Postsynaptic ERG potassium channels limit muscle excitability to allow distinct egg-laying behavior states in caenorhabditis elegans

Journal of Neuroscience

Volumn 33, Issue 2, 2013, Pages 761-775

  Collins, Kevin M ^a   Koelle, Michael R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL HERG;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EGG LAYING; GAIN OF FUNCTION MUTATION; MUSCLE CONTRACTION; NERVE EXCITABILITY; NONHUMAN; POLYMERASE CHAIN REACTION; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; VIDEORECORDING;

3' UNTRANSLATED REGIONS; ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; DNA; ETHER-A-GO-GO POTASSIUM CHANNELS; FEMALE; MICROSCOPY, CONFOCAL; MUSCLE CONTRACTION; MUSCLES; OVIPOSITION; PDZ DOMAINS; POLYMERASE CHAIN REACTION; SEROTONIN; SYNAPSES; TRANSGENES;

EID: 84872092156     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3896-12.2013     Document Type: Article

References (52)

1. Bany IA, Dong MQ, Koelle MR (2003) Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior. J Neurosci 23:8060-8069. Medline
2. Bellemer A, Hirata T, Romero MF, Koelle MR (2011) Two types of chloride transporters are required for GABA(A) receptor-mediated inhibition in C. elegans. EMBO J 30:1852-1863. CrossRef Medline
3. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94. Medline
4. Carnell L, Illi J, Hong SW, McIntire SL (2005) The G-protein-coupled serotonin receptor SER-1 regulates egg laying and male mating behaviors in Caenorhabditis elegans. J Neurosci 25:10671-10681. CrossRef Medline
5. Chase DL, Koelle MR (2004) Genetic analysis of RGS protein function in Caenorhabditis elegans. Meth Enzymol 389:305-320. CrossRef Medline
6. Clark SG, Lu X, Horvitz HR (1994) The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137:987-997. Medline
7. Dempsey CM, Mackenzie SM, Gargus A, Blanco G, Sze JY (2005) Serotonin (5HT), fluoxetine, imipramine and dopamine target distinct 5HT receptor signaling to modulate Caenorhabditis elegans egg-laying behavior. Genetics 169:1425-1436. Medline
8. Desai C, Garriga G, McIntire SL, Horvitz HR (1988) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336:638-646. CrossRef Medline
9. Dong MQ, Chase D, Patikoglou GA, Koelle MR (2000) Multiple RGS proteins alter neural G protein signaling to allow C. elegans to rapidly change behavior when fed. Genes Dev 14:2003-2014. Medline
10. Duerr JS, Gaskin J, Rand JB (2001) Identified neurons in C. elegans coexpress vesicular transporters for acetylcholine and monoamines. Am J Physiol Cell Physiol 280:C1616-C1622. Medline
11. Edwards SL, Charlie NK, Milfort MC, Brown BS, Gravlin CN, Knecht JE, Miller KG (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 6:e198. CrossRef Medline
12. Elkes DA, Cardozo DL, Madison J, Kaplan JM (1997) EGL-36 Shaw channels regulate C. elegans egg-laying muscle activity. Neuron 19:165-174. CrossRef Medline
13. Faumont S, Rondeau G, Thiele TR, Lawton KJ, McCormick KE, Sottile M, Griesbeck O, Heckscher ES, Roberts WM, Doe CQ, Lockery SR (2011) An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans. PLoS ONE 6:e24666. CrossRef Medline
14. Frøkjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, Grunnet M, Jorgensen EM (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40:1375-1383. CrossRef Medline
15. Gao S, Zhen M (2011) Action potentials drive body wall muscle contractions in Caenorhabditis elegans. Proc Natl Acad Sci U S A 108:2557-2562. CrossRef Medline
16. Garcia LR, Sternberg PW (2003) Caenorhabditis elegans UNC-103 ERG-like potassium channel regulates contractile behaviors of sex muscles in males before and during mating. J Neurosci 23:2696-2705. Medline
17. Hapiak VM, Hobson RJ, Hughes L, Smith K, Harris G, Condon C, Komuniecki P, Komuniecki RW (2009) Dual excitatory and inhibitory serotonergic inputs modulate egg laying in Caenorhabditis elegans. Genetics 181:153-163. Medline
18. Hardaker LA, Singer E, Kerr R, Zhou G, Schafer WR (2001) Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditis elegans. J Neurobiol 49:303-313. CrossRef Medline
19. Hobson RJ, Hapiak VM, Xiao H, Buehrer KL, Komuniecki PR, Komuniecki RW (2006) SER-7, a Caenorhabditis elegans 5-HT7-like receptor, is essential for the 5-HT stimulation of pharyngeal pumping and egg laying. Genetics 172:159-169. Medline
20. Hu Z, Pym EC, Babu K, Vashlishan Murray AB, Kaplan JM (2011) A neuropeptide-mediated stretch response links muscle contraction to changes in neurotransmitter release. Neuron 71:92-102. CrossRef Medline
21. Johnstone DB, Wei A, Butler A, Salkoff L, Thomas JH (1997) Behavioral defects in C. elegans egl-36 mutants result from potassium channels shifted in voltage-dependence of activation. Neuron 19:151-164. CrossRef Medline
22. Jose AM, Bany IA, Chase DL, Koelle MR (2007) Aspecific 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. Medline
23. Kim J, Poole DS, Waggoner LE, Kempf A, Ramirez DS, Treschow PA, Schafer WR (2001) Genes affecting the activity of nicotinic receptors involved in Caenorhabditis elegans egg-laying behavior. Genetics 157:1599-1610. Medline
24. Kuzhikandathil EV, Oxford GS (2000) Dominant-negative mutants identify a role for GIRK channels in D3 dopamine receptor-mediated regulation of spontaneous secretory activity. J Gen Physiol 115:697-706. CrossRef Medline
25. + channels. PLoS Genet 3:1622-1632. Medline
26. 2+ channel cause myotonia in Caenorhabditis elegans. EMBO J 16:6066-6076. CrossRef Medline
27. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461. CrossRef Medline
28. Li W, Feng Z, Sternberg PW, Xu XZ (2006) A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684-687. CrossRef Medline
29. Liu DW, Thomas JH (1994) Regulation of a periodic motor program in C. elegans. J Neurosci 14:1953-1962. Medline
30. Liu P, Ge Q, Chen B, Salkoff L, Kotlikoff MI, Wang ZW (2011) Genetic dissection of ion currents underlying all-or-none action potentials in C. elegans body-wall muscle cells. J Physiol 589:101-117. CrossRef Medline
31. Lüscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550. CrossRef Medline
32. Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69: 291-316. CrossRef Medline
33. McDonald TF, Pelzer S, Trautwein W, Pelzer DJ (1994) Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev 74:365-507. Medline
34. McNally K, Audhya A, Oegema K, McNally FJ (2006) Katanin controls mitotic and meiotic spindle length. J Cell Biol 175:881-891. CrossRef Medline
35. Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451-482. CrossRef Medline
36. o-coupled receptor, inhibits function of hermaphrodite-specific motor neurons to regulate Caenorhabditis elegans egg-laying behavior. J Neurosci 24:8522-8530. CrossRef Medline
37. Petersen CI, McFarland TR, Stepanovic SZ, Yang P, Reiner DJ, Hayashi K, George AL, Roden DM, Thomas JH, Balser JR (2004) In vivo identification of genes that modify ether-a-go-go-related gene activity in Caenorhabditis elegans may also affect human cardiac arrhythmia. Proc Natl Acad Sci U S A 101:11773-11778. CrossRef Medline
38. Reiner DJ, Weinshenker D, Tian H, Thomas JH, Nishiwaki K, Miwa J, Gruninger T, Leboeuf B, Garcia LR (2006) Behavioral genetics of Caenorhabditis elegans unc-103-encoded erg-like K(+) channel. J Neurogenet 20:41-66. CrossRef Medline
39. Ringstad N, Horvitz HR (2008) FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans. Nat Neurosci 11:1168-1176. CrossRef Medline
40. Sanguinetti MC, Tristani-Firouzi M (2006) hERG potassium channels and cardiac arrhythmia. Nature 440:463-469. CrossRef Medline
41. Shyn SI, Kerr R, Schafer WR (2003) Serotonin and Go modulate functional states of neurons and muscles controlling C. elegans egg-laying behavior. Curr Biol 13:1910-1915. CrossRef Medline
42. Spilker KA, Wang GJ, Tugizova MS, Shen K (2012) C. elegans Muscleblind homolog mbl-1 functions in neurons to regulate synapse formation. Neural Dev 7:7. CrossRef Medline
43. Tanis JE, Moresco JJ, Lindquist RA, Koelle MR (2008) Regulation of serotonin biosynthesis by the G proteins Galphao and Galphaq controls serotonin signaling in Caenorhabditis elegans. Genetics 178:157-169. CrossRef Medline
44. Tanis JE, Bellemer A, Moresco JJ, Forbush B, Koelle MR (2009) The potassium chloride cotransporter KCC-2 coordinates development of inhibitory neurotransmission and synapse structure in Caenorhabditis elegans. J Neurosci 29:9943-9954. CrossRef Medline
45. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improvedGCaMPcalcium indicators. Nat Methods 6:875-881. CrossRef Medline
46. Waggoner LE, Zhou GT, Schafer RW, Schafer WR (1998) Control of alternative behavioral states by serotonin in Caenorhabditis elegans. Neuron 21:203-214. CrossRef Medline
47. Waggoner LE, Dickinson KA, Poole DS, Tabuse Y, Miwa J, Schafer WR (2000) Long-term nicotine adaptation in Caenorhabditis elegans involves PKC-dependent changes in nicotinic receptor abundance. J Neurosci 20: 8802-8811. Medline
48. Wang ZW, Saifee O, Nonet ML, Salkoff L (2001) SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32:867-881. CrossRef Medline
49. Weinshenker D, Garriga G, Thomas JH (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15:6975-6985. Medline
50. Weinshenker D, Wei A, Salkoff L, Thomas JH (1999) Block of an ether-ago-go-like K(+) channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans. J Neurosci 19:9831-9840. Medline
51. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Phil Trans Royal Soc 314:1-340. CrossRef
52. Zhang M, Chung SH, Fang-Yen C, Craig C, Kerr RA, Suzuki H, Samuel AD, Mazur E, Schafer WR (2008) A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior. Curr Biol 18:1445-1455. CrossRef Medline