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Physiol. Rev. 79: 1-71, 1999;
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PHYSIOLOGICAL REVIEWS   Vol. 79 No. 1 January 1999, pp. 1-71
Copyright ©1999 The American Physiological Society

Regulation of the Hypothalamic-Pituitary-Adrenal Axis by Cytokines: Actions and Mechanisms of Action

ANDREW V. TURNBULL AND CATHERINE L. RIVIER

The Clayton Foundation Laboratories for Peptide Biology, The Salk Institute, La Jolla, California; and North Western Injury Research Centre, University of Manchester, Manchester, United Kingdom

Turnbull, Andrew V., and Catherine L. Rivier. Regulation of the Hypothalamic-Pituitary-Adrenal Axis by Cytokines: Actions and Mechanisms of Action. Physiol. Rev. 79: 1-71, 1999. --- Glucocorticoids are hormone products of the adrenal gland, which have long been recognized to have a profound impact on immunologic processes. The communication between immune and neuroendocrine systems is, however, bidirectional. The endocrine and immune systems share a common "chemical language," with both systems possessing ligands and receptors of "classical" hormones and immunoregulatory mediators. Studies in the early to mid 1980s demonstrated that monocyte-derived or recombinant interleukin-1 (IL-1) causes secretion of hormones of the hypothalamic-pituitary-adrenal (HPA) axis, establishing that immunoregulators, known as cytokines, play a pivotal role in this bidirectional communication between the immune and neuroendocrine systems. The subsequent 10-15 years have witnessed demonstrations that numerous members of several cytokine families increase the secretory activity of the HPA axis. Because this neuroendocrine action of cytokines is mediated primarily at the level of the central nervous system, studies investigating the mechanisms of HPA activation produced by cytokines take on a more broad significance, with findings relevant to the more fundamental question of how cytokines signal the brain. This article reviews published findings that have documented which cytokines have been shown to influence hormone secretion from the HPA axis, determined under what physiological/pathophysiological circumstances endogenous cytokines regulate HPA axis activity, established the possible sites of cytokine action on HPA axis hormone secretion, and identified the potential neuroanatomic and pharmacological mechanisms by which cytokines signal the neuroendocrine hypothalamus.




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 JEMHome page
T. Matsuki, R. Horai, K. Sudo, and Y. Iwakura
IL-1 Plays an Important Role in Lipid Metabolism by Regulating Insulin Levels under Physiological Conditions
J. Exp. Med., September 15, 2003; 198(6): 877 - 888.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. Kageyama and T. Suda
Urocortin-Related Peptides Increase Interleukin-6 Output via Cyclic Adenosine 5'-Monophosphate-Dependent Pathways in A7r5 Aortic Smooth Muscle Cells
Endocrinology, June 1, 2003; 144(6): 2234 - 2241.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
C. L. Rivier, D. E. Grigoriadis, and J. E. Rivier
Role of Corticotropin-Releasing Factor Receptors Type 1 and 2 in Modulating the Rat Adrenocorticotropin Response to Stressors
Endocrinology, June 1, 2003; 144(6): 2396 - 2403.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. V. Turnbull, S. Prehar, A. R. Kennedy, R. A. Little, and S. J. Hopkins
Interleukin-6 Is an Afferent Signal to the Hypothalamo-Pituitary-Adrenal Axis during Local Inflammation in Mice
Endocrinology, May 1, 2003; 144(5): 1894 - 1906.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
R. Silverstein and D. C. Johnson
Endogenous versus exogenous glucocorticoid responses to experimental bacterial sepsis
J. Leukoc. Biol., April 1, 2003; 73(4): 417 - 427.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. Kageyama, C. Li, and W. W. Vale
Corticotropin-Releasing Factor Receptor Type 2 Messenger Ribonucleic Acid in Rat Pituitary: Localization and Regulation by Immune Challenge, Restraint Stress, and Glucocorticoids
Endocrinology, April 1, 2003; 144(4): 1524 - 1532.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Y. Matsuoka, T. Furuyashiki, H. Bito, F. Ushikubi, Y. Tanaka, T. Kobayashi, S. Muro, N. Satoh, T. Kayahara, M. Higashi, et al.
Impaired adrenocorticotropic hormone response to bacterial endotoxin in mice deficient in prostaglandin E receptor EP1 and EP3 subtypes
PNAS, April 1, 2003; 100(7): 4132 - 4137.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
H. Watanobe and M. Yoneda
A mechanism underlying the sexually dimorphic ACTH response to lipopolysaccharide in rats: sex steroid modulation of cytokine binding sites in the hypothalamus
J. Physiol., February 15, 2003; 547(1): 221 - 232.
[Abstract] [Full Text] [PDF]

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 Innate ImmunityHome page
A. Beishuizen and L. G. Thijs
Review: Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis
Innate Immunity, February 1, 2003; 9(1): 3 - 24.
[Abstract] [PDF]

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 ChestHome page
P. E. Marik and G. P. Zaloga
Adrenal Insufficiency in the Critically Ill: A New Look at an Old Problem
Chest, November 1, 2002; 122(5): 1784 - 1796.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. Candolfi, V. Zaldivar, A. De Laurentiis, G. Jaita, D. Pisera, and A. Seilicovich
TNF-{alpha} Induces Apoptosis of Lactotropes from Female Rats
Endocrinology, September 1, 2002; 143(9): 3611 - 3617.
[Abstract] [Full Text] [PDF]

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 Biol Res NursHome page
S. A. Motzer, M. Jarrett, M. M. Heitkemper, and J. Tsuji
Natural Killer Cell Function and Psychological Distress in Women with and without Irritable Bowel Syndrome
Biol Res Nurs, July 1, 2002; 4(1): 31 - 42.
[Abstract] [PDF]

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 EndocrinologyHome page
S. D. Bilbo and R. J. Nelson
Melatonin Regulates Energy Balance and Attenuates Fever in Siberian Hamsters
Endocrinology, July 1, 2002; 143(7): 2527 - 2533.
[Abstract] [Full Text] [PDF]

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 Mult SclerHome page
Z A Erkut, E Endert, I Huitinga, and D F Swaab
Cortisol is increased in postmortem cerebrospinal fluid of multiple sclerosis patients: relationship with cytokines and sepsis
Multiple Sclerosis, June 1, 2002; 8(3): 229 - 236.
[Abstract] [PDF]

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 J. Appl. Physiol.Home page
E.-M. Harre, J. Roth, U. Pehl, M. Kueth, R. Gerstberger, and T. Hubschle
Molecular Biology of Thermoregulation: Selected Contribution: Role of IL-6 in LPS-induced nuclear STAT3 translocation in sensory circumventricular organs during fever in rats
J Appl Physiol, June 1, 2002; 92(6): 2657 - 2666.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
Y. Kiriyama, Y. Nomura, and Y. Tokumitsu
Calcitonin gene expression induced by lipopolysaccharide in the rat pituitary
Am J Physiol Endocrinol Metab, June 1, 2002; 282(6): E1380 - E1384.
[Abstract] [Full Text] [PDF]

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 J PsychopharmacolHome page
E. M. Cassidy, D. Manning, S. Byrne, E. Bolger, F. Murray, N. Sharifi, E. Wallace, M. Keogan, and V. O'Keane
Acute effects of low-dose interferon-{alpha} on serum cortisol and plasma interleukin-6
J Psychopharmacol, May 1, 2002; 16(3): 230 - 234.
[Abstract] [PDF]

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 EndocrinologyHome page
V. Chesnokova and S. Melmed
Minireview: Neuro-Immuno-Endocrine Modulation of the Hypothalamic-Pituitary-Adrenal (HPA) Axis by gp130 Signaling Molecules
Endocrinology, May 1, 2002; 143(5): 1571 - 1574.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. D. Bilbo, F. S. Dhabhar, K. Viswanathan, A. Saul, S. M. Yellon, and R. J. Nelson
Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function
PNAS, March 19, 2002; 99(6): 4067 - 4072.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
E. A. Elion
The Ste5p scaffold
J. Cell Sci., March 13, 2002; 114(22): 3967 - 3978.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
C. L. Coe, M. Kramer, C. Kirschbaum, P. Netter, and E. Fuchs
Prenatal Stress Diminishes the Cytokine Response of Leukocytes to Endotoxin Stimulation in Juvenile Rhesus Monkeys
J. Clin. Endocrinol. Metab., February 1, 2002; 87(2): 675 - 681.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
L. Vallieres, I. L. Campbell, F. H. Gage, and P. E. Sawchenko
Reduced Hippocampal Neurogenesis in Adult Transgenic Mice with Chronic Astrocytic Production of Interleukin-6
J. Neurosci., January 15, 2002; 22(2): 486 - 492.
[Abstract] [Full Text] [PDF]

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 CVIHome page
J. Jason, L. K. Archibald, O. C. Nwanyanwu, M. G. Byrd, P. N. Kazembe, H. Dobbie, and W. R. Jarvis
Comparison of Serum and Cell-Specific Cytokines in Humans
Clin. Vaccine Immunol., November 1, 2001; 8(6): 1097 - 1103.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. Bousquet, V. Chesnokova, A. Kariagina, A. Ferrand, and S. Melmed
cAMP Neuropeptide Agonists Induce Pituitary Suppressor of Cytokine Signaling-3: Novel Negative Feedback Mechanism for Corticotroph Cytokine Action
Mol. Endocrinol., November 1, 2001; 15(11): 1880 - 1890.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
J. Dahlgren, C. Nilsson, E. Jennische, H.-P. Ho, E. Eriksson, A. Niklasson, P. Bjorntorp, K. A. Wikland, and A. Holmang
Prenatal cytokine exposure results in obesity and gender-specific programming
Am J Physiol Endocrinol Metab, August 1, 2001; 281(2): E326 - E334.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. Xiao, L. Xia-Zhang, M. Ferin, and S. L. Wardlaw
Differential Effects of Estradiol on the Adrenocorticotropin Responses to Interleukin-6 and Interleukin-1 in the Monkey
Endocrinology, July 1, 2001; 142(7): 2736 - 2741.
[Abstract] [Full Text] [PDF]

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 Psychosom. Med.Home page
M. Haack, A. Schuld, T. Kraus, and T. Pollmacher
Effects of Sleep on Endotoxin-Induced Host Responses in Healthy Men
Psychosom Med, July 1, 2001; 63(4): 568 - 578.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
J. J. Puder, P. U. Freda, R. S. Goland, and S. L. Wardlaw
Estrogen Modulates the Hypothalamic-Pituitary-Adrenal and Inflammatory Cytokine Responses to Endotoxin in Women
J. Clin. Endocrinol. Metab., June 1, 2001; 86(6): 2403 - 2408.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
L. E. Goehler, R. P. A. Gaykema, M. K. Hansen, J. L. Kleiner, S. F. Maier, and L. R. Watkins
Staphylococcal enterotoxin B induces fever, brain c-Fos expression, and serum corticosterone in rats
Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2001; 280(5): R1434 - R1439.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
F. T. Bergh, T. Kümpfel, A. Grasser, R. Rupprecht, F. Holsboer, and C. Trenkwalder
Combined Treatment with Corticosteroids and Moclobemide Favors Normalization of Hypothalamo-Pituitary-Adrenal Axis Dysregulation in Relapsing-Remitting Multiple Sclerosis: A Randomized, Double Blind Trial
J. Clin. Endocrinol. Metab., April 1, 2001; 86(4): 1610 - 1615.
[Abstract] [Full Text]

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 Am. J. Physiol. Cell Physiol.Home page
R. L. Starkie, J. Rolland, D. J. Angus, M. J. Anderson, and M. A. Febbraio
Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-{alpha} levels after prolonged running
Am J Physiol Cell Physiol, April 1, 2001; 280(4): C769 - C774.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
A. Lacroix, N. N'Diaye, J. Tremblay, and P. Hamet
Ectopic and Abnormal Hormone Receptors in Adrenal Cushing's Syndrome
Endocr. Rev., February 1, 2001; 22(1): 75 - 110.
[Abstract] [Full Text]

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 GutHome page
E A MAYER
The neurobiology of stress and gastrointestinal disease
Gut, December 1, 2000; 47(6): 861 - 869.
[Full Text] [PDF]

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 J. Immunol.Home page
S. Sugama, Y. Kim, H. Baker, C. Tinti, H. Kim, T. H. Joh, and B. Conti
Tissue-Specific Expression of Rat IL-18 Gene and Response to Adrenocorticotropic Hormone Treatment
J. Immunol., December 1, 2000; 165(11): 6287 - 6292.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
V. Chesnokova and S. Melmed
Leukemia Inhibitory Factor Mediates the Hypothalamic Pituitary Adrenal Axis Response to Inflammation
Endocrinology, November 1, 2000; 141(11): 4032 - 4040.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
R L Starkie, D J Angus, J Rolland, M Hargreaves, and M A Febbraio
Effect of prolonged, submaximal exercise and carbohydrate ingestion on monocyte intracellular cytokine production in humans
J. Physiol., November 1, 2000; 528(3): 647 - 655.
[Abstract] [Full Text] [PDF]


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