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. 1993 Oct;183(Pt 2):277–289.

Noncholinergic control of adrenal catecholamine secretion.

B G Livett 1, P D Marley 1
PMCID: PMC1259908  PMID: 7507911

Abstract

It has been known for over 70 years that adrenal catecholamine secretion can be modulated or elicited by noncholinergic neurotransmitters and hormones. However, our understanding of the cellular mechanisms by which these agents produce their effects and the physiological conditions under which they act are not well characterised. Here we briefly review the mechanisms by which one such agent (the neuropeptide substance P) modulates the cholinergic secretory response of adrenal chromaffin cells, and another agent (angiotensin II) elicits catecholamine secretion independently of the cholinergic innervation.

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Selected References

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  1. Adams P. R. A study of desensitization using voltage clamp. Pflugers Arch. 1975 Oct 28;360(2):135–144. doi: 10.1007/BF00580536. [DOI] [PubMed] [Google Scholar]
  2. Akasu T., Kojima M., Koketsu K. Substance P modulates the sensitivity of the nicotinic receptor in amphibian cholinergic transmission. Br J Pharmacol. 1983 Sep;80(1):123–131. doi: 10.1111/j.1476-5381.1983.tb11057.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Badder E. M., Duarte B., Seaton J. F., Hamaji M., Harrison T. S. Angiotensin II restoration of reflex adrenal medullary secretion to anephric dogs is physiologically dose dependent. Endocrinology. 1985 Nov;117(5):1920–1929. doi: 10.1210/endo-117-5-1920. [DOI] [PubMed] [Google Scholar]
  4. Baker P. F., Rink T. J. Catecholamine release from bovine adrenal medulla in response to maintained depolarization. J Physiol. 1975 Dec;253(2):593–620. doi: 10.1113/jphysiol.1975.sp011209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Balla T., Baukal A. J., Eng S., Catt K. J. Angiotensin II receptor subtypes and biological responses in the adrenal cortex and medulla. Mol Pharmacol. 1991 Sep;40(3):401–406. [PubMed] [Google Scholar]
  6. Ballesta J. J., Palmero M., Hidalgo M. J., Gutierrez L. M., Reig J. A., Viniegra S., Garcia A. G. Separate binding and functional sites for omega-conotoxin and nitrendipine suggest two types of calcium channels in bovine chromaffin cells. J Neurochem. 1989 Oct;53(4):1050–1056. doi: 10.1111/j.1471-4159.1989.tb07394.x. [DOI] [PubMed] [Google Scholar]
  7. Belcher G., Ryall R. W. Substance P and Renshaw cells: a new concept of inhibitory synaptic interactions. J Physiol. 1977 Oct;272(1):105–119. doi: 10.1113/jphysiol.1977.sp012036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boarder M. R., Plevin R., Marriott D. B. Angiotensin II potentiates prostaglandin stimulation of cyclic AMP levels in intact bovine adrenal medulla cells but not adenylate cyclase in permeabilized cells. J Biol Chem. 1988 Oct 25;263(30):15319–15324. [PubMed] [Google Scholar]
  9. Boksa P. Effects of substance P on carbachol-stimulated 45Ca2+ uptake into cultured adrenal chromaffin cells. J Neurochem. 1985 Dec;45(6):1895–1902. doi: 10.1111/j.1471-4159.1985.tb10549.x. [DOI] [PubMed] [Google Scholar]
  10. Boksa P., Livett B. G. Desensitization to nicotinic cholinergic agonists and K+, agents that stimulate catecholamine secretion, in isolated adrenal chromaffin cells. J Neurochem. 1984 Mar;42(3):607–617. doi: 10.1111/j.1471-4159.1984.tb02726.x. [DOI] [PubMed] [Google Scholar]
  11. Boksa P., Livett B. G. Substance P protects against desensitization of the nicotinic response in isolated adrenal chromaffin cells. J Neurochem. 1984 Mar;42(3):618–627. doi: 10.1111/j.1471-4159.1984.tb02727.x. [DOI] [PubMed] [Google Scholar]
  12. Boksa P., Livett B. G. The substance P receptor subtype modulating catecholamine release from adrenal chromaffin cells. Brain Res. 1985 Apr 15;332(1):29–38. doi: 10.1016/0006-8993(85)90386-5. [DOI] [PubMed] [Google Scholar]
  13. Boksa P., St-Pierre S., Livett B. G. Characterization of substance P and somatostatin receptors on adrenal chromaffin cells using structural analogues. Brain Res. 1982 Aug 12;245(2):275–283. doi: 10.1016/0006-8993(82)90810-1. [DOI] [PubMed] [Google Scholar]
  14. Bommer M., Herz A. Neuropeptides and other secretagogues in bovine chromaffin cells: their effect on opioid peptide metabolism. Neuropeptides. 1989 May-Jun;13(4):243–251. doi: 10.1016/0143-4179(89)90077-2. [DOI] [PubMed] [Google Scholar]
  15. Bunn S. J., Marley P. D. Effects of angiotensin II on cultured, bovine adrenal medullary cells. Neuropeptides. 1989 Feb-Mar;13(2):121–132. doi: 10.1016/0143-4179(89)90009-7. [DOI] [PubMed] [Google Scholar]
  16. Bunn S. J., Marley P. D., Livett B. G. Receptor stimulated formation of inositol phosphates in cultures of bovine adrenal medullary cells: the effects of bradykinin, bombesin and neurotensin. Neuropeptides. 1990 Apr;15(4):187–194. doi: 10.1016/0143-4179(90)90012-n. [DOI] [PubMed] [Google Scholar]
  17. Burgoyne R. D. Control of exocytosis in adrenal chromaffin cells. Biochim Biophys Acta. 1991 Jul 22;1071(2):174–202. doi: 10.1016/0304-4157(91)90024-q. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Ceña V., Nicolas G. P., Sanchez-Garcia P., Kirpekar S. M., Garcia A. G. Pharmacological dissection of receptor-associated and voltage-sensitive ionic channels involved in catecholamine release. Neuroscience. 1983 Dec;10(4):1455–1462. doi: 10.1016/0306-4522(83)90126-4. [DOI] [PubMed] [Google Scholar]
  20. Chang R. S., Lotti V. J. Two distinct angiotensin II receptor binding sites in rat adrenal revealed by new selective nonpeptide ligands. Mol Pharmacol. 1990 Mar;37(3):347–351. [PubMed] [Google Scholar]
  21. Cheek T. R., Jackson T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Simultaneous measurements of cytosolic calcium and secretion in single bovine adrenal chromaffin cells by fluorescent imaging of fura-2 in cocultured cells. J Cell Biol. 1989 Sep;109(3):1219–1227. doi: 10.1083/jcb.109.3.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Chiu A. T., Herblin W. F., McCall D. E., Ardecky R. J., Carini D. J., Duncia J. V., Pease L. J., Wong P. C., Wexler R. R., Johnson A. L. Identification of angiotensin II receptor subtypes. Biochem Biophys Res Commun. 1989 Nov 30;165(1):196–203. doi: 10.1016/0006-291x(89)91054-1. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. DOUGLAS W. W., RUBIN R. P. The role of calcium in the secretory response of the adrenal medulla to acetylcholine. J Physiol. 1961 Nov;159:40–57. doi: 10.1113/jphysiol.1961.sp006791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Deschepper C. F., Mellon S. H., Cumin F., Baxter J. D., Ganong W. F. Analysis by immunocytochemistry and in situ hybridization of renin and its mRNA in kidney, testis, adrenal, and pituitary of the rat. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7552–7556. doi: 10.1073/pnas.83.19.7552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Douglas W. W., Kanno T., Sampson S. R. Effects of acetylcholine and other medullary secretagogues and antagonists on the membrane potential of adrenal chromaffin cells: an analysis employing techniques of tissue culture. J Physiol. 1967 Jan;188(1):107–120. doi: 10.1113/jphysiol.1967.sp008127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Dzau V. J., Ellison K. E., Brody T., Ingelfinger J., Pratt R. E. A comparative study of the distributions of renin and angiotensinogen messenger ribonucleic acids in rat and mouse tissues. Endocrinology. 1987 Jun;120(6):2334–2338. doi: 10.1210/endo-120-6-2334. [DOI] [PubMed] [Google Scholar]
  28. Elliott T. R. The control of the suprarenal glands by the splanchnic nerves. J Physiol. 1912 Jul 15;44(5-6):374–409. doi: 10.1113/jphysiol.1912.sp001521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. FELDBERG W., LEWIS G. P. FURTHER STUDIES ON THE EFFECTS OF PEPTIDES ON THE SUPRARENAL MEDULLA OF CATS. J Physiol. 1965 May;178:239–251. doi: 10.1113/jphysiol.1965.sp007625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. FELDBERG W., LEWIS G. P. THE ACTION OF PEPTIDES ON THE ADRENAL MEDULLA. RELEASE OF ADRENALINE BY BRADYKININ AND ANGIOTENSIN. J Physiol. 1964 May;171:98–108. doi: 10.1113/jphysiol.1964.sp007364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Feuerstein G., Boonyaviroj P., Gutman Y., Khosla M. C., Bumpus F. M. Adrenal catecholamine response to haemorrhage abolished by an angiotensin antagonist. Eur J Pharmacol. 1977 Jan 7;41(1):85–86. doi: 10.1016/0014-2999(77)90376-4. [DOI] [PubMed] [Google Scholar]
  33. Geraghty D. P., Livett B. G., Rogerson F. M., Burcher E. A novel substance P binding site in bovine adrenal medulla. Neurosci Lett. 1990 May 4;112(2-3):276–281. doi: 10.1016/0304-3940(90)90216-v. [DOI] [PubMed] [Google Scholar]
  34. HILLARP N. A. Isolation and some biochemical properties of the catechol amine granules in the cow adrenal medulla. Acta Physiol Scand. 1958 Jul 17;43(1):82–96. doi: 10.1111/j.1748-1716.1958.tb01579.x. [DOI] [PubMed] [Google Scholar]
  35. Hans M., Illes P., Takeda K. The blocking effects of omega-conotoxin on Ca current in bovine chromaffin cells. Neurosci Lett. 1990 Jun 22;114(1):63–68. doi: 10.1016/0304-3940(90)90429-d. [DOI] [PubMed] [Google Scholar]
  36. Healy D. P., Maciejewski A. R., Printz M. P. Autoradiographic localization of [125I]-angiotensin II binding sites in the rat adrenal gland. Endocrinology. 1985 Mar;116(3):1221–1223. doi: 10.1210/endo-116-3-1221. [DOI] [PubMed] [Google Scholar]
  37. Helle K. B. Some chemical and physical properties of the soluble protein fraction of bovine adrenal chromaffin granules. Mol Pharmacol. 1966 Jul;2(4):298–310. [PubMed] [Google Scholar]
  38. Higgins L. S., Berg D. K. A desensitized form of neuronal acetylcholine receptor detected by 3H-nicotine binding on bovine adrenal chromaffin cells. J Neurosci. 1988 Apr;8(4):1436–1446. doi: 10.1523/JNEUROSCI.08-04-01436.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Hwang B. H., Wu J. Y., Severs W. B. Effects of chronic dehydration on angiotensin II receptor binding in the subfornical organ, paraventricular hypothalamic nucleus and adrenal medulla of Long-Evans rats. Neurosci Lett. 1986 Mar 28;65(1):35–40. doi: 10.1016/0304-3940(86)90116-3. [DOI] [PubMed] [Google Scholar]
  40. Hökfelt T., Elde R., Johansson O., Luft R., Nilsson G., Arimura A. Immunohistochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in the rat. Neuroscience. 1976;1(2):131–136. doi: 10.1016/0306-4522(76)90008-7. [DOI] [PubMed] [Google Scholar]
  41. Hökfelt T., Kellerth J. O., Nilsson G., Pernow B. Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons. Brain Res. 1975 Dec 19;100(2):235–252. doi: 10.1016/0006-8993(75)90481-3. [DOI] [PubMed] [Google Scholar]
  42. Israel A., Barbella Y., Saavedra J. M. Compensatory increase in adrenomedullary angiotensin-converting enzyme activity (kininase II) after unilateral adrenalectomy. Regul Pept. 1986 Dec 22;16(2):97–105. doi: 10.1016/0167-0115(86)90053-4. [DOI] [PubMed] [Google Scholar]
  43. Jiang Z. G., Dun N. J. Facilitation of nicotinic response in the guinea pig prevertebral neurons by substance P. Brain Res. 1986 Jan 15;363(1):196–198. doi: 10.1016/0006-8993(86)90679-7. [DOI] [PubMed] [Google Scholar]
  44. Kellaway C. H., Cowell S. J. On the concentration of the blood and the effects of histamine in adrenal insufficiency. J Physiol. 1922 Dec 22;57(1-2):82–99. doi: 10.1113/jphysiol.1922.sp002045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kent-Braun J. A., Lyford L. K., Gross D. J., Westhead E. W. Effects of substance P on secretion of catecholamines from populations of bovine chromaffin cells and on calcium transients in individual cells. Ann N Y Acad Sci. 1991;632:241–248. doi: 10.1111/j.1749-6632.1991.tb33112.x. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Khalil Z., Marley P. D., Livett B. G. Mammalian tachykinins modulate the nicotinic secretory response of cultured bovine adrenal chromaffin cells. Brain Res. 1988 Sep 6;459(2):289–297. doi: 10.1016/0006-8993(88)90645-2. [DOI] [PubMed] [Google Scholar]
  48. Kilpatrick D. L., Slepetis R., Kirshner N. Inhibition of catecholamine secretion from adrenal medulla cells by neurotoxins and cholinergic antagonists. J Neurochem. 1981 Jul;37(1):125–131. doi: 10.1111/j.1471-4159.1981.tb05299.x. [DOI] [PubMed] [Google Scholar]
  49. Kim K. T., Westhead E. W. Cellular responses to Ca2+ from extracellular and intracellular sources are different as shown by simultaneous measurements of cytosolic Ca2+ and secretion from bovine chromaffin cells. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9881–9885. doi: 10.1073/pnas.86.24.9881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Knight D. E. Temperature sensitivity of catecholamine release in response to different secretagogues [proceedings]. J Physiol. 1980 Jan;298:41P–42P. [PubMed] [Google Scholar]
  51. Krnjević K., Lekić D. Substance P selectively blocks excitation of Renshaw cell by acetylcholine. Can J Physiol Pharmacol. 1977 Aug;55(4):958–961. doi: 10.1139/y77-129. [DOI] [PubMed] [Google Scholar]
  52. Kuramoto H., Kondo H., Fujita T. Calcitonin gene-related peptide (CGRP)-like immunoreactivity in scattered chromaffin cells and nerve fibers in the adrenal gland of rats. Cell Tissue Res. 1987 Feb;247(2):309–315. doi: 10.1007/BF00218312. [DOI] [PubMed] [Google Scholar]
  53. Kuramoto H., Kondo H., Fujita T. Neuropeptide tyrosine (NPY)-like immunoreactivity in adrenal chromaffin cells and intraadrenal nerve fibers of rats. Anat Rec. 1986 Mar;214(3):321–328. doi: 10.1002/ar.1092140312. [DOI] [PubMed] [Google Scholar]
  54. Laliberte F., Laliberte M. F., Alhenc-Gelas F., Chevillard C. Cellular and subcellular immunohistochemical localization of angiotensin-converting enzyme in the rat adrenal gland. Lab Invest. 1987 Apr;56(4):364–371. [PubMed] [Google Scholar]
  55. Lewis G. P., Reit E. Further studies on the actions of peptides on the superior cervical ganglion and suprarenal medulla. Br J Pharmacol Chemother. 1966 Feb;26(2):444–460. doi: 10.1111/j.1476-5381.1966.tb01925.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Linnoila R. I., Diaugustine R. P., Hervonen A., Miller R. J. Distribution of [Met5]- and [Leu5]-enkephalin-, vasoactive intestinal polypeptide- and substance P-like immunoreactivities in human adrenal glands. Neuroscience. 1980;5(12):2247–2259. doi: 10.1016/0306-4522(80)90141-4. [DOI] [PubMed] [Google Scholar]
  57. Livett B. G. Adrenal medullary chromaffin cells in vitro. Physiol Rev. 1984 Oct;64(4):1103–1161. doi: 10.1152/physrev.1984.64.4.1103. [DOI] [PubMed] [Google Scholar]
  58. Livett B. G., Boksa P., Dean D. M., Mizobe F., Lindenbaum M. H. Use of isolated chromaffin cells to study basic release mechanisms. J Auton Nerv Syst. 1983 Jan;7(1):59–86. doi: 10.1016/0165-1838(83)90069-3. [DOI] [PubMed] [Google Scholar]
  59. Livett B. G., Boksa P. Receptors and receptor modulation in cultured chromaffin cells. Can J Physiol Pharmacol. 1984 Apr;62(4):467–476. doi: 10.1139/y84-076. [DOI] [PubMed] [Google Scholar]
  60. Livett B. G., Day R., Elde R. P., Howe P. R. Co-storage of enkephalins and adrenaline in the bovine adrenal medulla. Neuroscience. 1982 May;7(5):1323–1332. doi: 10.1016/0306-4522(82)91138-1. [DOI] [PubMed] [Google Scholar]
  61. Livett B. G., Geffen L. B., Rush R. A. Immunohistochemical evidence for the transport of dopamine-B-hydroxylase and a catecholamine binding protein in sympathetic nerves. Biochem Pharmacol. 1969 Apr;18(4):923–924. doi: 10.1016/0006-2952(69)90063-x. [DOI] [PubMed] [Google Scholar]
  62. Livett B. G., Kozousek V., Mizobe F., Dean D. M. Substance P inhibits nicotinic activation of chromaffin cells. Nature. 1979 Mar 15;278(5701):256–257. doi: 10.1038/278256a0. [DOI] [PubMed] [Google Scholar]
  63. Livett B. G., Zhou X. F. Substance P interactions with the nicotinic response. Ann N Y Acad Sci. 1991;632:249–262. doi: 10.1111/j.1749-6632.1991.tb33113.x. [DOI] [PubMed] [Google Scholar]
  64. Lukas R. J., Audhya T., Goldstein G., Lucero L. Interactions of the thymic polypeptide hormone thymopoietin with neuronal nicotinic alpha-bungarotoxin binding sites and with muscle-type, but not ganglia-type, nicotinic acetylcholine receptor ligand-gated ion channels. Mol Pharmacol. 1990 Dec;38(6):887–894. [PubMed] [Google Scholar]
  65. Lundberg J. M., Hamberger B., Schultzberg M., Hökfelt T., Granberg P. O., Efendić S., Terenius L., Goldstein M., Luft R. Enkephalin- and somatostatin-like immunoreactivities in human adrenal medulla and pheochromocytoma. Proc Natl Acad Sci U S A. 1979 Aug;76(8):4079–4083. doi: 10.1073/pnas.76.8.4079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Lundberg J. M., Rökaeus A., Hökfelt T., Rosell S., Brown M., Goldstein M. Neurotensin-like immunoreactivity in the preganglionic sympathetic nerves and in the adrenal medulla of the cat. Acta Physiol Scand. 1982 Jan;114(1):153–155. doi: 10.1111/j.1748-1716.1982.tb06965.x. [DOI] [PubMed] [Google Scholar]
  67. Lyford L. K., Kent-Braun J. A., Westhead E. W. Substance P enhances desensitization of the nicotinic response in bovine chromaffin cells but enhances secretion upon removal. J Neurochem. 1990 Dec;55(6):1960–1965. doi: 10.1111/j.1471-4159.1990.tb05782.x. [DOI] [PubMed] [Google Scholar]
  68. MacLean M. R., Ungar A. Effects of the renin-angiotensin system on the reflex response of the adrenal medulla to hypotension in the dog. J Physiol. 1986 Apr;373:343–352. doi: 10.1113/jphysiol.1986.sp016051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Magazanik L. G., Vyskocit F. The effect of temperature on desensitization kinetics at the post-synaptic membrane of the frog muscle fibre. J Physiol. 1975 Jul;249(2):285–300. doi: 10.1113/jphysiol.1975.sp011016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Mantyh P. W., Pinnock R. D., Downes C. P., Goedert M., Hunt S. P. Correlation between inositol phospholipid hydrolysis and substance P receptors in rat CNS. 1984 Jun 28-Jul 4Nature. 309(5971):795–797. doi: 10.1038/309795a0. [DOI] [PubMed] [Google Scholar]
  71. Marley P. D., Bunn S. J., Wan D. C., Allen A. M., Mendelsohn F. A. Localization of angiotensin II binding sites in the bovine adrenal medulla using a labelled specific antagonist. Neuroscience. 1989;28(3):777–787. doi: 10.1016/0306-4522(89)90022-5. [DOI] [PubMed] [Google Scholar]
  72. Marley P. D., Livett B. G. Differences between the mechanisms of adrenaline and noradrenaline secretion from isolated, bovine, adrenal chromaffin cells. Neurosci Lett. 1987 Jun 1;77(1):81–86. doi: 10.1016/0304-3940(87)90611-2. [DOI] [PubMed] [Google Scholar]
  73. Maurer R., Reubi J. C. Distribution and coregulation of three peptide receptors in adrenals. Eur J Pharmacol. 1986 Jun 17;125(2):241–247. doi: 10.1016/0014-2999(86)90033-6. [DOI] [PubMed] [Google Scholar]
  74. McMillian M. K., Tuominen R. K., Hudson P. M., Suh H. H., Hong J. S. Angiotensin II receptors are coupled to omega-conotoxin-sensitive calcium influx in bovine adrenal medullary chromaffin cells. J Neurochem. 1992 Apr;58(4):1285–1291. doi: 10.1111/j.1471-4159.1992.tb11340.x. [DOI] [PubMed] [Google Scholar]
  75. Min C. K., Weiland G. A. Substance P inhibits carbamylcholine-stimulated 22Na+ efflux from acetylcholine receptor-enriched Torpedo electroplaque membrane vesicles. Brain Res. 1992 Jul 24;586(2):348–351. doi: 10.1016/0006-8993(92)91647-w. [DOI] [PubMed] [Google Scholar]
  76. Mizobe F., Kozousek V., Dean D. M., Livett B. G. Pharmacological characterization of adrenal paraneurons: substance P and somatostatin as inhibitory modulators of the nicotinic response. Brain Res. 1979 Dec 14;178(2-3):555–566. doi: 10.1016/0006-8993(79)90714-5. [DOI] [PubMed] [Google Scholar]
  77. Mohamed A. A., Parker T. L., Coupland R. E. The innervation of the adrenal gland. II. The source of spinal afferent nerve fibres to the guinea-pig adrenal gland. J Anat. 1988 Oct;160:51–58. [PMC free article] [PubMed] [Google Scholar]
  78. Mussap C. J., Geraghty D. P., Burcher E. Tachykinin receptors: a radioligand binding perspective. J Neurochem. 1993 Jun;60(6):1987–2009. doi: 10.1111/j.1471-4159.1993.tb03484.x. [DOI] [PubMed] [Google Scholar]
  79. Naruse M., Sussman C. R., Naruse K., Jackson R. V., Inagami T. Renin exists in human adrenal tissue. J Clin Endocrinol Metab. 1983 Sep;57(3):482–487. doi: 10.1210/jcem-57-3-482. [DOI] [PubMed] [Google Scholar]
  80. Nieber K., Oehme P., Arefolov V. A., Valdman A. V. Effect of the N-terminal tetrapeptide of substance P SP (1-4) and tuftsin on the pre- and postsynaptic transmitter outflow in rat adrenal gland slices. Biomed Biochim Acta. 1988;47(7):663–666. [PubMed] [Google Scholar]
  81. Nieber K., Oehme P. Effect of substance P (SP) and the N-terminal SP-analogue SP (1-4) on the pre- and postsynaptic transmitter release in rat adrenal gland slices. Biomed Biochim Acta. 1987;46(1):103–109. [PubMed] [Google Scholar]
  82. O'Sullivan A. J., Burgoyne R. D. A comparison of bradykinin, angiotensin II and muscarinic stimulation of cultured bovine adrenal chromaffin cells. Biosci Rep. 1989 Apr;9(2):243–252. doi: 10.1007/BF01116001. [DOI] [PubMed] [Google Scholar]
  83. O'Sullivan A. J., Cheek T. R., Moreton R. B., Berridge M. J., Burgoyne R. D. Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2. EMBO J. 1989 Feb;8(2):401–411. doi: 10.1002/j.1460-2075.1989.tb03391.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Owen P. J., Marriott D. B., Boarder M. R. Evidence for a dihydropyridine-sensitive and conotoxin-insensitive release of noradrenaline and uptake of calcium in adrenal chromaffin cells. Br J Pharmacol. 1989 May;97(1):133–138. doi: 10.1111/j.1476-5381.1989.tb11933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Pelto-Huikko M., Salminen T., Hervonen A. Localization of enkephalins in adrenaline cells and the nerves innervating adrenaline cells in rat adrenal medulla. Histochemistry. 1985;82(4):377–383. doi: 10.1007/BF00494067. [DOI] [PubMed] [Google Scholar]
  86. Plevin R., Boarder M. R. Stimulation of formation of inositol phosphates in primary cultures of bovine adrenal chromaffin cells by angiotensin II, histamine, bradykinin, and carbachol. J Neurochem. 1988 Aug;51(2):634–641. doi: 10.1111/j.1471-4159.1988.tb01085.x. [DOI] [PubMed] [Google Scholar]
  87. Powis D. A., O'Brien K. J. Angiotensin II increases catecholamine release from bovine adrenal medulla but does not enhance that evoked by K+ depolarization or by carbachol. J Neurochem. 1991 Nov;57(5):1461–1469. doi: 10.1111/j.1471-4159.1991.tb06339.x. [DOI] [PubMed] [Google Scholar]
  88. Quirion R., Finkel M. S., Mendelsohn F. A., Zamir N. Localization of opiate binding sites in kidney and adrenal gland of the rat. Life Sci. 1983;33 (Suppl 1):299–302. doi: 10.1016/0024-3205(83)90502-7. [DOI] [PubMed] [Google Scholar]
  89. Rang H. P., Ritter J. M. On the mechanism of desensitization at cholinergic receptors. Mol Pharmacol. 1970 Jul;6(4):357–382. [PubMed] [Google Scholar]
  90. Role L. W., Leeman S. E., Perlman R. L. Somatostatin and substance P inhibit catecholamine secretion from isolated cells of guinea-pig adrenal medulla. Neuroscience. 1981;6(9):1813–1821. doi: 10.1016/0306-4522(81)90215-3. [DOI] [PubMed] [Google Scholar]
  91. Role L. W. Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons. Proc Natl Acad Sci U S A. 1984 May;81(9):2924–2928. doi: 10.1073/pnas.81.9.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Rosario L. M., Soria B., Feuerstein G., Pollard H. B. Voltage-sensitive calcium flux into bovine chromaffin cells occurs through dihydropyridine-sensitive and dihydropyridine- and omega-conotoxin-insensitive pathways. Neuroscience. 1989;29(3):735–747. doi: 10.1016/0306-4522(89)90145-0. [DOI] [PubMed] [Google Scholar]
  93. Saavedra J. M., Alexander N. Angiotensin II receptors in adrenal gland, pituitary gland and brain of sino-aortic denervated rats. J Hypertens Suppl. 1986 Dec;4(5):S154–S157. [PubMed] [Google Scholar]
  94. Sasakawa N., Nakaki T., Yamamoto S., Kato R. Calcium uptake-dependent and -independent mechanisms of inositol trisphosphate formation in adrenal chromaffin cells: comparative studies with high K+, carbamylcholine and angiotensin II. Cell Signal. 1989;1(1):75–84. doi: 10.1016/0898-6568(89)90022-3. [DOI] [PubMed] [Google Scholar]
  95. Schultzberg M., Lundberg J. M., Hökfelt T., Terenius L., Brandt J., Elde R. P., Goldstein M. Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neuroscience. 1978;3(12):1169–1186. doi: 10.1016/0306-4522(78)90137-9. [DOI] [PubMed] [Google Scholar]
  96. Scubon-Mulieri B., Parsons R. L. Desensitization and recovery at the frog neuromuscular junction. J Gen Physiol. 1977 Apr;69(4):431–447. doi: 10.1085/jgp.69.4.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Shearman M. S., Sekiguchi K., Nishizuka Y. Modulation of ion channel activity: a key function of the protein kinase C enzyme family. Pharmacol Rev. 1989 Jun;41(2):211–237. [PubMed] [Google Scholar]
  98. Simasko S. M., Durkin J. A., Weiland G. A. Effects of substance P on nicotinic acetylcholine receptor function in PC12 cells. J Neurochem. 1987 Jul;49(1):253–260. doi: 10.1111/j.1471-4159.1987.tb03423.x. [DOI] [PubMed] [Google Scholar]
  99. Simasko S. M., Soares J. R., Weiland G. A. Structure-activity relationship for substance P inhibition of carbamylcholine-stimulated 22Na+ flux in neuronal (PC12) and non-neuronal (BC3H1) cell lines. J Pharmacol Exp Ther. 1985 Dec;235(3):601–605. [PubMed] [Google Scholar]
  100. Stachowiak M. K., Jiang H. K., Poisner A. M., Tuominen R. K., Hong J. S. Short and long term regulation of catecholamine biosynthetic enzymes by angiotensin in cultured adrenal medullary cells. Molecular mechanisms and nature of second messenger systems. J Biol Chem. 1990 Mar 15;265(8):4694–4702. [PubMed] [Google Scholar]
  101. Stallcup W. B., Patrick J. Substance P enhances cholinergic receptor desensitization in a clonal nerve cell line. Proc Natl Acad Sci U S A. 1980 Jan;77(1):634–638. doi: 10.1073/pnas.77.1.634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Staszewska-Barczak J., Vane J. R. The release of catecholamines from the adrenal medulla by peptides. Br J Pharmacol Chemother. 1967 Aug;30(3):655–667. doi: 10.1111/j.1476-5381.1967.tb02172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Stauderman K. A., Pruss R. M. Different patterns of agonist-stimulated increases of 3H-inositol phosphate isomers and cytosolic Ca2+ in bovine adrenal chromaffin cells: comparison of the effects of histamine and angiotensin II. J Neurochem. 1990 Mar;54(3):946–953. doi: 10.1111/j.1471-4159.1990.tb02342.x. [DOI] [PubMed] [Google Scholar]
  104. Stauderman K. A., Pruss R. M. Dissociation of Ca2+ entry and Ca2+ mobilization responses to angiotensin II in bovine adrenal chromaffin cells. J Biol Chem. 1989 Nov 5;264(31):18349–18355. [PubMed] [Google Scholar]
  105. Steinacker A. Calcium-dependent presynaptic action of substance P at the frog neuromuscular junction. Nature. 1977 May 19;267(5608):268–270. doi: 10.1038/267268a0. [DOI] [PubMed] [Google Scholar]
  106. Steinacker A., Highstein S. M. Pre- and postsynaptic action of substance P at the Mauther fiber-giant fiber synapse in the hatchetfish. Brain Res. 1976 Sep 10;114(1):128–133. doi: 10.1016/0006-8993(76)91013-1. [DOI] [PubMed] [Google Scholar]
  107. Strack A. M., Sawyer W. B., Hughes J. H., Platt K. B., Loewy A. D. A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res. 1989 Jul 3;491(1):156–162. doi: 10.1016/0006-8993(89)90098-x. [DOI] [PubMed] [Google Scholar]
  108. Strack A. M., Sawyer W. B., Marubio L. M., Loewy A. D. Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res. 1988 Jul 5;455(1):187–191. doi: 10.1016/0006-8993(88)90132-1. [DOI] [PubMed] [Google Scholar]
  109. Strack A. M., Sawyer W. B., Platt K. B., Loewy A. D. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res. 1989 Jul 10;491(2):274–296. doi: 10.1016/0006-8993(89)90063-2. [DOI] [PubMed] [Google Scholar]
  110. Strittmatter S. M., De Souza E. B., Lynch D. R., Snyder S. H. Angiotensin-converting enzyme localized in the rat pituitary and adrenal glands by [3H]captopril autoradiography. Endocrinology. 1986 Apr;118(4):1690–1699. doi: 10.1210/endo-118-4-1690. [DOI] [PubMed] [Google Scholar]
  111. TerBush D. R., Bittner M. A., Holz R. W. Ca2+ influx causes rapid translocation of protein kinase C to membranes. Studies of the effects of secretagogues in adrenal chromaffin cells. J Biol Chem. 1988 Dec 15;263(35):18873–18879. [PubMed] [Google Scholar]
  112. Terbush D. R., Holz R. W. Activation of protein kinase C is not required for exocytosis from bovine adrenal chromaffin cells. The effects of protein kinase C(19-31), Ca/CaM kinase II(291-317), and staurosporine. J Biol Chem. 1990 Dec 5;265(34):21179–21184. [PubMed] [Google Scholar]
  113. Tuominen R. K., Hudson P. M., McMillian M. K., Ye H., Stachowiak M. K., Hong J. S. Long-term activation of protein kinase C by angiotensin II in cultured bovine adrenal medullary cells. J Neurochem. 1991 Apr;56(4):1292–1298. doi: 10.1111/j.1471-4159.1991.tb11424.x. [DOI] [PubMed] [Google Scholar]
  114. Tuominen R. K., McMillian M. K., Ye H., Stachowiak M. K., Hudson P. M., Hong J. S. Long-term activation of protein kinase C by nicotine in bovine adrenal chromaffin cells. J Neurochem. 1992 May;58(5):1652–1658. doi: 10.1111/j.1471-4159.1992.tb10037.x. [DOI] [PubMed] [Google Scholar]
  115. Wan D. C., Livett B. G. Induction of phenylethanolamine N-methyltransferase mRNA expression by glucocorticoids in cultured bovine adrenal chromaffin cells. Eur J Pharmacol. 1989 May 11;172(2):107–115. doi: 10.1016/0922-4106(89)90002-3. [DOI] [PubMed] [Google Scholar]
  116. Wan D. C., Marley P. D., Livett B. G. Angiotensin II stimulates the expression of proenkephalin A mRNA in cultured bovine adrenal chromaffin cells. Neuropeptides. 1990 Jul;16(3):141–147. doi: 10.1016/0143-4179(90)90126-j. [DOI] [PubMed] [Google Scholar]
  117. Wan D. C., Marley P. D., Livett B. G. Coordinate and differential regulation of proenkephalin A and PNMT mRNA expression in cultured bovine adrenal chromaffin cells: responses to cAMP elevation and phorbol esters. Brain Res Mol Brain Res. 1991 Jan;9(1-2):135–142. doi: 10.1016/0169-328x(91)90138-n. [DOI] [PubMed] [Google Scholar]
  118. Wan D. C., Marley P. D., Livett B. G. Coordinate and differential regulation of proenkephalin A and PNMT mRNA expression in cultured bovine adrenal chromaffin cells: responses to secretory stimuli. Brain Res Mol Brain Res. 1991 Jan;9(1-2):103–111. doi: 10.1016/0169-328x(91)90135-k. [DOI] [PubMed] [Google Scholar]
  119. Weiland G. A., Durkin J. A., Henley J. M., Simasko S. M. Effects of substance P on the binding of ligands to nicotinic acetylcholine receptors. Mol Pharmacol. 1987 Nov;32(5):625–632. [PubMed] [Google Scholar]
  120. White T. D., Bourke J. E., Livett B. G. Direct and continuous detection of ATP secretion from primary monolayer cultures of bovine adrenal chromaffin cells. J Neurochem. 1987 Oct;49(4):1266–1273. doi: 10.1111/j.1471-4159.1987.tb10019.x. [DOI] [PubMed] [Google Scholar]
  121. Wong P. C., Hart S. D., Zaspel A. M., Chiu A. T., Ardecky R. J., Smith R. D., Timmermans P. B. Functional studies of nonpeptide angiotensin II receptor subtype-specific ligands: DuP 753 (AII-1) and PD123177 (AII-2). J Pharmacol Exp Ther. 1990 Nov;255(2):584–592. [PubMed] [Google Scholar]
  122. 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]
  123. Wurtman R. J., Axelrod J., Tramezzani J. Distribution of the adrenaline-forming enzyme in the adrenal gland of a snake, Xenodon merremii. Nature. 1967 Aug 19;215(5103):879–880. doi: 10.1038/215879b0. [DOI] [PubMed] [Google Scholar]
  124. Wurtman R. J. Control of epinephrine synthesis in the adrenal medulla by the adrenal cortex: hormonal specificity and dose-response characteristics. Endocrinology. 1966 Sep;79(3):608–614. doi: 10.1210/endo-79-3-608. [DOI] [PubMed] [Google Scholar]
  125. Zhou X. F., Livett B. G. Substance P has biphasic effects on catecholamine secretion evoked by electrical stimulation of perfused rat adrenal glands in vitro. J Auton Nerv Syst. 1990 Sep;31(1):31–39. doi: 10.1016/0165-1838(90)90169-j. [DOI] [PubMed] [Google Scholar]
  126. Zhou X. F., Livett B. G. Substance P increases catecholamine secretion from perfused rat adrenal glands evoked by prolonged field stimulation. J Physiol. 1990 Jun;425:321–334. doi: 10.1113/jphysiol.1990.sp018105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Zhou X. F., Marley P. D., Livett B. G. Role of capsaicin-sensitive neurons in catecholamine secretion from rat adrenal glands. Eur J Pharmacol. 1990 Sep 21;186(2-3):247–255. doi: 10.1016/0014-2999(90)90440-h. [DOI] [PubMed] [Google Scholar]
  128. Zhou X. F., Marley P. D., Livett B. G. Substance P modulates the time course of nicotinic but not muscarinic catecholamine secretion from perfused adrenal glands of rat. Br J Pharmacol. 1991 Sep;104(1):159–165. doi: 10.1111/j.1476-5381.1991.tb12401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Zhou X. F., Oldfield B. J., Livett B. G. Substance P-containing sensory neurons in the rat dorsal root ganglia innervate the adrenal medulla. J Auton Nerv Syst. 1991 May;33(3):247–254. doi: 10.1016/0165-1838(91)90025-x. [DOI] [PubMed] [Google Scholar]
  130. Zimlichman R., Goldstein D. S., Zimlichman S., Stull R., Keiser H. R. Angiotensin II increases cytosolic calcium and stimulates catecholamine release in cultured bovine adrenomedullary cells. Cell Calcium. 1987 Aug;8(4):315–325. doi: 10.1016/0143-4160(87)90006-6. [DOI] [PubMed] [Google Scholar]

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