Muscular dystrophy associated mutations in caveolin-1 induce neurotransmission and locomotion defects in Caenorhabditis elegans

Invertebrate Neuroscience

Volumn 7, Issue 3, 2007, Pages 157-164

  Parker, Scott ^a,b   Peterkin, Helen S ^a   Baylis, Howard A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aldicarb; Caveolin; Dynamin; Levamisole; Muscular dystrophy

Indexed keywords

CAVEOLIN 1; DYNAMIN; LEVAMISOLE;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENETIC ANALYSIS; LOCOMOTION; MUSCULAR DYSTROPHY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTINEMATODAL AGENTS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CAVEOLIN 1; DISEASE MODELS, ANIMAL; DYNAMIN I; HUMANS; LEVAMISOLE; MOVEMENT; MUSCULAR DYSTROPHIES; MUTATION; NEUROMUSCULAR JUNCTION; POLYMERASE CHAIN REACTION;

EID: 34548329670     PISSN: 13542516     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10158-007-0051-5     Document Type: Article

References (47)

1. Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199-225
2. Betz RC, Schoser BG, Kasper D, Ricker K, Ramirez A, Stein V, Torbergsen T, Lee YA, Nothen MM, Wienker TF, Malin JP, Propping P, Reis A, Mortier W, Jentsch TJ, Vorgerd M, Kubisch C (2001) Mutations in CAV3 cause mechanical hyperirritability of skeletal muscle in rippling muscle disease. Nat Genet 28:218-219
3. Carlson BM, Carlson JA, Dedkov EI, McLennan IS (2003) Concentration of caveolin-3 at the neuromuscular junction in young and old rat skeletal muscle fibers. J Histochem Cytochem 51:1113-1118
4. Carre-Pierrat M, Grisoni K, Gieseler K, Mariol MC, Martin E, Jospin M, Allard B, Segalat L (2006) 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
5. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956-964
6. Clark SG, Shurland DL, Meyerowitz EM, Bargmann CI, van der Bliek AM (1997) A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc Natl Acad Sci USA 94:10438-10443
7. Culetto E, Baylis HA, Richmond JE, Jones AK, Fleming JT, Squire MD, Lewis JA, Sattelle DB (2004) The Caenorhabditis elegans unc-63 gene encodes a levamisole-sensitive nicotinic acetylcholine receptor alpha subunit. J Biol Chem 279:42476-42483
8. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV (2001) Loss of caveolae vascular dysfunction and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449-2452
9. Fischer D, Schroers A, Blumcke I, Urbach H, Zerres K, Mortier W, Vorgerd M, Schroder R (2003) Consequences of a novel caveolin-3 mutation in a large German family. Ann Neurol 53:233-241
10. Fleming JT, Squire MD, Barnes TM, Tornoe C, Matsuda K, Ahnn J, Fire A, Sulston JE, Barnard EA, Sattelle DB, Lewis JA (1997) Caenorhabditis elegans levamisole resistance genes lev-1 unc-29 and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17:5843-5857
11. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408:325-330
12. Galbiati F, Razani B, Lisanti MP (2001) Caveolae and caveolin-3 in muscular dystrophy. Trends Mol Med 7:435-441
13. Hedgecock EM, Hall DH (1991) Motor vesicles. Curr Biol 1:77-79
14. Hedgecock EM, Culotti JG, Hall DH (1990) The unc-5 unc-6 and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61-85
15. Hernandez-Deviez DJ, Martin S, Laval SH, Lo HP, Cooper ST, North KN, Bushby K, Parton RG (2006) Aberrant dysferlin trafficking in cells lacking caveolin or expressing dystrophy mutants of caveolin-3. Hum Mol Genet 15:129-142
16. Herrmann R, Straub V, Blank M, Kutzick C, Franke N, Jacob EN, Lenard HG, Kroger S, Voit T (2000) Dissociation of the dystroglycan complex in caveolin-3-deficient limb girdle muscular dystrophy. Hum Mol Genet 9:2335-2340
17. Hobert O (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32:728-730
18. Hosono R, Kamiya Y (1991) Additional genes which result in an elevation of acetylcholine levels by mutations in Caenorhabditis elegans. Neurosci Lett 128:243-244
19. Kim YN, Bertics PJ (2002) The endocytosis-linked protein dynamin associates with caveolin-1 and is tyrosine phosphorylated in response to the activation of a noninternalizing epidermal growth factor receptor mutant. Endocrinology 143:1726-1731
20. Lewis JA, Wu CH, Berg H, Levine JH (1980) The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95:905-928
21. Lipardi C, Mora R, Colomer V, Paladino S, Nitsch L, Rodriguez-Boulan E, Zurzolo C (1998) Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J Cell Biol 140:617-626
22. Mariol MC, Martin E, Chambonnier L, Segalat L (2007) Dystrophin-dependent muscle degeneration requires a fully functional contractile machinery to occur in C. elegans. Neuromuscul Disord 17:56-60
23. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870-876
24. McNally EM, de Sa ME, Duggan DJ, Bonnemann CG, Lisanti MP, Lidov HG, Vainzof M, Passos-Bueno MR, Hoffman EP, Zatz M, Kunkel LM (1998) Caveolin-3 in muscular dystrophy. Hum Mol Genet 7:871-877
25. Minetti C, Sotgia F, Bruno C, Scartezzini P, Broda P, Bado M, Masetti E, Mazzocco M, Egeo A, Donati MA, Volonte D, Galbiati F, Cordone G, Bricarelli FD, Lisanti MP, Zara F (1998) Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nat Genet 18:365-368
26. Nguyen M, Alfonso A, Johnson CD, Rand JB (1995) Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140:527-535
27. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305
28. Nonet ML, Saifee O, Zhao H, Rand JB, Wei L (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J Neurosci 18:70-80
29. Nurrish S, Segalat L, Kaplan JM (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24:231-242
30. Oh P, McIntosh DP, Schnitzer JE (1998) Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141:101-114
31. Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4:724-738
32. Rand JB, Russell RL (1985) Molecular basis of drug-resistance mutations in C. elegans. Psychopharmacol Bull 21:623-630
33. Rayes D, Flamini M, Hernando G, Bouzat C (2007) Activation of single nicotinic receptor channels from Caenorhabditis elegans muscle. Mol Pharmacol 71:1407-1415
34. Richmond JE, Broadie KS (2002) The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans. Curr Opin Neurobiol 12:499-507
35. Scheel J, Srinivasan J, Honnert U, Henske A, Kurzchalia TV (1999) Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans. Nat Cell Biol 1:127-129
36. Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, Witke W, Huttner WB, Soling HD (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401:133-141
37. Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, van der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40:749-762
38. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, Fire A, Ahringer J, Plasterk RH (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12:1317-1319
39. Sulston JE (1983) Neuronal cell lineages in the nematode Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 48:443-452
40. Sulston J, Hodgkin J (1988) Methods. In: The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, New York
41. Takei K, Yoshida Y, Yamada H (2005) Regulatory mechanisms of dynamin-dependent endocytosis. J Biochem (Tokyo) 137:243-247
42. Tang Z, Okamoto T, Boontrakulpoontawee P, Katada T, Otsuka AJ, Lisanti MP (1997) Identification sequence and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J Biol Chem 272:2437-2445
43. Towers PR, Edwards B, Richmond JE, Sattelle DB (2005) The Caenorhabditis elegans lev-8 gene encodes a novel type of nicotinic acetylcholine receptor alpha subunit. J Neurochem 93:1-9
44. Towers PR, Lescure P, Baban D, Malek JA, Duarte J, Jones E, Davies KE, Segalat L, Sattelle DB (2006) Gene expression profiling studies on Caenorhabditis elegans dystrophin mutants dys-1(cx-35) and dys-1(cx18). Genomics 88:642-649
45. Vorgerd M, Bolz H, Patzold T, Kubisch C, Malin JP, Mortier W (1999) Phenotypic variability in rippling muscle disease. Neurology 52:1453-1459
46. Wakabayashi T, Kitagawa I, Shingai R (2004) Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci Res 50:103-111
47. Woodman SE, Sotgia F, Galbiati F, Minetti C, Lisanti MP (2004) Caveolinopathies: mutations in caveolin-3 cause four distinct autosomal dominant muscle diseases. Neurology 62:538-543