Dehydroepiandrosterone and metyrapone partially restore the adaptive humoral and cellular immune response in endotoxin immunosuppressed mice

Innate Immunity

Volumn 20, Issue 6, 2014, Pages 585-597

  Rearte, Bárbara ^a   Maglioco, Andrea ^a   Machuca, Damián ^a   Martire Greco, Daiana ^a   Landoni, Verónica I ^a   Rodriguez Rodrigues, Nahuel ^a   Meiss, Roberto ^a   Fernández, Gabriela C ^a   Isturiz, Martín A ^a  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

Author keywords

DHEA; Glucocorticoids; Immunosuppression; LPS; Metyrapone

Indexed keywords

CORTICOSTERONE; ENDOTOXIN; GLUCOCORTICOID; LIPOPOLYSACCHARIDE; METYRAPONE; MIFEPRISTONE; PRASTERONE; GLUCOCORTICOID RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4 LYMPHOCYTE COUNT; CELL COMPONENT; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; HORMONE SYNTHESIS; HUMORAL IMMUNITY; HYPERSENSITIVITY; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; SPLEEN; SPLEEN CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CELL PROLIFERATION; CYTOLOGY; DELAYED HYPERSENSITIVITY; DRUG EFFECTS; IMMUNOLOGY; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; RESPIRATORY BURST; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTACT ALLERGY; CYTOKINE PRODUCTION; HEMORRHAGIC SHOCK; IMMUNIZATION;

ADAPTIVE IMMUNITY; ANIMALS; CD4 LYMPHOCYTE COUNT; CELL PROLIFERATION; DEHYDROEPIANDROSTERONE; GLUCOCORTICOIDS; HYPERSENSITIVITY, DELAYED; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOSUPPRESSION; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; METYRAPONE; MICE; MICE, INBRED BALB C; PHAGOCYTOSIS; RECEPTORS, GLUCOCORTICOID; RESPIRATORY BURST; SPLEEN;

EID: 84907042357     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425913502243     Document Type: Article

References (64)

1. Levy MM, Artigas A, Phillips GS, et al. Outcomes of the surviving sepsis campaign in intensive care units in the USA and Europe: a prospective cohort study. Lancet Infect Dis 12: 919-924.
2. Adib-Conquy M and Cavaillon JM. Compensatory anti-inflammatory response syndrome. Thromb Haemost 2009; 101: 36-47.
3. Hotchkiss RS and Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 2003; 348: 138-150.
4. Lyn-Kew K and Standiford TJ. Immunosuppression in sepsis. Curr Pharm Des 2008; 14: 1870-1881.
5. Oberholzer A, Oberholzer C and Moldawer LL. Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 2001; 16: 83-96.
6. Osuchowski MF, Welch K, Siddiqui J and Remick DG. Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol 2006; 177: 1967-1974.
7. Wiersinga WJ, vant Veer C, van den Pangaart PS, et al. Immunosuppression associated with interleukin-1R-associatedkinase- M upregulation predicts mortality in Gram-negative sepsis (melioidosis). Crit Care Med 2009; 37: 569-576.
8. Hotchkiss RS, Coopersmith CM, McDunn JE and Ferguson TA. The sepsis seesaw: tilting toward immunosuppression. Nat Med 2009; 15: 496-497.
9. Hotchkiss RS, Monneret G and Payen D. Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 2013; 13: 260-268.
10. Venet F, Lukaszewicz AC, Payen D, et al. Monitoring the immune response in sepsis: a rational approach to administration of immunoadjuvant therapies. Curr Opin Immunol 2013; 25: 477-483.
11. Biswas SK and Lopez-Collazo E. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol 2009; 30: 475-487.
12. Beishuizen A and Thijs LG. Endotoxin and the hypothalamopituitary- adrenal (HPA) axis. J Endotoxin Res 2003; 9: 3-24.
13. Carroll JA, Reuter RR, Chase Jr CC, et al. Profile of the bovine acute-phase response following an intravenous bolus-dose lipopolysaccharide challenge. Innate Immun 2009; 15: 81-89.
14. Evans GF and Zuckerman SH. Glucocorticoid-dependent and - independent mechanisms involved in lipopolysaccharide tolerance. Eur J Immunol 1991; 21: 1973-1979.
15. Fock RA, Vinolo MA, Crisma AR, et al. Protein-energy malnutrition modifies the production of interleukin-10 in response to lipopolysaccharide (LPS) in a murine model. J Nutr Sci Vitaminol (Tokyo) 2008; 54: 371-377.
16. Riedemann NC, Guo RF and Ward PA. Novel strategies for the treatment of sepsis. Nat Med 2003; 9: 517-524.
17. Sanchez-Lemus E, Benicky J, Pavel J and Saavedra JM. In vivo angiotensin II AT(1) receptor blockade selectively inhibits LPSinduced innate immune response and ACTH release in rat pituitary gland. Brain Behav Immun 2009; 23: 945-957.
18. Cavaillon JM. The nonspecific nature of endotoxin tolerance. Trends Microbiol 1995; 3: 320-324.
19. Cavaillon JM, Adrie C, Fitting C and Adib-Conquy M. Endotoxin tolerance: is there a clinical relevance? J Endotoxin Res 2003; 9: 101-107.
20. Parrillo JE. Pathogenetic mechanisms of septic shock. N Engl J Med 1993; 328: 1471-1477.
21. West MA and Heagy W. Endotoxin tolerance: A review. Crit Care Med 2002; 30: S64-S73.
22. Limaye AP, Kirby KA, Rubenfeld GD, et al. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 2008; 300: 413-422.
23. Morrison DC, Silverstein R, Luchi M and Shnyra A. Structurefunction relationships of bacterial endotoxins Contribution to microbial sepsis. Infect Dis Clin North Am 1999; 13: 313-340.
24. Vasilescu C, Olteanu M and Flondor P. How relevant are in vivo and in vitro studies for clinical sepsis? A mathematical model of LPS signaling based on endotoxin tolerance. Chirurgia (Bucur) 2009; 104: 195-201.
25. Rearte B, Landoni V, Laborde E, et al. Differential effects of glucocorticoids in the establishment and maintenance of endotoxin tolerance. Clin Exp Immunol 2010; 159: 208-216.
26. Rearte B, Maglioco A, Balboa L, et al. Mifepristone (RU486) restores humoral and T cell-mediated immune response in endotoxin immunosuppressed mice. Clin Exp Immunol 2010; 162: 568-577.
27. Hazeldine J, Arlt W and Lord JM. Dehydroepiandrosterone as a regulator of immune cell function. J Steroid Biochem Mol Biol 2010; 120: 127-136.
28. Kalimi M, Shafagoj Y, Loria R, et al. Anti-glucocorticoid effects of dehydroepiandrosterone (DHEA). Mol Cell Biochem 1994; 131: 99-104.
29. Krugers HJ, Maslam S, Korf J, et al. The corticosterone synthesis inhibitor metyrapone prevents hypoxia/ischemia-induced loss of synaptic function in the rat hippocampus. Stroke 2000; 31: 1162-1172.
30. Shalet S and Mukherjee A. Pharmacological treatment of hypercortisolism. Curr Opin Endocrinol Diabetes Obes 2008; 15: 234-238.
31. National Institutes of Health. Guide for the care and use of laboratory animals. NIH Publication no. 85-23. Bethesda, MD: National Institutes of Health, 1985.
32. Angele MK, Catania RA, Ayala A, et al. Dehydroepiandrosterone: an inexpensive steroid hormone that decreases the mortality due to sepsis following trauma-induced hemorrhage. Arch Surg 1998; 133: 1281-1288.
33. Oberbeck R, Deckert H, Bangen J, et al. Dehydroepiandrosterone: a modulator of cellular immunity and heat shock protein 70 production during polymicrobial sepsis. Intensive Care Med 2007; 33: 2207-2213.
34. Deans KJ, Haley M, Natanson C, et al. Novel therapies for sepsis: a review. J Trauma 2005; 58: 867-874.
35. Luyt CE, Combes A, Deback C, et al. Herpes simplex virus lung infection in patients undergoing prolonged mechanical ventilation. Am J Respir Crit Care Med 2007; 175: 935-942.
36. Oberbeck R, Dahlweid M, Koch R, et al. Dehydroepiandrosterone decreases mortality rate and improves cellular immune function during polymicrobial sepsis. Crit Care Med 2001; 29: 380-384.
37. Oberbeck R, Nickel E, von Griensven M, et al. The effect of dehydroepiandrosterone on hemorrhage-induced suppression of cellular immune function. Intensive Care Med 2002; 28: 963-968.
38. Catania RA, Angele MK, Ayala A, et al. Dehydroepiandrosterone restores immune function following trauma-haemorrhage by a direct effect on T lymphocytes. Cytokine 1999; 11: 443-450.
39. Matsuda A, Furukawa K, Suzuki H, et al. Dehydroepiandrosterone modulates toll-like receptor expression on splenic macrophages of mice after severe polymicrobial sepsis. Shock 2005; 24: 364-369.
40. Schmitz D, Kobbe P, Wegner A, et al. Dehydroepiandrosterone during sepsis: does the timing of administration influence the effectiveness. J Surg Res 2010; 163: e73-e77.
41. Breivik T, Sluyter F, Hof M and Cools A. Differential susceptibility to periodontitis in genetically selected Wistar rat lines that differ in their behavioral and endocrinological response to stressors. Behav Genet 2000; 30: 123-130.
42. Baitharu I, Deep SN, Jain V, et al. Corticosterone synthesis inhibitor metyrapone ameliorates chronic hypobaric hypoxia induced memory impairment in rat. Behav Brain Res 2012; 228: 53-65.
43. Peruzzo DC, Benatti BB, Andersen ML, et al. Evidence that metyrapone in the presence of inflammation modulates cytokine mRNA expression. Cytokine 2010; 52: 184-189.
44. McLachlan JA, Serkin CD and Bakouche O. Dehydroepiandrosterone modulation of lipopolysaccharidestimulated monocyte cytotoxicity. J Immunol 1996; 156: 328-335.
45. Meikle AW, Dorchuck RW, Araneo BA, et al. The presence of a dehydroepiandrosterone-specific receptor binding complex in murine T cells. J Steroid Biochem Mol Biol 1992; 42: 293-304.
46. Okabe T, Haji M, Takayanagi R, et al. Up-regulation of highaffinity dehydroepiandrosterone binding activity by dehydroepiandrosterone in activated human T lymphocytes. J Clin Endocrinol Metab 1995; 80: 2993-2996.
47. Ben-Nathan D, Padgett DA and Loria RM. Androstenediol and dehydroepiandrosterone protect mice against lethal bacterial infections and lipopolysaccharide toxicity. J Med Microbiol 1999; 48: 425-431.
48. Padgett DA and Loria RM. In vitro potentiation of lymphocyte activation by dehydroepiandrosterone, androstenediol, and androstenetriol. J Immunol 1994; 153: 1544-1552.
49. Browne ES, Wright BE, Porter JR and Svec F. Dehydroepiandrosterone: antiglucocorticoid action in mice. Am J Med Sci 1992; 303: 366-371.
50. Blauer KL, Poth M, Rogers WM and Bernton EW. Dehydroepiandrosterone antagonizes the suppressive effects of dexamethasone on lymphocyte proliferation. Endocrinology 1991; 129: 3174-3179.
51. Hotchkiss RS, Tinsley KW, Swanson PE, et al. Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J Immunol 2001; 166: 6952-6963.
52. Black CA. Delayed type hypersensitivity: current theories with an historic perspective. Dermatol Online J 1999; 5: 7.
53. Butcher SK, Killampalli V, Lascelles D, et al. Raised cortisol:DHEAS ratios in the elderly after injury: potential impact upon neutrophil function and immunity. Aging Cell 2005; 4: 319-324.
54. Radford DJ, Wang K, McNelis JC, et al. Dehdyroepiandrosterone sulfate directly activates protein kinase C-beta to increase human neutrophil superoxide generation. Mol Endocrinol 24: 813-821.
55. Middelveld RJ, Wanecek M, Bergman D, et al. Effect of cortisolsynthesis inhibition on endotoxin-induced porcine acute lung injury, shock, and nitric oxide production. Shock 1999; 12: 382-390.
56. Cui K, Luheshi GN and Boksa P. Effects of endogenous glucocorticoid secretion on the interleukin-6 response to bacterial endotoxin in pregnant and non-pregnant rats. J Endocrinol 2011; 209: 95-103.
57. Fantuzzi G, Cantoni L, Sironi M and Ghezzi P. Inhibitors of cytochrome P450 suppress tumor necrosis factor production. Cell Immunol 1993; 150: 417-424.
58. Gower DB. Modifiers of steroid-hormone metabolism: a review of their chemistry, biochemistry and clinical applications. J Steroid Biochem 1974; 5: 501-523.
59. Lehner MD, Ittner J, Bundschuh DS, et al. Improved innate immunity of endotoxin-tolerant mice increases resistance to Salmonella enterica serovar typhimurium infection despite attenuated cytokine response. Infect Immun 2001; 69: 463-471.
60. Wheeler DS, Lahni PM, Denenberg AG, et al. Induction of endotoxin tolerance enhances bacterial clearance and survival in murine polymicrobial sepsis. Shock 2008; 30: 267-273.
61. del Fresno C, Garcia-Rio F, Gomez-Pina V, et al. Potent phagocytic activity with impaired antigen presentation identifying lipopolysaccharide- tolerant human monocytes: demonstration in isolated monocytes from cystic fibrosis patients. J Immunol 2009; 182: 6494-6507.
62. Muthukuru M and Cutler CW. Antigen capture of Porphyromonas gingivalis by human macrophages is enhanced but killing and antigen presentation are reduced by endotoxin tolerance. Infect Immun 2008; 76: 477-485.
63. Delano MJ, Thayer T, Gabrilovich S, et al. Sepsis induces early alterations in innate immunity that impact mortality to secondary infection. J Immunol 2010; 186: 195-202.
64. Ayala A, Chung CS, Xu YX, et al. Increased inducible apoptosis in CD4+ T lymphocytes during polymicrobial sepsis is mediated by Fas ligand and not endotoxin. Immunology 1999; 97: 45-55.