Molecules Altering the Intracellular Thiol Content Modulate NF-kB and STAT-1/IRF-1 Signalling Pathways and IL-12 p40 and IL-27 p28 Production in Murine Macrophages

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Fraternale, Alessandra ^a   Crinelli, Rita ^a   Casabianca, Anna ^a   Paoletti, Maria Filomena ^a   Orlandi, Chiara ^a   Carloni, Elisa ^a   Smietana, Michaël ^b   Palamara, Anna Teresa ^c,d   Magnani, Mauro ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; GLUTATHIONE; GLUTATHIONE C4; I 152; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOMODULATING AGENT; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 12P40; INTERLEUKIN 27; INTERLEUKIN 27P28; STAT1 PROTEIN; THIOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; IMMUNOMODULATION; MACROPHAGE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ANIMALS; CELL LINE; CYSTEAMINE; ENZYME ACTIVATION; FEMALE; GLUTATHIONE; INTERFERON REGULATORY FACTOR-1; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-27; MACROPHAGES; MICE; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; SULFHYDRYL COMPOUNDS;

EID: 84874881483     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057866     Document Type: Article

References (51)

1. Short S, Merkel BJ, Caffrey R, McCoy KL, (1996) Defective antigen processing correlates with a low level of intracellular glutathione. Eur J Immunol 26: 3015-3020.
2. Weiskopf D, Schwanninger A, Weinberger B, Almanzar G, Parson W, et al. (2010) Oxidative stress can alter the antigenicity of immunodominant peptides. J Leuk Biol 87: 1-8.
3. Preynat-Seauve O, Coudurier S, Favier A, Marche PN, Villiers C, (2003) Oxidative stress impairs intracellular events involved in antigen processing and presentation to T cells. Cell stress & Chaperones 8: 162-171.
4. Koike Y, Hisada T, Utsugi M, Ishizuka T, Shimizu Y, et al. (2007) Glutathione redox regulates airway hyperresponsiveness and airway inflammation in mice. Am J Respir Cell Mol Biol 37: 322-329.
5. Murata Y, Shimamura T, Hamuro J, (2002) The polarization of T(h)1 T(h)2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int Immunol 14: 201-212.
6. Murata Y, Amao M, Yoneda J, Hamuro J, (2001) Intracellular thiol redox status of macrophages directs the Th1 skewing in thioredoxin transgenic mice during aging. Molec Immunol 38: 747-757.
7. Dobashi K, Ahiara M, Araki T, Shimizu Y, Utsugi M, et al. (2001) Regulation of LPS induced IL-12 production by IFN-γ and IL-4 through intracellular glutathione status in human alveolar macrophages. Clin Exp Immunol 124: 290-296.
8. Kamide Y, Utsugi M, Dobashi K, Ono A, Ishizuka T, et al. (2011) Intracellular glutathione redox status in human dendritic cells regulates IL-27 production and T-cell polarization. Allergy 66: 1183-1192.
9. Murphy KM, Reiner SL, (2002) The lineage decisions of helper T cells. Nat Rev Immunol 2: 933-944.
10. Trinchieri G, (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3: 133-146.
11. Utsugi M, Dobashi K, Koga Y, Shimizu Y, Ishizuka T, et al. (2002) Glutathione redox regulates lipopolysaccharide-induced IL-12 production through p38 mitogen-activated protein kinase activation in human monocytes: role of glutathione redox in IFN-γ priming of IL-12 production. J Leuk Biol 71: 339-347.
12. Alam K, Ghousunnissa S, Nair S, Valluri VL, Mukhopadhyay S, (2010) Glutathione-redox balance regulates c-rel-driven IL-12 production in macrophages: possible implications in antituberculosis immunotherapy. J Immunol 184: 339-347.
13. Aihara M, Dobashi K, Akiyama M, Naruse I, Nakazawa T, et al. (2000) Effects of N-acetylcysteine and ambroxol on the production of IL-12 and IL-10 in human alveolar macrophages. Respiration 67: 662-671.
14. Pflanz S, Timans JC, Cheung J, Rosales R, Kanzler H, et al. (2002) IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naïve CD(+) T cells. Immunity 16: 779-790.
15. Batten M, Ghilardi N, (2007) The biology and therapeutic potential of interleukin 27. J Biol Med 85: 661-672.
16. Fraternale A, Paoletti MF, Dominici S, Caputo A, Castaldello A, et al. (2010) The increase in intra-macrophage thiols induced by new pro-GSH molecules directs the Th1 skewing in ovalbumin immunized mice. Vaccine 28: 7676-7682.
17. Fraternale A, Paoletti MF, Dominici S, Buondelmonte C, Caputo A, et al. (2011) Modulation of Th1/Th2 immune responses to HIV-1 Tat by new pro-GSH molecules. Vaccine 29: 6823-6829.
18. Palamara AT, Brandi G, Rossi L, Millo E, Benatti U, et al. (2004) New synthetic glutathione derivatives with increased antiviral activities. Antivir Chem Chemother 15: 83-91.
19. Sgarbanti R, Nencioni L, Amatore D, Coluccio P, Fraternale A, et al. (2011) Redox regulation of the influenza hemagglutinin maturation process: a new cell-mediated strategy for anti-influenza therapy. Antioxid Redox Signal 15: 593-606.
20. Oiry J, Mialocq P, Puy JY, Fretier P, Dereuddre-Bosquet N, et al. (2004) Synthesis and biological evaluation in human monocyte-derived macrophages of N-(N-acetyl-l-cysteinyl)-S-acetylcysteamine analogues with potent antioxidant and anti-HIV activities. J Med Chem 47: 1789-1795.
21. Fraternale A, Paoletti MF, Casabianca A, Orlandi C, Schiavano GF, et al. (2008) Inhibition of murine AIDS by pro-glutathione (GSH) molecules. Antiviral Res 77: 120-127.
22. Gubler U, Chua A, Schoenhaut D, Dwyer C, McComas W, et al. (1991) Co-expression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. USA 88: 4143-4147.
23. Takeda A, Hamnao S, Yamanaka A, Hanada T, Ishibashi T, et al. (2003) Cutting edge: role of IL-27/WSX-1 signalling for induction of T-bet through activation of STAT1 during initial Th1 commitment. J Immunol 170: 4886-4890.
24. Artis D, Johnson LM, Joyce K, Saris C, Villarino A, et al. (2004) Cutting edge: early IL-4 production governs the requirement for IL-27-WSX-1 signalling in the development of protective Th1 cytokine responses following Leishmania major infection. Immunol 172: 4672-4675.
25. Murphy TL, Cleveland MG, Kulesza P, Magram J, Murphy KM, (1995) Regulation of interleukin 12 p40 expression through an NF-kB half-site. Mol Cell Biol 17: 5258-5267.
26. Beg AA, Baldwin AS, (1993) The I kappa B proteins: Multifunctional regulators of Rel/NF-kappa transcription factors. Genes Dev 7: 2064-2070.
27. Ghosh S, May MJ, Kopp EB, (1998) NF-kB and Rel proteins: Evolutionary conserved mediators of immune response. Annu Rev Immunol 16: 225-260.
28. Hayden MS, Ghosh S, (2004) Signalling to NF-kB. Genes Dev 18: 2195-2224.
29. Liu J, Guan X, Ma X, (2007) Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-γ-mediated pathways. J Exp Med 204: 141-152.
30. Zhang J, Qian X, Ning H, Yang J, Xiong H, et al. (2010) Activation of IL-27 p28 gene transcription by interferon regulatory factor 8 in cooperation with interferon regulatory factor 1. J Biol Chem 285: 21269-21281.
31. Chatterjee-Kishore M, Kishore R, Hicklin DJ, Marincola FM, Ferrone S, (1998) Different requirements for signal transducer and activator of transcription 1α and interferon regulatory factor 1 in the regulation of low molecular mass polypeptide 2 and transporter associated with antigen processing 1 gene expression. J Biol Chem 273: 16177-16183.
32. Harada H, Takahashi E-I, Itoh S, Harada K, Hori T-A, et al. (1994) Structure and regulation of the human interferon regulatory factor 1 (IRF-1) and IRF-2 genes: implications for a gene network in the interferon system. Mol Cell Biol 14: 1500-1509.
33. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Thierfelder WE, et al. (1994) Signalling by the cytokine receptor superfamily: JAKs and STATs. Trends Biochem Sci 19: 222-227.
34. Oiry J, Mialocq P, Puy JY, Fretier P, Clayette P, et al. (2001) NAC/MEA coniugate: a new potent antioxidant which increases the GSH level in various cell lines. Bioorg Med Chem Lett 11: 1189-1191.
35. Tietze F, (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27: 502-522.
36. Beutler E (1984) Reduced glutathione (GSH). In: Red cell metabolism. A manual of biochemical methods. New York, USA Press. 131-133.
37. Sen CK, Packer L, (1996) Antioxidant and redox regulation of gene transcription. The FASEB J 10: 709-718.
38. Hayashi T, Ueno Y, Okamoto T, (1993) Oxidoreductive regulation of nuclear factor k B. Involvement of a cellular reducing catalyst thioredoxin. J Biol Chem 268: 11380-11388.
39. Toledano MB, Ghosh D, Trinh F, Leonard WJ, (1993) N-terminal DNA-binding domains contribute to differential DNA binding specificities of NFkB p50 and p65. Mol Cell Biol 13: 852-860.
40. Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, et al. (2006) Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 103: 13086-13091.
41. Kil IS, Kim SY, Park J-W, (2008) Glutathionylation regulates IkB. Biochem Biophys Res Comm 373: 169-173.
42. Seidel P, Roth M, Ge Q, Merfort I, S'ng CT, et al. (2011) IkBα glutathionylation and reduced histone H3 phosphorylation inhibit eotaxin and RANTES. Eur Respir J 38: 1444-1452.
43. Lou H, Kaplowitz N, (2007) Glutathione depletion down-regulates tumor necrosis factor (TNF) α-induced NF-kB activity via IkB kinase (IKK)-dependent and -independent mechanisms. J Biol Chem 282: 29470-29481.
44. Li YQ, Zhang ZX, Xu YJ, Ni W, Chen SX, et al. (2006) N-acetyl-L-cysteine and pyrrolidine dithiocarbamate inhibited nuclear factor-kappa B activation in alveolar macrophages by different mechanisms. Acta Pharmacol Sin 27: 339-346.
45. Smith JK, Patil CN, Patlolla S, Gunter BW, Booz GW, et al. (2012) Identification of a redox-sensitive switch within the JAK2 catalytic domain. Free Radic Biol Med 52: 1101-1110.
46. Salsman SJ, Hensley K, Floyd RA, (2005) Sensitivity of protein tyrosine phosphatase activity to the redox environment, cytochrome c, and microperoxidase. Antioxid Redox Signal 7: 1078-1088.
47. Dunston CR, Griffiths HR, (2010) The effect of ageing on macrophage Toll-like receptor-mediated responses in the fight against pathogens. Clin Exp Immunol 161: 407-416.
48. Frosch S, Bonifas U, Eck HP, Bockstette M, Droege W, et al. (1993) The efficient bovine insulin presentation capacity of bone marrow-derived macrophages activated by granulocyte-macrophage colony-stimulating factor correlates with a high level intracellular reducing thiols. Eur J Immunol 23: 1430-1434.
49. Ichiki H, Hoshino T, Kinoshita T, Imaoka H, Kato S, et al. (2005) Thioredoxin suppresses airway hyperresponsiveness and airway inflammation in ashma. Biochem Biophys Res Commun 334: 1141-1148.
50. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
51. Crinelli R, Carloni E, Giacomini E, Penna A, Dominici S, et al. (2012) Palytoxin and an Ostreopsis toxin extract increase the levels of mRNAs encoding inflammation-related proteins in human macrophages via p38 MAPK and NF-κB. PloS One 7: e38139.