Abstract
To examine whether the hypothalamic corticotropin-releasing hormone (CRH) neuron is regulated by CRH, by products of the proopiomelanocortin (POMC) gene, and/or by glucocorticoids, we used a rat hypothalamic organ culture system in which rat CRH secretion from single explanted hypothalami was evaluated by an RIA (iCRH) specific for rat CRH. The effects of graded concentrations of ovine CRH (oCRH), adrenocorticotropin hormone (ACTH), beta-endorphin (beta-EP), alpha-melanocyte-stimulating hormone (alpha-MSH), corticotropin-like intermediate lobe peptide (CLIP), ovine beta-lipotropin (ovine beta-LPH), and dexamethasone (DEX) upon unstimulated and serotonin- (5HT), acetylcholine- (ACh), and norepinephrine-(NE) stimulated CRH secretion were determined. oCRH and DEX inhibited unstimulated iCRH secretion with ID50 at the 10(-8) M range. ACTH had no detectable suppressive effect at 10(-8) M. oCRH, ACTH, and DEX inhibited 5HT-, ACh-, and NE-stimulated iCRH secretion in a dose-dependent fashion. beta-EP, alpha-MSH, and CLIP also inhibited 5HT-induced iCRH secretion. Of the latter peptides, the strongest inhibitor was beta-EP and the weakest was CLIP. Ovine beta-LPH had only a weak inhibitory effect on 5HT-induced iCRH secretion. Generally, the concentrations required for 50% suppression of neurotransmitter-stimulated iCRH secretion were significantly lower than those required for a similar suppression of unstimulated iCRH secretion. In conclusion, these data suggest the presence of multiple negative feedback loops involved in the regulation of the hypothalamic CRH neuron: an ultrashort CRH-mediated loop, a short, hypothalamic POMC-derived peptide loop, and a long, glucocorticoid-mediated negative feedback loop. The potency of these negative feedback loops may be determined by the state of activation of the CRH neuron.
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- Allen J. P., Kendall J. W., McGilvra R., Vancura C. Immunoreactive ACTH in cerebrospinal fluid. J Clin Endocrinol Metab. 1974 Apr;38(4):586–593. doi: 10.1210/jcem-38-4-586. [DOI] [PubMed] [Google Scholar]
- BOHUS B., ENDROECZI E. EFFECT OF INTRACEREBRAL IMPLANTATION OF HYDROCORTISONE ON ADRENOCORTICAL SECRETION AND ADRENAL WEIGHT AFTER UNILATERAL ADRENALECTOMY. Acta Physiol Acad Sci Hung. 1964;25:11–19. [PubMed] [Google Scholar]
- Beckford U., Holmes M. C., Gillham B., Jones M. T. Biphasic inhibition of bioactive hypothalamic corticotrophin releasing factor secretion in vitro by corticosterone and prevention of the second phase by various steroids. J Endocrinol. 1983 Jun;97(3):339–346. doi: 10.1677/joe.0.0970339. [DOI] [PubMed] [Google Scholar]
- Bohus B., Strashimirov D. Localization and specificity of corticosteroid "feedback receptors" at the hypothalamo-hypophyseal level; comparative effects of various steroids implanted in the median eminence or the anterior pituitary of the rat. Neuroendocrinology. 1970;6(4):197–209. doi: 10.1159/000121924. [DOI] [PubMed] [Google Scholar]
- Boscaro M., Sonino N., Paoletta A., Rampazzo A., Mantero F. Evidence for ultra-short loop autoregulation of adrenocorticotropin secretion in man. J Clin Endocrinol Metab. 1988 Feb;66(2):255–257. doi: 10.1210/jcem-66-2-255. [DOI] [PubMed] [Google Scholar]
- Brandt M. R., Korshin J., Hansen A. P., Hummer L., Madsen S. N., Rygg I., Kehlet H. Influence of morphine anaesthesia on the endocrine-metabolic response to open-heart surgery. Acta Anaesthesiol Scand. 1978;22(4):400–412. doi: 10.1111/j.1399-6576.1978.tb01316.x. [DOI] [PubMed] [Google Scholar]
- Buckingham J. C. Effects of adrenocortical and gonadal steroids on the secretion in vitro of corticotrophin and its hypothalamic releasing factor. J Endocrinol. 1982 Apr;93(1):123–132. doi: 10.1677/joe.0.0930123. [DOI] [PubMed] [Google Scholar]
- Buckingham J. C., Hodges J. R. The use of corticotrophin production by adenohypophysial tissue in vitro for the detection and estimation of potential corticotrophin releasing factors. J Endocrinol. 1977 Feb;72(2):187–193. doi: 10.1677/joe.0.0720187. [DOI] [PubMed] [Google Scholar]
- Buckingham J. C. Stimulation and inhibition of corticotrophin releasing factor secretion by beta endorphin. Neuroendocrinology. 1986;42(2):148–152. doi: 10.1159/000124266. [DOI] [PubMed] [Google Scholar]
- CHOWERS I., FELDMAN S., DAVIDSON J. M. EFFECTS OF INTRAHYPOTHALAMIC CRYSTALLINE STEROIDS ON ACUTE ACTH SECRETION. Am J Physiol. 1963 Oct;205:671–673. doi: 10.1152/ajplegacy.1963.205.4.671. [DOI] [PubMed] [Google Scholar]
- CORBIN A., MANGILI G., MOTTA M., MARTINI L. EFFECT OF HYPOTHALAMIC AND MESENCEPHALIC STEROID IMPLANTATIONS ON ACTH FEEDBACK MECHANISMS. Endocrinology. 1965 May;76:811–818. doi: 10.1210/endo-76-5-811. [DOI] [PubMed] [Google Scholar]
- Calogero A. E., Gallucci W. T., Bernardini R., Saoutis C., Gold P. W., Chrousos G. P. Effect of cholinergic agonists and antagonists on rat hypothalamic corticotropin-releasing hormone secretion in vitro. Neuroendocrinology. 1988 Apr;47(4):303–308. doi: 10.1159/000124929. [DOI] [PubMed] [Google Scholar]
- Chrousos G. P., Schulte H. M., Oldfield E. H., Gold P. W., Cutler G. B., Jr, Loriaux D. L. The corticotropin-releasing factor stimulation test. An aid in the evaluation of patients with Cushing's syndrome. N Engl J Med. 1984 Mar 8;310(10):622–626. doi: 10.1056/NEJM198403083101004. [DOI] [PubMed] [Google Scholar]
- DAVIDSON J. M., FELDMAN S. Cerebral involvement in the inhibition of ACTH secretion by hydrocortisone. Endocrinology. 1963 Jun;72:936–946. doi: 10.1210/endo-72-6-936. [DOI] [PubMed] [Google Scholar]
- De Souza E. B., Perrin M. H., Insel T. R., Rivier J., Vale W. W., Kuhar M. J. Corticotropin-releasing factor receptors in rat forebrain: autoradiographic identification. Science. 1984 Jun 29;224(4656):1449–1451. doi: 10.1126/science.6328656. [DOI] [PubMed] [Google Scholar]
- DeLean A., Munson P. J., Rodbard D. Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Physiol. 1978 Aug;235(2):E97–102. doi: 10.1152/ajpendo.1978.235.2.E97. [DOI] [PubMed] [Google Scholar]
- Edwardson J. A., Bennett G. W. Modulation of corticotrophin-releasing factor release from hypothalamic synaptosomes. Nature. 1974 Oct 4;251(5474):425–427. doi: 10.1038/251425a0. [DOI] [PubMed] [Google Scholar]
- Fehm H. L., Voigt K. H., Lang R., Pfeiffer E. F. No "ultra-short feedback mechanism" for ACTH. Neuroendocrinology. 1974;16(5-6):364–368. doi: 10.1159/000122582. [DOI] [PubMed] [Google Scholar]
- Fitzgerald P. A., Aron D. C., Findling J. W., Brooks R. M., Wilson C. B., Forsham P. H., Tyrrell J. B. Cushing's disease: transient secondary adrenal insufficiency after selective removal of pituitary microadenomas; evidence for a pituitary origin. J Clin Endocrinol Metab. 1982 Feb;54(2):413–422. doi: 10.1210/jcem-54-2-413. [DOI] [PubMed] [Google Scholar]
- Fuxe K., Wikström A. C., Okret S., Agnati L. F., Härfstrand A., Yu Z. Y., Granholm L., Zoli M., Vale W., Gustafsson J. A. Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor. Endocrinology. 1985 Nov;117(5):1803–1812. doi: 10.1210/endo-117-5-1803. [DOI] [PubMed] [Google Scholar]
- GOODFRIEND T. L., LEVINE L., FASMAN G. D. ANTIBODIES TO BRADYKININ AND ANGIOTENSIN: A USE OF CARBODIIMIDES IN IMMUNOLOGY. Science. 1964 Jun 12;144(3624):1344–1346. doi: 10.1126/science.144.3624.1344. [DOI] [PubMed] [Google Scholar]
- GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gibbs D. M., Vale W. Effect of the serotonin reuptake inhibitor fluoxetine on corticotropin-releasing factor and vasopressin secretion into hypophysial portal blood. Brain Res. 1983 Nov 28;280(1):176–179. doi: 10.1016/0006-8993(83)91189-7. [DOI] [PubMed] [Google Scholar]
- Gold P. W., Loriaux D. L., Roy A., Kling M. A., Calabrese J. R., Kellner C. H., Nieman L. K., Post R. M., Pickar D., Gallucci W. Responses to corticotropin-releasing hormone in the hypercortisolism of depression and Cushing's disease. Pathophysiologic and diagnostic implications. N Engl J Med. 1986 May 22;314(21):1329–1335. doi: 10.1056/NEJM198605223142101. [DOI] [PubMed] [Google Scholar]
- Hedge G. A., Smelik P. G. The action of dexamethasone and vasopressin on hypothalamic CRF production and release. Neuroendocrinology. 1969;4(4):242–253. doi: 10.1159/000121754. [DOI] [PubMed] [Google Scholar]
- Hillhouse E. W., Jones M. T. Effect of bilateral adrenalectomy and corticosteroid therapy on the secretion of corticotrophin-releasing factor activity from the hypothalamus of the rat in vitro. J Endocrinol. 1976 Oct;71(1):21–30. doi: 10.1677/joe.0.0710021. [DOI] [PubMed] [Google Scholar]
- Holmes M. C., Beckford U., Greenstein B. D., Gillham B., Jones M. T. A correlative study of the binding of dexamethasone in hypothalamic blocks in vitro with its ability to inhibit the release of bioactive corticotrophin-releasing factor. J Steroid Biochem. 1985 Jun;22(6):759–765. doi: 10.1016/0022-4731(85)90283-3. [DOI] [PubMed] [Google Scholar]
- Jingami H., Matsukura S., Numa S., Imura H. Effects of adrenalectomy and dexamethasone administration on the level of prepro-corticotropin-releasing factor messenger ribonucleic acid (mRNA) in the hypothalamus and adrenocorticotropin/beta-lipotropin precursor mRNA in the pituitary in rats. Endocrinology. 1985 Oct;117(4):1314–1320. doi: 10.1210/endo-117-4-1314. [DOI] [PubMed] [Google Scholar]
- Kaneko M., Hiroshige T. Fast, rate-sensitive corticosteroid negative feedback during stress. Am J Physiol. 1978 Jan;234(1):R39–R45. doi: 10.1152/ajpregu.1978.234.1.R39. [DOI] [PubMed] [Google Scholar]
- Keller-Wood M. E., Dallman M. F. Corticosteroid inhibition of ACTH secretion. Endocr Rev. 1984 Winter;5(1):1–24. doi: 10.1210/edrv-5-1-1. [DOI] [PubMed] [Google Scholar]
- Kovács K., Kiss J. Z., Makara G. B. Glucocorticoid implants around the hypothalamic paraventricular nucleus prevent the increase of corticotropin-releasing factor and arginine vasopressin immunostaining induced by adrenalectomy. Neuroendocrinology. 1986;44(2):229–234. doi: 10.1159/000124650. [DOI] [PubMed] [Google Scholar]
- Krieger D. T., Liotta A., Brownstein M. J. Presence of corticotropin in brain of normal and hypophysectomized rats. Proc Natl Acad Sci U S A. 1977 Feb;74(2):648–652. doi: 10.1073/pnas.74.2.648. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LEEMAN S. E., GLENISTER D. W., YATES F. E. Characterization of a calf hypothalamic extract with adrenocorticotropin-releasing properties: evidence for a central nervous system site for corticosteroid inhibition of adrenocorticotropin release. Endocrinology. 1962 Feb;70:249–262. doi: 10.1210/endo-70-2-249. [DOI] [PubMed] [Google Scholar]
- Lumpkin M. D., Samson W. K., McCann S. M. Effects of intraventricular growth hormone-releasing factor on growth hormone release: further evidence for ultrashort loop feedback. Endocrinology. 1985 May;116(5):2070–2074. doi: 10.1210/endo-116-5-2070. [DOI] [PubMed] [Google Scholar]
- Lumpkin M. D., Samson W. K., McCann S. M. Hypothalamic and pituitary sites of action of oxytocin to alter prolactin secretion in the rat. Endocrinology. 1983 May;112(5):1711–1717. doi: 10.1210/endo-112-5-1711. [DOI] [PubMed] [Google Scholar]
- Motta M., Mangili G., Martini L. A "short" feedback loop in the control of ACTH secretion. Endocrinology. 1965 Aug;77(2):392–395. doi: 10.1210/endo-77-2-392. [DOI] [PubMed] [Google Scholar]
- Nakagami Y., Suda T., Yajima F., Ushiyama T., Tomori N., Sumitomo T., Demura H., Shizume K. Effects of serotonin, cyproheptadine and reserpine on corticotropin-releasing factor release from the rat hypothalamus in vitro. Brain Res. 1986 Oct 29;386(1-2):232–236. doi: 10.1016/0006-8993(86)90159-9. [DOI] [PubMed] [Google Scholar]
- Newman C. B., Wardlaw S. L., Van Vugt D. A., Ferin M., Frantz A. G. Adrenocorticotropin immunoactivity in monkey hypophyseal portal blood. J Clin Endocrinol Metab. 1984 Jul;59(1):108–112. doi: 10.1210/jcem-59-1-108. [DOI] [PubMed] [Google Scholar]
- Nikolarakis K. E., Almeida O. F., Herz A. Stimulation of hypothalamic beta-endorphin and dynorphin release by corticotropin-releasing factor (in vitro). Brain Res. 1986 Dec 3;399(1):152–155. doi: 10.1016/0006-8993(86)90610-4. [DOI] [PubMed] [Google Scholar]
- Ono N., Bedran de Castro J. C., McCann S. M. Ultrashort-loop positive feedback of corticotropin (ACTH)-releasing factor to enhance ACTH release in stress. Proc Natl Acad Sci U S A. 1985 May;82(10):3528–3531. doi: 10.1073/pnas.82.10.3528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page R. B. Directional pituitary blood flow: a microcinephotographic study. Endocrinology. 1983 Jan;112(1):157–165. doi: 10.1210/endo-112-1-157. [DOI] [PubMed] [Google Scholar]
- Paterson S. J., Robson L. E., Kosterlitz H. W. Classification of opioid receptors. Br Med Bull. 1983 Jan;39(1):31–36. doi: 10.1093/oxfordjournals.bmb.a071787. [DOI] [PubMed] [Google Scholar]
- Pittman Q. J., Blume H. W., Renaud L. P. Connections of the hypothalamic paraventricular nucleus with the neurohypophysis, median eminence, amygdala, lateral septum and midbrain periaqueductal gray: an electrophysiological study in the rat. Brain Res. 1981 Jun 29;215(1-2):15–28. doi: 10.1016/0006-8993(81)90488-1. [DOI] [PubMed] [Google Scholar]
- Plotsky P. M. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology. 1987 Sep;121(3):924–930. doi: 10.1210/endo-121-3-924. [DOI] [PubMed] [Google Scholar]
- Plotsky P. M., Vale W. Hemorrhage-induced secretion of corticotropin-releasing factor-like immunoreactivity into the rat hypophysial portal circulation and its inhibition by glucocorticoids. Endocrinology. 1984 Jan;114(1):164–169. doi: 10.1210/endo-114-1-164. [DOI] [PubMed] [Google Scholar]
- Richardson S. B., Twente S. Inhibition of rat hypothalamic somatostatin release by somatostatin: evidence for somatostatin ultrashort loop feedback. Endocrinology. 1986 May;118(5):2076–2082. doi: 10.1210/endo-118-5-2076. [DOI] [PubMed] [Google Scholar]
- Richardson U. I. Self-regulation of adrenocorticotropin secretion by mouse pituitary tumor cells in culture. Endocrinology. 1978 Mar;102(3):910–917. doi: 10.1210/endo-102-3-910. [DOI] [PubMed] [Google Scholar]
- Rittmaster R. S., Cutler G. B., Jr, Sobel D. O., Goldstein D. S., Koppelman M. C., Loriaux D. L., Chrousos G. P. Morphine inhibits the pituitary-adrenal response to ovine corticotropin-releasing hormone in normal subjects. J Clin Endocrinol Metab. 1985 May;60(5):891–895. doi: 10.1210/jcem-60-5-891. [DOI] [PubMed] [Google Scholar]
- SMELIK P. G., SAWYER C. H. Effects of implantation of cortisol into the brain stem or pituitary gland on the adrenal response to stress in the rabbit. Acta Endocrinol (Copenh) 1962 Dec;41:561–570. doi: 10.1530/acta.0.0410561. [DOI] [PubMed] [Google Scholar]
- Sarkar D. K. In vivo secretion of LHRH in ovariectomized rats is regulated by a possible autofeedback mechanism. Neuroendocrinology. 1987 Jun;45(6):510–513. doi: 10.1159/000124783. [DOI] [PubMed] [Google Scholar]
- Sawchenko P. E. Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus. Brain Res. 1987 Feb 17;403(2):213–223. doi: 10.1016/0006-8993(87)90058-8. [DOI] [PubMed] [Google Scholar]
- Sawchenko P. E., Swanson L. W., Joseph S. A. The distribution and cells of origin of ACTH(1-39)-stained varicosities in the paraventricular and supraoptic nuclei. Brain Res. 1982 Jan 28;232(2):365–374. doi: 10.1016/0006-8993(82)90280-3. [DOI] [PubMed] [Google Scholar]
- Smith A. I., Keith A. B., Edwardson J. A., Biggins J. A., McDermott J. R. Characterization of corticotropin-like immunoreactive peptides in rat brain using high performance liquid chromatography. Neurosci Lett. 1982 May 28;30(2):133–138. doi: 10.1016/0304-3940(82)90285-3. [DOI] [PubMed] [Google Scholar]
- Suda T., Tomori N., Tozawa F., Mouri T., Demura H., Shizume K. Effect of dexamethasone on immunoreactive corticotropin-releasing factor in the rat median eminence and intermediate-posterior pituitary. Endocrinology. 1984 Mar;114(3):851–854. doi: 10.1210/endo-114-3-851. [DOI] [PubMed] [Google Scholar]
- Suda T., Tomori N., Tozawa F., Mouri T., Demura H., Shizume K. Effects of bilateral adrenalectomy on immunoreactive corticotropin-releasing factor in the rat median eminence and intermediate-posterior pituitary. Endocrinology. 1983 Sep;113(3):1182–1184. doi: 10.1210/endo-113-3-1182. [DOI] [PubMed] [Google Scholar]
- Suda T., Tomori N., Yajima F., Ushiyama T., Sumitomo T., Nakagami Y., Demura H., Shizume K. A short negative feedback mechanism regulating corticotropin-releasing hormone release. J Clin Endocrinol Metab. 1987 May;64(5):909–913. doi: 10.1210/jcem-64-5-909. [DOI] [PubMed] [Google Scholar]
- Suda T., Yajima F., Tomori N., Demura H., Shizume K. In vitro study of immunoreactive corticotropin-releasing factor release from the rat hypothalamus. Life Sci. 1985 Oct 21;37(16):1499–1505. doi: 10.1016/0024-3205(85)90181-x. [DOI] [PubMed] [Google Scholar]
- Suda T., Yajima F., Tomori N., Sumitomo T., Nakagami Y., Ushiyama T., Demura H., Shizume K. Inhibitory effect of adrenocorticotropin on corticotropin- releasing factor release from rat hypothalamus in vitro. Endocrinology. 1986 Jan;118(1):459–461. doi: 10.1210/endo-118-1-459. [DOI] [PubMed] [Google Scholar]
- Suda T., Yajima F., Tomori N., Sumitomo T., Nakagami Y., Ushiyama T., Demura H., Shizume K. Stimulatory effect of acetylcholine on immunoreactive corticotropin-releasing factor release from the rat hypothalamus in vitro. Life Sci. 1987 Feb 16;40(7):673–677. doi: 10.1016/0024-3205(87)90269-4. [DOI] [PubMed] [Google Scholar]
- Swanson L. W., Sawchenko P. E., Rivier J., Vale W. W. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology. 1983;36(3):165–186. doi: 10.1159/000123454. [DOI] [PubMed] [Google Scholar]
- Szafarczyk A., Malaval F., Laurent A., Gibaud R., Assenmacher I. Further evidence for a central stimulatory action of catecholamines on adrenocorticotropin release in the rat. Endocrinology. 1987 Sep;121(3):883–892. doi: 10.1210/endo-121-3-883. [DOI] [PubMed] [Google Scholar]
- Takebe K., Kunita H., Sakakura M., Horiuchi Y., Mashimo K. Suppressive effect of dexamethasone on the rise of CRF activity in the median eminence induced by stress. Endocrinology. 1971 Oct;89(4):1014–1019. doi: 10.1210/endo-89-4-1014. [DOI] [PubMed] [Google Scholar]
- Taylor T., Dluhy R. G., Williams G. H. beta-endorphin suppresses adrenocorticotropin and cortisol levels in normal human subjects. J Clin Endocrinol Metab. 1983 Sep;57(3):592–596. doi: 10.1210/jcem-57-3-592. [DOI] [PubMed] [Google Scholar]
- Tomori N., Suda T., Tozawa F., Demura H., Shizume K., Mouri T. Immunoreactive corticotropin-releasing factor concentrations in cerebrospinal fluid from patients with hypothalamic-pituitary-adrenal disorders. J Clin Endocrinol Metab. 1983 Dec;57(6):1305–1307. doi: 10.1210/jcem-57-6-1305. [DOI] [PubMed] [Google Scholar]
- Vermes I., Mulder G. H., Smelik P. G. A superfusion system technique for the study of the sites of action of glucocorticoids in the rat hypothalamus-pituitary-adrenal system in vitro. II. Hypothalamus-pituitary cell-adrenal cell superfusion. Endocrinology. 1977 Apr;100(4):1153–1159. doi: 10.1210/endo-100-4-1153. [DOI] [PubMed] [Google Scholar]
- Vernikos-Danellis J., Trigg L. N. Feedback mechanisms regulating pituitary ACTH secretion in rats bearing transplantable pituitary tumors. Endocrinology. 1967 Feb;80(2):345–350. doi: 10.1210/endo-80-2-345. [DOI] [PubMed] [Google Scholar]
- Weiner R. I., Ganong W. F. Role of brain monoamines and histamine in regulation of anterior pituitary secretion. Physiol Rev. 1978 Oct;58(4):905–976. doi: 10.1152/physrev.1978.58.4.905. [DOI] [PubMed] [Google Scholar]
- Yajima F., Suda T., Tomori N., Sumitomo T., Nakagami Y., Ushiyama T., Demura H., Shizume K. Effects of opioid peptides on immunoreactive corticotropin-releasing factor release from the rat hypothalamus in vitro. Life Sci. 1986 Jul 14;39(2):181–186. doi: 10.1016/0024-3205(86)90453-4. [DOI] [PubMed] [Google Scholar]