. Sci. 27: 115-117.
9. Close, P., N. Hawkes, I. Cornez, C. Creppe, C.A. Lambert et al., 2006 Transcription impairment and cell migration defects in elongator-depleted cells: implication for familial dysautonomia. Mol. Cell 22: 521-531.
10. Creppe C., L. Malinouskaya, M.L. Volvert, M. Gillard, P. Close et al., 2009 Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136: 551-564.
11. Cuajungco, M.P., M. Leyne, J. Mull, S.P. Gill, J.F. Gusella et al., 2001 Cloning, characterization, and genomic structure of the mouse Ikbkap gene. DNA Cell Biol. 20: 579-586.
12. Ekengren, S., and D. Hultmark, 2001 A family of Turandot-related genes in the humoral stress response of Drosophila. Biochem. Biophys. Res. Commun. 284: 998-1003.
13. Ekengren, S., Y. Tryselius, M.S. Dushay, G. Liu, H. Steiner et al., 2001 A humoral stress response in Drosophila. Curr. Biol. 11: 714-718.
14. Esberg A., B. Huang, M.J. Johansson and A. S. Bystrom, 2006 Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol. Cell 24: 139-148.
15. Fellows, J., H. Erdjument-Bromage, P. Tempst and J.Q. Svejstrup, 2000 The Elp2 subunit of elongator and elongating RNA polymerase II holoenzyme is a WD40 repeat protein. J. Biol. Chem. 275: 12896-12899.
16. Fletcher J.C., and C.S. Thummel, 1995 The ecdysone-inducible Broad-complex and E74 early genes interact to regulate target gene transcription and Drosophila metamorphosis. Genetics 141: 1025-1035.
17. Gentleman R.C., V.J. Carey, D.M. Bates, B. Bolstad, M. Dettlinget al., 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
18. Gilbert, C., A. Kristjuhan, G.S. Winkler and J.Q. Svejstrup, 2004 Elongator interactions with nascent mRNA revealed by RNA immunoprecipitation. Mol. Cell 14: 457-464.
19. Greenwood C., L.A. Selth, A.B. Dirac-Svejstrup and J.Q. Svejstrup, 2009 An iron-sulfur cluster domain in Elp3 important for the structural integrity of elongator. J. Biol. Chem. 284: 141-149.
20. Hanratty W.P., and C.R. Dearolf, 1993 The Drosophila Tumorouslethal hematopoietic oncogene is a dominant mutation in the hopscotch locus. Mol. Gen. Genet. 238: 33-37.
21. Harrison D.A., R. Binari, T.S. Nahreini, M. Gilman and N. Perrimon, 1995 Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J. 14: 2857-2865.
22. Hawkes N.A., G. Otero, G.S. Winkler, N. Marshall, M.E. Dahmus et al., 2002 Purification and characterization of the human elongator complex. J. Biol. Chem. 277: 3047-3052.
23. Huang B., M.J. Johansson and A.S. Bystrom, 2005 An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11: 424-436.
24. Irizarry R.A., B.M. Bolstad, F. Collin, L.M. Cope, B. Hobbs et al., 2003 Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: e15.
25. Irving P., J.M. Ubeda, D. Doucet, L. Troxler, M. Lagueux et al., 2005 New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 7: 335-350.
26. Kim J.H., W.S. Lane and D. Reinberg, 2002 Human Elongator facilitates RNA polymerase II transcription through chromatin. Proc. Natl. Acad. Sci. USA 99: 1241-1246.
27. Kiss I., A.H. Beaton, J. Tardiff, D. Fristrom and J.W. Fristrom, 1988 Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 118: 247-259.
28. Kouskouti A., and I. Talianidis, 2005 Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J. 24: 347-357.
29. Kristjuhan A., J. Walker, N. Suka, M. Grunstein, D. Roberts et al., 2002 Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region. Mol. Cell 10: 925-933.
30. Krogan N.J., and J. F. Greenblatt, 2001 Characterization of a sixsubunit Holo-Elongator complex required for the regulated expression of a group of genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 21: 8203-8212.
31. Kurucz, E., C.J. Zettervall, R. Sinka, P. Vilmos, A. Pivarcsi et al., 2003 Hemese, a hemocyte-specific transmembrane protein, affects the cellular immune response in Drosophila. Proc. Natl. Acad. Sci. USA 100: 2622-2627.
32. Kwon, S.Y., H. Xiao, B.P. Glover, R. Tjian, C. Wu et al., 2008 The nucleosome remodeling factor (NURF) regulates genes involved in Drosophila innate immunity. Dev. Biol. 316: 538-547.
33. Lagueux M., E. Perrodou, E.A. Levashina, M. Capovilla and J. A. Hoffmann, 2000 Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc. Natl. Acad. Sci. USA 97: 11427-11432.
34. Li H.M., G. Buczkowski, O. Mittapalli, J. Xie, J. Wu et al., 2008 Transcriptomic profiles of Drosophila melanogaster third instar larval midgut and responses to oxidative stress. Insect Mol. Biol. 17: 325-339.
35. Li Y., Y. Takagi, Y. Jiang, M. Tokunaga, H. Erdjument-Bromage et al., 2001 A multiprotein complex that interacts with RNA polymerase II elongator. J. Biol. Chem. 276: 29628-29631.
36. Metivier R., G. Penot, M.R. Hubner, G. Reid, H. Brand et al., 2003 Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763.
37. Nelissen H., D. Fleury, L. Bruno, P. Robles, L. De Veylder et al., 2005 The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc. Natl. Acad. Sci. USA 102: 7754-7759.
38. Nelissen, H., S. De Groeve, D. Fleury, P. Neyt, L. Bruno et al., 2010 Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. Proc. Natl. Acad. Sci. USA 107: 1678-1683.
39. Okada Y., K. Yamagata, K. Hong, T. Wakayama and Y. Zhang, 2010 A role for the elongator complex in zygotic paternal genome demethylation. Nature 463: 554-558.
40. Otero G., J. Fellows, Y. Li, T. de Bizemont, A.M.G. Dirac et al., 1999 Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Mol. Cell 3: 109-118.
41. Paraskevopoulou C., S.A. Fairhurst, D.J. Lowe, P. Brick and S. Onesti, 2006 The Elongator subunit Elp3 contains a Fe4S4 cluster and binds S-adenosylmethionine. Mol. Microbiol. 59: 795-806.
42. Parker L., S. Grossand L. Alphey, 2001 Vectors for the expression of tagged proteins in Drosophila. Biotechniques 31: 1280-1282, 1284, 1286.
43. Pokholok D.K., N.M. Hannett and R.A. Young, 2002 Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9: 799-809.
44. Qiu, P., P.C. Pan and S. Govind, 1998 A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125: 1909-1920.
45. Rahl, P.B., C.Z. Chen and R.N. Collins, 2005 Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol. Cell 17: 841-853.
46. Simpson, C.L., R. Lemmens, K. Miskiewicz, W.J. Broom, V.K. Hansen et al., 2009 Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum. Mol. Genet. 18: 472-481.
47. Sinenko, S.A., E.K. Kim, R. Wynn, P. Manfruelli, I. Ando et al., 2004 Yantar, a conserved arginine-rich protein is involved in Drosophila hemocyte development. Dev. Biol. 273: 48-62.
48. Solinger, J.A., R. Paolinelli, H. Kloss, F.B. Scorza, S. Marchesi et al., 2010 The Caenorhabditis elegans Elongator complex regulates neuronal alpha-tubulin acetylation. PLoS Genet. 6: e1000820.
49. Stergiopoulos K., P. Cabrero, S.A. Davies and J.A. Dow, 2009 Salty dog, an SLC5 symporter, modulates Drosophila response to salt stress. Physiol. Genomics 37: 1-11.
50. Stramer B., W. Wood, M.J. Galko, M.J. Redd, A. Jacinto et al., 2005 Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 168: 567-573.
51. Svejstrup, J.Q., 2007 Elongator complex: How many roles does it play? Curr. Opin. Cell Biol. 19: 331-336.
52. Winkler G.S., T.G. Petrakis, S. Ethelberg, M. Tokunaga, H. Erdjument-Bromage et al., 2001 RNA polymerase II Elongator holoenzyme is composed of two discrete subcomplexes. J. Biol. Chem. 276: 32743-32749.
53. Winkler G.S., A. Kristjuhan, H. Erdjument-Bromage, P. Tempst and J.Q. Svejstrup, 2002 Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99: 3517-3522.
54. Wittschieben B.O., G. Otero, T. de Bizemont, J. Fellows, H. Erdjument-Bromage et al., 1999 A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol. Cell 4: 123-128.
55. Wittschieben B.O., J. Fellows, W. Du, D.J. Stillman and J.Q. Svejstrup, 2000 Overlapping roles for the histone acetyltransferase activities of SAGA and Elongator in Vivo. EMBO J. 19: 3060-3068.
56. Zettervall C.J., I. Anderl, M.J. Williams, R. Palmer, E. Kurucz et al., 2004 A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101: 14192-14197.