Circadian characteristics of permissive and suppressive effects of cortisol and their role in homeostasis and the acute inflammatory response

Mathematical Biosciences

Volumn 260, Issue , 2015, Pages 54-64

  Mavroudis, Panteleimon D ^a   Corbett, Siobhan A ^a   Calvano, Steven E ^b   Androulakis, Ioannis P ^a,b,c  

^a The State University of New Jersey   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Cortisol permissive effects; Cortisol suppressive effects; Cytokine circadian rhythms; Inflammatory response

Indexed keywords

HYSTERESIS;

ACUTE INFLAMMATORY RESPONSE; CIRCADIAN RHYTHMS; CYTOKINE EXPRESSION; CYTOKINE RECEPTOR; HYSTERETIC BEHAVIOR; INFLAMMATORY RESPONSE; INFLAMMATORY STIMULI; SEMI-MECHANISTIC MODELS;

CORTISOL;

CYTOKINE RECEPTOR; GAMMA INTERFERON; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; INTERLEUKIN 1; LIPOPOLYSACCHARIDE; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

CIRCADIAN RHYTHM; HOMEOSTASIS; HORMONE; IMMUNE RESPONSE; IMMUNE SYSTEM; MODELING;

ACUTE STRESS; ARTICLE; CIRCADIAN RHYTHM; COMPUTER MODEL; CYTOKINE RELEASE; HOMEOSTASIS; IMMUNE RESPONSE; INFLAMMATION; PHARMACODYNAMICS; PROTEIN EXPRESSION; RECEPTOR BINDING; UPREGULATION; ANIMAL; HUMAN; IMMUNOLOGY; METABOLISM; THEORETICAL MODEL;

ANIMALS; CIRCADIAN RHYTHM; CYTOKINES; HOMEOSTASIS; HUMANS; HYDROCORTISONE; INFLAMMATION; MODELS, THEORETICAL;

EID: 84921417782     PISSN: 00255564     EISSN: 18793134     Source Type: Journal    
DOI: 10.1016/j.mbs.2014.10.006     Document Type: Article

References (75)

1. Hotchkiss R.S., Karl I.E. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 2003, 348(2):138-150.
2. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol. 2009, 5(7):374-381.
3. Tsigos C., Chrousos G.P. Physiology of the hypothalamic-pituitary-adrenal axis in health and dysregulation in psychiatric and autoimmune disorders. Endocrinol. Metab. Clin. North Am. 1994, 23(3):451-466.
4. Barnes P.J. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. (Lond.) 1998, 94(6):557-572.
5. Tracey K.J., et al. Shock and tissue injury induced by recombinant human cachectin. Science 1986, 234(4775):470-474.
6. Tracey K.J., et al. Cachectin/tumor necrosis factor induces lethal shock and stress hormone responses in the dog. Surg. Gynecol. Obstet. 1987, 164(5):415-422.
7. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21(1):55-89.
8. Gottschall P.E., et al. Glucocorticoid upregulation of interleukin 1 receptor expression in a glioblastoma cell line. Am. J. Physiol. 1991, 261(3 Pt 1):E362-E368.
9. Re F., et al. The type II "receptor" as a decoy target for interleukin 1 in polymorphonuclear leukocytes: characterization of induction by dexamethasone and ligand binding properties of the released decoy receptor. J. Exp. Med. 1994, 179(2):739-743.
10. Kamisoglu K., et al. Effects of coupled dose and rhythm manipulation of plasma cortisol levels on leukocyte transcriptional response to endotoxin challenge in humans. Innate Immun. 2013.
11. Snyers L., De Wit L., Content J. Glucocorticoid up-regulation of high-affinity interleukin 6 receptors on human epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 1990, 87(7):2838-2842.
12. Akahoshi T., Oppenheim J.J., Matsushima K. Induction of high-affinity interleukin 1 receptor on human peripheral blood lymphocytes by glucocorticoid hormones. J. Exp. Med. 1988, 167(3):924-936.
13. Munck A., Naray-Fejes-Toth A. The ups and downs of glucocorticoid physiology. Permissive and suppressive effects revisited. Mol. Cell. Endocrinol. 1992, 90(1):C1-C4.
14. Pratt W.B. Glucocorticoid receptor structure and the initial events in signal transduction. Prog. Clin. Biol. Res. 1990, 322:119-132.
15. Funder J.W. Mineralocorticoids, glucocorticoids, receptors and response elements. Science 1993, 259(5098):1132-1133.
16. Ramakrishnan R., et al. Fifth-generation model for corticosteroid pharmacodynamics: application to steady-state receptor down-regulation and enzyme induction patterns during seven-day continuous infusion of methylprednisolone in rats. J Pharmacokinet. Pharmacodyn. 2002, 29(1):1-24.
17. Arriza J.L., et al. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science 1987, 237(4812):268-275.
18. Joels M., de Kloet E.R. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Prog. Neurobiol. 1994, 43(1):1-36.
19. De Kloet E.R., et al. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19(3):269-301.
20. Jefferies W.M. Cortisol and immunity. Med. Hypotheses 1991, 34(3):198-208.
21. Jefferies W.M. Mild adrenocortical deficiency, chronic allergies, autoimmune disorders and the chronic fatigue syndrome: a continuation of the cortisone story. Med. Hypotheses 1994, 42(3):183-189.
22. Foteinou P.T., et al. In silico simulation of corticosteroids effect on an NFkB-dependent physicochemical model of systemic inflammation. PLoS One 2009, 4(3):e4706.
23. Foteinou P.T., et al. Modeling endotoxin-induced systemic inflammation using an indirect response approach. Math. Biosci. 2009, 217(1):27-42.
24. Scheff J.D., et al. Modeling the influence of circadian rhythms on the acute inflammatory response. J. Theor. Biol. 2010, 264(3):1068-1076.
25. Scheff J.D., et al. Modeling autonomic regulation of cardiac function and heart rate variability in human endotoxemia. Physiol. Genomics 2011, 43(16):951-964.
26. Scheff J.D., et al. Translational applications of evaluating physiologic variability in human endotoxemia. J. Clin. Monit. Comput. 2013, 27(4):405-415.
27. Scheff J.D., et al. Modeling physiologic variability in human endotoxemia. Crit. Rev. Biomed. Eng. 2012, 40(4):313-322.
28. Chakraborty A., Krzyzanski W., Jusko W.J. Mathematical modeling of circadian cortisol concentrations using indirect response models: comparison of several methods. J. Pharmacokinet. Biopharm. 1999, 27(1):23-43.
29. Tyson J.J., Chen K.C., Novak B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 2003, 15(2):221-231.
30. Frey F.J., Odermatt A., Frey B.M. Glucocorticoid-mediated mineralocorticoid receptor activation and hypertension. Curr. Opin. Nephrol. Hypertens. 2004, 13(4):451-458.
31. Sathiyaa R., Vijayan M.M. Autoregulation of glucocorticoid receptor by cortisol in rainbow trout hepatocytes. Am. J. Physiol. Cell Physiol. 2003, 284(6):C1508-C1515.
32. Jin J.Y., et al. Modeling of corticosteroid pharmacogenomics in rat liver using gene microarrays. J. Pharmacol. Exp. Ther. 2003, 307(1):93-109.
33. Sun Y.N., Jusko W.J. Transit compartments versus gamma distribution function to model signal transduction processes in pharmacodynamics. J. Pharm. Sci. 1998, 87(6):732-737.
34. Walker J.J., Terry J.R., Lightman S.L. Origin of ultradian pulsatility in the hypothalamic-pituitary-adrenal axis. Proc. Biol. Sci. 2010, 277(1688):1627-1633.
35. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418(6901):935-941.
36. Becker-Weimann S., et al. Modeling feedback loops of the Mammalian circadian oscillator. Biophys. J. 2004, 87(5):3023-3034.
37. Nagoshi E., et al. Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 2004, 119(5):693-705.
38. Welsh D.K., et al. Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr. Biol. 2004, 14(24):2289-2295.
39. Balsalobre A., et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 2000, 289(5488):2344-2347.
40. Balsalobre A. Clock genes in mammalian peripheral tissues. Cell Tissue Res. 2002, 309(1):193-199.
41. Burioka N., et al. Dexamethasone influences human clock gene expression in bronchial epithelium and peripheral blood mononuclear cells in vitro. Chronobiol. Int. 2005, 22(3):585-590.
42. Mavroudis P.D., et al. Entrainment of peripheral clock genes by cortisol. Physiol. Genomics 2012, 44(11):607-621.
43. So A.Y.L., et al. Glucocorticoid regulation of the circadian clock modulates glucose homeostasis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(41):17582-17587.
44. Yamamoto T., et al. Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. J. Biol. Chem. 2005, 280(51):42036-42043.
45. Keller M., et al. A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U.S.A. 2009.
46. Petrovsky N., Harrison L.C. Diurnal rhythmicity of human cytokine production: a dynamic disequilibrium in T helper cell type 1/T helper cell type 2 balance?. J. Immunol. 1997, 158(11):5163-5168.
47. Petrovsky N., McNair P., Harrison L.C. Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 1998, 10(4):307-312.
48. Petrovsky N., Harrison L.C. The chronobiology of human cytokine production. Int. Rev. Immunol. 1998, 16(5-6):635-649.
49. Knudsen P.J., Dinarello C.A., Strom T.B. Glucocorticoids inhibit transcriptional and post-transcriptional expression of interleukin 1 in U937 cells. J. Immunol. 1987, 139(12):4129-4134.
50. Paliogianni F., Boumpas D.T. Glucocorticoids regulate calcineurin-dependent trans-activating pathways for interleukin-2 gene transcription in human T lymphocytes. Transplantation 1995, 59(9):1333-1339.
51. Amano Y., Lee S.W., Allison A.C. Inhibition by glucocorticoids of the formation of interleukin-1 alpha, interleukin-1 beta, and interleukin-6: mediation by decreased mRNA stability. Mol. Pharmacol. 1993, 43(2):176-182.
52. Kutteh W.H., Rainey W.E., Carr B.R. Glucocorticoids inhibit lipopolysaccharide-induced production of tumor necrosis factor-alpha by human fetal Kupffer cells. J. Clin. Endocrinol. Metab. 1991, 73(2):296-301.
53. Sommer C., Kress M. Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci. Lett. 2004, 361(1-3):184-187.
54. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410(6824):37-40.
55. Akira S., et al. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J. 1990, 4(11):2860-2867.
56. Lowry S.F. Human endotoxemia: a model for mechanistic insight and therapeutic targeting. Shock 2005, 24:94-100.
57. Lee J.E., Edery I. Circadian regulation in the ability of Drosophila to combat pathogenic infections. Curr. Biol. 2008, 18(3):195-199.
58. Paladino N., et al. Paying the circadian toll: the circadian response to LPS injection is dependent on the Toll-like receptor 4. J. Neuroimmunol. 2010, 225(1-2):62-67.
59. Silver A.C., et al. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 2012, 36(2):251-261.
60. Feillet C.A., Albrecht U., Challet E. "Feeding time" for the brain: a matter of clocks. J. Physiol. Paris 2006, 100(5-6):252-260.
61. Edery I. Circadian rhythms in a nutshell. Physiol. Genomics 2000, 3(2):59-74.
62. Haus E., Smolensky M.H. Biologic rhythms in the immune system. Chronobiol. Int. 1999, 16(5):581-622.
63. Pollmacher T., et al. Diurnal variations in the human host response to endotoxin. J Infect Dis 1996, 174(5):1040-1045.
64. Alamili M., et al. Pronounced inflammatory response to endotoxaemia during nighttime: a randomised cross-over trial. PLoS One 2014, 9(1):e87413.
65. Jung C.M., et al. Acute effects of bright light exposure on cortisol levels. J. Biol. Rhythms 2010, 25(3):208-216.
66. Mavroudis P.D., et al. Mathematical modeling of light mediated HPA axis activity and downstream implications on the entrainment of peripheral clock genes. Physiol. Genomics 2014.
67. Mavroudis P.D., et al. Systems biology of circadian-immune interactions. J. Innate Immun. 2013, 5(2):153-162.
68. Haimovich B., et al. In vivo endotoxin synchronizes and suppresses clock gene expression in human peripheral blood leukocytes. Crit. Care Med. 2010, 38(3):751-758.
69. Cavadini G., et al. TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(31):12843-12848.
70. Ingle D.J. Permissibility of hormone action; a review. Acta Endocrinol. (Copenh.) 1954, 17(1-4):172-186.
71. Baker J.B., et al. Dexamethasone modulates binding and action of epidermal growth factor in serum-free cell culture. Proc. Natl. Acad. Sci. U.S.A. 1978, 75(4):1882-1886.
72. Angeli D., Ferrell J.E., Sontag E.D. Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(7):1822-1827.
73. Pomerening J.R., Sontag E.D., Ferrell J.E. Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat. Cell Biol. 2003, 5(4):346-351.
74. Barkai N., Leibler S. Circadian clocks limited by noise. Nature 2000, 403(6767):267-268.
75. Rao C.V., Wolf D.M., Arkin A.P. Control, exploitation and tolerance of intracellular noise. Nature 2002, 420(6912):231-237.