Altered LARK expression perturbs development and physiology of the Drosophila PDF clock neurons

Molecular and Cellular Neuroscience

Volumn 41, Issue 2, 2009, Pages 196-205

  Huang, Yanmei ^a   Howlett, Eric ^b   Stern, Michael ^b   Jackson, F Rob ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

Circadian; Development; Drosophila; Neuronal excitability; Post transcriptional; RBM4

Indexed keywords

LARK RNA BINDING PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; ELECTROPHYSIOLOGY; LARVA; LOCOMOTION; MALE; MOLECULAR CLOCK; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NEUROMUSCULAR SYNAPSE; NEUROPHYSIOLOGY; NONHUMAN; PIGMENT DISPERSING FACTOR NEURON; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MALE; MOTOR ACTIVITY; NEURONS; NEUROPEPTIDES; NUCLEAR PROTEINS; RECOMBINANT FUSION PROTEINS; RNA-BINDING PROTEINS;

ANIMALIA; MAMMALIA;

EID: 67349112370     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.02.013     Document Type: Article

References (69)

1. Antic D., Lu N., and Keene J.D. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13 (1999) 449-461
2. Belvin M.P., Zhou H., and Yin J.C. The Drosophila dCREB2 gene affects the circadian clock. Neuron 22 (1999) 777-787
3. Benito J., Zheng H., and Hardin P.E. PDP1epsilon functions downstream of the circadian oscillator to mediate behavioral rhythms. J. Neurosci. 27 (2007) 2539-2547
4. Blanchardon E., Grima B., Klarsfeld A., Chelot E., Hardin P.E., Preat T., and Rouyer F. Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression. Eur. J. Neurosci. 13 (2001) 871-888
5. Chouinard S.W., Wilson G.F., Schlimgen A.K., and Ganetzky B. A potassium channel beta subunit related to the aldo-keto reductase superfamily is encoded by the Drosophila hyperkinetic locus. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 6763-6767
6. Cyran S.A., Buchsbaum A.M., Reddy K.L., Lin M.C., Glossop N.R., Hardin P.E., Young M.W., Storti R.V., and Blau J. vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112 (2003) 329-341
7. Deschenes-Furry J., Perrone-Bizzozero N., and Jasmin B.J. The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. BioEssays 28 (2006) 822-833
8. Dockendorff T.C., Su H.S., McBride S.M., Yang Z., Choi C.H., Siwicki K.K., Sehgal A., and Jongens T.A. Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34 (2002) 973-984
9. Garbarino-Pico E., and Green C.B. Posttranscriptional regulation of mammalian circadian clock output. Cold Spring Harbor Symp. Quant. Biol. 72 (2007) 145-156
10. Glossop N.R., Lyons L.C., and Hardin P.E. Interlocked feedback loops within the Drosophila circadian oscillator. Science 286 (1999) 766-768
11. Harms E., Kivimae S., Young M.W., and Saez L. Posttranscriptional and posttranslational regulation of clock genes. J. Biol. Rhythms 19 (2004) 361-373
12. Harrisingh M.C., Wu Y., Lnenicka G.A., and Nitabach M.N. Intracellular Ca2+ regulates free-running circadian clock oscillation in vivo. J. Neurosci. 27 (2007) 12489-12499
13. Hay B.A., Wolff T., and Rubin G.M. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120 (1994) 2121-2129
14. Heintzen C., Nater M., Apel K., and Staiger D. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8515-8520
15. Helfrich-Forster C. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J. Comp. Neurol. 380 (1997) 335-354
16. Helfrich-Forster C. The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc. Res. Tech. 62 (2003) 94-102
17. Helfrich-Forster C., Shafer O.T., Wulbeck C., Grieshaber E., Rieger D., and Taghert P. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 500 (2007) 47-70
18. Hock J., Weinmann L., Ender C., Rudel S., Kremmer E., Raabe M., Urlaub H., and Meister G. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 8 (2007) 1052-1060
19. Hodge J.J., and Stanewsky R. Function of the Shaw potassium channel within the Drosophila circadian clock. PLoS ONE 3 (2008) e2274
20. Huang Y., and Stern M. In vivo properties of the Drosophila inebriated-encoded neurotransmitter transporter. J. Neurosci. 22 (2002) 1698-1708
21. Huang Y., Genova G., Roberts M., and Jackson F.R. The LARK RNA-binding protein selectively regulates the circadian eclosion rhythm by controlling E74 protein expression. PLoS ONE 2 (2007) e1107
22. Iliev D., Voytsekh O., Schmidt E.M., Fiedler M., Nykytenko A., and Mittag M. A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock. Plant Physiol. 142 (2006) 797-806
23. Jan Y.N., and Jan L.Y. Genetic dissection of short-term and long-term facilitation at the Drosophila neuromuscular junction. Proc. Natl. Acad. Sci. U. S. A. 75 (1978) 515-519
24. Jan Y.N., Jan L.Y., and Dennis M.J. Two mutations of synaptic transmission in Drosophila. Proc. R Soc. Lond. B Biol. Sci. 198 (1977) 87-108
25. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8 (2007) 533-543
26. Keene J.D., and Lager P.J. Post-transcriptional operons and regulons co-ordinating gene expression. Chromosome Res. 13 (2005) 327-337
27. Kojima S., Matsumoto K., Hirose M., Shimada M., Nagano M., Shigeyoshi Y., Hoshino S., Ui-Tei K., Saigo K., Green C.B., Sakaki Y., and Tei H. LARK activates posttranscriptional expression of an essential mammalian clock protein, PERIOD1. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 1859-1864
28. Lee A., Li W., Xu K., Bogert B.A., Su K., and Gao F.B. Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130 (2003) 5543-5552
29. Lee K., Dunlap J.C., and Loros J.J. Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163 (2003) 103-114
30. Levine, J.D., Funes, P., Dowse, H.B., Hall, J.C., 2002. Signal analysis of behavioral and molecular cycles. BMC Neurosci. 3 (1), 1.
31. Lim C., Lee J., Koo E., and Choe J. Targeted inhibition of Pdp1epsilon abolishes the circadian behavior of Drosophila melanogaster. Biochem. Biophys. Res. Commun. 364 (2007) 294-300
32. Liu Y. Analysis of posttranslational regulations in the Neurospora circadian clock. Methods Enzymol. 393 (2005) 379-393
33. Mallart A., Angaut-Petit D., Bourret-Poulain C., and Ferrus A. Nerve terminal excitability and neuromuscular transmission in T(X;Y)V7 and Shaker mutants of Drosophila melanogaster. J. Neurogenet. 7 (1991) 75-84
34. McGuire S.E., Mao Z., and Davis R.L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE (2004) pl6 2004
35. McNeil G.P., Zhang X., Genova G., and Jackson F.R. A molecular rhythm mediating circadian clock output in Drosophila. Neuron 20 (1998) 297-303
36. McNeil G.P., Schroeder A.J., Roberts M.A., and Jackson F.R. Genetic analysis of functional domains within the Drosophila LARK RNA-binding protein. Genetics 159 (2001) 229-240
37. Mee C.J., Pym E.C., Moffat K.G., and Baines R.A. Regulation of neuronal excitability through pumilio-dependent control of a sodium channel gene. J. Neurosci. 24 (2004) 8695-8703
38. Morales J., Hiesinger P.R., Schroeder A.J., Kume K., Verstreken P., Jackson F.R., Nelson D.L., and Hassan B.A. Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34 (2002) 961-972
39. Muraro N.I., Weston A.J., Gerber A.P., Luschnig S., Moffat K.G., and Baines R.A. Pumilio binds para mRNA and requires Nanos and Brat to regulate sodium current in Drosophila motoneurons. J. Neurosci. 28 (2008) 2099-2109
40. Newby L.M., and Jackson F.R. Drosophila ebony mutants have altered circadian activity rhythms but normal eclosion rhythms. J. Neurogenet. 7 (1991) 85-101
41. Newby L.M., and Jackson F.R. A new biological rhythm mutant of Drosophila melanogaster that identifies a gene with an essential embryonic function. Genetics 135 (1993) 1077-1090
42. Newby L.M., and Jackson F.R. Regulation of a specific circadian clock output pathway by lark, a putative RNA-binding protein with repressor activity. J. Neurobiol. 31 (1996) 117-128
43. Nimchinsky E.A., Oberlander A.M., and Svoboda K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21 (2001) 5139-5146
44. Nitabach M.N., and Taghert P.H. Organization of the Drosophila circadian control circuit. Curr. Biol. 18 (2008) R84-R93
45. Nitabach M.N., Blau J., and Holmes T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109 (2002) 485-495
46. Nitabach M.N., Wu Y., Sheeba V., Lemon W.C., Strumbos J., Zelensky P.K., White B.H., and Holmes T.C. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26 (2006) 479-489
47. Pan L., Zhang Y.Q., Woodruff E., and Broadie K. The Drosophila fragile X gene negatively regulates neuronal elaboration and synaptic differentiation. Curr. Biol. 14 (2004) 1863-1870
48. Park J.H., Helfrich-Forster C., Lee G., Liu L., Rosbash M., and Hall J.C. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3608-3613
49. Poulain C., Ferrus A., and Mallart A. Modulation of type A K+ current in Drosophila larval muscle by internal Ca2+; effects of the overexpression of frequenin. Pflugers. Arch. 427 (1994) 71-79
50. Renn S.C., Park J.H., Rosbash M., Hall J.C., and Taghert P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99 (1999) 791-802
51. Robinow S., and White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22 (1991) 443-461
52. Schroeder A.J., Genova G.K., Roberts M.A., Kleyner Y., Suh J., and Jackson F.R. Cell-specific expression of the lark RNA-binding protein in Drosophila results in morphological and circadian behavioral phenotypes. J. Neurogenet. 17 (2003) 139-169
53. Schweers B.A., Walters K.J., and Stern M. The Drosophila melanogaster translational repressor pumilio regulates neuronal excitability. Genetics 161 (2002) 1177-1185
54. Shang Y., Griffith L.C., and Rosbash M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 19587-19594
55. Sheeba V., Fogle K.J., Kaneko M., Rashid S., Chou Y.T., Sharma V.K., and Holmes T.C. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 18 (2008) 1537-1545
56. Sofola O., Sundram V., Ng F., Kleyner Y., Morales J., Botas J., Jackson F.R., and Nelson D.L. The Drosophila FMRP and LARK RNA-binding proteins function together to regulate eye development and circadian behavior. J. Neurosci. 28 (2008) 10200-10205
57. Stern M., and Ganetzky B. Altered synaptic transmission in Drosophila hyperkinetic mutants. J. Neurogenet. 5 (1989) 215-228
58. Stern M., and Ganetzky B. Identification and characterization of inebriated, a gene affecting neuronal excitability in Drosophila. J. Neurogenet. 8 (1992) 157-172
59. Stern M., Kreber R., and Ganetzky B. Dosage effects of a Drosophila sodium channel gene on behavior and axonal excitability. Genetics 124 (1990) 133-143
60. Taghert P.H., and Shafer O.T. Mechanisms of clock output in the Drosophila circadian pacemaker system. J. Biol. Rhythms 21 (2006) 445-457
61. Thyagarajan A., Strong M.J., and Szaro B.G. Post-transcriptional control of neurofilaments in development and disease. Exp. Cell Res. 313 (2007) 2088-2097
62. Vanselow K., and Kramer A. Role of phosphorylation in the mammalian circadian clock. Cold Spring Harbor Symp. Quant. Biol. 72 (2007) 167-176
63. Wu Y., Cao G., and Nitabach M.N. Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J. Biol. Rhythms 23 (2008) 117-128
64. Yeh E., Gustafson K., and Boulianne G.L. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7036-7040
65. Young M.W., and Kay S.A. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2 (2001) 702-715
66. Zearfoss N.R., Farley B.M., and Ryder S.P. Post-transcriptional regulation of myelin formation. Biochim. Biophys. Acta 1779 (2008) 486-494
67. Zhang X., McNeil G.P., Hilderbrand-Chae M.J., Franklin T.M., Schroeder A.J., and Jackson F.R. Circadian regulation of the lark RNA-binding protein within identifiable neurosecretory cells. J. Neurobiol. 45 (2000) 14-29
68. Zhang Y.Q., Bailey A.M., Matthies H.J., Renden R.B., Smith M.A., Speese S.D., Rubin G.M., and Broadie K. Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107 (2001) 591-603
69. Zheng X., and Sehgal A. Probing the relative importance of molecular oscillations in the circadian clock. Genetics 178 (2008) 1147-1155