Identification of major classes of cholinergic neurons in the nematode Caenorhabditis elegans

Journal of Comparative Neurology

Volumn 506, Issue 3, 2008, Pages 398-408

  Duerr, Janet S ^a,b   Han, He Ping ^a,c   Fields, Stephen D ^a,d   Rand, James B ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b OHIO UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d EAST CENTRAL UNIVERSITY   (United States)

Author keywords

Acetylcholine; C. elegans; ChAt; Choline acetyltransferase; VAChT; Vesicular acetylcholine transporter

Indexed keywords

ACETYLCHOLINE; ACYLTRANSFERASE; PROTEIN ANTIBODY;

ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CYTOSOL; INTERNEURON; LARVA; NEMATODE; NERVE CORD; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIBODIES; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CHOLINE O-ACETYLTRANSFERASE; GAMMA-AMINOBUTYRIC ACID; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; NEMATODA; NEURONS; PARASYMPATHETIC NERVOUS SYSTEM; RECOMBINANT FUSION PROTEINS; SUBCELLULAR FRACTIONS; SYNAPSES; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 38049075304     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21551     Document Type: Article

References (63)

1. Alfonso A, Grundahl K, Duerr JS, Han HP, Rand JB. 1993. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261:617-619.
2. Alfonso A, Grundahl K, McManus JR, Rand JB. 1994a. Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans. J Neurosci 14:2290-2300.
3. Alfonso A, Grundahl K, McManus JR, Asbury JM, Rand JB. 1994b. Alternative splicing leads to two cholinergic proteins in Caenorhabditis elegans. J Mol Biol 241:627-630.
4. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
5. Brown LA, Jones AK, Buckingham SD, Mee CJ, Sattelle DB. 2006. Contributions from Caenorhabditis elegans functional genetics to antiparasitic drug target identification and validation: nicotinic acetylcholine receptors, a case study. Int J Parasitol 36:617-624.
6. Chen R, Wei J, Fowler SC, Wu JY. 2003. Demonstration of functional coupling between dopamine synthesis and its packaging into synaptic vesicles. J Biomed Sci 10:774-781.
7. Collier B, Katz HS. 1974. Acetylcholine synthesis from recaptured choline by a sympathetic ganglion. J Physiol 238:639-655.
8. del Castillo J, de Mello WC, Morales T. 1963. The physiological role of acetylcholine in the neuromuscular system of Ascaris lumbricoides. Arch Int Physiol Biochim 71:741-757.
9. 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.
10. Duerr JS. 2006. Immunohistochemistry. In: The C. elegans Research Community, editors. WormBook. http://www.wormbook.org
11. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE, Rand JB. 1999. The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 19:72-84.
12. 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.
13. Eiden LE. 1998. The cholinergic gene locus. J Neurochem 70:2227-2240.
14. Eraly SA, Monte JC, Nigam SK. 2004. Novel slc22 transporter homologs in fly, worm, and human clarify the phylogeny of organic anion and cation transporters. Physiol Genom 18:12-24.
15. Finney M, Ruvkun G. 1990. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895-905.
16. Francis MM, Mellem JE, Maricq AV. 2003. Bridging the gap between genes and behavior: recent advances in the electrophysiological analysis of neural function in Caenorhabditis elegans. Trends Neurosci 26:90-99.
17. Garriga G, Desai C, Horvitz HR. 1993. Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117:1071-1087.
18. Gilmor ML, Nash NR, Roghani A, Edwards RH, Yi H, Hersch SM, Levey AI. 1996. Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J Neurosci 16:2179-2190.
19. Hall DH, Hedgecock EM. 1991. Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837-847.
20. Hall DH, Russell RL. 1991. The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J Neurosci 11:1-22.
21. Hobert O, D'Alberti T, Liu Y, Ruvkun G. 1998. Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J Neurosci 18:2084-2096.
22. Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, Floor E, Hsu CC, Kopke RD, Wu JY. 2003. Demonstration of functional coupling between gamma-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci U S A 100:4293-4298.
23. Johnson CD, Stretton AOW. 1985. Localization of choline acetyltransferase within identified motoneurons of the nematode Ascaris. J Neurosci 5:1984-1992.
24. Johnson CD, Stretton AOW. 1987. GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. J Neurosci 7:223-235.
25. Kanaani J, Lissin D, Kash SF, Baekkeskov S. 1999. The hydrophilic isoform of glutamate decarboxylase, GAD67, is targeted to membranes and nerve terminals independent of dimerization with the hydrophobic membrane-anchored isoform, GAD65. J Biol Chem 274: 37200-37209.
26. Kuczenski RT, Mandell AJ. 1972. Regulatory properties of soluble and particulate rat brain tyrosine hydroxylase. J Biol Chem 247:3114-3122.
27. Lee YS, Park YS, Chang DJ, Hwang JM, Min CK, Kaang BK, Cho NJ. 1999. Cloning and expression of a G protein-linked acetylcholine receptor from Caenorhabditis elegans. J Neurochem 72:58-65.
28. Lee YS, Park YS, Nam S, Suh SJ, Lee J, Kaang BK, Cho NJ. 2000. Characterization of GAR-2, a novel G protein-linked acetylcholine receptor from Caenorhabditis elegans. J Neurochem 75:1800-1809.
29. Li C, Chalfie M. 1990. Organogenesis in C. elegans: Positioning of neurons and muscles in the egg-laying system. Neuron 4:681-695.
30. Matthies DS, Fleming PA, Wilkes DM, Blakely RD. 2006. The Caenorhabditis elegans choline transporter CHO-1 sustains acetylcholine synthesis and motor function in an activity-dependent manner. J Neurosci 26:6200-6212.
31. McGeer EG, McGeer PL, Wada JA. 1971. Distribution of tyrosine hydroxylase in human and animal brain. J Neurochem 18:1647-1658.
32. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. 1993. The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337-341.
33. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature 389:870-876.
34. Mello C, Fire A. 1995. DNA transformation. Methods Cell Biol 46:339-360.
35. 2+/calmodulin-dependent protein kinase II, and tyrosine phosphorylation are involved in carbachol-induced phospholipase D activation in Chinese hamster ovary cells expressing muscarinic acetylcholine receptor of Caenorhabditis elegans. J Neurochem 75:274-281.
36. 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.
37. Oda Y. 1999. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 49:921-937.
38. Okuda T, Haga T, Kanai Y, Endou H, Ishihara T, Katsura I. 2000. Identification and characterization of the high-affinity choline transporter. Nat Neurosci 3:120-125.
39. Otsuka AJ, Jeyaprakash A, Garcia-Anoveros J, Tang LZ, Fisk G, Hartshorne T, Franco R, Born T. 1991. The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron 6:113-122.
40. Pahud G, Salem N, van de Goor J, Medilanski J, Pellegrinelli N, Eder-Colli L. 1998. Study of subcellular localization of membrane-bound choline acetyltransferase in Drosophila central nervous system and its association with membranes. Eur J Neurosci 10:1644-1653.
41. Putrenko I, Zakikhani M, Dent JA. 2005. A family of acetylcholine-gated chloride channel subunits in Caenorhabditis elegans. J Biol Chem 280:6392-6398.
42. Racke K, Juergens UR, Mattiesen S. 2006. Control by cholinergic mechanisms. Eur J Pharmacol 533:57-68.
43. Rand JB. 1989. Genetic analysis of the cha-1-unc-17 gene complex in Caenorhabditis. Genetics 122:73-80.
44. Rand JB, Russell RL. 1984. Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 106:227-248.
45. Rand JB, Russell RL. 1985. Properties and partial purification of choline acetyltransferase from the nematode Caenorhabditis elegans. J Neurochem 44:189-200.
46. Reetz A, Solimena M, Matteoli M, Folli F, Takei K, De Camilli P. 1991. GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J 10:1275-1284.
47. Sandoval GM, Duerr JS, Hodgkin J, Rand JB, Ruvkun G. 2006. A genetic interaction between the vesicular acetylcholine transporter VAChT/UNC-17 and synaptobrevin/SNB-1 in C. elegans. Nat Neurosci 9:599-601.
48. Schafer WR. 2006. Genetics of egg-laying in worms. Annu Rev Genet 40:487-509.
49. Schinkmann K, Li C. 1992. Localization of FMRFamide-like peptides in Caenorhabditis elegans. J Comp Neurol 316:251-260.
50. Stiernagle T. 2006. Maintenance of C. elegans. In: The C. elegans Research Community, editors. WormBook. http://www.wormbook.org.
51. Sulston JE. 1976. Post-embryonic development in the ventral cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:287-297.
52. Suzuki Y, Tandell MD, Roy PJ, Krishna S, Savage C, Ross RM, Padgett RW, Wood WB. 1999. A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans. Development 126:241-250.
53. Tsalik EL, Nicaris T, Wenick AS, Pau K, Avery L, Hobert O. 2003. LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev Biol 263:81-102.
54. Walrond JP, Kass IS, Stretton AO, Donmoyer JE. 1985. Identification of excitatory and inhibitory motoneurons in the nematode Ascaris by electrophysiological techniques. J Neurosci 5:1-8.
55. Weihe E, Tao-Cheng JH, Schafer MK, Erickson JD, Eiden LE. 1996. Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc Natl Acad Sci U S A 93:3547-3552.
56. White JG, Southgate E, Thomson JN, Brenner S. 1976. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:327-348.
57. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340.
58. WormAtlas. 2007. Altun ZF, Hall DH, editors. http://www.wormatlas.org.
59. WormBase. 2007. The WormBase Consortium, editors. http://www.wormbase. org.
60. WormBook. 2007. The C. elegans Research Community, editors. http://www.wormbook.org.
61. Yang H, Kunes S. 2004. Nonvesicular release of acetylcholine is required for axon targeting in the Drosophila visual system. Proc Natl Acad Sci U S A 101:15213-15218.
62. Yasuyama K, Meinertzhagen IA, Schurmann FW. 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.
63. Zahn TR, MacMorris MA, Dong W, Day R, Hutton JC. 2001. IDA-1, a Caenorhabditis elegans homolog of the diabetic autoantigens IA-2 and phogrin, is expressed in peptidergic neurons in the worm. J Comp Neurol 429:12-14.