Impact of melatonin receptor deletion on intracellular signaling in spleen cells of mice after polymicrobial sepsis

Inflammation Research

Volumn 63, Issue 12, 2014, Pages 1023-1033

  Kleber, Astrid ^a   Altmeyer, Sarah ^a   Wolf, Beate ^a   Wolf, Alexander ^a   Volk, Thomas ^a   Fink, Tobias ^a   Kubulus, Darius ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

ERK1 2; JNK; Melatonin; p38; Sepsis; Splenocyte

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CXCL2 CHEMOKINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 2; L SELECTIN; MELATONIN; MELATONIN RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR; MELATONIN 1 RECEPTOR; MELATONIN 2 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PRIMER DNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BINDING SITE; CECUM LIGATION AND INCISION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EX VIVO STUDY; FEMALE; INTESTINE SURGERY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; LEUKOCYTE COUNT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SEPSIS; SHAM PROCEDURE; SPLEEN CELL; WILD TYPE; ANIMAL; C3H MOUSE; CHEMISTRY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; IMMUNE SYSTEM; INFLAMMATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPLEEN;

ANIMALS; BASE SEQUENCE; BINDING SITES; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; IMMUNE SYSTEM; INFLAMMATION; LEUKOCYTE COUNT; MELATONIN; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RECEPTOR, MELATONIN, MT1; RECEPTOR, MELATONIN, MT2; SEPSIS; SIGNAL TRANSDUCTION; SPLEEN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84911380198     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-014-0779-4     Document Type: Article

References (48)

1. Machado FR, Mazza BF. Improving mortality in sepsis: analysis of clinical trials. Shock. 2010;34(Suppl 1):54–8. doi:10.1097/SHK.0b013e3181e7e8b4.
2. Carrillo-Vico A, Lardone PJ, Naji L, Fernandez-Santos JM, Martin-Lacave I, Guerrero JM, Calvo JR. 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;39:400–8. doi:10.1111/j.1600-079X.2005.00265.x.
3. Fink T, Glas M, Wolf A, Kleber A, Reus E, Wolff M, Kiefer D, Wolf B, Rensing H, Volk T, Mathes AM. Melatonin receptors mediate improvements of survival in a model of polymicrobial sepsis. Crit Care Med. 2014;42(1):e22–31.
4. Wu JY, Tsou MY, Chen TH, Chen SJ, Tsao CM, Wu CC. Therapeutic effects of melatonin on peritonitis-induced septic shock with multiple organ dysfunction syndrome in rats. J Pineal Res. 2008;45:106–16. doi:10.1111/j.1600-079X.2008.00567.x.
5. Galano A, Tan DX, Reiter RJ. On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J Pineal Res. 2013;54:245–57. doi:10.1111/jpi.12010.
6. Mathes AM. Hepatoprotective actions of melatonin: possible mediation by melatonin receptors. World J Gastroenterol. 2010;16:6087–97.
7. Carrillo-Vico A, Garcia-Perganeda A, Naji L, Calvo JR, Romero MP, Guerrero JM. Expression of membrane and nuclear melatonin receptor mRNA and protein in the mouse immune system. Cell Mol Life Sci. 2003;60:2272–8. doi:10.1007/s00018-003-3207-4.
8. Ishii H, Tanaka N, Kobayashi M, Kato M, Sakuma Y. Gene structures, biochemical characterization and distribution of rat melatonin receptors. J Physiol Sci. 2009;59:37–47. doi:10.1007/s12576-008-0003-9.
9. Pozo D, Delgado M, Fernandez-Santos JM, Calvo JR, Gomariz RP, Martin-Lacave I, Ortiz GG, Guerrero JM. Expression of the Mel1a-melatonin receptor mRNA in T and B subsets of lymphocytes from rat thymus and spleen. FASEB J. 1997;11:466–73.
10. Drazen DL, Bilu D, Bilbo SD, Nelson RJ. Melatonin enhancement of splenocyte proliferation is attenuated by luzindole, a melatonin receptor antagonist. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1476–82.
11. Wei W, Shen YX, Dai M, Chen Q. Effects and mechanisms of melatonin on immune responses in mice of different months. Acta Pharmacol Sin. 2003;24:719–23.
12. Sze SF, Liu WK, Ng TB. Stimulation of murine splenocytes by melatonin and methoxytryptamine. J Neural Transm Gen Sect. 1993;94:115–26.
13. Calvo JR, Gonzalez-Yanes C, Maldonado MD. The role of melatonin in the cells of the innate immunity: a review. J Pineal Res. 2013;55:103–20. doi:10.1111/jpi.12075.
14. Jockers R, Maurice P, Boutin JA, Delagrange P. Melatonin receptors, heterodimerization, signal transduction and binding sites: what’s new? Br J Pharmacol. 2008;154:1182–95. doi:10.1038/bjp.2008.184.
15. Caligioni CS. Assessing reproductive status/stages in mice. Curr Protoc Neurosci. 2009; Appendix 4:Appendix. doi:10.1002/0471142301.nsa04is48.
16. Scheiermann P, Hoegl S, Revermann M, Ahluwalia D, Zander J, Boost KA, Nguyen T, Zwissler B, Muhl H, Hofstetter C. Cecal ligation and incision: an acute onset model of severe sepsis in rats. J Surg Res. 2009;151:132–7. doi:10.1016/j.jss.2008.02.032.
17. Guescini M, Sisti D, Rocchi MB, Stocchi L, Stocchi V. A new real-time PCR method to overcome significant quantitative inaccuracy due to slight amplification inhibition. BMC Bioinform. 2008;9:326. doi:10.1186/1471-2105-9-326.
18. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods. 2001;25:402–8. doi:10.1006/meth.2001.1262.
19. 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;72:248–54.
20. Redl H, Schlag G, Bahrami S, Schade U, Ceska M, Stutz P. Plasma neutrophil-activating peptide-1/interleukin-8 and neutrophil elastase in a primate bacteremia model. J Infect Dis. 1991;164:383–8.
21. van der Poll T, Coyle SM, Levi M, Jansen PM, Dentener M, Barbosa K, Buurman WA, Hack CE, ten Cate JW, Agosti JM, Lowry SF. Effect of a recombinant dimeric tumor necrosis factor receptor on inflammatory responses to intravenous endotoxin in normal humans. Blood. 1997;89:3727–34.
22. Hegde A, Uttamchandani M, Moochhala SM, Bhatia M. Plasma cytokine profiles in preprotachykinin-A knockout mice subjected to polymicrobial sepsis. Mol Med. 2010;16:45–52. doi:10.2119/molmed.2009.00112.
23. Walley KR, Lukacs NW, Standiford TJ, Strieter RM, Kunkel SL. Balance of inflammatory cytokines related to severity and mortality of murine sepsis. Infect Immun. 1996;64:4733–8.
24. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612–6. doi:10.1126/science.1175202.
25. Morgan TL, Tomich EB. Overwhelming post-splenectomy infection (OPSI): a case report and review of the literature. J Emerg Med. 2012;43:758–63. doi:10.1016/j.jemermed.2011.10.029.
26. Huston JM. The vagus nerve and the inflammatory reflex: wandering on a new treatment paradigm for systemic inflammation and sepsis. Surg Infect (Larchmt). 2012;13:187–93. doi:10.1089/sur.2012.126.
27. Bazwinsky-Wutschke I, Bieseke L, Muhlbauer E, Peschke E. Influence of melatonin receptor signalling on parameters involved in blood glucose regulation. J Pineal Res. 2014;56:82–96. doi:10.1111/jpi.12100.
28. Zetterqvist AV, Berglund LM, Blanco F, Garcia-Vaz E, Wigren M, Duner P, Andersson AM, To F, Spegel P, Nilsson J, Bengtsson E, Gomez MF. Inhibition of nuclear factor of activated T-cells (NFAT) suppresses accelerated atherosclerosis in diabetic mice. PLoS One. 2013;8:e65020. doi:10.1371/journal.pone.0065020.
29. Sasaki M, Jordan P, Joh T, Itoh M, Jenkins M, Pavlick K, Minagar A, Alexander SJ. Melatonin reduces TNF-a induced expression of MAdCAM-1 via inhibition of NF-kappaB. BMC Gastroenterol. 2002;2:9.
30. Whitmarsh AJ. A central role for p38 MAPK in the early transcriptional response to stress. BMC Biol. 2010;8:47. doi:10.1186/1741-7007-8-47.
31. Chen J, Liao MY, Gao XL, Zhong Q, Tang TT, Yu X, Liao YH, Cheng X. IL-17A induces pro-inflammatory cytokines production in macrophages via MAPkinases, NF-kappaB and AP-1. Cell Physiol Biochem. 2013;32:1265–74. doi:10.1159/000354525.
32. Chow JY, Wong CK, Cheung PF, Lam CW. Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: implications for allergic inflammation. Cell Mol Immunol. 2010;7:26–34. doi:10.1038/cmi.2009.106.
33. Kawamura H, Kawamura T, Kanda Y, Kobayashi T, Abo T. Extracellular ATP-stimulated macrophages produce macrophage inflammatory protein-2 which is important for neutrophil migration. Immunology. 2012;136:448–58. doi:10.1111/j.1365-2567.2012.03601.x.
34. Zumwalde NA, Domae E, Mescher MF, Shimizu Y. ICAM-1-dependent homotypic aggregates regulate CD8 T cell effector function and differentiation during T cell activation. J Immunol. 2013;191:3681–93. doi:10.4049/jimmunol.1201954.
35. Kesteman N, Vansanten G, Pajak B, Goyert SM, Moser M. Injection of lipopolysaccharide induces the migration of splenic neutrophils to the T cell area of the white pulp: role of CD14 and CXC chemokines. J Leukoc Biol. 2008;83:640–7. doi:10.1189/jlb.0807578.
36. Ahmad R, Haldar C, Gupta S. Melatonin membrane receptor type MT1 modulates cell-mediated immunity in the seasonally breeding tropical rodent Funambuluspennanti. Neuroimmunomodulation. 2012;19:50–9. doi:10.1159/000327293.
37. Garcia-Maurino S, Gonzalez-Haba MG, Calvo JR, Goberna R, Guerrero JM. 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 S0165-5728(98)00179-9.
38. Guerrero JM, Pozo D, Garcia-Maurino S, Osuna C, Molinero P, Calvo JR. Involvement of nuclear receptors in the enhanced IL-2 production by melatonin in Jurkat cells. Ann N Y Acad Sci. 2000;917:397–403.
39. Slominski RM, Reiter RJ, Schlabritz-Loutsevitch N, Ostrom RS, Slominski AT. Melatonin membrane receptors in peripheral tissues: distribution and functions. Mol Cell Endocrinol. 2012;351:152–66. doi:10.1016/j.mce.2012.01.004.
40. Wang M, Wang H, Tang Y, Kang D, Gao Y, Ke M, Dou J, Xi T, Zhou C. Effective inhibition of a Strongylocentrotus nudus eggs polysaccharide against hepatocellular carcinoma is mediated via immunoregulation in vivo. Immunol Lett. 2011;141:74–82. doi:10.1016/j.imlet.2011.08.001.
41. Budai MM, Varga A, Milesz S, Tozser J, Benko S. Aloe vera downregulates LPS-induced inflammatory cytokine production and expression of NLRP3 inflammasome in human macrophages. Mol Immunol. 2013;56:471–9. doi:10.1016/j.molimm.2013.05.005.
42. Hsu HY, Wen MH. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem. 2002;277:22131–9. doi:10.1074/jbc.M111883200.
43. Luchetti F, Canonico B, Betti M, Arcangeletti M, Pilolli F, Piroddi M, Canesi L, Papa S, Galli F. Melatonin signaling and cell protection function. FASEB J. 2010;24:3603–24. doi:10.1096/fj.10-154450.
44. Gerdin MJ, Masana MI, Rivera-Bermudez MA, Hudson RL, Earnest DJ, Gillette MU, Dubocovich ML. Melatonin desensitizes endogenous MT2 melatonin receptors in the rat suprachiasmatic nucleus: relevance for defining the periods of sensitivity of the mammalian circadian clock to melatonin. FASEB J. 2004;18:1646–56.
45. Kennaway DJ, Voultsios A, Varcoe TJ, Moyer RW. Melatonin in mice: rhythms, response to light, adrenergic stimulation, and metabolism. Am J Physiol Regul Integr Comp Physiol. 2002;282:R358–65.
46. Rousseau A, Petren S, Plannthin J, Eklundh T, Nordin C. Serum and cerebrospinal fluid concentrations of melatonin: a pilot study in healthy male volunteers. J Neural Transm. 1999;106:883–8.
47. Imbesi M, Uz T, Dzitoyeva S, Giusti P, Manev H. Melatonin signaling in mouse cerebellar granule cells with variable native MT1 and MT2 melatonin receptors. Brain Res. 2008;1227:19–25. doi:10.1016/j.brainres.2008.06.082.
48. Chan AS, Lai FP, Lo RK, Voyno-Yasenetskaya TA, Stanbridge EJ, Wong YH. Melatonin mt1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins. Cell Signal. 2002;14:249–57.