Melatonin synthesized by T lymphocytes as a ligand of the retinoic acid-related orphan receptor

Journal of Pineal Research

Volumn 51, Issue 4, 2011, Pages 454-462

  Lardone, Patricia J ^a   Guerrero, Juan M ^b   Fernández Santos, José M ^a   Rubio, Amalia ^a   Martín Lacave, Inés ^a   Carrillo Vico, Antonio ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

autoimmunity; IL 2; Jurkat cells; melatonin receptor; retinoic acid related orphan receptor

Indexed keywords

MELATONIN; RECEPTOR PROTEIN; RETINOIC ACID RELATED ORPHAN RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; GRAFT REJECTION; HORMONE ACTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH17 CELL;

BLOTTING, WESTERN; HUMANS; IMMUNOPRECIPITATION; JURKAT CELLS; MELATONIN; PROTEIN BINDING; RECEPTORS, RETINOIC ACID; T-LYMPHOCYTES;

EID: 80054817139     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00909.x     Document Type: Article

References (65)

1. Carrillo-Vico A, Reiter RJ, Lardone PJ, et al., The modulatory role of melatonin on immune responsiveness. Curr Opin Investig Drugs 2006; 7: 423-431. (Pubitemid 43772981)
2. Garcia-Maurino S, Gonzalez-Haba MG, Calvo JR, et al., 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 1997; 159: 574-581. (Pubitemid 127484205)
3. Garcia-Maurino S, Pozo D, Carrillo-Vico A, et al., Melatonin activates Th1 lymphocytes by increasing IL-12 production. Life Sci 1999; 65: 2143-2150. (Pubitemid 29524863)
4. Kuhlwein E, Irwin M,. Melatonin modulation of lymphocyte proliferation and Th1/Th2 cytokine expression. J Neuroimmunol 2001; 117: 51-57. (Pubitemid 32595492)
5. Annane D, Bellissant E, Cavaillon JM,. Septic shock. Lancet 2005; 365: 63-78.
6. Lopes C, Mariano M, Markus RP,. Interaction between the adrenal and the pineal gland in chronic experimental inflammation induced by BCG in mice. Inflamm Res 2001; 50: 6-11. (Pubitemid 32156113)
7. Carrillo-Vico A, Lardone PJ, Naji L, et al., Beneficial pleiotropic actions of melatonin in an experimental model of septic shock in mice: regulation of pro-/anti-inflammatory cytokine network, protection against oxidative damage and anti-apoptotic effects. J Pineal Res 2005; 39: 400-408.
8. Jung KH, Hong SW, Zheng HM, et al., Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. J Pineal Res 2010; 48: 239-250.
9. Chahbouni M, Escames G, Venegas C, et al., Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy. J Pineal Res 2010; 48: 282-289.
10. Carrillo-Vico A, Guerrero JM, Lardone PJ, et al., A review of the multiple actions of melatonin on the immune system. Endocrine 2005; 27: 189-200. (Pubitemid 41558451)
11. Wiesenberg I, Missbach M, Carlberg C,. The potential role of the transcription factor RZR/ROR as a mediator of nuclear melatonin signaling. Restor Neurol Neurosci 1998; 12: 143-150. (Pubitemid 28368295)
12. Giguere V,. Orphan nuclear receptors: from gene to function. Endocr Rev 1999; 20: 689-725. (Pubitemid 30654814)
13. Becker-Andre M, Andre E, Delamarter JF,. Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem Biophys Res Commun 1993; 194: 1371-1379. (Pubitemid 23255034)
14. Carlberg C, Hooft Van HR, Staple JK, et al., RZRs, a new family of retinoid-related orphan receptors that function as both monomers and homodimers. Mol Endocrinol 1994; 8: 757-770. (Pubitemid 24179668)
15. Hirose T, Smith RJ, Jetten AM,. ROR gamma: the third member of ROR/RZR orphan receptor subfamily that is highly expressed in skeletal muscle. Biochem Biophys Res Commun 1994; 205: 1976-1983.
16. Dzhagalov I, Zhang N, He YW,. The roles of orphan nuclear receptors in the development and function of the immune system. Cell Mol Immunol 2004; 1: 401-407.
17. Dzhagalov I, Giguere V, He YW,. Lymphocyte development and function in the absence of retinoic acid-related orphan receptor alpha. J Immunol 2004; 173: 2952-2959. (Pubitemid 39141999)
18. Dussault I, Giguere V,. Differential regulation of the N-myc proto-oncogene by ROR alpha and RVR, two orphan members of the superfamily of nuclear hormone receptors. Mol Cell Biol 1997; 17: 1860-1867. (Pubitemid 27133271)
19. Steinhilber D, Brungs M, Werz O, et al., The nuclear receptor for melatonin represses 5-lipoxygenase gene expression in human B lymphocytes. J Biol Chem 1995; 270: 7037-7040.
20. Jin P, Sun Y, Grabowski GA,. Role of Sp proteins and RORalpha in transcription regulation of murine prosaposin. J Biol Chem 1998; 273: 13208-13216. (Pubitemid 28246892)
21. Vu-Dac N, Chopin-Delannoy S, Gervois P, et al., The nuclear receptors peroxisome proliferator-activated receptor alpha and Rev-erbalpha mediate the species-specific regulation of apolipoprotein A-I expression by fibrates. J Biol Chem 1998; 273: 25713-25720. (Pubitemid 28475794)
22. Delerive P, Chin WW, Suen CS,. Identification of Reverb(alpha) as a novel ROR(alpha) target gene. J Biol Chem 2002; 277: 35013-35018.
23. Raspe E, Mautino G, Duval C, et al., Transcriptional regulation of human Rev-erbalpha gene expression by the orphan nuclear receptor retinoic acid-related orphan receptor alpha. J Biol Chem 2002; 277: 49275-49281. (Pubitemid 36014356)
24. Wada T, Kang HS, Angers M, et al., Identification of oxysterol 7alpha-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor alpha (RORalpha) (NR1F1) target gene and a functional cross-talk between RORalpha and liver X receptor (NR1H3). Mol Pharmacol 2008; 73: 891-899. (Pubitemid 351397893)
25. Becker-Andre M, Wiesenberg I, Schaeren-Wiemers N, et al., Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. J Biol Chem 1994; 269: 28531-28534. (Pubitemid 24366678)
26. Yang XO, Pappu BP, Nurieva R, et al., T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008; 28: 29-39.
27. Bettelli E, Oukka M, Kuchroo VK,. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007; 8: 345-350. (Pubitemid 46745409)
28. Jin D, Zhang L, Zheng J, et al., The inflammatory Th 17 subset in immunity against self and non-self antigens. Autoimmunity 2008; 41: 154-162. (Pubitemid 351372298)
29. Bradford MM,. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
30. Wiesenberg I, Missbach M, Kahlen JP, et al., Transcriptional activation of the nuclear receptor RZR alpha by the pineal gland hormone melatonin and identification of CGP 52608 as a synthetic ligand. Nucleic Acids Res 1995; 23: 327-333.
31. Zhang L, Su P, Xu C, et al., Melatonin inhibits adipogenesis and enhances osteogenesis of human mesenchymal stem cells by suppressing PPARgamma expression and enhancing Runx2 expression. J Pineal Res 2010; 49: 364-372.
32. Missbach M, Jagher B, Sigg I, et al., Thiazolidine diones, specific ligands of the nuclear receptor retinoid Z receptor/retinoid acid receptor-related orphan receptor alpha with potent antiarthritic activity. J Biol Chem 1996; 271: 13515-13522. (Pubitemid 26187977)
33. Garcia-Maurino S, Gonzalez-Haba MG, Calvo JR, et al., Involvement of nuclear binding sites for melatonin in the regulation of IL-2 and IL-6 production by human blood mononuclear cells. J Neuroimmunol 1998; 92: 76-84. (Pubitemid 29015992)
34. Carrillo-Vico A, Lardone PJ, Fernandez-Santos JM, et al., Human lymphocyte-synthesized melatonin is involved in the regulation of the interleukin-2/interleukin-2 receptor system. J Clin Endocrinol Metab 2005; 90: 992-1000. (Pubitemid 40279225)
35. Pozo D, Garcia-Maurino S, Guerrero JM, et al., mRNA expression of nuclear receptor RZR/RORalpha, melatonin membrane receptor MT, and hydroxindole-O- methyltransferase in different populations of human immune cells. J Pineal Res 2004; 37: 48-54. (Pubitemid 38969020)
36. Garcia-Maurino S, Pozo D, Calvo JR, et al., Correlation between nuclear melatonin receptor expression and enhanced cytokine production in human lymphocytic and monocytic cell lines. J Pineal Res 2000; 29: 129-137.
37. Carrillo-Vico A, Garcia-Perganeda A, Naji L, et al., Expression of membrane and nuclear melatonin receptor mRNA and protein in the mouse immune system. Cell Mol Life Sci 2003; 60: 2272-2278. (Pubitemid 37357434)
38. Becker-Andre M, Wiesenberg I, Schaeren-Wiemers N, et al., Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. Erratum. J Biol Chem 1997; 272: 16707.
39. Ram PT, Dai J, Yuan L, et al., Involvement of the mt1 melatonin receptor in human breast cancer. Cancer Lett 2002; 179: 141-150. (Pubitemid 34215105)
40. Dai J, Ram PT, Yuan L, et al., Transcriptional repression of RORalpha activity in human breast cancer cells by melatonin. Mol Cell Endocrinol 2001; 176: 111-120. (Pubitemid 32454942)
41. Delerive P, Monte D, Dubois G, et al., The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response. EMBO Rep 2001; 2: 42-48. (Pubitemid 32229720)
42. Aschrafi A, Meindl N, Firla B, et al., Intracellular localization of RORalpha is isoform and cell line-dependent. Biochim Biophys Acta 2006; 1763: 805-814. (Pubitemid 44205277)
43. Guiochon-Mantel A, Lescop P, Christin-Maitre S, et al., Nucleocytoplasmic shuttling of the progesterone receptor. EMBO J 1991; 10: 3851-3859. (Pubitemid 21905413)
44. Muratani M, Tansey WP,. How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol 2003; 4: 192-201. (Pubitemid 36288041)
45. Dennis AP, Haq RU, Nawaz Z,. Importance of the regulation of nuclear receptor degradation. Front Biosci 2001; 6: D954-D959.
46. Lonard DM, Nawaz Z, Smith CL, et al., The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol Cell 2000; 5: 939-948.
47. Boudjelal M, Wang Z, Voorhees JJ, et al., Ubiquitin/proteasome pathway regulates levels of retinoic acid receptor gamma and retinoid X receptor alpha in human keratinocytes. Cancer Res 2000; 60: 2247-2252. (Pubitemid 30225190)
48. Dace A, Zhao L, Park KS, et al., Hormone binding induces rapid proteasome-mediated degradation of thyroid hormone receptors. Proc Natl Acad Sci U S A 2000; 97: 8985-8990. (Pubitemid 30626660)
49. Syvala H, Pekki A, Blauer M, et al., Hormone-dependent changes in A and B forms of progesterone receptor. J Steroid Biochem Mol Biol 1996; 58: 517-524. (Pubitemid 126657497)
50. Wallace AD, Cidlowski JA,. Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. J Biol Chem 2001; 276: 42714-42721.
51. Moraitis AN, Giguere V,. The co-repressor hairless protects RORalpha orphan nuclear receptor from proteasome-mediated degradation. J Biol Chem 2003; 278: 52511-52518. (Pubitemid 38035845)
52. Kopf E, Plassat JL, Vivat V, et al., Dimerization with retinoid X receptors and phosphorylation modulate the retinoic acid-induced degradation of retinoic acid receptors alpha and gamma through the ubiquitin-proteasome pathway. J Biol Chem 2000; 275: 33280-33288.
53. Lardone PJ, Carrillo-Vico A, Naranjo MC, et al., Melatonin synthesized by Jurkat human leukemic T cell line is implicated in IL-2 production. J Cell Physiol 2006; 206: 273-279. (Pubitemid 41740741)
54. Stehlin C, Wurtz JM, Steinmetz A, et al., X-ray structure of the orphan nuclear receptor RORbeta ligand-binding domain in the active conformation. EMBO J 2001; 20: 5822-5831. (Pubitemid 33049258)
55. Kim HP, Imbert J, Leonard WJ,. Both integrated and differential regulation of components of the IL-2/IL-2 receptor system. Cytokine Growth Factor Rev 2006; 17: 349-366. (Pubitemid 44604346)
56. Cavallini L, Francesconi MA, Zoccarato F, et al., Involvement of nuclear factor-kappa B (NF-kappaB) activation in mitogen-induced lymphocyte proliferation: inhibitory effects of lymphoproliferation by salicylates acting as NF-kappaB inhibitors. Biochem Pharmacol 2001; 62: 141-147. (Pubitemid 32488985)
57. Ranjan D, Chen C, Johnston TD, et al., Curcumin inhibits mitogen stimulated lymphocyte proliferation, NFkappaB activation, and IL-2 signaling. J Surg Res 2004; 121: 171-177. (Pubitemid 39387457)
58. Bettelli E, Korn T, Kuchroo VK,. Th17: the third member of the effector T cell trilogy. Curr Opin Immunol 2007; 19: 652-657. (Pubitemid 350236805)
59. Germain RN,. Special regulatory T-cell review: a rose by any other name: from suppressor T cells to Tregs, approbation to unbridled enthusiasm. Immunology 2008; 123: 20-27. (Pubitemid 350256015)
60. Korn T, Anderson AC, Bettelli E, et al., The dynamics of effector T cells and Foxp3+ regulatory T cells in the promotion and regulation of autoimmune encephalomyelitis. J Neuroimmunol 2007; 191: 51-60. (Pubitemid 350060999)
61. Afzali B, Lombardi G, Lechler RI, et al., The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin Exp Immunol 2007; 148: 32-46. (Pubitemid 46365005)
62. Haxhinasto S, Mathis D, Benoist C,. The AKT-mTOR axis regulates de novo differentiation of CD4+Foxp3+ cells. J Exp Med 2008; 205: 565-574. (Pubitemid 351439304)
63. Du J, Huang C, Zhou B, et al., Isoform-specific inhibition of ROR{alpha}-mediated transcriptional activation by human FOXP3. J Immunol 2008; 180: 4785-4792.
64. Lardone PJ, Carrillo-Vico A, Molinero P, et al., A novel interplay between membrane and nuclear melatonin receptors in human lymphocytes: significance in IL-2 production. Cell Mol Life Sci 2009; 66: 516-525.
65. Carrillo-Vico A, Garcia-Maurino S, Calvo JR, et al., Melatonin counteracts the inhibitory effect of PGE2 on IL-2 production in human lymphocytes via its mt1 membrane receptor. FASEB J 2003; 17: 755-757.