SLO-2 potassium channel is an important regulator of neurotransmitter release in Caenorhabditis elegans

Nature Communications

Volumn 5, Issue , 2014, Pages

  Liu, Ping ^a   Chen, Bojun ^a   Wang, Zhao Wen ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; POSTSYNAPTIC RECEPTOR; POTASSIUM CHANNEL; POTASSIUM CHANNEL SLO 2; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CAENORHABDITIS ELEGANS PROTEIN; CALCIUM CHANNEL; CARRIER PROTEIN; EGL-19 PROTEIN, C ELEGANS; MUSCLE PROTEIN; SLO-2 PROTEIN, C ELEGANS;

BRAIN; MUTATION; NEMATODE; NEUROLOGY; POTASSIUM; SIGNALING;

ARTICLE; CAENORHABDITIS ELEGANS; CALCIUM CELL LEVEL; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; LOSS OF FUNCTION MUTATION; MEMBRANE POTENTIAL; MOTONEURON; MUSCLE CELL; NEUROMUSCULAR TRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHYSIOLOGICAL PROCESS; POSTSYNAPTIC POTENTIAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; METABOLISM; NEUROMUSCULAR SYNAPSE;

CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM CHANNELS; GABAERGIC NEURONS; MEMBRANE TRANSPORT PROTEINS; MOTOR NEURONS; MUSCLE CELLS; MUSCLE PROTEINS; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS;

EID: 84923346293     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6155     Document Type: Article

References (63)

1. Trussell, L. O. & Roberts, M. T. in Molecular Mechanisms of Neurotransmitter Release (ed. Wang, Z. W.) (Humana Press, 2008).
2. Bhattacharjee, A., Gan, L. & Kaczmarek, L. K. Localization of the Slack potassium channel in the rat central nervous system. J. Comp. Neurol. 454, 241-254 (2002).
3. Bhattacharjee, A., von Hehn, C. A., Mei, X. & Kaczmarek, L. K. Localization of the Na+-activated K+ channel Slick in the rat central nervous system. J. Comp. Neurol. 484, 80-92 (2005).
4. Hage, T. A. & Salkoff, L. Sodium-activated potassium channels are functionally coupled to persistent sodium currents. J. Neurosci. 32, 2714-2721 (2012).
5. Budelli, G. et al. Na+-activated K+ channels express a large delayed outward current in neurons during normal physiology. Nat. Neurosci. 12, 745-750 (2009).
6. Lu, S., Das, P., Fadool, D. A. & Kaczmarek, L. K. The slack sodium-activated potassium channel provides a major outward current in olfactory neurons of Kv1.3-/-super-smeller mice. J. Neurophysiol. 103, 3311-3319 (2010).
7. Huang, F. et al. TMEM16C facilitates Na+-activated K+ currents in rat sensory neurons and regulates pain processing. Nat. Neurosci. 16, 1284-1290 (2013).
8. Nuwer, M. O., Picchione, K. E. & Bhattacharjee, A. PKA-induced internalization of slack KNa channels produces dorsal root ganglion neuron hyperexcitability. J. Neurosci. 30, 14165-14172 (2010).
9. Zhang, Y. et al. Regulation of neuronal excitability by interaction of fragile x mental retardation protein with slack potassium channels. J. Neurosci. 32, 15318-15327 (2012).
10. Barcia, G. et al. De novo gain-of-function KCNT1 channel mutations cause malignant migrating partial seizures of infancy. Nat. Genet. 44, 1255-1259 (2012).
11. Heron, S. E. et al. Missense mutations in the sodium-gated potassium channel gene KCNT1 cause severe autosomal dominant nocturnal frontal lobe epilepsy. Nat. Genet. 44, 1188-1190 (2012).
12. Vanderver, A. et al. Identification of a novel de novo p.Phe932Ile KCNT1 mutation in a patient with leukoencephalopathy and severe epilepsy. Pediatr. Neurol. 50, 112-114 (2014).
13. Ishii, A. et al. A recurrent KCNT1 mutation in two sporadic cases with malignant migrating partial seizures in infancy. Gene 531, 467-471 (2013).
14. Dhamija, R., Wirrell, E., Falcao, G., Kirmani, S. & Wong-Kisiel, L. C. Novel de novo SCN2A mutation in a child with migrating focal seizures of infancy. Pediatr. Neurol. 49, 486-488 (2013).
15. Yuan, A. et al. The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37, 765-773 (2003).
16. Bhattacharjee, A. et al. Slick (Slo2.1), a rapidly-gating sodium-activated potassium channel inhibited by ATP. J. Neurosci. 23, 11681-11691 (2003).
17. Dryer, S. E. Molecular identification of the Na+-activated K+ channel. Neuron 37, 727-728 (2003).
18. Kaczmarek, L. K. Slack, slick and sodium-activated potassium channels. ISRN Neurosci. 2013 pii 354262 (2013).
19. Bhattacharjee, A. & Kaczmarek, L. K. For K+ channels, Na+ is the new Ca2+. Trends Neurosci. 28, 422-428 (2005).
20. Wallen, P. et al. Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J. Physiol. 585, 75-90 (2007).
21. Yang, B., Desai, R. & Kaczmarek, L. K. Slack and Slick KNa channels regulate the accuracy of timing of auditory neurons. J. Neurosci. 27, 2617-2627 (2007).
22. Nanou, E. et al. Na+-mediated coupling between AMPA receptors and KNa channels shapes synaptic transmission. Proc. Natl Acad. Sci. USA 105, 20941-20946 (2008).
23. Yuan, A. et al. SLO-2, a K+ channel with an unusual Cl-dependence. Nat. Neurosci. 3, 771-779 (2000).
24. Salkoff, L., Butler, A., Ferreira, G., Santi, C. & Wei, A. High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7, 921-931 (2006).
25. Liu, P. et al. Genetic dissection of ion currents underlying all-or-none action potentials in C. elegans body-wall muscle cells. J. Physiol. 589, 101-117 (2011).
26. Lim, H. H. et al. Identification and characterization of a putative C. elegans potassium channel gene (Ce-slo-2) distantly related to Ca2+-activated K+ channels. Gene 240, 35-43 (1999).
27. Liu, P., Chen, B. & Wang, Z. W. Postsynaptic current bursts instruct action potential firing at a graded synapse. Nat. Commun. 4, 1911 (2013).
28. de Bono, M. & Maricq, A. V. Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 28, 451-501 (2005).
29. Chalfie, M. White, J. in The Nematode Caenorhabditis elegans. (ed. Wood,W. B., Researchers TCoCe) (Cold Spring Harbor Laboratory Press, 1988).
30. Wei, A. et al. Efficient isolation of targeted Caenorhabditis elegans deletion strains using highly thermostable restriction endonucleases and PCR. Nucleic Acids Res. 30, e110 (2002).
31. Mahoney, T. R. et al. Regulation of synaptic transmission by RAB-3 and RAB-27 in Caenorhabditis elegans. Mol. Biol. Cell. 17, 2617-2625 (2006).
32. Nonet, M. L. et al. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8061-8073 (1997).
33. Salkoff, L. et al. in WormBook (ed. The C. elegans Research Community) doi:doi/10.1895/wormbook.1.42.1 (2005).
34. Santi, C. M. et al. Dissection of K+ currents in Caenorhabditis elegans muscle cells by genetics and RNA interference. Proc. Natl Acad. Sci. USA 100, 14391-14396 (2003).
35. Fawcett, G. L. et al. Mutant analysis of the Shal (Kv4) voltage-gated fast transient K+ channel in Caenorhabditis elegans. J. Biol. Chem. 281, 30725-30735 (2006).
36. Wang, Z. W., Saifee, O., Nonet, M. L. & Salkoff, L. SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32, 867-881 (2001).
37. Liu, Q., Chen, B., Ge, Q. & Wang, Z. W. Presynaptic Ca2+/calmodulindependent protein kinase II modulates neurotransmitter release by activating BK channels at Caenorhabditis elegans neuromuscular junction. J. Neurosci. 27, 10404-10413 (2007).
38. Zhang, Z. et al. SLO-2 isoforms with unique Ca2+-and voltage-dependence characteristics confer sensitivity to hypoxia in C. elegans. Channels (Austin) 7, 194-205 (2013).
39. Bargmann, C. I. Neurobiology of the Caenorhabditis elegans genome. Science 282, 2028-2033 (1998).
40. Bauer Huang, S. L. et al. Left-right olfactory asymmetry results from antagonistic functions of voltage-activated calcium channels and the Raw repeat protein OLRN-1 in C. elegans. Neural. Dev. 2, 24 (2007).
41. Steger, K. A., Shtonda, B. B., Thacker, C., Snutch, T. P. & Avery, L. The C. elegans T-type calcium channel CCA-1 boosts neuromuscular transmission. J. Exp. Biol. 208, 2191-2203 (2005).
42. Lee, R. Y., Lobel, L., Hengartner, M., Horvitz, H. R. & Avery, L. Mutations in the a1 subunit of an L-type voltage-activated Ca2+ channel cause myotonia in Caenorhabditis elegans. EMBO J. 16, 6066-6076 (1997).
43. Feng, Z. et al. A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels. Cell 127, 621-633 (2006).
44. Tanis, J. E. et al. CLHM-1 is a functionally conserved and conditionally toxic Ca2+-permeable ion channel in Caenorhabditis elegans. J. Neurosci. 33, 12275-12286 (2013).
45. Yeh, E. et al. A putative cation channel, NCA-1, and a novel protein, UNC-80, transmit neuronal activity in C. elegans. PLoS Biol. 6, e55 (2008).
46. Jospin, M. et al. UNC-80 and the NCA ion channels contribute to endocytosis defects in synaptojanin mutants. Curr. Biol. 17, 1595-1600 (2007).
47. Maryon, E. B., Coronado, R. & Anderson, P. unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J. Cell Biol. 134, 885-893 (1996).
48. Liu, Q. et al. Presynaptic ryanodine receptors are required for normal quantal size at the Caenorhabditis elegans neuromuscular junction. J. Neurosci. 25, 6745-6754 (2005).
49. Hyde, R., Corkins, M. E., Somers, G. A. & Hart, A. C. PKC-1 acts with the ERK MAPK signaling pathway to regulate Caenorhabditis elegans mechanosensory response. Genes Brain Behav. 10, 286-298 (2011).
50. Glauser, D. A. et al. Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics 188, 91-103 (2011).
51. Humphrey, J. A. et al. A putative cation channel and its novel regulator: cross-species conservation of effects on general anesthesia. Curr. Biol. 17, 624-629 (2007).
52. Enyedi, P. & Czirjak, G. Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol. Rev. 90, 559-605 (2010).
53. Chen, B., Liu, P., Zhan, H. & Wang, Z. W. Dystrobrevin controls neurotransmitter release and muscle Ca2+ transients by localizing BK channels in Caenorhabditis elegans. J. Neurosci. 31, 17338-17347 (2011).
54. Saheki, Y. & Bargmann, C. I. Presynaptic CaV2 calcium channel traffic requires CALF-1 and the a2d subunit UNC-36. Nat. Neurosci. 12, 1257-1265 (2009).
55. Davies, A. G. et al. A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 115, 655-666 (2003).
56. Chen, B. et al. A novel auxiliary subunit critical to BK channel function in Caenorhabditis elegans. J. Neurosci. 30, 16651-16661 (2010).
57. Kim, H. et al. The dystrophin complex controls bk channel localization and muscle activity in Caenorhabditis elegans. PLoS Genet. 5, e1000780 (2009).
58. Carre-Pierrat, M. et al. The SLO-1 BK channel of Caenorhabditis elegans is critical for muscle function and is involved in dystrophin-dependent muscle dystrophy. J. Mol. Biol. 358, 387-395 (2006).
59. Abraham, L. S., Oh, H. J., Sancar, F., Richmond, J. E. & Kim, H. An alpha-catulin homologue controls neuromuscular function through localization of the dystrophin complex and BK channels in Caenorhabditis elegans. PLoS Genet. 6 pii e1001077 (2010).
60. Chen, B. et al. a-Catulin CTN-1 is required for BK channel subcellular localization in C. elegans body-wall muscle cells. EMBO J. 29, 3184-3195 (2010).
61. Jegla, T. J., Zmasek, C. M., Batalov, S. & Nayak, S. K. Evolution of the human ion channel set. Comb. Chem. High. Throughput. Screen. 12, 2-23 (2009).
62. Evans, T. in WormBook (ed. The C. elegans Research Community) doi:doi/10.1895/wormbook.1.108.1 (2006).
63. White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1-340 (1986).