Reduced Sleep-Like Quiescence in Both Hyperactive and Hypoactive Mutants of the Galphaq Gene egl-30 during lethargus in Caenorhabditis elegans

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Schwarz, Juliane ^a   Bringmann, Henrik ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR; CAENORHABDITIS ELEGANS; CELL ACTIVITY; CONTROLLED STUDY; EGL 30 GENE; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; LARVAL STAGE; LOSS OF FUNCTION MUTATION; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; REGULATOR GENE; SIGNAL TRANSDUCTION; SLEEP LIKE BEHAVIOR;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; LARVA; LETHARGY; MECHANOTRANSDUCTION, CELLULAR; MUTATION; NEURONS; SIGNAL TRANSDUCTION; SLEEP; WAKEFULNESS;

EID: 84884483775     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075853     Document Type: Article

References (56)

1. Campbell SS, Tobler I, (1984) Animal sleep: a review of sleep duration across phylogeny. Neurosci Biobehav Rev 8: 269-300. doi:10.1016/0149-7634(84)90054-X. PubMed: 6504414.
2. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, et al. (2008) Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451: 569-572. doi:10.1038/nature06535. PubMed: 18185515.
3. Cassada RC, Russell RL, (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46: 326-342. doi:10.1016/0012-1606(75)90109-8. PubMed: 1183723.
4. Schwarz J, Lewandrowski I, Bringmann H, (2011) Reduced activity of a sensory neuron during a sleep-like state in Caenorhabditis elegans. Curr Biol 21: R983-R984. doi:10.1016/j.cub.2011.10.046. PubMed: 22192827.
5. Schwarz J, Spies J, Bringmann H, (2012) Reduced muscle contraction and a relaxed posture during sleep-like Lethargus. Worm 1: 12-14.
6. Iwanir S, Tramm N, Nagy S, Wrigth C, et al DI,. (2012) The microarchiteture of C. elegans behavior during lethargus: homeostatic bout dynamics, a typical body-posture and regulation by a central neuron. Sleep.
7. Singh K, Huang H, Hart AC, (2013) Do C. elegans Sleep? A Closer Look. Sleep 36: 307-308. PubMed: 23450901.
8. Jeon M, Gardner HF, Miller EA, Deshler J, Rougvie AE, (1999) Similarity of the C. elegans developmental timing protein LIN-42 to circadian rhythm proteins. Science 286: 1141-1146. doi:10.1126/science.286.5442.1141. PubMed: 10550049.
9. Monsalve GC, Van Buskirk C, Frand AR, (2011) LIN-42/PERIOD controls cyclical and developmental progression of C. elegans molts. Curr Biol 21: 2033-2045. doi:10.1016/j.cub.2011.10.054. PubMed: 22137474.
10. Avery L, (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917. PubMed: 8462849.
11. Van Buskirk C, Sternberg PW, (2007) Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans. Nat Neurosci 10: 1300-1307. doi:10.1038/nn1981. PubMed: 17891142.
12. Singh K, Chao MY, Somers GA, Komatsu H, Corkins ME, et al. (2011) C. elegans Notch Signaling Regulates Adult Chemosensory Response and Larval Molting Quiescence. Curr Biol 21: 825-834. doi:10.1016/j.cub.2011.07.043. PubMed: 21549604.
13. Brundage L, Avery L, Katz A, Kim UJ, Mendel JE, et al. (1996) Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16: 999-1009. doi:10.1016/S0896-6273(00)80123-3. PubMed: 8630258.
14. Lackner MR, Nurrish SJ, Kaplan JM, (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335-346. doi:10.1016/S0896-6273(00)80848-X. PubMed: 10571228.
15. Trent C, Tsuing N, Horvitz HR, (1983) Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104: 619-647. PubMed: 11813735.
16. Park EC, Horvitz HR, (1986) Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics 113: 821-852. PubMed: 3744028.
17. Doi M, Iwasaki K, (2002) Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33: 249-259. doi:10.1016/S0896-6273(01)00587-6. PubMed: 11804572.
18. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94. PubMed: 4366476.
19. Bringmann H, (2011) Agarose hydrogel microcompartments for imaging sleep- and wake-like behavior and nervous system development in Caenorhabditis elegans larvae. J Neurosci Methods 201: 78-88. doi:10.1016/j.jneumeth.2011.07.013. PubMed: 21801751.
20. Iglewicz B, Hoaglin DC, (1993) How to Detect and Handle Outliers. Milwaukee, WI: Amercian Society for Quality Control.
21. Rogulja D, Young MW, (2012) Control of sleep by cyclin A and its regulator. Science 335: 1617-1621. doi:10.1126/science.1212476. PubMed: 22461610.
22. Koh K, Joiner WJ, Wu MN, Yue Z, Smith CJ, et al. (2008) Identification of SLEEPLESS, a sleep-promoting factor. Science 321: 372-376. doi:10.1126/science.1155942. PubMed: 18635795.
23. Schade MA, Reynolds NK, Dollins CM, Miller KG, (2005) Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha(s) pathway and define a third major branch of the synaptic signaling network. Genetics 169: 631-649. doi:10.1534/genetics.104.032334. PubMed: 15489510.
24. Robatzek M, Thomas JH, (2000) Calcium/calmodulin-dependent protein kinase II regulates Caenorhabditis elegans locomotion in concert with a G(o)/G(q) signaling network. Genetics 156: 1069-1082. PubMed: 11063685.
25. Koelle MR, Horvitz HR, (1996) EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-125. doi:10.1016/S0092-8674(00)80998-8. PubMed: 8548815.
26. Miller KG, Emerson MD, McManus JR, Rand JB, (2000) RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system. Neuron 27: 289-299. doi:10.1016/S0896-6273(00)00037-4. PubMed: 10985349.
27. Avery L, Bargmann CI, Horvitz HR, (1993) The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions. Genetics 134: 455-464. PubMed: 8325482.
28. Maruyama IN, Brenner S, (1991) A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc Natl Acad Sci U S A 88: 5729-5733. doi:10.1073/pnas.88.13.5729. PubMed: 2062851.
29. Tabuse Y, Nishiwaki K, Miwa J, (1989) Mutations in a protein kinase C homolog confer phorbol ester resistance on Caenorhabditis elegans. Science 243: 1713-1716. doi:10.1126/science.2538925. PubMed: 2538925.
30. Weinshenker D, Garriga G, Thomas JH, (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15: 6975-6985. PubMed: 7472454.
31. Williams SL, Lutz S, Charlie NK, Vettel C, Ailion M, et al. (2007) Trio's Rho-specific GEF domain is the missing Galpha q effector in C. elegans. Genes Dev 21: 2731-2746. doi:10.1101/gad.1592007. PubMed: 17942708.
32. Hajdu-Cronin YM, Chen WJ, Patikoglou G, Koelle MR, Sternberg PW, (1999) Antagonism between G(o)alpha and G(q)alpha in Caenorhabditis elegans: the RGS protein EAT-16 is necessary for G(o)alpha signaling and regulates G(q)alpha activity. Genes Dev 13: 1780-1793. doi:10.1101/gad.13.14.1780. PubMed: 10421631.
33. Moorman C, Plasterk RH, (2002) Functional characterization of the adenylyl cyclase gene sgs-1 by analysis of a mutational spectrum in Caenorhabditis elegans. Genetics 161: 133-142. PubMed: 12019229.
34. Schafer WR, Kenyon CJ, (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375: 73-78. doi:10.1038/375073a0. PubMed: 7723846.
35. Schafer WR, Sanchez BM, Kenyon CJ, (1996) Genes affecting sensitivity to serotonin in Caenorhabditis elegans. Genetics 143: 1219-1230. PubMed: 8807295.
36. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G, (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564. doi:10.1038/35000609. PubMed: 10676966.
37. Jansen G, Weinkove D, Plasterk RH, (2002) The G-protein gamma subunit gpc-1 of the nematode C.elegans is involved in taste adaptation. EMBO J 21: 986-994. doi:10.1093/emboj/21.5.986. PubMed: 11867526.
38. Shcherbo D, Murphy CS, Ermakova GV, Solovieva EA, Chepurnykh TV, et al. (2009) Far-red fluorescent tags for protein imaging in living tissues. Biochem J 418: 567-574. doi:10.1042/BJ20081949. PubMed: 19143658.
39. Redemann S, Schloissnig S, Ernst S, Pozniakowsky A, Ayloo S, et al. (2011) Codon adaptation-based control of protein expression in C. elegans. Nat Methods 8: 250-252. doi:10.1038/nmeth.1565. PubMed: 21278743.
40. Jose AM, Bany IA, Chase DL, Koelle MR, (2007) A specific subset of transient receptor potential vanilloid-type channel subunits in Caenorhabditis elegans endocrine cells function as mixed heteromers to promote neurotransmitter release. Genetics 175: 93-105. PubMed: 17057248.
41. Hughes TE, Zhang H, Logothetis DE, Berlot CH, (2001) Visualization of a functional Galpha q-green fluorescent protein fusion in living cells. Association with the plasma membrane is disrupted by mutational activation and by elimination of palmitoylation sites, but not be activation mediated by receptors or AlF4. J Biol Chem 276: 4227-4235. doi:10.1074/jbc.M007608200. PubMed: 11076942.
42. Maduro M, Pilgrim D, (1995) Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141: 977-988. PubMed: 8582641.
43. Fire A, Waterston RH, (1989) Proper expression of myosin genes in transgenic nematodes. EMBO J 8: 3419-3428. PubMed: 2583105.
44. Kaplan JM, Horvitz HR, (1993) A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci U S A 90: 2227-2231. doi:10.1073/pnas.90.6.2227. PubMed: 8460126.
45. Guo ZV, Hart AC, Ramanathan S, (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods 6: 891-896. doi:10.1038/nmeth.1397. PubMed: 19898486.
46. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI, (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207-218. doi:10.1016/0092-8674(95)90162-0. PubMed: 7585938.
47. Ezcurra M, Tanizawa Y, Swoboda P, Schafer WR, (2011) Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling. EMBO J 30: 1110-1122. doi:10.1038/emboj.2011.22. PubMed: 21304491.
48. Edwards SL, Charlie NK, Milfort MC, Brown BS, Gravlin CN, et al. (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLOS Biol 6: e198. doi:10.1371/journal.pbio.0060198. PubMed: 18687026.
49. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, et al. (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5: 956-964. PubMed: 3981252.
50. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR, (2005) Tyramine Functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46: 247-260. doi:10.1016/j.neuron.2005.02.024. PubMed: 15848803.
51. Berger AJ, Hart AC, Kaplan JM, (1998) G alphas-induced neurodegeneration in Caenorhabditis elegans. J Neurosci 18: 2871-2880. PubMed: 9526004.
52. Miller KG, Emerson MD, Rand JB, (1999) Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24: 323-333. doi:10.1016/S0896-6273(00)80847-8. PubMed: 10571227.
53. Llinás R, Jahnsen H, (1982) Electrophysiology of mammalian thalamic neurones in vitro. Nature 297: 406-408. doi:10.1038/297406a0. PubMed: 7078650.
54. Zhan XJ, Cox CL, Rinzel J, Sherman SM, (1999) Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat's lateral geniculate nucleus. J Neurophysiol 81: 2360-2373. PubMed: 10322072.
55. Steriade M, McCormick DA, Sejnowski TJ, (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685. doi:10.1126/science.8235588. PubMed: 8235588.
56. Coulon P, Kanyshkova T, Broicher T, Munsch T, Wettschureck N, et al. (2010) Activity Modes in Thalamocortical Relay Neurons are Modulated by G(q)/G(11) Family G-proteins- Serotonergic and Glutamatergic Signaling. Front Cell Neurosci 4: 132. PubMed: 21267426.