The hypothalamic—pituitary—adrenal axis and immune-mediated inflammation

New England Journal of Medicine

Volumn 332, Issue 20, 1995, Pages 1351-1363

  Flier, Jeffrey S ^a   Underhill, Lisa H ^a   Chrousos, George P ^b  

^a National Institutes of Health ^*

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTEROID; CORTICOTROPIN RELEASING FACTOR; HYPOPHYSIS HORMONE; HYPOTHALAMUS HORMONE; INTERLEUKIN 1; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; HORMONAL REGULATION; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW;

ADRENAL CORTEX HORMONES; HUMAN; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION; PITUITARY HORMONES; PITUITARY-ADRENAL SYSTEM;

EID: 0029037126     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJM199505183322008     Document Type: Review

References (132)

1. Eustachio B. Opuscula anatomica. Venice, Italy: Vicentius Luchinus, 1563-64.
2. Gordon BL. Medicine throughout antiquity. Philadelphia: F.A. Davis, 1949.
3. Selye H A syndrome produced by diverse nocuous agents. Nature 1936; 138: 32-32
4. Nobelstiftelsen. Les Prix Nobel: en 1951. Stockholm, Sweden: Imprimerie Royal. P.A. Norstedt and Söner, 1951:195-243.
5. Hench PS, Kendall EC, Slocumb CH, Polley HF The effect of a hormone of the adrenal cortex (17-hydroxy-11-dehydro-corticosterone: compound E) and of pituitary adrenocorticotropic hormone on rheumatoid arthritis. Mayo Clin Proc 1949; 24: 181-197
6. Chrousos GP, Gold PW The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. JAMA 1992; 267: 1244-1252 [Erratum, JAMA 1992;268:200.]
7. Chrousos GP Regulation and dysregulation of the hypothalamic-pituitary-adrenal axis: the corticotropin-releasing hormone perspective. Endocrinol Metab Clin North Am 1992; 21: 833-858
8. Sawchenko PE, Imaki T, Potter E, Kovács K, Imaki J, Vale W. The functional neuroanatomy of corticotropin-releasing factor. In: Chadwick DJ, Marsh J, Ackrill K, eds. Corticotropin-releasing factor. Ciba Foundation Symposium 172. Chichester, United Kingdom: John Wiley, 1993:5-29.
9. Saper CB, Lowey AD, Swanson LW, Cowan WM Direct hypothalamo-autonomic connections. Brain Res 1976; 117: 305-312
10. Larsen PJ, Jessop D, Patel H, Lightman SL, Chowdrey HS Substance P inhibits the release of anterior pituitary adrenocorticotrophin via a central mechanism involving corticotrophin-releasing factor-containing neurons in the hypothalamic paraventricular nucleus. J Neuroendocrinol 1993; 5: 99-105
11. Culman J, Tschope C, Jost N, Itoi K, Unger T Substance P and neurokinin A induced desensitization to cardiovascular and behavioral effects: evidence for the involvement of different tachykinin receptors. Brain Res 1993; 625: 75-83
12. Jessop DS, Chowdrey HS, Larsen PJ, Lightman S Substance P: multifunctional peptide in the hypothalamo-pituitary system? J Endocrinol 1992; 132: 331-337
13. Whitnall MH Stress selectively activates the vasopressin-containing subset of corticotropin-releasing hormone neurons. Neuroendocrinology 1989; 50: 702-707
14. de Goeij DCE, Kvetnansky R, Whitnall MH, Jezova D, Berkenbosch F, Tilders FJH Repeated stress-induced activation of corticotropin-releasing factor neurons enhances vasopressin stores and colocalization with corticotropin-releasing factor in the median eminence of rats. Neuroendocrinology 1991; 53: 150-159
15. Nikolarakis KE, Almeida OFX, Herz A Stimulation of hypothalamic β-endorphin and dynorphin release by corticotropin-releasing factor (in vitro). Brain Res 1986; 399: 152-155
16. Burns G, Almeida OFX, Passarelli F, Herz A A two-step mechanism by which corticotropin-releasing hormone releases hypothalamic β-endorphin: the role of vasopressin and G-proteins. Endocrinology 1989; 125: 1365-1372
17. Lamberts SWJ, Verleun T, Oosterom R, de Jong F, Hackeng WHL Corticotropin-releasing factor (ovine) and vasopressin exert a synergistic effect on adrenocorticotropin release in man. J Clin Endocrinol Metab 1984; 58: 298-303
18. Rittmaster RS, Cutler GB Jr, Gold PW, The relationship of saline-induced changes in vasopressin secretion to basal and corticotropin-releasing hormone-stimulated adrenocorticotropin and cortisol secretion in man. J Clin Endocrinol Metab 1987; 64: 371-376
19. Elkabir DR, Wyatt ME, Vellucci SV, Herbert J The effects of separate or combined infusions of corticotropin-releasing factor and vasopressin either intraventricularly or into the amygdala on aggressive and investigative behavior in the rat. Regul Pept 1990; 28: 199-214
20. Redekopp C, Irvine CHG, Donald RA, Spontaneous and stimulated adrenocorticotropin and vasopressin pulsatile secretion in the pituitary venous effluent of the horse. Endocrinology 1986; 118: 1410-1416
21. Ixart G, Barbanel G, Conte-Devolx B, Grino M, Oliver C, Assenmacher I Evidence for basal and stress-induced release of corticotropin releasing factor in the push-pull cannulated median eminence of conscious free-moving rats. Neurosci Lett 1987; 74: 85-89
22. Engler D, Pham T, Fullerton MJ, Ooi G, Funder JW, Clark IJ Studies of the secretion of corticotropin-releasing factor and arginine vasopressin into the hypophysial-portal circulation of the conscious sheep. I. Effect of an audiovisual stimulus and insulin-induced hypoglycemia. Neuroendocrinology 1989; 49: 367-381
23. Carnes M, Lent SJ, Goodman B, Mueller C, Saydoff J, Erisman S Effect of immunoneutralization of corticotropin-releasing hormone on ultradian rhythms of plasma adrenocorticotropin. Endocrinology 1990; 126: 1904-1913
24. Calogero AE, Norton JA, Sheppard BC, Pulsatile activation of the hypothalamic-pituitary-adrenal axis during major surgery. Metabolism 1992; 41: 839-845
25. Holmes MC, Antoni FA, Aguilera G, Catt KJ Magnocellular axons in passage through the median eminence release vasopressin. Nature 1986; 319: 326-329
26. Phillips MI functions of angiotensin in the central nervous system. Annu Rev Physiol 1987; 49: 413-435
27. Hinson JP Paracrine control of adrenocortical function: a new role for the medulla? J Endocrinol 1990; 124: 7-9
28. Andreis PG, Neri G, Mazzocchi G, Musajo F, Nussdorfer GG Direct secretagogue effect of corticotropin-releasing factor on the rat adrenal cortex: the involvement of the zona medullaris. Endocrinology 1992; 131: 69-72
29. Vinson GP, Whitehouse BJ, Henvill KL, et al. In: Hadley ME, ed. The actions of α-MSH on the adrenal cortex, the melanotropic peptides. Vol. II. Biological roles. Boca Raton, Fla.: CRC Press, 1988:87-133.
30. Ottenweller JE, Meier AH Adrenal innervation may be an extrapituitary mechanism able to regulate adrenocortical rhythmicity in rats. Endocrinology 1982; 111: 1334-1338
31. Gallin JI, Goldstein IM, Snyderman R. Overview. In: Gallin JI, Goldstein IM, Snyderman R, eds. Inflammation: basic principles and clinical correlates. New York: Raven Press, 1988:1-3.
32. Paul WE, Seder RA Lymphocyte responses and cytokines. Cell 1994; 76: 241-251
33. Celander DR, Folkow B The nature and distribution of afferent fibers provided with the axon reflex arrangements. Acta Physiol Scand 1953; 29: 359-370
34. Payan DG, Goetzl EJ Modulation of lymphocyte function by sensory neuropeptides. J Immunol 1985; 135: Suppl: 783s-786s
35. Engel D The influence of the sympathetic nervous system on capillary permeability. Res Exp Med (Berl) 1978; 173: 1-8
36. Holzer P Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 1988; 24: 739-768
37. Coderre TJ, Basbaum AI, Levine JD Neural control of vascular permeability: interactions between primary afferents, mast cells, and sympathetic efferents. J Neurophysiol 1989; 62: 48-58
38. Boumpas DT, Chrousos GP, Wilder RL, Cupps TR, Balow JE Glucocorticoid therapy for immune-mediated diseases: basic and clinical correlates. Ann Intern Med 1993; 119: 1198-1208
39. Chrousos GP, Detera-Wadleigh SD, Karl M Syndromes of glucocorticoid resistance. Ann Intern Med 1993; 119: 1113-1124
40. Cronstein BN, Kimmel SC, Levin RI, Martiniuk F, Weissmann G A mechanism for the antiinflammatory effects of corticosteroids: the glucocorticoid receptor regulates leukocyte adhesion to endothelial cells and expression of endothelial-leukocyte adhesion molecule 1 and intracellular adhesion molecule 1. Proc Natl Acad Sci U S A 1992; 89: 9991-9995
41. Hirano T, Akira S, Taga T, Kishimoto T Biological and clinical aspects of interleukin 6. Immunol Today 1990; 11: 443-449
42. Lee SW, Tsou AP, Chan H, Glucocorticoids selectively inhibit the transcription of the interleukin 1β gene and decrease the stability of interleukin 1β mRNA. Proc Natl Acad Sci U S A 1988; 85: 1204-1208
43. Zanker B, Walz G, Wieder KJ, Strom TB Evidence that glucocorticosteroids block expression of the human interleukin-6 gene by accessory cells. Transplantation 1990; 49: 183-185
44. Zitnik RJ, Whiting NL, Elias JA Glucocorticoid inhibition of interleukin-1-induced interleukin-6 production by human lung fibroblasts: evidence for transcriptional and post-transcriptional regulatory mechanisms. Am J Respir Cell Mol Biol 1994; 10: 643-650
45. Nakano T, Ohara O, Teraoka H, Arita H Glucocorticoids suppress group II phospholipase A2 production by blocking mRNA synthesis and post-transcriptional expression. J Biol Chem 1990; 265: 12745-12748
46. Vishwanath BS, Frey FJ, Bradbury MJ, Dallman MF, Frey BM Glucocorticoid deficiency increases phospholipase A2 activity in rats. J Clin Invest 1993; 92: 1974-1980
47. O'Banion MK, Winn VD, Young DA cDNA cloning and functional activity of a glucocorticoid-regulated inflammatory cyclooxygenase. Proc Natl Acad Sci U S A 1992; 89: 4888-4892
48. Conrad DJ, Kuhn H, Mulkins M, Highland E, Sigal E Specific inflammatory cytokines regulate the expression of human monocyte 15-lipoxygenase. Proc Natl Acad Sci U S A 1992; 89: 217-221
49. Moncada S, Higgs A The arginine-nitric oxide pathway. N Engl J Med 1993; 329: 2002-2012
50. Cove-Smith JR, Kabler P, Pownall R, Knapp MS Circadian variation in an immune response in man. BMJ 1978; 2: 253-254
51. Harkness JAL, Richter MB, Panayi GS, Circadian variation in disease activity in rheumatoid arthritis. BMJ 1982; 284: 551-554
52. Mastorakos G, Chrousos GP. Adrenal hyperandrogenism. In: Adashi E, Rock J, Rosenwaks Z, eds. Reproductive endocrinology, surgery and technology. New York: Raven Press (in press).
53. Daynes RA, Dudley DJ, Araneo BA Regulation of murine lymphokine production in vivo. II. Dehydroepiandrosterone is a natural enhancer of interleukin 2 synthesis by helper T cells. Eur J Immunol 1990; 20: 793-802
54. Blauer KL, Poth M, Rogers WM, Bernton EW Dehydroepiandrosterone antagonizes the suppressive effects of dexamethasone on lymphocyte proliferation. Endocrinology 1991; 129: 3174-3179
55. Suzuki T, Suzuki N, Daynes RA, Engelman EG Dehydroepiandrosterone enhances IL2 production and cytotoxic effector function of human T cells. Clin Immunol Immunopathol 1991; 61: 202-211
56. Meikle AW, Dorchuck RW, Araneo BA, The presence of a dehydroepiandrosterone-specific receptor binding complex in murine T cells. J Steroid Biochem Mol Biol 1992; 42: 293-304
57. Blalock JE A molecular basis for bidirectional communication between the immune and neuroendocrine systems. Physiol Rev 1989; 69: 1-32
58. Bateman A, Singh A, Kral T, Solomon S the immune-hypothalamic-pituitary-adrenal axis. Endocr Rev 1989; 10: 92-112
59. Schafer M, Carter L, Stein C Interleukin 1β and corticotropin-releasing factor inhibit pain by releasing opioids from immune cells in inflamed tissue. Proc Natl Acad Sci U S A 1994; 91: 4219-4223
60. Karalis K, Sano H, Redwine J, Listwak S, Wilder RL, Chrousos GP Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 1991; 254: 421-423
61. Crofford LJ, Sano H, Karalis K, Local secretion of corticotropin-releasing hormone in the joints of Lewis rats with inflammatory arthritis. J Clin Invest 1992; 90: 2555-2564
62. Crofford LJ, Sano H, Karalis K, Corticotropin-releasing hormone in synovial fluids and tissues of patients with rheumatoid arthritis and osteoarthritis. J Immunol 1993; 151: 1587-1596
63. Scopa CD, Mastorakos G, Friedman TC, Melachrinou MC, Merino MJ, Chrousos GP Presence of immunoreactive corticotropin releasing hormone in thyroid lesions. Am J Pathol 1994; 145: 1159-1167
64. Patchev VK, Mastorakos G, Brady LS, Redwine J, Wilder RL, Chrousos GP Increased arginine vasopressin secretion may participate in the enhanced susceptibility of Lewis rats to inflammatory disease. Neuroendocrinology 1993; 58: 106-110
65. Stephanou A, Jessop DS, Knight RA, Lightman SL Corticotrophin-releasing factor-like immunoreactivity and mRNA in human leukocytes. Brain Behav Immun 1990; 4: 67-73
66. Ekman RE, Servenius B, Castro MG, Biosynthesis of corticotropin-releasing hormone in human T-lymphocytes. J Neuroimmunol 1993; 44: 7-13
67. Aird F, Clevenger CV, Prystowsky MB, Redei E Corticotropin-releasing factor mRNA in rat thymus and spleen. Proc Natl Acad Sci U S A 1993; 90: 7104-7108
68. Woods RJ, Grossman A, Saphier P, Association of human corticotropin-releasing hormone to its binding protein in blood may trigger clearance of the complex. J Clin Endocrinol Metab 1994; 78: 73-76
69. Witorsch RJ, Brodish A Evidence for acute ACTH release by extrahypothalamic mechanisms. Endocrinology 1972; 90: 1160-1167
70. Akira S, Hirano T, Taga T, Kishimoto T Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J 1990; 4: 2860-2867
71. Hesse DG, Tracey KJ, Fong Y, Cytokine appearance in human endotoxemia and primate bacteremia. Surg Gynecol Obstet 1988; 166: 147-153
72. van Deventer SJH, Buller HR, ten Cate JW, Aarden LA, Hack CE, Sturk A Experimental endotoxemia in humans: analysis of cytokine release and coagulation, fibrinolytic, and complement pathways. Blood 1990; 76: 2520-2526
73. van Gool J, van Vugt H, Helle M, Aarden LA The relation among stress, adrenalin, interleukin 6 and acute phase proteins in the rat. Clin Immunol Immunopathol 1990; 57: 200-210
74. Kowaki G, Gottschall PE, Somogyvari-Vigh A, Rapid increase in plasma IL-6 after hemorrhage, and posthemorrhage reduction of the IL-6 response to LPS in conscious rats: interrelations with plasma corticosterone levels. Neuroimmunomodulation 1994; 1: 127-134
75. Imura H, Fukata J, Mori T Cytokines and endocrine functions: an interaction between the immune and neuroendocrine systems. Clin Endocrinol (Oxf) 1991; 35: 107-115
76. Bernardini R, Kamilaris TC, Calogero AE, Interactions between tumor necrosis factor-α, hypothalamic corticotropin-releasing hormone, and adrenocorticotropin secretion in the rat. Endocrinology 1990; 126: 2876-2881
77. Sapolsky R, Rivier C, Yamamoto G, Plotsky P, Vale W Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science 1987; 238: 522-524
78. Naitoh Y, Fukata J, tominaga T, Interleukin-6 stimulates the secretion of adrenocorticotropic hormone in conscious, free-moving rats. Biochem Biophys Res Commun 1988; 155: 1459-1463
79. Perlstein RS, Mougey EH, Jackson WE, Neta R Interleukin-1 and interleukin-6 act synergistically to stimulate the release of adrenocorticotropic hormone in vivo. Lymphokine Cytokine Res 1991; 10: 141-146
80. Perlstein RS, Whitnall MH, Abrams JS, Mougey EH, Neta R Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology 1993; 132: 946-952
81. Mastorakos G, Chrousos GP, Weber JS Recombinant interleukin-6 activates the hypothalamic-pituitary-adrenal axis in humans. J Clin Endocrinol Metab 1993; 77: 1690-1694
82. Mastorakos G, Weber JS, Magiakou MA, Gunn H, Chrousos GP Hypothalamic-pituitary-adrenal axis activation and stimulation of systemic vasopressin secretion by recombinant interleukin 6 in humans: potential implications for the syndrome of inappropriate vasopressin secretion. J Clin Endocrinol Metab 1994; 79: 934-939
83. Tilders FJH, DeRijk RH, Van Dam AM, Vincent VA, Schotanus K, Persoons THA Activation of the hypothalamic-pituitary-adrenal axis by bacterial endotoxins: routes and intermediate signals. Psychoneuroendocrinology 1994; 19: 209-232
84. Reichlin S Neuroendocrine-immune interactions. N Engl J Med 1993; 329: 1246-1253
85. De Simoni MG, Sironi M, De Luigi A, Manfridi A, Mantovani A, Ghezzi P Intracerebroventricular injection of interleukin 1 induces high circulating levels of interleukin 6. J Exp Med 1990; 171: 1773-1778
86. Gordon ML An evaluation of afferent nervous impulses in the adrenal cortical response to trauma. Endocrinology 1950; 47: 347-350
87. Chapman LF, Goodell H The participation of the nervous system in the inflammatory reaction. Ann N Y Acad Sci 1963; 116: 990-1017
88. Uehara A, Gillis S, Arimura A Effects of interleukin-1 on hormone release from normal rat pituitary cells in primary culture. Neuroendocrinology 1987; 45: 343-347
89. Spangelo BL, Judd AM, Isakson PC, MacLeod RM Interleukin-6 stimulates anterior pituitary hormone release in vitro. Endocrinology 1989; 125: 575-577
90. Roh MS, Drazenovich KA, Barbose JJ, Dinarello CA, Cobb CF Direct stimulation of the adrenal cortex by interleukin-1. Surgery 1987; 102: 140-146
91. Salas MA, Evans SW, Levell MJ, Whicher JT Interleukin-6 and ACTH act synergistically to stimulate the release of corticosterone from adrenal gland cells. Clin Exp Immunol 1990; 79: 470-473
92. Tominaga T, Fukata J, Naito Y, Prostaglandin-dependent in vitro stimulation of adrenocortical steroidogenesis by interleukins. Endocrinology 1991; 128: 526-531
93. Vankelecom H, Carmeliet P, Van Damme J, Billiau A, Denef C Production of interleukin-6 by folliculo-stellate cells of the anterior pituitary gland in a histiotypic cell aggregate culture system. Neuroendocrinology 1989; 49: 102-106
94. Schultzberg M, Andersson C, Unden A, Troye-Blomberg M, Svenson SB, Bartfai T Interleukin-1 in adrenal chromaffin cells. Neuroscience 1989; 30: 805-810
95. Vankelecom H, Carmeliet P, Heremans H, Interferon-γ inhibits stimulated adrenocorticotropin, prolactin, and growth hormone secretion in normal rat anterior pituitary cell cultures. Endocrinology 1990; 126: 2919-2926
96. Gaillard RC, Turnill D, Sappino P, Muller AF Tumor necrosis factor α inhibits the hormonal response of the pituitary gland to hypothalamic releasing factors. Endocrinology 1990; 127: 101-106
97. Jaattela M, Ilvesmaki V, Voutilainen R, Stenman U-H, Saksela E Tumor necrosis factor as a potent inhibitor of adrenocorticotropin-induced cortisol production and steroidogenic P450 enzyme gene expression in cultured human fetal adrenal cells. Endocrinology 1991; 128: 623-629
98. Almawi WY, Lipman ML, Stevens AC, Zanker B, Hadro ET, Strom TB Abrogation of glucocortico-mediated inhibition of T cell proliferation by the synergistic action of IL-1, IL-6 and IFN-γ. J Immunol 1991; 146: 3523-3527
99. Kam JC, Szefler SJ, Surs W, Sher ER, Leung DYM Combination IL-2 and IL-4 reduces glucocorticoid receptor-binding affinity and T cell response to glucocorticoids. J Immunol 1993; 151: 3460-3466
100. Klein A, Buskila D, Gladman D, Bruser B, Malkin A Cortisol catabolism by lymphocytes of patients with systemic lupus erythematosus and rheumatoid arthritis. J Rheumatol 1990; 17: 30-33
101. Harbuz MS, Lightman SL Stress and the hypothalamo-pituitary-adrenal axis: acute, chronic and immunological activation. J Endocrinol 1992; 134: 327-339
102. Dallman MF Stress update: adaptation of the hypothalamic-pituitary-adrenal axis to chronic stress. Trends Endocrinol Metab 1993; 4: 62-69
103. Swain MG, Patchev V, Vergalla J, Chrousos GP, Jones EA Suppression of hypothalamic-pituitary-adrenal axis responsiveness to stress in a rat model of acute cholestasis. J Clin Invest 1993; 91: 1903-1908
104. Rothwell PM, Udwadia ZF, Lawler PG Cortisol response to corticotropin and survival in septic shock. Lancet 1991; 337: 582-583
105. Kidess AI, Caplan RH, Reynertson RH, Wickus CG, Goodnough DE Transient corticotropin deficiency in critical illness. Mayo Clin Proc 1993; 68: 435-441
106. Dluhy RG The growing spectrum of HIV-related endocrine abnormalities. J Clin Endocrinol Metab 1990; 70: 563-565
107. Reincke M, Heppner C, Petzke F, Impairment of adrenocortical function with increased plasma tumor necrosis factor-alpha and interleukin-6 concentrations in African trypanosomiasis. Neuroimmunomodulation 1994; 1: 14-22
108. Parker LN, Levin ER, Lifrak ET Evidence for adrenocortical adaptation to severe illness. J Clin Endocrinol Metab 1985; 60: 947-952
109. Berczi I. Gonadotropins and sex hormones. In: Berczi I, ed. Pituitary function and immunity. Boca Raton, Fla.: CRC Press, 1986:185-211.
110. Raveche ES, Steinberg AD. Sex hormones and autoimmunity. In: Berczi I, ed. Pituitary function and immunity. Boca Raton, Fla.: CRC Press, 1986:283-301.
111. Cid MC, Kleinman HK, Grant DS, Schnaper W, Fauci AS, Hoffman GS Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1. J Clin Invest 1994; 93: 17-25
112. Vamvakopoulos NC, Chrousos GP Evidence of direct estrogen regulation of human corticotropin-releasing hormone gene expression: potential implications for the sexual dimorphism of the stress response and immune/inflammatory reaction. J Clin Invest 1993; 92: 1896-1902
113. Berczi I, Nagy E. Prolactin and other lactogenic hormones. In: Berczi I, ed. Pituitary function and immunity. Boca Raton, Fla.: CRC Press, 1986:161-83.
114. Gellersen B, Kempf R, Telgmann R, DiMattia GE Nonpituitary human prolactin gene transcription is independent of pit-1 and differentially controlled in lymphocytes and in endometrial stroma. Mol Endocrinol 1994; 8: 356-373
115. Sternberg EM, Hill JM, Chrousos GP, Inflammatory mediator-induced hypothalamic-pituitary-adrenal axis activation is defective in streptococcal cell wall arthritis-susceptible Lewis rats. Proc Natl Acad Sci U S A 1989; 86: 2374-2378
116. Sternberg EM, Young WS III, Bernardini R, A central nervous system defect in biosynthesis of corticotropin-releasing hormone is associated with susceptibility to streptococcal cell wall-induced arthritis in Lewis rats. Proc Natl Acad Sci U S A 1989; 86: 4771-4775
117. Calogero AE, Sternberg EM, Bagdy G, Neurotransmitter-induced hypothalamic-pituitary-adrenal axis responsiveness is defective in inflammatory disease-susceptible Lewis rats: in vivo and in vitro studies suggesting globally defective hypothalamic secretion of corticotropin-releasing hormone. Neuroendocrinology 1992; 55: 600-608
118. Patchev VK, Kalogeras KT, Zelazowski P, Wilder RL, Chrousos GP Increased plasma concentrations, hypothalamic content, and in vitro release of arginine vasopressin in inflammatory disease-prone, hypothalamic corticotropin-releasing hormone-deficient Lewis rats. Endocrinology 1992; 131: 1453-1457
119. Sternberg ER, Glowa JR, Smith MA, Corticotropin releasing hormone related behavioral and neuroendocrine responses to stress in Lewis and Fischer rats. Brain Res 1992; 570: 54-60
120. Neeck G, Federlin K, Graef V, Rusch D, Schmidt KL Adrenal secretion of cortisol in patients with rheumatoid arthritis. J Rheumatol 1990; 17: 24-29
121. Chikanza IC, Petrou P, Kingsley G, Chrousos GP, Panayi GS Defective hypothalamic response to immune and inflammatory stimuli in patients with rheumatoid arthritis. Arthritis Rheum 1992; 35: 1281-1288
122. Masi AT, Chatterton RT, Comstock GW, Malamet RL, Hochberg MC. Decreased androgenic-anabolic (AA) hormone levels in sera of white women before onset of RA: a controlled, prospective study. Presented at the 57th Annual Scientific Meeting of the American College of Rheumatology, San Antonio, Texas, November 7-11, 1993:S176. abstract.
123. Sternberg EM Hyperimmune fatigue syndromes: diseases of the stress response? J Rheumatol 1993; 20: 418-421
124. Dekaris D, Sabioncello A, Mazuran R, Multiple changes of immunologic parameters in prisoners of war: assessments after release from a camp in Manjaca, Bosnia. JAMA 1993; 270: 595-599
125. Schlaghecke R, Kornely E, Wollenhaupt J, Specker C Glucocorticoid receptors in rheumatoid arthritis. Arthritis Rheum 1992; 35: 740-744
126. Kirkham BW, Corkill MM, Davison SC, Panayi GS Response to glucocorticoid treatment in rheumatoid arthritis: in vitro cell mediated immune assay predicts in vivo responses. J Rheumatol 1991; 18: 821-825
127. Corrigan CJ, Brown PH, Barnes NC, Tsai JJ, Frew AJ, Kay AB Glucocorticoid resistance in chronic asthma: peripheral blood T lymphocyte activation and comparison of the T lymphocyte inhibitory effects of glucocorticoids and cyclosporin A. Am Rev Respir Dis 1991; 144: 1026-1032
128. Sher ER, Leung DYM, Surs W, Steroid-resistant asthma: cellular mechanisms contributing to inadequate response to glucocorticoid therapy. J Clin Invest 1994; 93: 33-39
129. Norbiato G, Bevilacqua M, Vago T, Cortisol resistance in acquired immunodeficiency syndrome. J Clin Endocrinol Metab 1992; 74: 608-613
130. DiBattista JA, Martel-Pelletier J, Antakly T, Tardif G, Cloutier JM, Pelletier JP Reduced expression of glucocorticoid receptor levels in human osteoarthritic chondrocytes: role in the suppression of metalloprotease synthesis. J Clin Endocrinol Metab 1993; 76: 1128-1134
131. Barton BE, Jackson JV Protective role of interleukin 6 in the lipopolysaccharide-galactosamine septic shock model. Infect Immun 1993; 61: 1496-1499
132. Engelman EG, Lambert RE, Lee L, McGuire JL. Treatment of systemic lupus erythematosus with dihydroepiandrosterone: interim analysis of a double-blinded, randomized, placebo controlled, clinical trial. Presented at the 57th Annual Scientific Meeting of the American College of Rheumatology, San Antonio, Texas, November 7-11, 1993:S92. abstract.