Overexpression of GILZ in macrophages limits systemic inflammation while increasing bacterial clearance in sepsis in mice.
Animals
Anti-Inflammatory Agents
/ metabolism
Bacterial Load
Cells, Cultured
Cytokines
/ metabolism
Disease Models, Animal
Gene Expression Regulation
Glucocorticoids
/ metabolism
Humans
Immunity, Innate
Immunomodulation
Inflammation
/ metabolism
Inflammation Mediators
/ metabolism
Macrophages
/ immunology
Mice
Mice, Transgenic
Monocytes
/ immunology
Sepsis
/ metabolism
Transcription Factors
/ genetics
GILZ
inflammation
monocytes/macrophages
phagocytosis
sepsis
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
27
06
2019
revised:
06
11
2019
accepted:
12
12
2019
pubmed:
17
12
2019
medline:
11
8
2020
entrez:
17
12
2019
Statut:
ppublish
Résumé
Studies support the beneficial effects of glucocorticoids (GCs) during septic shock, steering research toward the potential role of GC-induced proteins in controlling excessive inflammatory responses. GILZ is a glucocorticoid-induced protein involved in the anti-inflammatory effects of GCs. We investigated whether the overexpression of GILZ specifically limited to monocytes and macrophages (M/M) alone could control inflammation, thus improving the outcome of septic shock in animal models. We also monitored the expression of GILZ in M/M from septic mice and septic-shock patients. M/M from patients and septic mice displayed significantly lower expression of GILZ than those isolated from controls. Furthermore, transgenic mice (Tg-mice) experiencing sepsis, with increased expression of GILZ restricted to M/M, showed lower frequencies of inflammatory monocytes than their littermates and lower plasma levels of inflammatory cytokines. Tg-mice also had lower blood bacterial counts. We further established that the upregulation of GILZ in M/M enhanced their phagocytic capacity in in vivo assays. The increase of GILZ in M/M was also sufficient to improve the survival rates of septic mice. These results provide evidence for a central role of both GILZ and M/M in the pathophysiology of septic shock and a possible clue for the modulation of inflammation in this disease.
Identifiants
pubmed: 31840802
doi: 10.1002/eji.201948278
doi:
Substances chimiques
Anti-Inflammatory Agents
0
Cytokines
0
Glucocorticoids
0
Inflammation Mediators
0
TSC22D3 protein, human
0
Transcription Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
589-602Subventions
Organisme : Vaccine Research Institute
ID : ANR-10-LABX-77
Pays : International
Organisme : Université Paris Sud
Pays : International
Organisme : Ecole Doctorale Sciences de la Vie et de la Santé
Pays : International
Organisme : Institut National de la Santé et de la Recherche Médicale
Pays : International
Organisme : Université Paris-Est Créteil
Pays : International
Informations de copyright
© 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Annane, D., Bellissant, E. and Cavaillon, J. M., Septic shock. Lancet 2005. 365: 63-78.
Angus, D. C. and van der Poll, T., Severe sepsis and septic shock. N. Engl. J. Med. 2013. 369: 2063.
Annane, D. and Sharshar, T., Cognitive decline after sepsis. Lancet. Respir. Med. 2015. 3: 61-69.
Rhodes, A., Evans, L. E., Alhazzani, W., Levy, M. M., Antonelli, M., Ferrer, R., Kumar, A. et al., Surviving sepsis campaign: international guidelines for management of sepsis and septic shock: 2016. Intensive Care Med. 2017. 43: 304-377.
Levy, M. M., Artigas, A., Phillips, G. S., Rhodes, A., Beale, R., Osborn, T., Vincent, J. L. et al., Outcomes of the Surviving Sepsis Campaign in intensive care units in the USA and Europe: a prospective cohort study. Lancet Infect. Dis. 2012. 12: 919-924.
Annane, D., Renault, A., Brun-Buisson, C., Megarbane, B., Quenot, J. P., Siami, S., Cariou, A. et al., Hydrocortisone plus fludrocortisone for adults with septic shock. N. Engl. J. Med. 2018. 378: 809-818.
Ayroldi, E. and Riccardi, C., Glucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action. FASEB J. 2009. 23: 3649-3658.
Cannarile, L., Zollo, O., D'Adamio, F., Ayroldi, E., Marchetti, C., Tabilio, A., Bruscoli, S. et al., Cloning, chromosomal assignment and tissue distribution of human GILZ, a glucocorticoid hormone-induced gene. Cell Death Differ. 2001. 8: 201-203.
Berrebi, D., Bruscoli, S., Cohen, N., Foussat, A., Migliorati, G., Bouchet-Delbos, L., Maillot, M. C. et al., Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 2003. 101: 729-738.
Espinasse, M. A., Hajage, D., Montravers, P., Piednoir, P., Dufour, G., Tubach, F., Granger, V. et al., Neutrophil expression of glucocorticoid-induced leucine zipper (GILZ) anti-inflammatory protein is associated with acute respiratory distress syndrome severity. Ann. Intensive Care 2016. 6: 105.
Espinasse, M. A., Pepin, A., Virault-Rocroy, P., Szely, N., Chollet-Martin, S., Pallardy, M. and Biola-Vidamment, A., Glucocorticoid-induced leucine zipper is expressed in human neutrophils and promotes apoptosis through Mcl-1 down-regulation. J. Innate. Immun. 2016. 8: 81-96.
Ayroldi, E., Migliorati, G., Bruscoli, S., Marchetti, C., Zollo, O., Cannarile, L., D'Adamio, F. et al., Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kappaB. Blood 2001. 98: 743-753.
Hamdi, H., Godot, V., Maillot, M. C., Prejean, M. V., Cohen, N., Krzysiek, R., Lemoine, F. M. et al., Induction of antigen-specific regulatory T lymphocytes by human dendritic cells expressing the glucocorticoid-induced leucine zipper. Blood 2007. 110: 211-219.
Karaki, S., Garcia, G., Tcherakian, C., Capel, F., Tran, T., Pallardy, M., Humbert, M. et al., Enhanced glucocorticoid-induced leucine zipper in dendritic cells induces allergen-specific regulatory CD4(+) T-cells in respiratory allergies. Allergy 2014. 69: 624-631.
Godot, V., Garcia, G., Capel, F., Arock, M., Durand-Gasselin, I., Asselin-Labat, M. L., Emilie, D. et al., Dexamethasone and IL-10 stimulate glucocorticoid-induced leucine zipper synthesis by human mast cells. Allergy 2006. 61: 886-890.
Cheng, Q., Fan, H., Ngo, D., Beaulieu, E., Leung, P., Lo, C. Y., Burgess, R. et al., GILZ overexpression inhibits endothelial cell adhesive function through regulation of NF-kappaB and MAPK activity. J. Immunol. 2013. 191: 424-433.
Wang, Y., Lu, Y., Yu, D., Wang, Y., Chen, F., Yang, H. and Zheng, S. J., Enhanced resistance of restraint-stressed mice to sepsis. J. Immunol. 2008. 181: 3441-3448.
Bereshchenko, O., Coppo, M., Bruscoli, S., Biagioli, M., Cimino, M., Frammartino, T., Sorcini, D. et al., GILZ promotes production of peripherally induced Treg cells and mediates the crosstalk between glucocorticoids and TGF-beta signaling. Cell Rep. 2014. 7: 464-475.
Calmette, J., Ellouze, M., Tran, T., Karaki, S., Ronin, E., Capel, F., Pallardy, M. et al., Glucocorticoid-induced leucine zipper enhanced expression in dendritic cells is sufficient to drive regulatory T cells expansion in vivo. J. Immunol. 2014. 193: 5863-5872.
Ballegeer, M., Vandewalle, J., Eggermont, M., Van Isterdael, G., Dejager, L., De Bus, L., Decruyenaere, J. et al., Overexpression of gilz protects mice against lethal septic peritonitis. Shock 2018.
Pinheiro, I., Dejager, L., Petta, I., Vandevyver, S., Puimege, L., Mahieu, T., Ballegeer, M. et al., LPS resistance of SPRET/Ei mice is mediated by gilz, encoded by the Tsc22d3 gene on the X chromosome. EMBO Mol. Med. 2013. 5: 456-470.
Bruscoli, S., Donato, V., Velardi, E., Di Sante, M., Migliorati, G., Donato, R. and Riccardi, C., Glucocorticoid-induced leucine zipper (GILZ) and long GILZ inhibit myogenic differentiation and mediate anti-myogenic effects of glucocorticoids. J. Biol. Chem. 2010. 285: 10385-10396.
Xiong, J., Xu, L., Qu, W. M., Li, Z. L., Shang, Z. H., Li, Y. H., Yang, S. H. et al., Roles of GILZ in protein metabolism of L6 muscle cells exposed to serum from septic rats. Genet. Mol. Res. 2014. 13: 8209-8219.
Shi, X., Shi, W., Li, Q., Song, B., Wan, M., Bai, S. and Cao, X., A glucocorticoid-induced leucine-zipper protein, GILZ, inhibits adipogenesis of mesenchymal cells. EMBO Rep. 2003. 4: 374-380.
Zhang, W., Yang, N. and Shi, X. M., Regulation of mesenchymal stem cell osteogenic differentiation by glucocorticoid-induced leucine zipper (GILZ). J. Biol. Chem. 2008. 283: 4723-4729.
Pan, G., Cao, J., Yang, N., Ding, K., Fan, C., Xiong, W. C., Hamrick, M. et al., Role of glucocorticoid-induced leucine zipper (GILZ) in bone acquisition. J. Biol. Chem. 2014. 289: 19373-19382.
Ghosn, E. E., Cassado, A. A., Govoni, G. R., Fukuhara, T., Yang, Y., Monack, D. M., Bortoluci, K. R. et al., Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. U. S. A. 2010. 107: 2568-2573.
Robert, O., Boujedidi, H., Bigorgne, A., Ferrere, G., Voican, C. S., Vettorazzi, S., Tuckermann, J. P. et al., Decreased expression of the glucocorticoid receptor-GILZ pathway in Kupffer cells promotes liver inflammation in obese mice. J. Hepatol. 2016. 64: 916-924.
Hoppstadter, J., Kessler, S. M., Bruscoli, S., Huwer, H., Riccardi, C. and Kiemer, A. K., Glucocorticoid-induced leucine zipper: a critical factor in macrophage endotoxin tolerance. J. Immunol. 2015. 194: 6057-6067.
Beaulieu, E., Ngo, D., Santos, L., Yang, Y. H., Smith, M., Jorgensen, C., Escriou, V. et al., Glucocorticoid-induced leucine zipper is an endogenous antiinflammatory mediator in arthritis. Arthritis Rheum. 2010. 62: 2651-2661.
Yang, Y. H., Aeberli, D., Dacumos, A., Xue, J. R. and Morand, E. F., Annexin-1 regulates macrophage IL-6 and TNF via glucocorticoid-induced leucine zipper. J. Immunol. 2009. 183: 1435-1445.
Chignard, M. and Balloy, V., Neutrophil recruitment and increased permeability during acute lung injury induced by lipopolysaccharide. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000. 279: L1083-1090.
O'Connell, P. A., Surette, A. P., Liwski, R. S., Svenningsson, P. and Waisman, D. M., S100A10 regulates plasminogen-dependent macrophage invasion. Blood 2010. 116: 1136-1146.
Biswas, S. K. and Lopez-Collazo, E., Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 2009. 30: 475-487.
Pepin, A., Biola-Vidamment, A., Latre de Late, P., Espinasse, M. A., Godot, V. and Pallardy, M., [TSC-22D proteins: new regulators of cell homeostasis?]. Med. Sci. (Paris) 2015. 31: 75-83.
Hoppstadter, J., Diesel, B., Eifler, L. K., Schmid, T., Brune, B. and Kiemer, A. K., Glucocorticoid-induced leucine zipper is downregulated in human alveolar macrophages upon Toll-like receptor activation. Eur. J. Immunol. 2012. 42: 1282-1293.
Hoppstadter, J., Diesel, B., Linnenberger, R., Hachenthal, N., Flamini, S., Minet, M., Leidinger, P. et al., Amplified host defense by toll-like receptor-mediated downregulation of the glucocorticoid-induced leucine zipper (GILZ) in macrophages. Front. Immunol. 2018. 9: 3111.
Calmette, J., Bertrand, M., Vetillard, M., Ellouze, M., Flint, S., Nicolas, V., Biola-Vidamment, A. et al., Glucocorticoid-induced leucine zipper protein controls macropinocytosis in dendritic cells. J. Immunol. 2016. 197: 4247-4256.
Ricci, E., Ronchetti, S., Gabrielli, E., Pericolini, E., Gentili, M., Roselletti, E., Vecchiarelli, A. et al., GILZ restrains neutrophil activation by inhibiting the MAPK pathway. J. Leukoc. Biol. 2019. 105: 187-194.
Rittirsch, D., Huber-Lang, M. S., Flierl, M. A. and Ward, P. A., Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 2009. 4: 31-36.
Yang, N., Zhang, W. and Shi, X. M., Glucocorticoid-induced leucine zipper (GILZ) mediates glucocorticoid action and inhibits inflammatory cytokine-induced COX-2 expression. J. Cell. Biochem. 2008. 103: 1760-1771.
Katsenos, C. S., Antonopoulou, A. N., Apostolidou, E. N., Ioakeimidou, A., Kalpakou, G. T., Papanikolaou, M. N., Pistiki, A. C. et al., Early administration of hydrocortisone replacement after the advent of septic shock: impact on survival and immune response*. Crit. Care Med. 2014. 42: 1651-1657.
McCubbrey, A. L., Allison, K. C., Lee-Sherick, A. B., Jakubzick, C. V. and Janssen, W. J., Promoter Specificity and Efficacy in Conditional and Inducible Transgenic Targeting of Lung Macrophages. Front. Immunol. 2017. 8: 1618.
Ray, A. and Dittel, B. N., Isolation of mouse peritoneal cavity cells. J. Vis. Exp. 2010. 1488
Campeau, E., Ruhl, V. E., Rodier, F., Smith, C. L., Rahmberg, B. L., Fuss, J. O., Campisi, J. et al., A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009. 4: e6529.
Dahdah, A., Gautier, G., Attout, T., Fiore, F., Lebourdais, E., Msallam, R., Daeron, M. et al., Mast cells aggravate sepsis by inhibiting peritoneal macrophage phagocytosis. J. Clin. Invest. 2014. 124: 4577-4589.
Toscano, M. G., Ganea, D. and Gamero, A. M., Cecal ligation puncture procedure. J. Vis. Exp. 2011. 2860.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S., Agace, W. W. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.