Evaluation of the immunomodulatory effect of melatonin on the T-cell response in peripheral blood from systemic lupus erythematosus patients

Journal of Pineal Research

Volumn 58, Issue 2, 2015, Pages 219-226

  Medrano Campillo, Pablo ^a   Sarmiento Soto, Helia ^a   Álvarez Sánchez, Nuria ^a   Álvarez Ríos, Ana I ^a   Guerrero, Juan M ^a,b   Rodríguez Prieto, Ismael ^a   Castillo Palma, María Jesús ^a   Lardone, Patricia J ^a,b   Carrillo Vico, Antonio ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

BAFF; IL 5; IL 9; lupus; Melatonin; T cell; treg

Indexed keywords

B CELL ACTIVATING FACTOR; CD3 ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; MELATONIN; MESSENGER RNA; PHYTOHEMAGGLUTININ; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; CYTOKINE; IMMUNOLOGIC FACTOR;

ADULT; ARTICLE; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EVALUATION STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; LEUKOCYTE; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; TH9 CELL; AGED; BLOOD; CONTROLLED CLINICAL TRIAL; FLOW CYTOMETRY; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; METABOLISM; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CYTOKINES; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC FACTORS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MELATONIN; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY;

EID: 84922772222     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12208     Document Type: Article

References (53)

1. Rahman A, Isenberg DA,. Systemic lupus erythematosus. N Engl J Med 2008; 358: 929-939.
2. Crispin JC, Liossis SN, Kis-Toth K, et al. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 2010; 16: 47-57.
3. Crispin JC, Kyttaris VC, Terhorst C, et al. T cells as therapeutic targets in SLE. Nat Rev Rheumatol 2010; 6: 317-325.
4. Jager A, Kuchroo VK,. Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand J Immunol 2010; 72: 173-184.
5. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235-238.
6. Funauchi M, Ikoma S, Enomoto H, et al. Decreased Th1-like and increased Th2-like cells in systemic lupus erythematosus. Scand J Rheumatol 1998; 27: 219-224.
7. Gomez D, Correa PA, Gomez LM, et al. Th1/Th2 cytokines in patients with systemic lupus erythematosus: is tumor necrosis factor alpha protective? Semin Arthritis Rheum 2004; 33: 404-413.
8. Wong CK, Ho CY, Li EK, et al. Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus. Lupus 2000; 9: 589-593.
9. Ouyang H, Shi Y, Liu Z, et al. Increased interleukin-9 and CD4+ IL-9+ T cells in patients with systemic lupus erythematosus. Mol Med Rep 2013; 7: 1031-1037.
10. Stohl W, Metyas S, Tan SM, et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum 2003; 48: 3475-3486.
11. Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011; 377: 721-731.
12. Garcia JJ, Lopez-Pingarron L, Almeida-Souza P, et al. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J Pineal Res 2014; 56: 225-237.
13. Hardeland R,. Melatonin and the theories of aging: a critical appraisal of melatonin's role in antiaging mechanisms. J Pineal Res 2013; 55: 325-356.
14. Reiter RJ, Tan DX, Galano A,. Melatonin: exceeding expectations. Physiology (Bethesda) 2014; 29: 325-333.
15. Carrillo-Vico A, Lardone PJ, Alvarez-Sanchez N, et al. Melatonin: buffering the immune system. Int J Mol Sci 2013; 14: 8638-8683.
16. Lenz SP, Izui S, Benediktsson H, et al. Lithium chloride enhances survival of NZB/W lupus mice: influence of melatonin and timing of treatment. Int J Immunopharmacol 1995; 17: 581-592.
17. Haga HJ, Brun JG, Rekvig OP, et al. Seasonal variations in activity of systemic lupus erythematosus in a subarctic region. Lupus 1999; 8: 269-273.
18. Lechner O, Dietrich H, Oliveira Dos Santos A, et al. Altered circadian rhythms of the stress hormone and melatonin response in lupus-prone MRL/MP-fas(Ipr) mice. J Autoimmun 2000; 14: 325-333.
19. Jimenez-Caliani AJ, Jimenez-Jorge S, Molinero P, et al. Sex-dependent effect of melatonin on systemic erythematosus lupus developed in Mrl/Mpj-Faslpr mice: it ameliorates the disease course in females, whereas it exacerbates it in males. Endocrinology 2006; 147: 1717-1724.
20. Zhou LL, Wei W, Si JF, et al. Regulatory effect of melatonin on cytokine disturbances in the pristane-induced lupus mice. Mediators Inflamm 2010; 2010: 1-7.
21. Hochberg MC,. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40: 1725.
22. Jang CH, Choi JH, Byun MS, et al. Chloroquine inhibits production of TNF-alpha, IL-1beta and IL-6 from lipopolysaccharide-stimulated human monocytes/macrophages by different modes. Rheumatology (Oxford) 2006; 45: 703-710.
23. Calandra T, Bernhagen J, Metz CN, et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995; 377: 68-71.
24. Walchner M, Meurer M, Plewig G, et al. Clinical and immunologic parameters during thalidomide treatment of lupus erythematosus. Int J Dermatol 2000; 39: 383-388.
25. Cepika AM, Bendelja K, Vergles JM, et al. Monocyte response to LPS after exposure to corticosteroids and chloroquine with implications for systemic lupus erythematosus. Scand J Immunol 2010; 72: 434-443.
26. Brunetti M, Martelli N, Colasante A, et al. Spontaneous and glucocorticoid-induced apoptosis in human mature T lymphocytes. Blood 1995; 86: 4199-4205.
27. Tak PP, Firestein GS,. NF-kappaB: a key role in inflammatory diseases. J Clin Invest 2001; 107: 7-11.
28. Carrillo-Vico A, Guerrero JM, Lardone PJ, et al. A review of the multiple actions of melatonin on the immune system. Endocrine 2005b; 27: 189-200.
29. Calvo JR, Gonzalez-Yanes C, Maldonado MD,. The role of melatonin in the cells of the innate immunity: a review. J Pineal Res 2013; 55: 103-120.
30. di Stefano A, Paulesu L,. Inhibitory effect of melatonin on production of IFN gamma or TNF alpha in peripheral blood mononuclear cells of some blood donors. J Pineal Res 1994; 17: 164-169.
31. Shi D, Xiao X, Wang J, et al. Melatonin suppresses proinflammatory mediators in lipopolysaccharide-stimulated CRL1999 cells via targeting MAPK, NF-kappaB, c/EBPbeta, and p300 signaling. J Pineal Res 2012; 53: 154-165.
32. Leckie MJ, ten Brinke A, Khan J, et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 2000; 356: 2144-2148.
33. Schmitt E, Klein M, Bopp T,. Th9 cells, new players in adaptive immunity. Trends Immunol 2014; 35: 61-68.
34. Hu ZP, Fang XL, Fang N, et al. Melatonin ameliorates vascular endothelial dysfunction, inflammation, and atherosclerosis by suppressing the TLR4/NF-kappaB system in high-fat-fed rabbits. J Pineal Res 2013; 55: 388-398.
35. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
36. Franco DG, Markus RP,. The cellular state determines the effect of melatonin on the survival of mixed cerebellar cell culture. PLoS ONE 2014; 9: e106332.
37. Valencia X, Yarboro C, Illei G, et al. Deficient CD4+ CD25 high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007; 178: 2579-2588.
38. Liu MF, Wang CR, Fung LL, et al. Decreased CD4+ CD25+ T cells in peripheral blood of patients with systemic lupus erythematosus. Scand J Immunol 2004; 59: 198-202.
39. Fujio K, Okamura T, Sumitomo S, et al. Regulatory cell subsets in the control of autoantibody production related to systemic autoimmunity. Ann Rheum Dis 2013; 72 (Suppl 2): ii85-ii89.
40. Lopez P, Gomez J, Prado C, et al. Influence of functional interleukin 10/tumor necrosis factor-alpha polymorphisms on interferon-alpha, IL-10, and regulatory T cell population in patients with systemic lupus erythematosus receiving antimalarial treatment. J Rheumatol 2008; 35: 1559-1566.
41. Thome R, Moraes AS, Bombeiro AL, et al. Chloroquine treatment enhances regulatory T cells and reduces the severity of experimental autoimmune encephalomyelitis. PLoS ONE 2013; 8: e65913.
42. Braitch M, Harikrishnan S, Robins RA, et al. Glucocorticoids increase CD4CD25 cell percentage and Foxp3 expression in patients with multiple sclerosis. Acta Neurol Scand 2009; 119: 239-245.
43. Juang YT, Wang Y, Solomou EE, et al. Systemic lupus erythematosus serum IgG increases CREM binding to the IL-2 promoter and suppresses IL-2 production through CaMKIV. J Clin Invest 2005; 115: 996-1005.
44. Koga T, Ichinose K, Mizui M, et al. Calcium/calmodulin-dependent protein kinase IV suppresses IL-2 production and regulatory T cell activity in lupus. J Immunol 2012; 189: 3490-3496.
45. Ichinose K, Juang YT, Crispin JC, et al. Suppression of autoimmunity and organ pathology in lupus-prone mice upon inhibition of calcium/calmodulin-dependent protein kinase type IV. Arthritis Rheum 2011; 63: 523-529.
46. Bazwinsky-Wutschke I, Muhlbauer E, Wolgast S, et al. Transcripts of calcium/calmodulin-dependent kinases are changed after forskolin- or IBMX-induced insulin secretion due to melatonin treatment of rat insulinoma beta-cells (INS-1). Horm Metab Res 2009; 41: 805-813.
47. Cheema GS, Roschke V, Hilbert DM, et al. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum 2001; 44: 1313-1319.
48. Lahiri A, Pochard P, le Pottier L, et al. The complexity of the BAFF TNF-family members: implications for autoimmunity. J Autoimmun 2012; 39: 189-198.
49. Toubi E, Kessel A, Rosner I, et al. The reduction of serum B-lymphocyte activating factor levels following quinacrine add-on therapy in systemic lupus erythematosus. Scand J Immunol 2006; 63: 299-303.
50. Ju S, Zhang D, Wang Y, et al. Correlation of the expression levels of BLyS and its receptors mRNA in patients with systemic lupus erythematosus. Clin Biochem 2006; 39: 1131-1137.
51. Lopez De Padilla CM, Mcnallan KT, Crowson CS, et al. BAFF expression correlates with idiopathic inflammatory myopathy disease activity measures and autoantibodies. J Rheumatol 2013; 40: 294-302.
52. Collins CE, Gavin AL, Migone TS, et al. B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels. Arthritis Res Ther 2006; 8: R6.
53. Cepika AM, Soldo Juresa D, Morovic Vergles J, et al. Decrease in circulating DNA, IL-10 and BAFF levels in newly-diagnosed SLE patients after corticosteroid and chloroquine treatment. Cell Immunol 2012; 276: 196-203.