Abstract
Chromaffin cells were observed singly or in clusters in the heart and sympathetic cord of 2 genera of dipnoan fish, Protopterus and Lepidosiren. They were invariably found in close association with the autonomic sympathetic nervous system and at sites where chromaffin cells or their precursors are situated in mammals during ontogenetic development. X-ray microanalysis demonstrated that they contained a primary catecholamine which was identified microspectrofluorometrically as dopamine. The chromaffin cells were innervated by efferent axons with typical preganglionic sympathetic terminals which were acetylcholinesterase-positive. Although the general morphology and cytochemistry agree with those of developing intra-adrenal chromaffin cells in mammals, the morphological characteristics implicate them as active secretory gland cells. The dopamine transmitter phenotype seems to be determined by the maintenance throughout life of the separate and distant location of steroidogenic interrenal tissue from suprarenal elements.
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- AUGUSTINSSON K. B., FANGE R., JOHNELS A., OSTLUND E. Histological, physiological and biochemical studies on the heart of two cyclostomes, hagfish (Myxine) and lamprey (Lampetra). J Physiol. 1956 Feb 28;131(2):257–276. doi: 10.1113/jphysiol.1956.sp005461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Abrahamsson T., Holmgren S., Nilsson S., Pettersson K. On the chromaffin system of the African lungfish, Protopterus aethiopicus. Acta Physiol Scand. 1979 Oct;107(2):135–139. doi: 10.1111/j.1748-1716.1979.tb06452.x. [DOI] [PubMed] [Google Scholar]
- Abrahamsson T., Jönsson A. C., Nilsson S. Catecholamine synthesis in the chromaffin tissue of the African lungfish, Protopterus aethiopicus. Acta Physiol Scand. 1979 Oct;107(2):149–151. doi: 10.1111/j.1748-1716.1979.tb06454.x. [DOI] [PubMed] [Google Scholar]
- Accordi F. The chromaffin cells of urodele amphibians. J Anat. 1991 Dec;179:1–8. [PMC free article] [PubMed] [Google Scholar]
- Andrew A. Further evidence that enterochromaffin cells are not derived from the neural crest. J Embryol Exp Morphol. 1974 Jun;31(3):589–598. [PubMed] [Google Scholar]
- Angelakos E. T., King M. P., Millard R. W. Regional distribution of catecholamines in the hearts of various species. Ann N Y Acad Sci. 1969 Jan 31;156(1):219–240. doi: 10.1111/j.1749-6632.1969.tb16730.x. [DOI] [PubMed] [Google Scholar]
- BLASCHKO H. The development of current concepts of catecholamine formation. Pharmacol Rev. 1959 Jun;11(2 Pt 2):307–316. [PubMed] [Google Scholar]
- BLOOM G., OSTLUND E., von EULER U., LISHAJKO F., RITZEN M., ADAMS-RAY J. Studies on catecholamine-containing granules of specific cells in cyclostome hearts. Acta Physiol Scand Suppl. 1961;53(185):1–34. [PubMed] [Google Scholar]
- Battaglia G. Ultrastructural observations on the biogenic amines in the carotid and aortic-abdominal bodies of the human fetus. Z Zellforsch Mikrosk Anat. 1969;99(4):529–537. doi: 10.1007/BF00340944. [DOI] [PubMed] [Google Scholar]
- Benedeczky I., Smith A. D. Ultrastructural studies on the adrenal medulla of golden hamster: origin and fate of secretory granules. Z Zellforsch Mikrosk Anat. 1972;124(3):367–386. doi: 10.1007/BF00355037. [DOI] [PubMed] [Google Scholar]
- Björklund A., Cegrell L., Falck B., Ritzén M., Rosengren E. Dopamine-containing cells in sympathetic ganglia. Acta Physiol Scand. 1970 Mar;78(3):334–338. doi: 10.1111/j.1748-1716.1970.tb04668.x. [DOI] [PubMed] [Google Scholar]
- Björklund A., Ehinger B., Falck B. Z. Analysis of fluorescence excitation peak ratios for the cellular identification of noradrenaline, dopamine or their mixtures. J Histochem Cytochem. 1972 Jan;20(1):56–64. doi: 10.1177/20.1.56. [DOI] [PubMed] [Google Scholar]
- Björklund A., Ehinger B., Falck B. A method for differentiating dopamine from noradrenaline in tissue sections by microspectrofluorometry. J Histochem Cytochem. 1968 Apr;16(4):263–270. doi: 10.1177/16.4.263. [DOI] [PubMed] [Google Scholar]
- Brundin T. Studies on the preaortal paraganglia of newborn rabbits. Acta Physiol Scand Suppl. 1966;290:1–54. [PubMed] [Google Scholar]
- CORRODI H., HILLARP N. A., JONSSON G. FLUORESCENCE METHODS FOR THE HISTOCHEMICAL DEMONSTRATION OF MONOAMINES. 3. SODIUM BOROHYDRIDE REDUCTION OF THE FLUORESCENT COMPOUNDS AS A SPECIFICITY TEST. J Histochem Cytochem. 1964 Aug;12:582–586. doi: 10.1177/12.8.582. [DOI] [PubMed] [Google Scholar]
- COUPLAND R. E. (ELECTRON MICROSCOPIC OBSERVATIONS ON THE STRUCTURE OF THE RAT ADRENAL MEDULLA. I. THE ULTRASTRUCTURE AND ORGANIZATION OF CHROMAFFIN CELLS IN THE NORMAL ADRENAL MEDULLA.) J Anat. 1965 Apr;99:231–254. [PMC free article] [PubMed] [Google Scholar]
- COUPLAND R. E. On the morphology and adrenaline-nor-adrenaline content of chromaffin tissue. J Endocrinol. 1953 Apr;9(2):194–203. doi: 10.1677/joe.0.0090194. [DOI] [PubMed] [Google Scholar]
- COUPLAND R. E., PYPER A. S., HOPWOOD D. A METHOD FOR DIFFERENTIATING BETWEEN NORADRENALINE- AND ADRENALINE-STORING CELLS IN THE LIGHT AND ELECTRON MICROSCOPE. Nature. 1964 Mar 21;201:1240–1242. doi: 10.1038/2011240b0. [DOI] [PubMed] [Google Scholar]
- COUPLAND R. E. The development and fate of the abdominal chromaffin tissue in the rabbit. J Anat. 1956 Oct;90(4):527–537. [PMC free article] [PubMed] [Google Scholar]
- COUPLAND R. E. The prenatal development of the abdominal para-aortic bodies in man. J Anat. 1952 Oct;86(4):357–372. [PMC free article] [PubMed] [Google Scholar]
- Call R. N., Janssens P. A. Histochemical studies of the adrenocortical homologue in the kidney of the Australian lungfish, Neoceratodus forsteri. Cell Tissue Res. 1975;156(4):533–538. doi: 10.1007/BF00225111. [DOI] [PubMed] [Google Scholar]
- Cannata M. A., Chiocchio S. R., Tramezzani J. H. Specificity of the glutaraldehyde silver technique for catecholamines and related compounds. Histochemie. 1968;12(3):253–264. doi: 10.1007/BF00306003. [DOI] [PubMed] [Google Scholar]
- Carmichael S. W., Blair B. C. Normal ultrastructure of the day old dog adrenal medulla. J Anat. 1973 May;115(Pt 1):113–118. [PMC free article] [PubMed] [Google Scholar]
- Carmichael S. W., Winkler H. The adrenal chromaffin cell. Sci Am. 1985 Aug;253(2):40–49. doi: 10.1038/scientificamerican0885-40. [DOI] [PubMed] [Google Scholar]
- Chiba T., Black A. C., Jr, Williams T. H. Evidence for dopamine-storing interneurons and paraneurons in rhesus monkey sympathetic ganglia. J Neurocytol. 1977 Aug;6(4):441–453. doi: 10.1007/BF01178227. [DOI] [PubMed] [Google Scholar]
- Chiba T., Williams T. H. Histofluorescence characteristics and quantification of small intensely fluorescent (SIF) cells in sympathetic ganglia of several species. Cell Tissue Res. 1975 Oct 13;162(3):331–341. doi: 10.1007/BF00220179. [DOI] [PubMed] [Google Scholar]
- Coupland R. E. Corticosterone and methylation of noradrenaline by extra-adrenal chromaffin tissue. J Endocrinol. 1968 Aug;41(4):487–490. doi: 10.1677/joe.0.0410487. [DOI] [PubMed] [Google Scholar]
- Coupland R. E. Electron microscopic observations on the structure of the rat adrenal medulla: II. Normal innervation. J Anat. 1965 Apr;99(Pt 2):255–272. [PMC free article] [PubMed] [Google Scholar]
- Coupland R. E., Hopwood D. The mechanism of the differential staining reaction for adrenaline-and noreadrenaline-storing granules in tissues fixed in glutaraldehyde. J Anat. 1966 Apr;100(Pt 2):227–243. [PMC free article] [PubMed] [Google Scholar]
- Coupland R. E., Kobayashi S., Crowe J. On the fixation of catecholamines including adrenaline in tissue sections. J Anat. 1976 Nov;122(Pt 2):403–413. [PMC free article] [PubMed] [Google Scholar]
- Coupland R. E., MacDougall J. D. Adrenaline formation in noradrenaline-storing chromaffin cells in vitro induced by corticosterone. J Endocrinol. 1966 Nov;36(3):317–324. doi: 10.1677/joe.0.0360317. [DOI] [PubMed] [Google Scholar]
- Coupland R. E., Parker T. L., Kesse W. K., Mohamed A. A. The innervation of the adrenal gland. III. Vagal innervation. J Anat. 1989 Apr;163:173–181. [PMC free article] [PubMed] [Google Scholar]
- Coupland R. E. The natural history of the chromaffin cell--twenty-five years on the beginning. Arch Histol Cytol. 1989;52 (Suppl):331–341. doi: 10.1679/aohc.52.suppl_331. [DOI] [PubMed] [Google Scholar]
- Coupland R. E., Weakley B. S. Developing chromaffin tissue in the rabbit: an electron microscopic study. J Anat. 1968 Mar;102(Pt 3):425–455. [PMC free article] [PubMed] [Google Scholar]
- Coupland R. E., Weakley B. S. Electron microscopic observation on the adrenal medulla and extra-adrenal chromaffin tissue of the postnatal rabbit. J Anat. 1970 Mar;106(Pt 2):213–231. [PMC free article] [PubMed] [Google Scholar]
- EADE N. R. The distribution of the catechol amines in homogenates of the bovine adrenal medulla. J Physiol. 1958 Apr 3;141(1):183–192. doi: 10.1113/jphysiol.1958.sp005966. [DOI] [PMC free article] [PubMed] [Google Scholar]
- ERANKO O., RAISANEN L. Cytophotometric study on the chromaffin reaction, the iodate reaction and formalin-induced fluorescence as indicators of adrenaline and noradrenaline concentrations in the adrenal medulla. J Histochem Cytochem. 1961 Jan;9:54–58. doi: 10.1177/9.1.54. [DOI] [PubMed] [Google Scholar]
- Ehinger B., Falck B., Persson H., Sporrong B. Adrenergic and cholinesterase-containing neurons of the heart. Histochemie. 1968;16(3):197–205. doi: 10.1007/BF00307848. [DOI] [PubMed] [Google Scholar]
- Elfvin L. G., Hökfelt T., Goldstein M. Fluorescence microscopical, immunohistochemical and ultrastructural studies on sympathetic ganglia of the guinea pig, with special reference to the sif cells and their catecholamine content. J Ultrastruct Res. 1975 Jun;51(3):377–396. doi: 10.1016/s0022-5320(75)80101-8. [DOI] [PubMed] [Google Scholar]
- Ellison J. P., Hibbs R. G. Catecholamine-containing cells of the guinea pig heart: an ultrastructural study. J Mol Cell Cardiol. 1974 Feb;6(1):17–26. doi: 10.1016/0022-2828(74)90003-0. [DOI] [PubMed] [Google Scholar]
- Eränkö L., Eränkö O. Effect of hydrocortisone on histochemically demonstrable catecholamines in the sympathetic ganglia and extra-adrenal chromaffin tissue of the rat. Acta Physiol Scand. 1972 Jan;84(1):125–133. doi: 10.1111/j.1748-1716.1972.tb05161.x. [DOI] [PubMed] [Google Scholar]
- Eränkö L., Päivärinta H., Soinila S., Häppölä O. Transmitters and modulators in the superior cervical ganglion of the rat. Med Biol. 1986;64(2-3):75–83. [PubMed] [Google Scholar]
- Eränkö O., Lempinen M., Räisänen L. Adrenaline and noradrenaline in the organ of Zuckerkandl and adrenals of newborn rats treated with hydrocortisone. Acta Physiol Scand. 1966 Jan-Feb;66(1):253–254. doi: 10.1111/j.1748-1716.1966.tb03196.x. [DOI] [PubMed] [Google Scholar]
- Eränkö O., Pickel V. M., Härkönen M., Eränko L., Joh T. H., Reis D. J. Effect of hydrocortisone on catecholamines and the enzymes synthesizing them in the developing sympathetic ganglion. Histochem J. 1982 May;14(3):461–478. doi: 10.1007/BF01011857. [DOI] [PubMed] [Google Scholar]
- Feldberg W., Minz B., Tsudzimura H. The mechanism of the nervous discharge of adrenaline. J Physiol. 1934 Jun 9;81(3):286–304. doi: 10.1113/jphysiol.1934.sp003136. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fenwick E. M., Fajdiga P. B., Howe N. B., Livett B. G. Functional and morphological characterization of isolated bovine adrenal medullary cells. J Cell Biol. 1978 Jan;76(1):12–30. doi: 10.1083/jcb.76.1.12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontaine J., Le Douarin N. M. Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol. 1977 Oct;41:209–222. [PubMed] [Google Scholar]
- Forsgren S., Moravec M., Moravec J. Catecholamine-synthesizing enzymes and neuropeptides in rat heart epicardial ganglia; an immunohistochemical study. Histochem J. 1990 Dec;22(12):667–676. doi: 10.1007/BF01047451. [DOI] [PubMed] [Google Scholar]
- GHOSH A. A comparative study of the histochemistry of the avian adrenals. Gen Comp Endocrinol. 1962;Suppl 1:75–80. doi: 10.1016/0016-6480(62)90079-5. [DOI] [PubMed] [Google Scholar]
- Gannon B. J., Campbell G. D., Satchell G. H. Monoamine storage in relation to cardiac regulation in the Port Jackson shark Heterodontus portusjacksoni. Z Zellforsch Mikrosk Anat. 1972;131(4):437–450. doi: 10.1007/BF00306963. [DOI] [PubMed] [Google Scholar]
- Gaskell J. F. The distribution and physiological action of the suprarenal medullary tissue in petromyzon fluviatilis. J Physiol. 1912 Mar 29;44(1-2):59–67. doi: 10.1113/jphysiol.1912.sp001502. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gewirtz G. P., Kvetnanský R., Weise V. K., Kopin I. J. Effect of hypophysectomy on adrenal dopamine -hydroxylase activity in the rat. Mol Pharmacol. 1971 Mar;7(2):163–168. [PubMed] [Google Scholar]
- Gorgas K., Böck P. Morphology and histochemistry of the adrenal medulla. I. Various types of primary catecholamine-storing cells in the mouse adrenal medulla. Histochemistry. 1976 Nov 19;50(1):17–31. doi: 10.1007/BF00492782. [DOI] [PubMed] [Google Scholar]
- Grönblad M., Akerman K. E., Eränkö O. Ultrastructural evidence of exocytosis from glomus cells after incubation of adult rat carotid bodies in potassium-rich calcium-containing media. Brain Res. 1980 May 12;189(2):576–581. doi: 10.1016/0006-8993(80)90372-8. [DOI] [PubMed] [Google Scholar]
- HAEGGENDAL J. AN IMPROVED METHOD FOR FLUORIMETRIC DETERMINATION OF SMALL AMOUNTS OF ADRENALINE AND NORADRENALINE IN PLASMA AND TISSUES. Acta Physiol Scand. 1963 Nov;59:242–254. doi: 10.1111/j.1748-1716.1963.tb02739.x. [DOI] [PubMed] [Google Scholar]
- HAMBERGER B., MALMFORS T., SACHS C. STANDARDIZATION OF PARAFORMALDEHYDE AND OF CERTAIN PROCEDURES FOR THE HISTOCHEMICAL DEMONSTRATION OF CATECHOLAMINES. J Histochem Cytochem. 1965 Feb;13:147–147. doi: 10.1177/13.2.147. [DOI] [PubMed] [Google Scholar]
- HOLMES W. The adrenal homologues in the lungfish Protopterus. Proc R Soc Lond B Biol Sci. 1950 Nov;137(889):549–562. doi: 10.1098/rspb.1950.0066. [DOI] [PubMed] [Google Scholar]
- Hanker J. S., Thornburg L. P., Yates P. E., Moore H. G., 3rd The demonstration of cholinesterases by the formation of osmium blacks at the sites of Hatchett's brown. Histochemie. 1973 Jun;37(3):223–242. doi: 10.1007/BF00304184. [DOI] [PubMed] [Google Scholar]
- Hartwig H. G., Reinhold C., Lyncker I. Distribution patterns of formaldehyde-induced fluorescence of hypothalamic monoamines. Cell Tissue Res. 1979 Oct;201(3):499–502. doi: 10.1007/BF00237008. [DOI] [PubMed] [Google Scholar]
- Hervonen A., Alho H., Helen P., Kanerva L. Small, intensely fluorescent cells of human sympathetic ganglia. Neurosci Lett. 1979 Apr;12(1):97–101. doi: 10.1016/0304-3940(79)91487-3. [DOI] [PubMed] [Google Scholar]
- Hervonen A. Development of catecholamine--storing cells in human fetal paraganglia and adrenal medulla. A histochemical and electron microscopical study. Acta Physiol Scand Suppl. 1971;368:1–94. [PubMed] [Google Scholar]
- Heym C., Addicks K., Gerold N., Schröder H., König R., Wedel C. Catecholamines in paraganglionic cells of the rat superior cervical ganglion: functional aspects. Adv Biochem Psychopharmacol. 1980;25:87–94. [PubMed] [Google Scholar]
- JANSSENS P. A., VINSON G. P., JONES I. C., MOSLEY W. AMPHIBIAN CHARACTERISTICS OF THE ADRENAL CORTEX OF THE AFRICAN LUNGFISH (PROTOPTERUS SP.). J Endocrinol. 1965 Jul;32:373–382. doi: 10.1677/joe.0.0320373. [DOI] [PubMed] [Google Scholar]
- Jacobowitz D. Histochemical studies of the relationship of chromaffin cells and adrenergic nerve fibers to the cardiac ganglia of several species. J Pharmacol Exp Ther. 1967 Nov;158(2):227–240. [PubMed] [Google Scholar]
- Kajihara H., Akimoto T., Iijima S. On the chromaffin cells in dog adrenal medulla; with special reference to the small granule chromaffin cells (SGC cells). Cell Tissue Res. 1978 Jul 13;191(1):1–14. doi: 10.1007/BF00223211. [DOI] [PubMed] [Google Scholar]
- Kesse W. K., Parker T. L., Coupland R. E. The innervation of the adrenal gland. I. The source of pre- and postganglionic nerve fibres to the rat adrenal gland. J Anat. 1988 Apr;157:33–41. [PMC free article] [PubMed] [Google Scholar]
- Kobayashi S., Coupland R. F. Two populations of microvesicles in the SGC (small granule chromaffin) cells of the mouse adrenal medulla. Arch Histol Jpn. 1977 Jun;40(3):251–259. doi: 10.1679/aohc1950.40.251. [DOI] [PubMed] [Google Scholar]
- Kobayashi S., Serizawa Y. Stress-induced degranulation accompanied by vesicle formation in the adrenal chromaffin cells of the mouse. Arch Histol Jpn. 1979 Jul;42(3):375–388. doi: 10.1679/aohc1950.42.375. [DOI] [PubMed] [Google Scholar]
- Libet B., Owman C. Concomitant changes in formaldehyde-induced fluorescence of dopamine interneurones and in slow inhibitory post-synaptic potentials of the rabbit superior cervical ganglion, induced by stimulation of the preganglionic nerve or by a muscarinic agent. J Physiol. 1974 Mar;237(3):635–662. doi: 10.1113/jphysiol.1974.sp010502. [DOI] [PMC free article] [PubMed] [Google Scholar]
- NIEMINEVA K., PEKKARINEN A. Determination of adrenalin and noradrenalin in the human foetal adrenals and aortic bodies. Nature. 1953 Mar 7;171(4349):436–437. doi: 10.1038/171436b0. [DOI] [PubMed] [Google Scholar]
- Nagasawa J. Exocytosis: the common release mechanism of secretory granules in glandular cells, neurosecretory cells, neurons and paraneurons. Arch Histol Jpn. 1977;40 (Suppl):31–47. doi: 10.1679/aohc1950.40.supplement_31. [DOI] [PubMed] [Google Scholar]
- Neff N. H., Karoum F., Hadjiconstantinou M. Dopamine-containing small intensely fluorescent cells and sympathetic ganglion function. Fed Proc. 1983 Oct;42(13):3009–3011. [PubMed] [Google Scholar]
- Norberg K. A., Ritzén M., Ungerstedt U. Histochemical studies on a special catecholamine-containing cell type in sympathetic ganglia. Acta Physiol Scand. 1966 Jul-Aug;67(3):260–270. doi: 10.1111/j.1748-1716.1966.tb03311.x. [DOI] [PubMed] [Google Scholar]
- OSTLUND E., BLOOM G., ADAMS-RAY J., RITZEN M., SIEGMAN M., NORDENSTAM H., LISHAJKO F., von EULER U. Storage and release of catecholamines, and the occurrence of a specific submicroscopic granulation in hearts of cyclostomes. Nature. 1960 Oct 22;188:324–325. doi: 10.1038/188324a0. [DOI] [PubMed] [Google Scholar]
- Papka R. E. A study of catecholamine-containing cells in the hearts of fetal and postnatal rabbits by fluorescence and electron microscopy. Cell Tissue Res. 1974;154(4):471–484. doi: 10.1007/BF00219668. [DOI] [PubMed] [Google Scholar]
- Papka R. E. Studies of cardiac ganglia in pre- and postnatal rabbits. Cell Tissue Res. 1976 Nov 24;175(1):17–35. doi: 10.1007/BF00220820. [DOI] [PubMed] [Google Scholar]
- Parker T. L., Mohamed A. A., Coupland R. E. The innervation of the adrenal gland. IV. The source of pre- and postganglionic nerve fibres to the guinea-pig adrenal gland. J Anat. 1990 Oct;172:17–24. [PMC free article] [PubMed] [Google Scholar]
- RICHARDSON K. C. THE FINE STRUCTURE OF THE ALBINO RABBIT IRIS WITH SPECIAL REFERENCE TO THE IDENTIFICATION OF ADRENERGIC AND CHOLINERGIC NERVES AND NERVE ENDINGS IN ITS INTRINSIC MUSCLES. Am J Anat. 1964 Mar;114:173–205. doi: 10.1002/aja.1001140202. [DOI] [PubMed] [Google Scholar]
- Reinhold C., Hartwig H. G. Progress in microfluorometric identification of monoamine fluorophores. Brain Res Bull. 1982 Jul-Dec;9(1-6):97–105. doi: 10.1016/0361-9230(82)90125-3. [DOI] [PubMed] [Google Scholar]
- SHEPHERD D. M., WEST G. B. Hydroxytyramine and the adrenal medulla. J Physiol. 1953 Apr 28;120(1-2):15–19. doi: 10.1113/jphysiol.1953.sp004868. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SHEPHERD D. M., WEST G. B. Noradrenaline and accessory chromaffin tissue. Nature. 1952 Jul 5;170(4314):42–43. doi: 10.1038/170042b0. [DOI] [PubMed] [Google Scholar]
- SHEPHERD D. M., WEST G. B. Noradrenaline and the suprarenal medulla. Br J Pharmacol Chemother. 1951 Dec;6(4):665–674. doi: 10.1111/j.1476-5381.1951.tb00678.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheuermann D. W. A study of chromaffin cells in the heart of Protopterus. Folia Morphol (Praha) 1980;28(1):93–98. [PubMed] [Google Scholar]
- Scheuermann D. W., De Groodt-Lasseel M. H., Stilman C. A light and fluorescence cytochemical and electron microscopic study of granule-containing cells in the intrapulmonary ganglia of Pseudemys scripta elegans. Am J Anat. 1984 Dec;171(4):377–399. doi: 10.1002/aja.1001710404. [DOI] [PubMed] [Google Scholar]
- Scheuermann D. W., Stilman C., Reinhold C., De Groodt-Lasseel M. H. Microspectrofluorometric study of monoamines in the auricle of the heart of Protopterus aethiopicus. Cell Tissue Res. 1981;217(2):443–449. doi: 10.1007/BF00233594. [DOI] [PubMed] [Google Scholar]
- Schröder H., Gerold N., Heym C. Immunofluorescence of dopamine-beta-hydroxylase in small intensely fluorescent cells of human sympathetic ganglia. Acta Anat (Basel) 1981;109(1):47–50. doi: 10.1159/000145364. [DOI] [PubMed] [Google Scholar]
- Schröder H., Lackner K., Heym C. Simultaneous demonstration of catecholamines and phenylethanolamine-N-methyltransferase in the same tissue section by means of formaldehyde-induced fluorescence (FIF) and tetramethyl-rhodamine-isothiocyanate (MRITC) immunofluorescence. J Neurosci Methods. 1982 Sep;6(3):281–286. doi: 10.1016/0165-0270(82)90091-7. [DOI] [PubMed] [Google Scholar]
- Siegrist G., Dolivo M., Dunant Y., Foroglou-Kerameus C., De Ribaupierre F., Rouiller C. Ultrastructure and function of the chromaffin cells in the superior cervical ganglion of the rat. J Ultrastruct Res. 1968 Dec;25(5):381–407. doi: 10.1016/s0022-5320(68)80093-0. [DOI] [PubMed] [Google Scholar]
- Smith A. D. Summing up: some implications of the neuron as a secreting cell. Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):423–437. doi: 10.1098/rstb.1971.0076. [DOI] [PubMed] [Google Scholar]
- Stilman C., Scheuermann D. W. Computer-operated microspectrofluorimetry to identify formaldehyde-induced fluorophores of biogenic monoamines and precursor substances in models and tissue sections. Histochemistry. 1987;86(3):255–267. doi: 10.1007/BF00490256. [DOI] [PubMed] [Google Scholar]
- TRAMEZZANI J. H., CHIOCCHIO S., WASSERMANN G. F. A TECHNIQUE FOR LIGHT AND ELECTRON MICROSCOPIC IDENTIFICATION OF ADRENALIN- AND NORADRENALIN-STORING CELLS. J Histochem Cytochem. 1964 Dec;12:890–899. doi: 10.1177/12.12.890. [DOI] [PubMed] [Google Scholar]
- Unsicker K. Chromaffin, small granule-containing and ganglion cells in the adrenal gland of reptiles: A comparative ultrastructural study. Cell Tissue Res. 1976 Jan 28;165(4):477–508. doi: 10.1007/BF00224477. [DOI] [PubMed] [Google Scholar]
- Unsicker K. Fine structure and innervation of the avian adrenal gland. I. Fine structure of adrenal chromaffin cells and ganglion cells. Z Zellforsch Mikrosk Anat. 1973 Dec 6;145(3):389–416. doi: 10.1007/BF00307164. [DOI] [PubMed] [Google Scholar]
- Unsicker K., Habura-Flüh O., Zwarg U. Different types of small granule-containing cells and neurons in the guinea-pig adrenal medulla. Cell Tissue Res. 1978 May 18;189(1):109–130. doi: 10.1007/BF00223124. [DOI] [PubMed] [Google Scholar]
- Verna A. Ulstrastructure of the carotid body in the mammals. Int Rev Cytol. 1979;60:271–330. doi: 10.1016/s0074-7696(08)61265-6. [DOI] [PubMed] [Google Scholar]
- WEST G. B., SHEPHERD D. M., HUNTER R. B. Adrenaline and noradrenaline concentrations in adrenal glands at different ages and in some diseases. Lancet. 1951 Nov 24;2(6691):966–969. doi: 10.1016/s0140-6736(51)91928-9. [DOI] [PubMed] [Google Scholar]
- WEST G. B. The comparative pharmacology of the suprarenal medulla. Q Rev Biol. 1955 Jun;30(2):116–137. doi: 10.1086/400758. [DOI] [PubMed] [Google Scholar]
- WOOD J. G., BARRNETT R. J. HISTOCHEMICAL DEMONSTRATION OF NOREPINEPHRINE AT A FINE STRUCTURAL LEVEL. J Histochem Cytochem. 1964 Mar;12:197–209. doi: 10.1177/12.3.197. [DOI] [PubMed] [Google Scholar]
- WRIGHT A., JONES I. C. Chromaffin tissue in the lizard adrenal gland. Nature. 1955 Jun 4;175(4466):1001–1002. doi: 10.1038/1751001b0. [DOI] [PubMed] [Google Scholar]
- Wood J. E. Letter: Positive identification of intracellular biogenic amine reaction product with electron microscopic x-ray analysis. J Histochem Cytochem. 1974 Nov;22(11):1060–1063. doi: 10.1177/22.11.1060. [DOI] [PubMed] [Google Scholar]
- Wurtman R. J., Axelrod J. Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem. 1966 May 25;241(10):2301–2305. [PubMed] [Google Scholar]
- von EULER U., FANGE R. Catecholamines in nerves and organs of Myxine glutinosa, Squalus acanthias, and Gadus callarias. Gen Comp Endocrinol. 1961 Sep;1:191–194. doi: 10.1016/0016-6480(61)90028-4. [DOI] [PubMed] [Google Scholar]