Innervation of Rat Iris by Trigeminal and Ciliary Neurons Expressing pChAT, a Novel Splice Variant of Choline Acetyltransferase

Journal of Comparative Neurology

Volumn 472, Issue 2, 2004, Pages 232-245

  Yasuhara, Osamu ^a   Aimi, Yoshinari ^a   Shibano, Akira ^a   Matsuo, Akinori ^a   Bellier, Jean Pierre ^a   Park, Masami ^a   Tooyama, Ikuo ^a   Kimura, Hiroshi ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Acetylcholine; Alternative splicing; Ciliary ganglion; Denervation; Trigeminal ganglion

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; CILIARY GANGLION; CONTROLLED STUDY; DENERVATION; ENZYME ACTIVITY; ENZYME ASSAY; IMMUNOHISTOCHEMISTRY; INNERVATION; IRIS; MALE; NERVE CELL; NONHUMAN; OPHTHALMIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; STAINING; TRIGEMINAL NERVE; TRIGEMINUS GANGLION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CILIARY BODY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IRIS; MALE; NEURONS; RATS; RATS, WISTAR; TRIGEMINAL NERVE;

EID: 1842615109     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20077     Document Type: Article

References (46)

1. 2 muscarinic receptors on the iris sphincter muscle differ from those on iris noradrenergic nerves. Eur J Pharmacol 163:263-274.
2. Brice A, Berrard S, Raynaud B, Ansieau S, Coppola T, Weber MJ, Mallet J. 1989. Complete sequence of a cDNA encoding an active rat choline acetyltransferase: a tool to investigate the plasticity of cholinergic phenotype expression. J Neurosci Res 23:266-273.
3. Bruce G, Hersh LB. 1987. Studies on detergent released choline acetyltransferase from membrane fractions of rat and human brain. Neurochem Res 12:1059-1066.
4. Bruce G, Wainer BH, Hersh LB. 1985. Immunoaffinity purification of human choline acetyltransferase: comparison of the brain and placental enzymes. J Neurochem 45:611-620.
5. Chiocchetti R, Poole DP, Kimura H, Aimi Y, Robbins HL, Castelucci P, Furness JB. 2003. Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 311:11-22.
6. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
7. Coulombe J, Bronner-Fraser M. 1990. Development of cholinergic traits in the quail ciliary ganglion: expression of choline acetyltransferase-like immunoreactivity. Neuroscience 37:259-270.
8. Csillik B, Koelle GB. 1965. Histochemistry of the adrenergic and the cholinergic autonomic innervation apparatus as represented by the rat iris. Acta Histochem 22:350-363.
9. Ehinger B. 1966. Ocular and orbital vegetative nerves. Acta Physiol Scand 67(Suppl 268):1-35.
10. Ehinger B, Falck B. 1966. Concomitant adrenergic and parasympathetic fibers in the rat iris. Acta Physiol Scand 67:201-207.
11. Ehinger B, Falck B, Sporrong B. 1970. Possible axo-axonal synapses between peripheral adrenergic and cholinergic nerve terminals. Z Zellforsch Mikrosk Anat 107:508-521.
12. Eränkö O, Huikuri K, Räisänen L. 1967. The effect of denervation on the adrenergic and cholinergic innervation apparatus of the rat iris. Scand J Clin Lab Invest 19(Suppl 95):75.
13. Fonnum F. 1975. A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407-409.
14. 3H]-noradrenaline release in rat or guinea-pig iris and the contraction of the rabbit iris sphincter muscle. Naunyn Schmied Arch Pharmacol 340:597-604.
15. 3-adrenergic relaxation of bovine iris sphincter. FEBS Lett 429:356-358.
16. Hagen JJ, van der Heijden B, Broekkamp CLE. 1988. The relative potencies of cholinomimetics and muscarinic antagonists on the rat iris in vivo: effects of pH on potency of pirenzepine and telenzepine. Naunyn Schmied Arch Pharmacol 338:476-483.
17. Hahn M, Hahn SL, Stone DM, Joh TH. 1992. Cloning of the rat gene encoding choline acetyltransferase, a cholinergic neuron-specific marker. Proc Natl Acad Sci U S A 89:4387-4391.
18. Hedlund K-O, Ayer-Lelievre C, Björklund H, Hultgren L, Seigér Å. 1984. Ultrastructural and histochemical studies of the rat iris: identified neuronal inputs and supportive glia. J Neurocytol 13:703-725.
19. Hoffman BB, Taylor P. 2001. Neurotransmission: the autonomic and somatic motor nervous system. In: Hardman JG, Limbird LE, Molinoff PB, Gilman AG, editors. The pharmacological basis of therapeutics. New York: McGraw-Hill. p 115-153.
20. Huhtala A. 1976. Origin of myelinated nerves in the rat iris. Exp Eye Res 22:259-265.
21. Huhtala A, Tervo T, Huikuri KT, Palkama A. 1976. Effects of denervations on the acetylcholinesterase-containing and fluorescent nerves of the rat iris. Acta Ophthalmol 54:85-98.
22. Ivens C, Mottram DR, Lever JD, Presley R, Howells G. 1973. Studies on the acetylcholinesterase (AChE)-positive and -negative autonomic axons supplying smooth muscle in the normal and 6-hydroxydopamine (6-OHDA) treated rat iris. Z Zellforsch Mikrosk Anat 138:211-222.
23. 2-type muscarinic receptors mediate prejunctional inhibition of norepinephrine release in the human irisciliary body. Exp Eye Res 58:175-180.
24. Kanayama H, Yasuhara O, Matsuo A, Tooyama I, Aimi Y, Bellier J-P, Nagy JI, Fukui K, Kimura H. 2003. Expression of a splice variant of choline acetyltransferase in magnocellular neurons of the tuberomammillary nucleus of rat. Neuroscience 118:243-251.
25. Kessler JA. 1985. Parasympathetic, sympathetic, and sensory interactions in the iris: nerve growth factor regulates cholinergic ciliary ganglion innervation in vivo. J Neurosci 5:2719-2725.
26. Kuchiiwa S, Kuchiiwa T, Suzuki T. 1989. Comparative anatomy of the accessory ciliary ganglion in mammals. Anat Embryol 180:199-205.
27. Kuwayama Y, Grimes PA, Ponte B, Stone RA. 1987. Autonomic neurons supplying the rat eye and the intraorbital distribution of vasoactive intestinal polypeptide (VIP)-like immunoreactivity. Exp Eye Res 44: 907-922.
28. Landis SC, Jackson PC, Fredieu JR, Thibault J. 1987. Catecholaminergic properties of cholinergic neurons and synapses in adult rat ciliary ganglion. J Neurosci 7:3574-3587.
29. Leblanc GG, Trimmer BA, Landis SC. 1987. Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase. Proc Natl Acad Sci U S A 84:3511-3515.
30. Lowry OH, Rossbourgh NI, Farr AL, Randall RJ. 1951. Protein measurement with folin phenol reagent. J Biol Chem 193:265-275.
31. Malmfors T, Nilsson O. 1964. Parasympathetic post-ganglionic denervation of the iris and the parotid gland in the rat. Acta Morphol Neerl Scand 6:81-85.
32. Masuda Y, Yamahara NS, Tanaka M, Ryang S, Kawai T, Imaizumi Y, Watanabe M. 1995. Characterization of muscarinic receptors mediating relaxation and contraction in the rat iris dilator muscle. Br J Pharmacol 114:769-776.
33. Miller A, Costa M, Furness JB, Chubb IW. 1981. Substance P immunoreactive nerves supply the rat iris and cornea. Neurosci Lett 23:243-249.
34. Mussini I, Paggi P, Leone F, Scarsella G, Toschi G. 1984. Degeneration and regeneration of neuromuscular junctions in chicken iris muscle after crush of the ciliary nerves: a study of ultrastructural changes and of cholinergic enzymes. Neuroscience 12:53-66.
35. Nakajima K, Tooyama I, Yasuhara O, Aimi Y, Kimura H. 2000. Immunohistochemical demonstration of choline acetyltransferase of a peripheral type (pChAT) in the enteric nervous system of rats. J Chem Neuroanat 18:31-40.
36. Nakanishi Y, Tooyama I, Yasuhara O, Aimi Y, Kitajima K, Kimura H. 1999. Immunohistochemical localization of choline acetyltransferase of a peripheral type in rat larynx. J Chem Neuroanat 17:21-32.
37. Olson L, Lièvre CA-L, Björklund H, Ebendal T, Granholm A-C, Hedlund K-O, Hökfelt T, Melander T, Seiger Å, Strömberg I. 1988. The innervation apparatus of the rodent iris. In: Björklund A, Hökfelt T, Owman C, editors. Handbook of chemical neuroanatomy, vol. 6. The peripheral nervous system. Amsterdam: Elsevier. p 545-597.
38. Ryan R, McClure WO. 1980. Physical and kinetic properties of choline acetyl transferase from rat and bovine brain. J Neurochem 34:395-403.
39. Sann H, McCarthy PW, Mader M, Schemann M. 1995. Choline acetyltransferase-like immunoreactivity in small diameter neurones of the rat dorsal root ganglion. Neurosci Lett 198:17-20.
40. Seiger Å, Selin U-B, Kessler J, Black I, Ayer-LeLievre C. 1985. Substance P-containing sensory nerves in the rat iris. Normal distribution, ontogeny and innervation of intraocular iris grafts. Neuroscience 15:519-528.
41. Stone RA, McGlinn AM, Kuwayama Y, Grimes PA. 1988. Peptide immunoreactivity of the ciliary ganglion and its accessory cells in the rat. Brain Res 475:389-392.
42. Tago H, Kimura H, Maeda T. 1986. Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem 34:1431-1438.
43. Tooyama I, Kimura H. 2000. An alternative splice variant of choline acetyltransferase is localized preferentially in peripheral nerve cells and fibers: implication for a peripheral cholinergic marker. J Chem Neuroanat 17:217-226.
44. Wessler I, Kirkpatrick CJ, Racké K. 1998. Non-neuronal acetylcholine, a locally acting molecule, widely distributed in biological systems: expression and function in humans. Pharmacol Ther 77:59-79.
45. Wu D, Hersh LB. 1995. Identification of an active site arginine in rat choline acetyltransferase by alanine scanning mutagenesis. J Biol Chem 270:29111-29116.
46. Yasuhara O, Tooyama I, Aimi Y, Bellier J-P, Hisano T, Matsuo A, Park M, Kimura H. 2003. Demonstration of cholinergic ganglion cells in rat retina: expression of an alternative splice variant of choline acetyltransferase. J Neurosci 23:2872-2881.