Dystrobrevin controls neurotransmitter release and muscle Ca 2+transients by localizing BK channels in Caenorhabditis elegans

Journal of Neuroscience

Volumn 31, Issue 48, 2011, Pages 17338-17347

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

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROBREVIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; BK CHANNEL GENE SLO 1; CAENORHABDITIS ELEGANS; CALCIUM TRANSPORT; DYSTROBREVIN GENE DYB 1; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC SCREENING; MUSCLE CELL; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPTOSOME; WESTERN BLOTTING;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; DYSTROPHIN-ASSOCIATED PROTEINS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; NEURONS; PHENOTYPE; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION;

EID: 82555169475     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3638-11.2011     Document Type: Article

References (48)

1. Abraham LS, Oh HJ, Sancar F, Richmond JE, Kim H (2010) An alphacatulin homologue controls neuromuscular function through localization of the dystrophin complex and BK channels in Caenorhabditis elegans. PLoS Genet 6:e1001077.
2. Allen DG, Gervasio OL, Yeung EW, Whitehead NP (2010) Calcium and the damage pathways in muscular dystrophy. Can J Physiol Pharmacol 88:83-91.
3. Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331-346.
4. Bargmann CI (1998) Neurobiology of the Caenorhabditis elegans genome. Science 282:2028-2033.
5. Blake DJ, Hawkes R, Benson MA, Beesley PW (1999) Different dystrophinlike complexes are expressed in neurons and glia. J Cell Biol 147:645-658.
6. Blatz AL, Magleby KL (1984) Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle. J Gen Physiol 84:1-23.
7. Carre-Pierrat M, Grisoni K, Gieseler K, Mariol MC, Martin E, Jospin M, Allard B, Ségalat L (2006) The SLO-1 BK channel of Caenorhabditis elegans is critical for muscle function and is involved in dystrophindependent muscle dystrophy. J Mol Biol 358:387-395.
8. Chen B, Liu P, Wang SJ, Ge Q, Zhan H, Mohler WA, Wang ZW (2010a) α-Catulin CTN-1 is required for BK channel subcellular localization in C. elegans body-wall muscle cells. EMBO J 29:3184-3195.
9. Chen B, Ge Q, Xia XM, Liu P, Wang SJ, Zhan H, Eipper BA, Wang ZW (2010b) A novel auxiliary subunit critical to BK channel function in Caenorhabditis elegans. J Neurosci 30:16651-16661.
10. Constantin B, Sebille S, Cognard C (2006) New insights in the regulation of calcium transfers by muscle dystrophin-based cytoskeleton: implications in DMD. J Muscle Res Cell Motil 27:375-386.
11. Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7:762-773.
12. Davis MW, Hammarlund M, Harrach T, Hullett P, Olsen S, Jorgensen EM (2005) Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6:118.
13. Deconinck N, Dan B (2007) Pathophysiology of duchenne muscular dystrophy: current hypotheses. Pediatr Neurol 36:1-7.
14. Duncan CJ (1978) Role of intracellular calcium in promoting muscle damage: a strategy for controlling the dystrophic condition. Experientia 34:1531-1535.
15. Francis GR, Waterston RH (1985) Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol 101:1532-1549.
16. Gieseler K, Bessou C, Ségalat L (1999) Dystrobrevin- and dystrophin-like mutants display similar phenotypes in the nematode Caenorhabditis elegans. Neurogenetics 2:87-90.
17. Giugia J, Gieseler K, Arpagaus M, Ségalat L (1999) Mutations in the dystrophin-like dys-1 gene of Caenorhabditis elegans result in reduced acetylcholinesterase activity. FEBS Lett 463:270-272.
18. Grady RM, Grange RW, Lau KS, Maimone MM, Nichol MC, Stull JT, Sanes JR (1999) Role for alpha-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat Cell Biol 1:215-220.
19. Grady RM, Wozniak DF, Ohlemiller KK, Sanes JR (2006) Cerebellar synaptic defects and abnormal motor behavior in mice lacking α- and β-dystrobrevin. J Neurosci 26:2841-2851.
20. Holzfeind PJ, Ambrose HJ, Newey SE, Nawrotzki RA, Blake DJ, Davies KE (1999) Tissue-selective expression of alpha-dystrobrevin is determined by multiple promoters. J Biol Chem 274:6250-6258.
21. + channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci 21:9585-9597.
22. Jones KJ, Compton AG, Yang N, Mills MA, Peters MF, Mowat D, Kunkel LM, Froehner SC, North KN (2003) Deficiency of the syntrophins and alpha-dystrobrevin in patients with inherited myopathy. Neuromuscul Disord 13:456-467.
23. 2+ channel EGL-19 controls body wall muscle function in Caenorhabditis elegans. J Cell Biol 159:337-348.
24. Kim H, Pierce-Shimomura JT, Oh HJ, Johnson BE, Goodman MB, McIntire SL (2009) The dystrophin complex controls bk channel localization and muscle activity in Caenorhabditis elegans. PLoS Genet 5:e1000780.
25. + channel. J Biol Chem 270:22434-22439.
26. Koushika SP, Richmond JE, Hadwiger G, Weimer RM, Jorgensen EM, Nonet ML (2001) A post-docking role for active zone protein Rim. Nat Neurosci 4:997-1005.
27. + channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci U S A 79:805-809.
28. 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.
29. +/calmodulindependent protein kinase II modulates neurotransmitter release by activating BK channels at Caenorhabditis elegans neuromuscular junction. J Neurosci 27:10404-10413.
30. Moerman DG, Fire A (1997) Muscle: structure, function, and development. In: C. elegans II (Riddle RL, Blumenthal T, Meyer BJ, Priess JR, eds), pp 417-470.
31. Plainview, NY: Cold Spring Harbor Laboratory Press. Ohlendieck K, Campbell KP (1991) Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 115:1685-1694.
32. Pawlikowski BT, MaimoneMM (2008) alpha-Dystrobrevin isoforms differ in their colocalization with and stabilization of agrin-induced acetylcholine receptor clusters. Neuroscience 154:582-594.
33. Peters MF, Sadoulet-Puccio HM, Grady MR, Kramarcy NR, Kunkel LM, Sanes JR, Sealock R, Froehner SC (1998) Differential membrane localization and intermolecular associations of alpha-dystrobrevin isoforms in skeletal muscle. J Cell Biol 142:1269-1278.
34. Raffaelli G, Saviane C, Mohajerani MH, Pedarzani P, Cherubini E (2004) BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J Physiol 557:147-157.
35. Rees ML, Lien CF, Górecki DC (2007) Dystrobrevins in muscle and nonmuscle tissues. Neuromuscul Disord 17:123-134.
36. Richmond JE, Davis WS, Jorgensen EM (1999) UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci 2:959-964.
37. Richmond JE, Weimer RM, Jorgensen EM (2001) An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412:338-341.
38. Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717-720.
39. Ríos E, Pizarro G, Stefani E (1992) Charge movement and the nature of signal transduction in skeletal muscle excitation-contraction coupling. Annu Rev Physiol 54:109-133.
40. Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10:3664-3684.
41. Robitaille R, Garcia ML, Kaczorowski GJ, Charlton MP (1993) Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron 11:645-655.
42. Saheki Y, Bargmann CI (2009) Presynaptic CaV2 calcium channel traffic requires CALF-1 and the alpha(2)delta subunit UNC-36. Nat Neurosci 12:1257-1265.
43. Schneider MF (1994) Control of calcium release in functioning skeletal muscle fibers. Annu Rev Physiol 56:463-484.
44. Takeshima H, Iino M, Takekura H, Nishi M, Kuno J, Minowa O, Takano H, Noda T (1994) Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 369:556-559.
45. Ueda H, Baba T, Kashiwagi K, Iijima H, Ohno S (2000) Dystrobrevin localization in photoreceptor axon terminals and at blood-ocular barrier sites. Invest Ophthalmol Vis Sci 41:3908-3914.
46. Wang ZW (2008) Regulation of synaptic transmission by presynaptic CaMKII and BK channels. Mol Neurobiol 38:153-166.
47. 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.
48. + channels. Nat Neurosci 3:566-571.