Melatonin protects CD4+ T cells from activation-induced cell death by blocking NFAT-mediated CD95 ligand upregulation

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3487-3494

  Pedrosa, Alziana Moreno Da Cunha ^a   Weinlich, Ricardo ^b,c   Mognol, Giuliana Patricia ^d   Robbs, Bruno Kaufmann ^d   Viola, João Paulo De Biaso ^d   Campa, Ana ^a   Amarante Mendes, Gustavo Pessini ^b,c  

^a Faculdade de Ciências Farm acêuticas   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Instituto Nacional de Ciencia e Tecnologia   (Brazil)

^d INSTITUTO NACIONAL DE CÂNCER   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; CALRETICULIN; FAS ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MELATONIN; TRANSCRIPTION FACTOR NFAT; FAS LIGAND;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; HORMONAL REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL SEPARATION; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; FAS LIGAND PROTEIN; FLOW CYTOMETRY; HUMANS; LYMPHOCYTE ACTIVATION; MELATONIN; MICE; MICE, INBRED BALB C; NFATC TRANSCRIPTION FACTORS; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 77951638135     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902961     Document Type: Article

References (78)

1. Lerner, A. B., J. D. Case, and Y. Takahashi. 1960. Isolation of melatonin and 5-methoxyindole-3-acetic acid from bovine pineal glands. J. Biol. Chem. 235: 1992-1997.
2. Kumar, V. 1996. Melatonin: a master hormone and a candidate for universal panacea. Indian J. Exp. Biol. 34: 391-402.
3. Reiter, R. J. 1986. Normal patterns of melatonin levels in the pineal gland and body fluids of humans and experimental animals. J. Neural Transm. Suppl. 21: 35-54.
4. Guerrero, J. M., and R. J. Reiter. 2002. Melatonin-immune system relationships. Curr. Top. Med. Chem. 2: 167-179.
5. Mayo, J. C., R. M. Sainz, D. X. Tan, R. Hardeland, J. Leon, C. Rodriguez, and R. J. Reiter. 2005. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine (AMK), in macrophages. J. Neuroimmunol. 165: 139-149.
6. Pierrefiche, G., G. Topall, G. Courboin, I. Henriet, and H. Laborit. 1993. Antioxidant activity of melatonin in mice. Res. Commun. Chem. Pathol. Pharmacol. 80: 211-223.
7. Bubenik, G. A. 2002. Gastrointestinal melatonin: localization, function, and clinical relevance. Dig. Dis. Sci. 47: 2336-2348.
8. Slominski, A., D. J. Tobin, M. A. Zmijewski, J. Wortsman, and R. Paus. 2008. Melatonin in the skin: synthesis, metabolism and functions. Trends Endocrinol. Metab. 19: 17-24.
9. Tan, D. X., L. C. Manchester, S. Burkhardt, R. M. Sainz, J. C. Mayo, R. Kohen, E. Shohami, Y. S. Huo, R. Hardeland, and R. J. Reiter. 2001. N1-acetyl-N2-formyl-5-methoxykynuramine, a biogenic amine and melatonin metabolite, functions as a potent antioxidant. FASEB J. 15: 2294-2296.
10. Carrillo-Vico, A., J. R. Calvo, P. Abreu, P. J. Lardone, S. García-Mauriño, R. J. Reiter, and J. M. Guerrero. 2004. Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine, autocrine, and/or paracrine substance. FASEB J. 18: 537-539.
11. Lopez-Gonzalez, M. A., J. R. Calvo, J. J. Segura, and J. M. Guerrero. 1993. Characterization of melatonin binding sites in human peripheral blood neutrophils. Biotechnol. Ther. 4: 253-262.
12. Barjavel, M. J., Z. Mamdouh, N. Raghbate, and O. Bakouche. 1998. Differential expression of the melatonin receptor in human monocytes. J. Immunol. 160: 1191-1197. (Pubitemid 28093414)
13. Lopez-Gonzalez, M. A., J. R. Calvo, C. Osuna, and J. M. Guerrero. 1992. Interaction of melatonin with human lymphocytes: evidence for binding sites coupled to potentiation of cyclic AMP stimulated by vasoactive intestinal peptide and activation of cyclic GMP. J. Pineal Res. 12: 97-104.
14. Persengiev, S. P., and S. Kyurkchiev. 1993. Selective effect of melatonin on the proliferation of lymphoid cells. Int. J. Biochem. 25: 441-444.
15. Vijayalaxmi, R. J. Reiter, B. Z. Leal, and M. L. Meltz. 1996. Effect of melatonin on mitotic and proliferation indices, and sister chromatid exchange in human blood lymphocytes. Mutat. Res. 351: 187-192.
16. García-Mauriño, S., D. Pozo, A. Carrillo-Vico, J. R. Calvo, and J. M. Guerrero. 1999. Melatonin activates Th1 lymphocytes by increasing IL-12 production. Life Sci. 65: 2143-2150. (Pubitemid 29524863)
17. Lotufo, C. M., C. Lopes, M. L. Dubocovich, S. H. Farsky, and R. P. Markus. 2001. Melatonin and N-acetylserotonin inhibit leukocyte rolling and adhesion to rat microcirculation. Eur. J. Pharmacol. 430: 351-357.
18. Di Stefano, A., and L. Paulesu. 1994. Inhibitory effect of melatonin on production of IFN gamma or TNF alpha in peripheral blood mononuclear cells of some blood donors. J. Pineal Res. 17: 164-169.
19. Garcia-Mauriño, S., M. G. Gonzalez-Haba, J. R. Calvo, M. Rafii-El-Idrissi, V. Sanchez-Margalet, R. Goberna, and J. M. Guerrero. 1997. Melatonin enhances IL-2, IL-6, and IFN-gamma production by human circulating CD4+ cells: a possible nuclear receptor-mediated mechanism involving T helper type 1 lymphocytes and monocytes. J. Immunol. 159: 574-581. (Pubitemid 127484205)
20. Carrillo-Vico, A., P. J. Lardone, J. M. Fernández-Santos, I. Martín-Lacave, J. R. Calvo, M. Karasek, and J. M. Guerrero. 2005. Human lymphocyte-synthesized melatonin is involved in the regulation of the interleukin-2/interleukin-2 receptor system. J. Clin. Endocrinol. Metab. 90: 992-1000.
21. Shi, Y. F., M. G. Szalay, L. Paskar, B. M. Sahai, M. Boyer, B. Singh, and D. R. Green. 1990. Activation-induced cell death in T cell hybridomas is due to apoptosis. Morphologic aspects and DNA fragmentation. J. Immunol. 144: 3326-3333.
22. Ramsdell, F., M. S. Seaman, R. E. Miller, K. S. Picha, M. K. Kennedy, and D. H. Lynch. 1994. Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. Int. Immunol. 6: 1545-1553.
23. Zhang, Y., G. Xu, L. Zhang, A. I. Roberts, and Y. Shi. 2008. Th17 cells undergo Fas-mediated activation-induced cell death independent of IFN-gamma. J. Immunol. 181: 190-196.
24. Brunner, T., R. J. Mogil, D. LaFace, N. J. Yoo, A. Mahboubi, F. Echeverri, S. J. Martin, W. R. Force, D. H. Lynch, C. F. Ware, et al. 1995. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373: 441-444.
25. Zhang, J., T. Bárdos, K. Mikecz, A. Finnegan, and T. T. Glant. 2001. Impaired Fas signaling pathway is involved in defective T cell apoptosis in autoimmune murine arthritis. J. Immunol. 166: 4981-4986. (Pubitemid 32280709)
26. Van Parijs, L., D. A. Peterson, and A. K. Abbas. 1998. The Fas/Fas ligand pathway and Bcl-2 regulate T cell responses to model self and foreign antigens. Immunity 8: 265-274. (Pubitemid 28123753)
27. Hughes, P. D., G. T. Belz, K. A. Fortner, R. C. Budd, A. Strasser, and P. Bouillet. 2008. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 28: 197-205.
28. Cohen, P. L., and R. A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9: 243-269.
29. Poppema, S., E. Maggio, and A. van den Berg. 2004. Development of lymphoma in Autoimmune Lymphoproliferative Syndrome (ALPS) and its relationship to Fas gene mutations. Leuk. Lymphoma 45: 423-431. (Pubitemid 38196023)
30. Amarante-Mendes, G. P., T. Jascur, W. K. Nishioka, T. Mustelin, and D. R. Green. 1997. Bcr - Abl-mediated resistance to apoptosis is independent of PI 3-kinase activity. Cell Death Differ. 4: 548-554.
31. McGahon, A. J., D. G. Brown, S. J. Martin, G. P. Amarante-Mendes, T. G. Cotter, G. M. Cohen, and D. R. Green. 1997. Downregulation of Bcr-Abl in K562 cells restores susceptibility to apoptosis: characterization of the apoptotic death. Cell Death Differ. 4: 95-104.
32. Weinlich, R., K. R. Bortoluci, C. F. Chehab, C. H. Serezani, A. G. Ulbrich, M. Peters-Golden, M. Russo, and G. P. Amarante-Mendes. 2008. TLR4/MYD88-dependent, LPS-induced synthesis of PGE2 by macrophages or dendritic cells prevents anti-CD3-mediated CD95L upregulation in T cells. Cell Death Differ. 15: 1901-1909.
33. Brumatti, G., R. Weinlich, C. F. Chehab, M. Yon, and G. P. Amarante-Mendes. 2003. Comparison of the anti-apoptotic effects of Bcr-Abl, Bcl-2 and Bcl-x(L) following diverse apoptogenic stimuli. FEBS Lett. 541: 57-63.
34. Shapiro, V. S., M. N. Mollenauer, W. C. Greene, and A. Weiss. 1996. c-rel regulation of IL-2 gene expression may be mediated through activation of AP-1. J. Exp. Med. 184: 1663-1669.
35. Kasibhatla, S., T. Brunner, L. Genestier, F. Echeverri, A. Mahboubi, and D. R. Green. 1998. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell 1: 543-551. (Pubitemid 128374690)
36. Robbs, B. K., A. L. Cruz, M. B. Werneck, G. P. Mognol, and J. P. Viola. 2008. Dual roles for NFAT transcription factor genes as oncogenes and tumor suppressors. Mol. Cell. Biol. 28: 7168-7181.
37. Carvalho, L. D., L. K. Teixeira, N. Carrossini, A. T. Caldeira, K. M. Ansel, A. Rao, and J. P. Viola. 2007. The NFAT1 transcription factor is a repressor of cyclin A2 gene expression. Cell Cycle 6: 1789-1795. (Pubitemid 47327933)
38. Ju, S. T., D. J. Panka, H. Cui, R. Ettinger, M. el-Khatib, D. H. Sherr, B. Z. Stanger, and A. Marshak-Rothstein. 1995. Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373: 444-448.
39. Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schröter, K. Burns, C. Mattmann, et al. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195.
40. Loh, C., K. T. Shaw, J. Carew, J. P. Viola, C. Luo, B. A. Perrino, and A. Rao. 1996. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271: 10884-10891.
41. Sainz, R. M., J. C. Mayo, C. Rodriguez, D. X. Tan, S. Lopez-Burillo, and R. J. Reiter. 2003. Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell. Mol. Life Sci. 60: 1407-1426.
42. Csaba, G., and P. Baráth. 1975. Morphological changes of thymus and the thyroid gland after postnatal extirpation of pineal body. Endocrinol. Exp. 9: 59-67.
43. Janković, B. D., K. Isaković, and S. Petrović. 1970. Effect of pinealectomy on immune reactions in the rat. Immunology 18: 1-6.
44. Vaughan, M. K., and R. J. Reiter. 1971. Transient hypertrophy of the ventral prostate and coagulating glands and accelerated thymic involution following pinealectomy in the mouse. Tex. Rep. Biol. Med. 29: 579-586.
45. Sharma, S., C. Haldar, and S. K. Chaube. 2008. Effect of exogenous melatonin on X-ray induced cellular toxicity in lymphatic tissue of Indian tropical male squirrel, Funambulus pennanti. Int. J. Radiat. Biol. 84: 363-374.
46. Majsterek, I., E. Gloc, J. Blasiak, and R. J. Reiter. 2005. A comparison of the action of amifostine and melatonin on DNA-damaging effects and apoptosis induced by idarubicin in normal and cancer cells. J. Pineal Res. 38: 254-263. (Pubitemid 41475437)
47. Wölfler, A., H. C. Caluba, P. M. Abuja, G. Dohr, K. Schauenstein, and P. M. Liebmann. 2001. Prooxidant activity of melatonin promotes fas-induced cell death in human leukemic Jurkat cells. FEBS Lett. 502: 127-131. (Pubitemid 32728274)
48. Alderson, M. R., T. W. Tough, T. Davis-Smith, S. Braddy, B. Falk, K. A. Schooley, R. G. Goodwin, C. A. Smith, F. Ramsdell, and D. H. Lynch. 1995. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 181: 71-77.
49. Romero, M. P., A. García-Pergañeda, J. M. Guerrero, and C. Osuna. 1998. Membrane-bound calmodulin in Xenopus laevis oocytes as a novel binding site for melatonin. FASEB J. 12: 1401-1408.
50. Turjanski, A. G., D. A. Estrin, R. E. Rosenstein, J. E. McCormick, S. R. Martin, A. Pastore, R. R. Biekofsky, and V. Martorana. 2004. NMR and molecular dynamics studies of the interaction of melatonin with calmodulin. Protein Sci. 13: 2925-2938.
51. Kiani, A., A. Rao, and J. Aramburu. 2000. Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity 12: 359-372.
52. Holtz-Heppelmann, C. J., A. Algeciras, A. D. Badley, and C. V. Paya. 1998. Transcriptional regulation of the human FasL promoter-enhancer region. J. Biol. Chem. 273: 4416-4423.
53. Latinis, K. M., L. A. Norian, S. L. Eliason, and G. A. Koretzky. 1997. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J. Biol. Chem. 272: 31427-31434.
54. Shi, Y. F., B. M. Sahai, and D. R. Green. 1989. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature 339: 625-626.
55. Benítez-King, G., A. Ríos, A. Martínez, and F. Antón-Tay. 1996. In vitro inhibition of Ca2+/calmodulin-dependent kinase II activity by melatonin. Biochim. Biophys. Acta 1290: 191-196.
56. Benítez-King, G., L. Huerto-Delgadillo, and F. Antón-Tay. 1991. Melatonin modifies calmodulin cell levels in MDCK and N1E-115 cell lines and inhibits phosphodiesterase activity in vitro. Brain Res. 557: 289-292.
57. Okamura, H., J. Aramburu, C. García-Rodríguez, J. P. Viola, A. Raghavan, M. Tahiliani, X. Zhang, J. Qin, P. G. Hogan, and A. Rao. 2000. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6: 539-550.
58. Benítez-King, G., L. Huerto-Delgadillo, and F. Antón-Tay. 1993. Binding of 3H-melatonin to calmodulin. Life Sci. 53: 201-207.
59. Ouyang, H., and H. J. Vogel. 1998. Melatonin and serotonin interactions with calmodulin: NMR, spectroscopic and biochemical studies. Biochim. Biophys. Acta 1383: 37-47.
60. Wölfler, A., K. Schauenstein, and P. M. Liebmann. 1998. Lack of calmodulin antagonism of melatonin in T-lymphocyte activation. Life Sci. 63: 835-842. (Pubitemid 28378322)
61. Menendez-Pelaez, A., B. Poeggeler, R. J. Reiter, L. Barlow-Walden, M. I. Pablos, and D. X. Tan. 1993. Nuclear localization of melatonin in different mammalian tissues: immunocytochemical and radioimmunoassay evidence. J. Cell. Biochem. 53: 373-382.
62. Huerto-Delgadillo, L., F. Antón-Tay, and G. Benítez-King. 1994. Effects of melatonin on microtubule assembly depend on hormone concentration: role of melatonin as a calmodulin antagonist. J. Pineal Res. 17: 55-62.
63. de Almeida-Paula, L. D., L. V. Costa-Lotufo, Z. Silva Ferreira, A. E. Monteiro, M. C. Isoldi, R. O. Godinho, and R. P. Markus. 2005. Melatonin modulates rat myotube-acetylcholine receptors by inhibiting calmodulin. Eur. J. Pharmacol. 525: 24-31.
64. León, J., M. Macías, G. Escames, E. Camacho, H. Khaldy, M. Martín, A. Espinosa, M. A. Gallo, and D. Acuña-Castroviejo. 2000. Structure-related inhibition of calmodulin-dependent neuronal nitric-oxide synthase activity by melatonin and synthetic kynurenines. Mol. Pharmacol. 58: 967-975.
65. del Río, B., J. M. García Pedrero, C. Martínez- Campa, P. Zuazua, P. S. Lazo, and S. Ramos. 2004. Melatonin, an endogenous-specific inhibitor of estrogen receptor alpha via calmodulin. J. Biol. Chem. 279: 38294-38302.
66. Benítez-King, G., and F. Antón-Tay. 1993. Calmodulin mediates melatonin cytoskeletal effects. Experientia 49: 635-641. (Pubitemid 23256788)
67. Akel, I., G. Demirkiran, A. Alanay, S. Karahan, R. Marcucio, and E. Acaroglu. 2009. The effect of calmodulin antagonists on scoliosis: bipedal C57BL/6 mice model. Eur. Spine J. 18: 499-505.
68. Machida, M., J. Dubousset, Y. Imamura, Y. Miyashita, T. Yamada, and J. Kimura. 1996. Melatonin. A possible role in pathogenesis of adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 21: 1147-1152.
69. Regodón, S., A. Ramos, S. Morgado, R. Tarazona, P. Martín-Palomino, J. A. Rosado, and Mdel. P. Míguez. 2009. Melatonin enhances the immune response to vaccination against A1 and C strains of Dichelobacter nodosus. Vaccine 27: 1566-1570.
70. Negrette, B., E. Bonilla, N. Valero, H. Pons, J. Garcia Tamayo, L. Chacín-Bonilla, S. Medina-Leendertz, and F. Añez. 2001. Melatonin treatment enhances the efficiency of mice immunization with Venezuelan equine encephalomyelitis virus TC-83. Neurochem. Res. 26: 767-770.
71. Boissonnas, A., and B. Combadiere. 2004. Interplay between cell division and cell death during TCR triggering. Eur. J. Immunol. 34: 2430-2438.
72. Thompson, B. S., V. Mata-Haro, C. R. Casella, and T. C. Mitchell. 2005. Peptide-stimulated DO11.10 T cells divide well but accumulate poorly in the absence of TLR agonist treatment. Eur. J. Immunol. 35: 3196-3208.
73. Umeshappa, C. S., H. Huang, Y. Xie, Y. Wei, S. J. Mulligan, Y. Deng, and J. Xiang. 2009. CD4+ Th-APC with acquired peptide/MHC class I and II complexes stimulate type 1 helper CD4+ and central memory CD8+ T cell responses. J. Immunol. 182: 193-206.
74. Collette, Y., A. Benziane, D. Razanajaona, and D. Olive. 1998. Distinct regulation of T-cell death by CD28 depending on both its aggregation and T-cell receptor triggering: a role for Fas-FasL. Blood 92: 1350-1363. (Pubitemid 28369049)
75. Hansson, I., R. Holmdahl, and R. Mattsson. 1992. The pineal hormone melatonin exaggerates development of collagen-induced arthritis in mice. J. Neuroimmunol. 39: 23-30.
76. Constantinescu, C. S., B. Hilliard, E. Ventura, and A. Rostami. 1997. Luzindole, a melatonin receptor antagonist, suppresses experimental autoimmune encephalomyelitis. Pathobiology 65: 190-194.
77. Nunnari, G., L. Nigro, F. Palermo, D. Leto, R. J. Pomerantz, and B. Cacopardo. 2003. Reduction of serum melatonin levels in HIV-1-infected individuals' parallel disease progression: correlation with serum interleukin-12 levels. Infection 31: 379-382. (Pubitemid 38005366)
78. Lissoni, P., L. Vigorè, R. Rescaldani, F. Rovelli, F. Brivio, L. Giani, S. Barni, G. Tancini, A. Ardizzoia, and M. G. Viganò. 1995. Neuroimmunotherapy with low-dose subcutaneous interleukin-2 plus melatonin in AIDS patients with CD4 cell number below 200/mm3: a biological phase-II study. J. Biol. Regul. Homeost. Agents 9: 155-158.