Effects of voltage-gated calcium channel subunit genes on calcium influx in cultured C. elegans mechanosensory neurons

Journal of Neurobiology

Volumn 66, Issue 10, 2006, Pages 1125-1139

  Frøkjær Jensen, Christian ^a,b   Kindt, Katie S ^a   Kerr, Rex A ^a   Suzuki, Hiroshi ^a   Melnik Martinez, Katya ^a   Gerstbreih, Beate ^c   Driscol, Monica ^c   Schafer, William R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

C. elegans; Calcium channel; Genetics; Mechanosensation; Neuroimaging

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM ION; CALCIUM SENSING RECEPTOR; CELL PROTEIN; GADOLINIUM; PROTEIN EGL 19; PROTEIN SUBUNIT; PROTEIN UNC 36; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; CAENORHABDITIS ELEGANS; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FUNCTION; CONTROLLED STUDY; CULTURE TECHNIQUE; EGL 19 GENE; EXTRACELLULAR CALCIUM; GENE; GENE CONTROL; GENE MUTATION; GENE REPRESSION; GENETIC ANALYSIS; GENETIC ENGINEERING; MEMBRANE DEPOLARIZATION; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NEUROIMAGING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SENSORY NERVE CELL; STIMULUS RESPONSE; UNC 36 GENE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CALCIUM CHANNELS; CELLS, CULTURED; MECHANORECEPTORS; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MUTATION; NEURONS, AFFERENT; PROTEIN SUBUNITS; TOUCH;

EID: 33747623548     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/neu.20261     Document Type: Article

References (57)

1. Baba A, Yasui T, Fujisawa S, Yamada RX, Yamada MK, Nishiyama N, Matsuki N, et al. 2003. Activity-Evoked Capacitative Ca2+ Entry: Implications in Synaptic Plasticity. J Neurosci 23:7737-7741.
2. Biagi BA, Enyeart JJ. 1990. Gadolinium blocks low- and high-threshold calcium currents in pituitary cells. Am J Physiol 259:C515-520.
3. Bianchi L, Gerstbrein B, Frøkjær-Jensen C, Royal DC, Mukherjee G, Royal MA, Xue J, et al. 2004. The neurotoxic MEC-4(d) DEG/ENaC sodium channel conducts calcium: implications for necrosis initiation. Nat Neurosci 7:1337-1344.
4. Bleakman D, Bowman D, Bath CP, Brust PF, Johnson EC, Deal CR, Miller RJ, et al. 1995. Characteristics of a Human N-type Calcium Channel Expressed in HEK293 Cells. Neuropharmacology 34:753-765.
5. Bootman MD, Collins TJ, MacKenzie L. Roderick HL, Berridge MJ, Peppiatt CM. 2002. 2-Aminoethozydiphenyl borate (2-APB) is a reliable blocker of store-operated Ca2+ entry but an inconsistent inhibitor of InsP3-induced Ca2+ release. FASEB 16:1145-1150.
6. 2+ channels. Annu Rev Cell Dev Biol 16:521-555.
7. Christensen M, Estevez A, Yin X, Fox R, Morrison R, McDonnell M, Gleason C, et al. 2002. A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 33:503-514.
8. Dal Santo P, Logan MA, Chisholm AD, Jorgensen EM. 1999. The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98:757-767.
9. Dobrev D, Milde AS, Andreas K, Ravens U. 1999. The effects of verapamil and diltiazem on N-, P- and Q-type calcium channels mediating dopamine release in rat striatum. Br J Pharmacol 127:576-582.
10. Ertel SI, Ertel EA, Clozel JP. 1997. T-type Ca2+ channels and pharmacological Blockade: Potential Pathophysiological Relevance. Cardiovasc Drugs Ther 11:723-739.
11. Estevez AY, Roberts RK, Strange K. 2005. Identification of Store-independent and Store-operated Ca2+ conductances in Caenorhabditis elegans Intestinal Epithelial Cells. J Gen Physiol 122:207-223.
12. Evanko DS, Haydon PG. 2005. Elimination of environmental sensitivity in a cameleon FRET-based calcium sensor via replacement of the acceptor with Venus. Cell Calcium 37:341-348.
13. Gee NS, Brown JP, Dissanayake VU, Offord J, Thurlow R, Woodruff GN. 1996. The novel anticonvulsant drug, gabapentin (Neurontin), binds to the alpha2delta subunit of a calcium channel. J Biol Chem 271:5768-5776.
14. Goodman MB, Hall DH, Avery L, Lockery SR. 1998. Active Currents Regulate Sensitivity and Dynamic Range in C. elegans Neurons. Neuron 20:763-772.
15. Gregory RB, Rychkov G, Barritt GJ. 2001. Evidence that 2-aminoethyl dephenylborate is a novel inhibitor of store-operated Ca2+ channels in liver cells, and acts through a mechanism which does not involve inositol triphosphate receptors. Biochem J 354:285-290.
16. 2+. J Gen Phys 109:147-167.
17. Hille B. 2001. Ionic Channels of Excitable Membranes, 3rd Ed. Sunderland, MA: Sinauer, 814 p.
18. Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, Schafer WR. 2005. In vivo imaging of C. elegans ASH neurons: cellular responses and adaptation to chemical repellents. EMBO J 24:63-72.
19. Hobert O. 2002. PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32:728-730.
20. 2+ channels. Mol Pharmacol 58:1264-1270.
21. Jay SD, Sharp AH, Kahl SD, Vedvick TS, Harpold MM, Campbell KP. 1991. Structural characterization of the dihydropyridine-sensitive calcium channel alpha 2-subunit and the associated delta peptides. J Biol Chem 15:3287-3293.
22. Jospin M, Jacquemond V, Mariol MC, Segalat L, Allard B. 2002. The L-type voltage-dependent Ca2+ channel EGL-19 controls body wall muscle function in Caenorhabditis elegans. J Cell Biol 159:337-348.
23. Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR. 2000. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26:583-594.
24. Kimitsuki T, Nakagawa T, Hisashi K, Komune S, Komiyama S. 1996. Gadonolinium blocks mechano-electric transducer current in chick cochlear hair cells. Hearing Res 101:75-80.
25. Kimura KD, Miyawaki A, Matsumoto K, Mori I. 2004. The C. elegans Thermosensory Neuron AFD Responds to Warming. Curr Biol 14:1291-1295.
26. Kindt KS, Tam T, Whiteman S, Schafer WR. 2002. Serotonin promotes G(o)-dependent neuronal migration in Caenorhabditis elegans. Curr Biol 12:1738-1747.
27. Klugbauer N, Marais E, Hofmann F. 2003. Calcium channel alpha2delta subunits: Differential Expression, Function, and Drug binding. J Bioenerg Biomembr 35:639-647.
28. Lee JH, Gomora JC, Cribbs LL, Perez-Reyes E. 1999. Nickel Block of Three Cloned T-type Calcium Channels: Low Concentrations Selectively Block alpha1H. Biophys J 77:3034-3042.
29. 2+ channel cause myotonia in Caenorhabditis elegans. EMBO 16:6066-6076.
30. 2+-channel gamma subunit. Nat Genet 19:340-347.
31. 2/δ subunits - Structure and Gabapentin Binding. Mol Pharmacol 59:1243-1248.
32. Martin DJ, McClelland D, Herd MB, Sutton KG, Hall MD, Lee K, Pinnock RD, et al. 2001. Gabapentin-mediated inhibition of voltage-activated Ca2+ channel currents in cultured sensory neurones is dependent on culture conditions and channel subunit expression. Neuropharmacology 42:353-366.
33. Maryon EB, Coronado R, Anderson P. 1996. Unc-68 Encodes a Ryanodine Receptor Involved in Regulating C. elegans Body-Wall Muscle Contraction. J Cell Biol 134:885-893.
34. Mathews EA, Garcia E, Santi CM, Mullen GP, Thacker C, Moerman DG, Snutch TP. 2003. Critical residues of the Caenorhabditis elegans unc-2 voltage-gated calcium channel that affect behavioral and physiological properties. J Neurosci 23:6537-6545.
35. Mello C, Fire A. 1995. DNA transformation. In: Epstein HF, Shakes DC, editors. Caenorhabditis elegans: Modern Biological Analysis of an Organism, Methods in Cell Biology, Volume 48. San Diego, CA: Academic Press, pp. 451-482.
36. Miyawaki A, Griesbeck O, Heim R, Tsien RY. 1999. Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc Natl Acad Sci USA 96:2135-2140.
37. O'Hagan R, Chalfie M, Goodman MB. 2004. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature Neurosci 8:43-50.
38. Parekh AB, Putney JW Jr. 2005. Store-operated calcium channels. Physiol Rev 85:757-810.
39. Putney JW Jr. 2001. The Pharmacology of capacitative calcium entry. Mol Interventions 1:84-94.
40. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A. 2005. In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25:4766-4778.
41. Sárközi S, Szegedi C, Lukács B, Ronjat M, Jóna I. 2005. Effect of gadolinium on the ryanodine receptor/sarcoplasmatic reticulum calcium release channel of skeletal muscle. FEBS J 272:464-471.
42. Schafer WR, Kenyon CJ. 1995. A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375:73-78.
43. Shtonda B, Avery L. 2005. CCA-1, EGL-19 and EXP-2 currents shape action potentials in Caenorhabditis elegans pharynx. J Exp Biol 208:2177-2190.
44. 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.
45. Singer D, Biel M, Lotan I, Flockerzi V, Hofmann F, Dascal N. 1991. The roles of the subunits in the function of the calcium channel. Science 253:1553-1557.
46. Snutch TP, Tomlinson WJ, Leonard JP, Gilbert MM. 1991. Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron 7:45-57.
47. Steger KA, Shtonda BB, Thacker C, Snutch TP, Avery L. 2005. The C. elegans T-type calcium channel CCA-1 boosts neuromuscular transmission. J Exp Biol 208:2191-2203.
48. Striessnig J, Grabner M, Mitterdorfer J, Hering S, Sinnegger MJ, Glossman H. 1998. Structural basis of drug binding to L Ca2+ channels. Trends Pharm Sci 19:108-115.
49. Sutton KG, Martin DJ, Pinnock RD, Lee K, Scott RH. 2002. Gabapentin inhibits high-threshold calcium channel currents in cultured rat dorsal root ganglion neurones. Br J Pharmacology 135:257-265.
50. Suzuki H, Kerr R, Bianchi L, Frøkjær-Jensen C, Slone D, Xue J, Gerstbrein B, et al. 2003. In vivo imaging of C. elegans mechanosensory neurons demonstrate a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39:1005-1017.
51. Tarn T, Mathews E, Snutch TP, Schafer WR. 2000. Voltage-Gated Calcium Channels Direct Neuronal Migration in Caenorhabditis elegans. Dev Biol 226:104-117.
52. Thomas JH, Lockery S. 1999. Neurobiology. In: C. elegans: a Practical Approach, ed. I. Hope, Oxford University Press.
53. Truong K, Sawano A, Mizuno H, Hama H, Tong KI, Mal TK, Miyawaki A, et al. 2001. FRET-based in vivo Ca2+ imaging by a new calmodulin-GFP fusion molecule. Nat Struct Biol 8:1069-1073.
54. 2δ for gabapentin binding. Biochem J 342:313-320.
55. Xu K, Tavernarakis N, Driscoll M. 2001. Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca2+ release from the endoplasmic reticulum. Neuron 31:957-971.
56. Yang X-C, Sachs F. 1989. Block of Stretch-Activated Ion Channels in Xenopus Oocytes by Gadolinium and Calcium ions. Science 243:1068-1071.
57. Zamponi GW, Bourinet E, Snutch TP. 1996. Nickel Block of a Family of Neuronal Calcium Channels: Subtype- and Subunit-Dependent Action at Multiple Sites. J Membr Biol 151:77-90.