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Choline Acetyltransferase in Ocular Tissues of Rabbits, Cats, Cattle, and Man

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Choline Acetyltransferase in Ocular Tissues of Rabbits, Cats, Cattle, and Man Choline acetyltransferase in ocular tissues of rabbits, cats, cattle, and man Joel S. Mindel* and Thomas W. Mittag The variation of choline acetyltransferase activity in ocular tissues of four mammalian species, rabbits, cats, cattle, and man, was determined. Enzyme activity of irides and ciliary bodies, i.e., parasympathetically innervated structures, tended to be similar in all four species. Two exceptions were bovine irides and human ciliary bodies; these two tissues had higlier enzyme activities. Choline acetyltransferase activity was present in the corneal epithelium of rabbit, bovine, and human eyes, but little or none could be detected in that of cats. Feline retina and pigment epithelium-choroid also contained far less choline acetyltransferase activity than the same tissues in the other three species. Key words: choline acetyltransferase, eye, ocular, cornea, iris, ciliary body, aqueous humor, retina, choroid. Choline acetyltransferase, the enzyme optic nerve. In recent years, the retinal and responsible for acetylcholine synthesis, has corneal epithelial choline acetyltransferases been assayed in a number of ocular tis- have attracted the most interest. Ross and sues. 1"s This enzyme is a more specific McDougal" have found that the inner plexi- marker of cholinergic activity than are the form layer contains high levels of choline ubiquitous cholinesterases. The first esti- acetyltransferase activity. Van Alphen7 and mates of ocular choline acetyltransferase Williams and Coopers reported high con- activity appeared in 19461'2; low enzyme centrations of the enzyme in rabbit and levels were reported for canine and rabbit bovine corneal epithelium. The corneal epi- thelium contains none of those structures normally associated with cholinergic ac- From the Departments of Pharmacology and tivity, i.e., synapses, myoneural junctions, Ophthalmology, Mount Sinai School of Medi- cine, City University of New York, and the or parasympathetic motor axons. The pres- Bronx Veterans Hospital, New York, N. Y. ence of choline acetyltransferase activity Supported in part by a Fight-for-Sight Grant-in- in corneal epithelium, which consists pri- Aid and National Eye Institute Grant I RO1 marily of epithelial cells and sensory nerve EY01243. endings, has elicited several theories at- "Chief of Ophthalmology, Bronx Veterans Ad- tempting to link cholinergic activity with ministration Hospital. Dr. Mindel is the re- corneal touch sensitivity0"11 and epithelial cipient of a Research Career Development ion transport.s> 12 Award from the National Eye Institute. Submitted for publication Feb. 12, 1976. Although the choline acetyltransferase of Reprint requests: J. S. Mindel, The Mount Sinai specific tissues has interested different School of Medicine, Fifth Avenue & 100th St., workers, no general survey of ocular struc- New York, N. Y. 10029. tures has been reported. This paper de- 808 Downloaded from iovs.arvojournals.org on 09/30/2021 Volume 15 Ocular choline acetyltransferase 809 Number JO scribes the distribution of choline acetyl- on kinetic studies of rabbit tissues where transferase activity in the eyes of four the concentration of choline was varied species: rabbit, cat, cattle, and man. between 25 /xM and 10 mM and the con- centration of acetyl-coenzyme A was Materials and methods varied between 10 and 400 /xM. Using a Eyes of adult female Dutch Belt rabbits and double reciprocal plot by the method of female mongrel cats, killed with parenteral pento- Lineweaver-Burk, the Michaelis-Menton barbital or secobarbital, were studied. Bovine constants (Km's) were calculated from the eyes were supplied on ice by an abattoir within 5 hours of death. Human eyes were obtained extrapolated intercepts. The Km for choline hours to days after death from the Eye Bank was 500 /xM for all four ocular tissues, for Sight Restoration, New York, N. Y. corneal epithelium, iris-ciliary body, retina, Corneas were removed by trephine as full thick- and pigment epithelium-choroid. The Km ness buttons. In rabbits, the ciliary body is poorly for acetyl-coenzyme A was 20 ju,M for developed and both it and the iris were excised corneal epithelium, iris-ciliary body, and and assayed together. In all four species, the pigment epithelium and choroid were dissected pigment epithelium-choroid; the Km for out and assayed together. retinal acetyl-coenzyme A was 50 /xM. The Choline acetyltransferase was assayed by a ocular tissues from eight eyes were pooled modification of the methods of Schrier and and the specific activities determined (ex- 11 Sinister™ and McCaman and Hunt. Tissues pressed as nanomoles acetylcholine formed were homogenized on ice in pH 7.4 buffer solu- per hour per milligram [nmole ACh tion of sufficient volume to give a concentration of less than 10 per cent weight/volume. The formed/hr./mg.] of protein)—comeal epi- concentrations of buffer ingredients during in- thelial protein, 18.1; iris-ciliary body pro- cubation were 0.5 per cent Triton-X, 10 mM tein, 1.6; retinal protein, 58.4; and pigment ethylenediamine tetraacetic acid (EDTA), 300 epithelium-choroid protein, 6.7. The rates mM sodium chloride, and 150 mM potassium of reaction were found to be linear during hydrogen phosphate. The assay was performed in duplicate 6 by 50 mm. tubes containing 200 the incubation period used in the assay. fil of homogenate and 20 <ul of a solution giving Enzyme activities of individual tissues a final concentration of 2 mM dithiothreitol, 0.1 were then assayed and calculated on a per mM physostigmine, 5 mM choline chloride, and milligram of protein basis and/or a per 0.2 mM acetyl-coenzyme A. The last contained whole tissue basis. sufficient acetyl-1-C1 '-coenzyme A to give ap- proximately 1 c.p.m. per picomole. A third tube Variation in ocular choline acetyltrans- served as blank and contained 0.1 mM naphthyl- ferase activity of rabbit, cat, cattle, and vinylpyridinium hydroxyethyl bromidelr> but no choline. After a 30 min. incubation at 37.5° C, human ocular tissues (per milligram of the reaction was terminated with 1 drop of protein). The corneal epithelium of cats, CuCl;, 2.5 per cent, per tube. The contents of unlike the other three mammalian species, each tube were quantitatively transferred, using had little or no detectable choline acetyl- 1 ml. of H-O, to a 3 by 0.6 cm. column of Bio- transferase activity (Tables I to IV). Rad AC1-X8, 200 to 400 mesh chloride form ion exchange resin in water. Effluents were collected Rabbit, bovine, and human corneal epi- directly in scintillation vials and counted in 10 thelia had high levels of enzyme activity. ml. of Bray's solution. Protein content of tissues The corneal stroma and endothelium of all was determined by the method of Lowry and four species had little or no choline acetyl- 1 <: associates. Naphthylvinylpyridinium hydroxyethyl transferase activity. bromide, dithiotreitol, choline chloride, and acetyl-coenzyme A solutions were made up weekly The enzyme activity of human, rabbit, and stored frozen. Physostigmine solutions were and cat iris was, on the average, approxi- made up daily. mately 2 nmole ACh formed/hr./mg. of protein. However, the average bovine iris Results contained four to five times this activity. The choline acetyltransferase activities The ciliary bodies of cattle, rabbits, and of all four species were measured with a cats formed 2 to 3 nmole ACh/hr./mg. of standardized assay. This assay was based protein, whereas the average human ciliary Downloaded from iovs.arvojournals.org on 09/30/2021 810 Minclel and Mittag Investigative Ophthalmology October 1976 Table I. Distribution of choline Table III. Distribution of choline acetyltransferase activity (per milligram acetyltransf erase activity (per milligram of protein) in the ocular tissues of Dutch of protein) in the ocular tissues of cattle Aver- Std. Aver- Std. Tissue age* Range* Dev. n Tissue age* Range* Dev. n Cornea: Conjunctiva 0.3 _ 0.0 3 Epithelium 46.5 11.6-89.2 27.5 8 Cornea: Stroma-endo- 0.4 0.0- 1.4 0.6 8 Epithelium 20.6 3.9-41.2 13.6 21 thelium Stroma-endo- 0.0f 0.0 8 IrJs 10.8 1.6-22.2 6.5 10 thelium Ciliary body 1.9 0.3- 6.9 2.1 10 Iris-ciliary body 2.6 0.2- 4.9 1.7 5i Lens o.ot — 0.1 2 Lens 0.0$ 0.0 13 Vitreous 0.9 0.5- 1.3 0.6 2 Vitreous 0.5 0.0- 2.1 0.7 g Retina 13.0 4.0-31.4 9.8 10 Retina 26.1 5.8-94.4 20.5 46 Pigment epithelium- 4.6 0.0-10.9 4.5 10 Pigment epithelium- 3.4 0.2-12.4 3.1 47 choroid choroid Optic nerve 0.3 — — 1 Optic nerve 0.0 0.0- 0.1 0.0 g Sclera 1.8 — — 1 Sclera o.o§ — 0.0 8 °Nanomoles ACh formed/hr./mg. of protein °Nanomoles ACh formed/hr./mg. of protein. f-0.15. t< 0.036. }< 0.003. 5< 0.010. Table IV. Distribution of choline acetyltransf erase activity (per milligram Table II. Distribution of choline of protein) in the ocular tissues of man acetyltransf erase activity (per milligram Aver- Std. of protein) in ocular tissues of cats Tissue age* Range* Dev. Aver- Cornea: Std. 11.2 Tissue age* Range* Dev. n Epithelium — — t Strnma-enrio- 0.4 | Cornea: thelium Epithelium 0.1 0.0-0.6 0.2 8 Iris 2.5 0.1- 5.3 1.8 10 Stroma-endo- 0.0f — 0.0 4 Ciliary body 16.8 0.1-38.0 14.3 11 thelium Lens 0.0$ — 0.0 6 Full thickness 0.0 0.0-0.3 0.1 12 Vitreous 2.2 — — t Iris 2.0 0.3-5.5 1.5 16 Retina 6.1 0.9-23.1 6.7 10 Ciliary body 2.9 0.5-6.6 2.2 16 Pigment epithelium- 5.1 0.6-11.0 4.5 10 Lens 0.0$ — 0.0 4 choroid Vitreous 0.0§ — 0.0 4 Optic nerve 0.7 — — t Retina 0.7 0.4-1.2 0.3 12 Sclera 1.2 — — t Pigment epithelium- 0.5 0.2-0.7 0.2 6 "Nanomoles ACh formed/hr./m{%.
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