Expression of muscarinic acetylcholine receptors and choline acetyltransferase enzyme in cultured antennal sensory neurons and non-neural cells of the developing moth Manduca sexta

Journal of Neurobiology

Volumn 62, Issue 3, 2005, Pages 316-329

  Torkkeli, Päivi H ^a   Widmer, Alexandre ^a   Meisner, Shannon ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Chemosensory; Glia; Mechanosensory; Muscarinic receptor

Indexed keywords

CHOLINE ACETYLTRANSFERASE; MUSCARINIC RECEPTOR; PIRENZEPINE; SYNAPSIN;

ADOLESCENT; ANIMAL CELL; ANTENNA; ARTICLE; CELL NUCLEUS; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EPIDERMIS CELL; FILOPODIUM; FLUORESCENCE; GLIA CELL; IMMUNOCYTOCHEMISTRY; LAMELLIPODIUM; MANDUCA SEXTA; NERVE CELL CULTURE; NERVE FIBER; NERVE SHEATH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SYNAPSE VESICLE; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BINDING, COMPETITIVE; BLOTTING, WESTERN; CELL COUNT; CELL NUCLEUS; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; DROSOPHILA; FLUORESCENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MANDUCA; MUSCARINIC ANTAGONISTS; NEUROGLIA; NEURONS, AFFERENT; PIRENZEPINE; RECEPTORS, MUSCARINIC; SENSE ORGANS; SYNAPSINS; TIME FACTORS;

EID: 12744259896     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20097     Document Type: Article

References (47)

1. Andre C, Guillet JG, De Backer JP, Vanderheyden P, Hoebeke J, Strosberg AD. 1984. Monoclonal antibodies against the native or denatured forms of muscarinic acetylcholine receptors. Embo J 3:17-21.
2. Bate M, Broadie K. 1995. Wiring by fly: the neuromuscular system of the Drosophila embryo. Neuron 15:513-525.
3. Blake AD, Anthony NM, Chen HH, Harrison JB, Nathanson NM, Sattelle DB. 1993. Drosophila nervous system muscarinic acetylcholine receptor: transient functional expression and localization by immunocytochemistry. Mol Pharmacol 44:716-724.
4. Burrows M. 1996. The neurobiology of an insect brain. Oxford: Oxford University Press. 682 p.
5. Caulfield MP, Birdsall NJ. 1998. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279-290.
6. Eide PE, Caldwell JM, Marks EP. 1975. Establishment of two cell lines from embryonic tissue of the tobacco hornworm, Manduca sexta (L.). In vitro 11:395-399.
7. Fitzsimonds RM, Poo MM. 1998. Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143-170.
8. French AS. 1988. Transduction mechanisms of mechanosensilla. Annu Rev Entomol 33:39-58.
9. Goldberg F, Grunewald B, Rosenboom H, Menzel R. 1999. Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. J Physiol 514:759-768.
10. Goutsouliak V, Wang Y, Cynader MS, Rabkin SW. 1997. Visualization of muscarinic cholinergic receptors on chick cardiomyocytes and their involvement in phosphatidylcholine hydrolysis. Biochem Cell Biol 75:127-136.
11. Grando SA. 1997. Biological functions of keratinocyte cholinergic receptors. J Investig Dermatol Symp Proc 2:41-48.
12. Hildebrand JG. 1980. Development of putative acetylcholine receptors in normal and deafferented antennal lobes during metamorphosis of Manduca sexta. In: Sattelle DB, Hall LM, Hildebrand JG, editors. Receptors for neurotransmitters, hormones and pheromones in insects. Amsterdam: Elsevier, North Holland Biomedical Press, p 209-220.
13. Hwang JM, Chang DJ, Kim US, Lee YS, Park YS, Kaang BK, Cho NJ. 1999. Cloning and functional characterization of a Caenorhabditis elegans muscarinic acetylcholine receptor. Receptors Channels 6:415-424.
14. Itoh N, Slemmon JR, Hawke DH, Williamson R, Morita E, Itakura K, Roberts E, Shively JE, Crawford GD, Salvaterra PM. 1986. Cloning of Drosophila choline acetyltransferase cDNA. Proc Natl Acad Sci USA 83:4081-4085.
15. Jackson C, Bermudez I, Beadle DJ. 2002. Pharmacological properties of nicotinic acetylcholine receptors in isolated Locusta migratoria neurones. Microsc Res Tech 56:249-255.
16. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
17. Kloppenburg P, Camazine SM, Sun XJ, Randolph P, Hildebrand JG. 1997. Organization of the antennal motor system in the sphinx moth Manduca sexta. Cell Tissue Res 287:425-433.
18. Lehr HA, Mankoff DA, Corwin D, Santeusanio G, Gown AM. 1997. Application of photoshop-based image analysis to quantification of hormone receptor expression in breast cancer. J Histochem Cytochem 45:1559-1565.
19. McIver SB. 1986. Mechanoreception. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology, biochemistry and pharmacology. Oxford: Pergamon, p 71-132.
20. Millar NS, Baylis HA, Reaper C, Bunting R, Mason WT, Sattelle DB. 1995. Functional expression of a cloned Drosophila muscarinic acetylcholine receptor in a stable Drosophila cell line. J Exp Biol 198:1843-1850.
21. Munoz-Maines VJ, Slemmon JR, Panicker MM, Neighbor N, Salvaterra PM. 1988. Production of polyclonal antisera to choline acetyltransferase using a fusion protein produced by a cDNA clone. J Neurochem 50:167-175.
22. Onai T, FitzGerald MG, Arakawa S, Gocayne JD, Urquhart DA, Hall LM, Fraser CM, McCombie WR, Venter JC. 1989. Cloning, sequence analysis and chromosome localization of a Drosophila muscarinic acetylcholine receptor. FEBS Lett 255:219-225.
23. Prokop A. 1999. Integrating bits and pieces: synapse structure and formation in Drosophila embryos. Cell Tissue Res 297:169-186.
24. Qazi S, Proulx D, Trimmer BA. 1996. Characterization of muscarinic binding sites in the central nervous system of larval Manduca sexta. Insect Biochem Mol Biol 26:721-732.
25. 3H] (-) quinuclidinylbenzilate binding to soluble rat brain muscarinic receptors indicates that pirenzepine binds to an allosteric state of the muscarinic receptor. Biochem Biophys Res Commun 118:950-957.
26. Rössler W, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP. 1999. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 19:9865-9877.
27. Sanes JR, Hildebrand JG. 1976a. Structure and development of antennae in a moth. Manduca sexta. Dev Biol 51:282-299.
28. Sanes JR, Hildebrand JG. 1976b. Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51: 300-319.
29. Sanes JR, Hildebrand JG. 1976c. Acetylcholine and its metabolic enzymes in developing antennae of the moth, Manduca sexta. Dev Biol 52:105-120.
30. Shapiro RA, Wakimoto BT, Subers EM, Nathanson NM. 1989. Characterization and functional expression in mammalian cells of genomic and cDNA clones encoding a Drosophila muscarinic acetylcholine receptor. Proc Natl Acad Sci USA 86:9039-9043.
31. Slemmon JR, Campbell GA, Selski DJ, Bramson HN. 1991. The amino terminus of the putative Drosophila choline acetyltransferase precursor is cleaved to yield the 67 kDa enzyme. Brain Res Mol Brain Res 9:245-252.
32. Stengl M, Hildebrand JG. 1990. Insect olfactory neurons in vitro: Morphological and immunocytochemical characterization of male-specific antennal receptor cells from developing antennae of male Manduca sexta. J Neurosci 10:837-847.
33. Stengl M, Homberg U, Hildebrand JG. 1990. Acetylcholinesterase activity in antennal receptor neurons of the sphinx moth Manduca sexta. Cell Tissue Res 262:245-252.
34. Takagawa K, Salvaterra P. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24:237-243.
35. Torkkeli PH, French AS. 1999. Primary culture of antennal mechanoreceptor neurons of Manduca sexta. Cell Tissue Res 297:301-309.
36. Trimmer BA. 1995. Current excitement from insect muscarinic receptors. TINS 18:104-111.
37. Trimmer BA, Weeks JC. 1989. Effects of nicotinic and muscarinic agents on an identified motoneurone and its direct afferent inputs in larval Manduca sexta. J Exp Biol 144:303-337.
38. Trimmer BA, Weeks JC. 1993. Muscarinic acetylcholine receptors modulate the excitability of an identified insect motoneuron. J Neurophysiol 69:1821-1836.
39. Tucker ES, Tolbert LP. 2003. Reciprocal interactions between olfactory receptor axons and olfactory nerve glia cultured from the developing moth Manduca sexta. Dev Biol 260:9-30.
40. Van der Zee EA, Luiten PG. 1999. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog Neurobiol 58:409-471.
41. 1 muscarinic ACh receptors in visual cortex neuronal cultures. J Neurosci 14:4147-4158.
42. Wessler I, Kirkpatrick CJ, Racke K. 1999. The cholinergic 'pitfall': acetylcholine, a universal cell molecule in biological systems, including humans. Clin Exp Pharmacol Physiol 26:198-205.
43. Yasuyama K, Kitamoto T, Salvaterra PM. 1996. Differential regulation of choline acetyltransferase expression in adult Drosophila melanogaster brain. J Neurobiol 30:205-218.
44. Yasuyama K, Meinertzhagen IA, Schurmann FW. 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.
45. Yasuyama K, Meinertzhagen IA, Schurmann FW. 2003. Synaptic connections of cholinergic antennal lobe relay neurons innervating the lateral horn neuropile in the brain of Drosophila melanogaster. J Comp Neurol 466:299-315.
46. Younossi-Hartenstein A, Hartenstein V. 1993. The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev Biol 158:430-447.
47. Younossi-Hartenstein A, Hartenstein V. 1997. Pattern, time of birth, and morphogenesis of sensillum progenitors in Drosophila. Microsc Res Tech 39:479-491.