Kismet positively regulates glutamate receptor localization and synaptic transmission at the drosophila neuromuscular junction

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Ghosh, Rupa ^a   Vegesna, Srikar ^a   Safi, Ramia ^d   Bao, Hong ^b   Zhang, Bing ^b   Marenda, Daniel R ^a,c   Liebl, Faith L W ^d  

^a DREXEL UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d SOUTHERN ILLINOIS UNIVERSITY EDWARDSVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; DISCS LARGE PROTEIN; DNA BINDING PROTEIN; FASCICLIN II; GLUTAMATE RECEPTOR; KISMET PROTEIN; NERVE PROTEIN; UNCLASSIFIED DRUG; DNA HELICASE; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; KIS PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; LARVA; MOTOR PERFORMANCE; NEUROANATOMY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNAPTIC TRANSMISSION; ANIMAL; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; LOCOMOTION; METABOLISM; MOTONEURON; MUSCLE; PATHOLOGY; PHYSIOLOGY; SYNAPSE;

ANIMALS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; LARVA; LOCOMOTION; MOTOR NEURONS; MUSCLES; NEUROMUSCULAR JUNCTION; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84912013824     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113494     Document Type: Article

References (84)

1. Budnik V, Salinas PC (2011) Wnt signaling during synaptic development and plasticity. Curr Opin Neurobiol 21: 151-159.
2. Dickins EM, Salinas PC (2013) Wnts in action: from synapse formation to synaptic maintenance. Front Cell Neurosci 7: 162.
3. Bayat V, Jaiswal M, Bellen HJ (2011) The BMP signaling pathway at the Drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr Opin Neurobiol 21: 182-188.
4. Gomez-Palacio-Schjetnan A, Escobar ML (2013) Neurotrophins and synaptic plasticity. Curr Top Behav Neurosci 15: 117-136.
5. Lipsky RH (2013) Epigenetic mechanisms regulating learning and long-term memory. Int J Dev Neurosci 31: 353-358.
6. Middei S, Houeland G, Cavallucci V, Ammassari-Teule M, D'Amelio M, et al. (2013) CREB is necessary for synaptic maintenance and learning-induced changes of the AMPA receptor GluA1 subunit. Hippocampus 23: 488-499.
7. Ran I, Laplante I, Lacaille JC (2012) CREB-dependent transcriptional control and quantal changes in persistent long-term potentiation in hippocampal interneurons. J Neurosci 32: 6335-6350.
8. Kida S, Serita T (2014) Functional roles of CREB as a positive regulator in the formation and enhancement of memory. Brain Res Bull.
9. Day JJ, Sweatt JD (2011) Epigenetic mechanisms in cognition. Neuron 70: 813-829.
10. Bird A (2007) Perceptions of epigenetics. Nature 447: 396-398.
11. Murawska M, Brehm A (2011) CHD chromatin remodelers and the transcription cycle. Transcription 2: 244-253.
12. Srinivasan S, Armstrong JA, Deuring R, Dahlsveen IK, McNeill H, et al. (2005) The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132: 1623-1635.
13. Adams ME, Hurd EA, Beyer LA, Swiderski DL, Raphael Y, et al. (2007) Defects in vestibular sensory epithelia and innervation in mice with loss of Chd7 function: implications for human CHARGE syndrome. J Comp Neurol 504: 519-532.
14. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, et al. (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463: 958-962.
15. Hurd EA, Adams ME, Layman WS, Swiderski DL, Beyer LA, et al. (2011) Mature middle and inner ears express Chd7 and exhibit distinctive pathologies in a mouse model of CHARGE syndrome. Hear Res 282: 184-195.
16. Hurd EA, Poucher HK, Cheng K, Raphael Y, Martin DM (2010) The ATPdependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development 137: 3139-3150.
17. Layman WS, McEwen DP, Beyer LA, Lalani SR, Fernbach SD, et al. (2009) Defects in neural stem cell proliferation and olfaction in Chd7 deficient mice indicate a mechanism for hyposmia in human CHARGE syndrome. Hum Mol Genet 18: 1909-1923.
18. Melicharek DJ, Ramirez LC, Singh S, Thompson R, Marenda DR (2010) Kismet/CHD7 regulates axon morphology, memory and locomotion in a Drosophila model of CHARGE syndrome. Hum Mol Genet 19: 4253-4264.
19. Srinivasan S, Dorighi KM, Tamkun JW (2008) Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet 4: e1000217.
20. Dorighi KM, Tamkun JW (2013) The trithorax group proteins Kismet and ASH1 promote H3K36 dimethylation to counteract Polycomb group repression in Drosophila. Development 140: 4182-4192.
21. Dubruille R, Murad A, Rosbash M, Emery P (2009) A constant light-genetic screen identifies KISMET as a regulator of circadian photoresponses. PLoS Genet 5: e1000787.
22. Feng W, Khan MA, Bellvis P, Zhu Z, Bernhardt O, et al. (2013) The chromatin remodeler CHD7 regulates adult neurogenesis via activation of SoxC transcription factors. Cell Stem Cell 13: 62-72.
23. Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29: 307-323.
24. Ljaschenko D, Ehmann N, Kittel RJ (2013) Hebbian plasticity guides maturation of glutamate receptor fields in vivo. Cell Rep 3: 1407-1413.
25. Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7: 563-574.
26. Turrigiano G (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol 4: a005736.
27. Jakawich SK, Nasser HB, Strong MJ, McCartney AJ, Perez AS, et al. (2010) Local presynaptic activity gates homeostatic changes in presynaptic function driven by dendritic BDNF synthesis. Neuron 68: 1143-1158.
28. Beique JC, Na Y, Kuhl D, Worley PF, Huganir RL (2011) Arc-dependent synapse-specific homeostatic plasticity. Proc Natl Acad Sci U S A 108: 816-821.
29. Melicharek D, Shah A, DiStefano G, Gangemi AJ, Orapallo A, et al. (2008) Identification of Novel Regulators of Atonal Expression in the Developing Drosophila Retina. Genetics 180: 2095-2110.
30. Ashley J, Packard M, Ataman B, Budnik V (2005) Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J Neurosci 25: 5943-5955.
31. Budnik V, Koh YH, Guan B, Hartmann B, Hough C, et al. (1996) Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17: 627-640.
32. Buszczak M, Paterno S, Lighthouse D, Bachman J, Planck J, et al. (2007) The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 175: 1505-1531.
33. Mhatre SD, Satyasi V, Killen M, Paddock BE, Moir RD, et al. (2014) Synaptic abnormalities in a Drosophila model of Alzheimer's disease. Dis Model Mech 7: 373-385.
34. Johnson AA, Sarthi J, Pirooznia SK, Reube W, Elefant F (2013) Increasing Tip60 HAT levels rescues axonal transport defects and associated behavioral phenotypes in a Drosophila Alzheimer's disease model. J Neurosci 33: 7535-7547.
35. Mudher A, Shepherd D, Newman TA, Mildren P, Jukes JP, et al. (2004) GSK- 3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol Psychiatry 9: 522-530.
36. Augustin H, Grosjean Y, Chen K, Sheng Q, Featherstone DE (2007) Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci 27: 111-123.
37. Marrus SB, Portman SL, Allen MJ, Moffat KG, DiAntonio A (2004) Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24: 1406-1415.
38. Featherstone DE, Rushton E, Broadie K (2002) Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat Neurosci 5: 141-146.
39. Vanlandingham PA, Barmchi MP, Royer S, Green R, Bao H, et al. (2014) AP180 couples protein retrieval to clathrin-mediated endocytosis of synaptic vesicles. Traffic 15: 433-450.
40. Bainbridge SP, Bownes M (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66: 57-80.
41. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
42. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
43. Dickinson WJ (1980) Tissue specificity of enzyme expression regulated by diffusible factors: evidence in Drosophila hybrids. Science 207: 995-997.
44. Graze RM, McIntyre LM, Main BJ, Wayne ML, Nuzhdin SV (2009) Regulatory divergence in Drosophila melanogaster and D. simulans, a genomewide analysis of allele-specific expression. Genetics 183: 547-561, 541SI-521SI.
45. Goellner B, Aberle H (2012) The synaptic cytoskeleton in development and disease. Dev Neurobiol 72: 111-125.
46. Trotta N, Orso G, Rossetto MG, Daga A, Broadie K (2004) The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr Biol 14: 1135-1147.
47. Yan Y, Broadie K (2007) In vivo assay of presynaptic microtubule cytoskeleton dynamics in Drosophila. J Neurosci Methods 162: 198-205.
48. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, et al. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325: 834-840.
49. Park EJ, Hur SK, Lee HS, Lee SA, Kwon J (2011) The human Ino80 binds to microtubule via the E-hook of tubulin: implications for the role in spindle assembly. Biochem Biophys Res Commun 416: 416-420.
50. Yokoyama H, Rybina S, Santarella-Mellwig R, Mattaj IW, Karsenti E (2009) ISWI is a RanGTP-dependent MAP required for chromosome segregation. J Cell Biol 187: 813-829.
51. Roch F, Serras F, Cifuentes FJ, Corominas M, Alsina B, et al. (1998) Screening of larval/pupal P-element induced lethals on the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs. Mol Gen Genet 257: 103-112.
52. Small J, Rottner K, Hahne P, Anderson KI (1999) Visualising the actin cytoskeleton. Microsc Res Tech 47: 3-17.
53. Garnham CP, Roll-Mecak A (2012) The chemical complexity of cellular microtubules: tubulin post-translational modification enzymes and their roles in tuning microtubule functions. Cytoskeleton (Hoboken) 69: 442-463.
54. Sanyal S, Sandstrom DJ, Hoeffer CA, Ramaswami M (2002) AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature 416: 870-874.
55. Vogler G, Urban J (2008) The transcription factor Zfh1 is involved in the regulation of neuropeptide expression and growth of larval neuromuscular junctions in Drosophila melanogaster. Dev Biol 319: 78-85.
56. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
57. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
58. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, et al. (2006) Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312: 1051-1054.
59. Chen K, Featherstone DE (2005) Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 3: 1.
60. Stewart BA, McLean JR (2004) Population density regulates Drosophila synaptic morphology in a Fasciclin-II-dependent manner. J Neurobiol 61: 392-399.
61. DiAntonio A, Petersen SA, Heckmann M, Goodman CS (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19: 3023-3032.
62. Qin G, Schwarz T, Kittel RJ, Schmid A, Rasse TM, et al. (2005) Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25: 3209-3218.
63. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19: 1237-1248.
64. Gjorgjieva J, Berni J, Evers JF, Eglen SJ (2013) Neural circuits for peristaltic wave propagation in crawling Drosophila larvae: analysis and modeling. Front Comput Neurosci 7: 24.
65. Heckscher ES, Lockery SR, Doe CQ (2012) Characterization of Drosophila larval crawling at the level of organism, segment, and somatic body wall musculature. J Neurosci 32: 12460-12471.
66. Sandstrom DJ (2004) Isoflurane depresses glutamate release by reducing neuronal excitability at the Drosophila neuromuscular junction. J Physiol 558: 489-502.
67. Daubresse G, Deuring R, Moore L, Papoulas O, Zakrajsek I, et al. (1999) The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development 126: 1175-1187.
68. Terriente-Felix A, Molnar C, Gomez-Skarmeta JL, de Celis JF (2011) A conserved function of the chromatin ATPase Kismet in the regulation of hedgehog expression. Dev Biol 350: 382-392.
69. Therrien M, Morrison DK, Wong AM, Rubin GM (2000) A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 156: 1231-1242.
70. Riccio A (2010) Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways. Nat Neurosci 13: 1330-1337.
71. Wu JI, Lessard J, Olave IA, Qiu Z, Ghosh A, et al. (2007) Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56: 94-108.
72. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, et al. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60.
73. Shi W, Chen Y, Gan G, Wang D, Ren J, et al. (2013) Brain tumor regulates neuromuscular synapse growth and endocytosis in Drosophila by suppressing mad expression. J Neurosci 33: 12352-12363.
74. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43: 193-205.
75. Winther AM, Jiao W, Vorontsova O, Rees KA, Koh TW, et al. (2013) The dynamin-binding domains of Dap160/intersectin affect bulk membrane retrieval in synapses. J Cell Sci 126: 1021-1031.
76. Wang D, Zhang L, Zhao G, Wahlstrom G, Heino TI, et al. (2010) Drosophila twinfilin is required for cell migration and synaptic endocytosis. J Cell Sci 123: 1546-1556.
77. Viquez NM, Fuger P, Valakh V, Daniels RW, Rasse TM, et al. (2009) PP2A and GSK-3beta act antagonistically to regulate active zone development. J Neurosci 29: 11484-11494.
78. Graf ER, Daniels RW, Burgess RW, Schwarz TL, DiAntonio A (2009) Rab3 dynamically controls protein composition at active zones. Neuron 64: 663-677.
79. Blake KD, Prasad C (2006) CHARGE syndrome. Orphanet J Rare Dis 1: 34.
80. Sanlaville D, Verloes A (2007) CHARGE syndrome: an update. Eur J Hum Genet 15: 389-399.
81. Zentner GE, Layman WS, Martin DM, Scacheri PC (2010) Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A 152A: 674-686.
82. Bergman JE, Janssen N, Hoefsloot LH, Jongmans MC, Hofstra RM, et al. (2011) CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J Med Genet 48: 334-342.
83. Blake KD, Hartshorne TS, Lawand C, Dailor AN, Thelin JW (2008) Cranial nerve manifestations in CHARGE syndrome. Am J Med Genet A 146A: 585-592.
84. Hartshorne TS, Hefner MA, Davenport SL (2005) Behavior in CHARGE syndrome: introduction to the special topic. Am J Med Genet A 133A: 228-231