The histone acetyltransferase Elp3 plays in active role in the control of synaptic bouton expansion and sleep in Drosophila

Journal of Neurochemistry

Volumn 115, Issue 2, 2010, Pages 493-504

  Singh, Neetu ^a   Lorbeck, Meridith T ^a   Zervos, Ashley ^a   Zimmerman, John ^b   Elefant, Felice ^a  

^a DREXEL UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chromatin; Drosophila; ELP3; Histone acetyltransferase; Plasticity; Synapse

Indexed keywords

ELONGATOR PROTEIN 3; HISTONE ACETYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; DROSOPHILA; GELSOLIN GENE; GENE; GENE EXPRESSION; HSC70 3 GENE; HSC70 4 GENE; HYPERACTIVITY; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SLEEP; SLEEPLESS GENE; SUPEROXIDE DISMUTASE GENE; SYNAPTOBREVIN GENE; SYNAPTOGENESIS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE ACETYLTRANSFERASES; HUMANS; LARVA; MALE; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; RNA INTERFERENCE; SLEEP DEPRIVATION; SLEEP INITIATION AND MAINTENANCE DISORDERS;

ANIMALIA;

EID: 78651267261     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06892.x     Document Type: Article

References (73)

1. Alarcon J. M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E. R. and Barco A. (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947-959.
2. Andretic R. and Shaw P. J. (2005) Essentials of sleep recordings in Drosophila: Moving beyond sleep time. Methods Enzymol. 393, 759-772.
3. Axelrod F. B. (2004) Familial dysautonomia. Muscle Nerve 29, 352-363.
4. Berger S. L. (2001) An embarrassment of niches: The many covalent modifications of histones in transcriptional regulation. Oncogene 20, 3007-3013.
5. Berger S. L. (2002) Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12, 142-148.
6. Bhattacharya S., Stewart B. A., Niemeyer B. A., Burgess R. W., McCabe B. D., Lin P., Boulianne G., O'Kane C. J. and Schwarz T. L. (2002) Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable in vivo for neurotransmitter release and cell viability. Proc. Natl Acad. Sci. USA 99, 13867-13872.
7. 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.
8. Broadie K. S. and Bate M. (1993) Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J. Neurosci. 13, 144-166. (Pubitemid 23028734)
9. Bronk P., Nie Z., Klose M. K., Dawson-Scully K., Zhang J., Robertson R. M., Atwood H. L. and Zinsmaier K. E. (2005) The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J. Neurosci. 25, 2204-2214.
10. Cerrato A., Parisi M., Santa Anna S. et al. (2006) Genetic interactions between Drosophila melanogaster menin and Jun/Fos. Dev. Biol. 298, 59-70.
11. Chan H. Y. and Bonini N. M. (2000) Drosophila models of human neurodegenerative disease. Cell Death Differ. 7, 1075-1080.
12. Chan Y. B. and Kravitz E. A. (2007) Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 104, 19577-19582.
13. Chen L. and Feany M. B. (2005) Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat. Neurosci. 8, 657-663.
14. Close P., Hawkes N., Cornez I. et al. (2006) Transcription impairment and cell migration defects in elongator-depleted cells: Implication for familial dysautonomia. Mol. Cell 22, 521-531.
15. Collins C. A. and DiAntonio A. (2007) Synaptic development: Insights from Drosophila. Curr. Opin. Neurobiol. 17, 35-42.
16. Colon-Ramos D. A. (2009) Synapse formation in developing neural circuits. Curr. Top. Dev. Biol. 87, 53-79.
17. Creppe C., Malinouskaya L., Volvert M. L. et al. (2009) Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136, 551-564.
18. Davids E., Zhang K., Tarazi F. I. and Baldessarini R. J. (2003) Animal models of attention-deficit hyperactivity disorder. Brain Res. Brain Res. Rev. 42, 1-21.
19. Dawson-Scully K., Bronk P., Atwood H. L. and Zinsmaier K. E. (2000) Cysteine-string protein increases the calcium sensitivity of neurotransmitter exocytosis in Drosophila. J. Neurosci. 20, 6039-6047.
20. Dent E. W. and Gertler F. B. (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40, 209-227.
21. Dent E. W. and Kalil K. (2001) Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21, 9757-9769.
22. Donlea J. M., Ramanan N. and Shaw P. J. (2009) Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324, 105-108.
23. Duffy J. B. (2002) GAL4 system in Drosophila: A fly geneticist's Swiss army knife. Genesis 34, 1-15.
24. Elefant F. and Palter K. B. (1999) Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol. Biol. Cell 10, 2101-2117.
25. Elefant F., Cooke N. E. and Liebhaber S. A. (2000a) Targeted recruitment of histone acetyltransferase activity to a locus control region. J. Biol. Chem. 275, 13827-13834.
26. Elefant F., Su Y., Liebhaber S. A. and Cooke N. E. (2000b) Patterns of histone acetylation suggest dual pathways for gene activation by a bifunctional locus control region. EMBO J. 19, 6814-6822.
27. Esberg A., Huang B., Johansson M. J. and Bystrom A. S. (2006) Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol. Cell 24, 139-148.
28. Feany M. B. and Bender W. W. (2000) A Drosophila model of Parkinson's disease. Nature 404, 394-398.
29. Felsenfeld G. and Groudine M. (2003) Controlling the double helix. Nature 421, 448-453.
30. FischleW.,Wang Y. and Allis C. D. (2003) Histone and chromatin crosstalk. Curr. Opin. Cell Biol. 15, 172-183.
31. Fortier E. and Belote J. M. (2000) Temperature-dependent gene silencing by an expressed inverted repreat in Drosophila. Genesis 26, 240-244.
32. Gardiner J., Barton D., Marc J. and Overall R. (2007) Potential role of tubulin acetylation and microtubule-based protein trafficking in familial dysautonomia. Traffic 8, 1145-1149.
33. Gilestro G. F., Tononi G. and Cirelli C. (2009) Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324, 109-112.
34. Guan J. S., Haggarty S. J., Giacometti E. et al. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60.
35. Halpain S., Hipolito A. and Saffer L. (1998) Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. Neurosci. 18, 9835-9844.
36. Hawkes N. A., Otero G., Winkler G. S. et al. (2002) Purification and characterization of the human elongator complex. J. Biol. Chem. 277, 3047-3052.
37. Hendricks J. C., Lu S., Kume K., Yin J. C., Yang Z. and Sehgal A. (2003) Gender dimorphism in the role of cycle (BMAL1) in rest, rest regulation, and longevity in Drosophila melanogaster. J. Biol. Rhythms 18, 12-25.
38. Huang B., Johansson M. J. and Bystrom A. S. (2005) An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11, 424-436.
39. Huber R., Hill S. L., Holladay C., Biesiadecki M., Tononi G. and Cirelli C. (2004) Sleep homeostasis in Drosophila melanogaster. Sleep 27, 628-639.
40. Jenuwein T. and Allis C. D. (2001) Translating the histone code. Science 293, 1074-1080.
41. Kiefer J. C. (2007) Epigenetics in development. Dev. Dyn. 236, 1144-1156.
42. Kim J. H., Lane W. S. and Reinberg D. (2002) Human Elongator facilitates RNA polymerase II transcription through chromatin. Proc. Natl Acad. Sci. USA 99, 1241-1246.
43. Koh Y. H., Gramates L. S. and Budnik V. (2000) Drosophila larval neuromuscular junction: Molecular components and mechanisms underlying synaptic plasticity. Microsc. Res. Tech. 49, 14-25.
44. Koh K., Joiner W. J., Wu M. N., Yue Z., Smith C. J. and Sehgal A. (2008) Identification of SLEEPLESS, a sleep-promoting factor. Science 321, 372-376.
45. Korzus E., Rosenfeld M. G. and Mayford M. (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972.
46. Kristjuhan A. and Svejstrup J. Q. (2004) Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23, 4243-4252.
47. Kristjuhan A., Walker J., Suka N., Grunstein M., Roberts D., Cairns B. R. and Svejstrup J. Q. (2002) Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region. Mol. Cell 10, 925-933.
48. Livak K. J. and Schmittgen T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
49. Mackiewicz M., Naidoo N., Zimmerman J. E. and Pack A. I. (2008) Molecular mechanisms of sleep and wakefulness. Ann. N Y Acad. Sci. 1129, 335-349.
50. Margueron R., Trojer P. and Reinberg D. (2005) The key to development: Interpreting the histone code? Curr. Opin. Genet. Dev. 15, 163-176.
51. Naidoo N., Casiano V., Cater J., Zimmerman J. and Pack A. I. (2007) A role for the molecular chaperone protein BiP/GRP78 in Drosophila sleep homeostasis. Sleep 30, 557-565.
52. Orphanides G. and Reinberg D. (2002) A unified theory of gene expression. Cell 108, 439-451.
53. Petrakis T. G., Wittschieben B. O. and Svejstrup J. Q. (2004) Molecular architecture, structure-function relationship, and importance of the Elp3 subunit for the RNA binding of holo-elongator. J. Biol. Chem. 279, 32087-32092.
54. Rahl P. B., Chen C. Z. and Collins R. N. (2005) Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol. Cell 17, 841-853.
55. Ramachandran B. and Frey J. U. (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J. Neurosci. 29, 12167-12173.
56. Reik W. (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432.
57. Rushton E., Rohrbough J. and Broadie K. (2009) Presynaptic secretion of mind-the-gap organizes the synaptic extracellular matrix-integrin interface and postsynaptic environments. Dev. Dyn. 238, 554-571.
58. Shaw P. J., Cirelli C., Greenspan R. J. and Tononi G. (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834-1837.
59. Shaw P. J., Tononi G., Greenspan R. J. and Robinson D. F. (2002) Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417, 287-291.
60. Simpson C. L., Lemmens R., Miskiewicz K. et al. (2009) Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum. Mol. Genet. 18, 472-481.
61. Slaugenhaupt S. A. and Gusella J. F. (2002) Familial dysautonomia. Curr. Opin. Genet. Dev. 12, 307-311.
62. Strahl B. D. and Allis C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45.
63. Svejstrup J. Q. (2007) Elongator complex: How many roles does it play? Curr. Opin. Cell Biol. 19, 331-336.
64. Tononi G. and Cirelli C. (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10, 49-62.
65. Wallis D., Russell H. F. and Muenke M. (2008) Review: Genetics of attention deficit/hyperactivity disorder. J. Pediatr. Psychol. 33, 1085-1099.
66. Winkler G. S., Petrakis T. G., Ethelberg S., Tokunaga M., Erdjument- Bromage H., Tempst P. and Svejstrup J. Q. (2001) RNA polymerase II elongator holoenzyme is composed of two discrete subcomplexes. J. Biol. Chem. 276, 32743-32749.
67. Winkler G. S., Kristjuhan A., Erdjument-Bromage H., Tempst P. and Svejstrup J. Q. (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.
68. Wynshaw-Boris A. (2009) Elongator bridges tubulin acetylation and neuronal migration. Cell 136, 393-394.
69. Yuan J. S., Reed A., Chen F. and Stewart Jr C. N. (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.
70. Zhu X., Singh N., Donnelly C., Boimel P. and Elefant F. (2007) The cloning and characterization of the histone acetyltransferase human homolog Dmel\TIP60 in Drosophila melanogaster: Dmel\TIP60 is essential for multicellular development. Genetics 175, 1229-1240.
71. Zimmerman J. E., Naidoo N., Raizen D. M. and Pack A. I. (2008a) Conservation of sleep: Insights from non-mammalian model systems. Trends Neurosci. 31, 371-376.
72. Zimmerman J. E., Raizen D. M., Maycock M. H., Maislin G. and Pack A. I. (2008b) A video method to study Drosophila sleep. Sleep 31, 1587-1598.
73. Zinsmaier K. E., Eberle K. K., Buchner E., Walter N. and Benzer S. (1994) Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263, 977-980.