Elevated sodium chloride drives type I interferon signaling in macrophages and increases antiviral resistance

Journal of Biological Chemistry

Volumn 293, Issue 3, 2018, Pages 1030-1039

  Zhang, Wu Chang ^a   Du, Lin Juan ^a,b   Zheng, Xiao Jun ^a,b   Chen, Xiao Qing ^a   Shi, Chaoji ^a   Chen, Bo Yan ^a   Sun, Xue Nan ^a,b   Li, Chao ^a,b   Zhang, Yu Yao ^a,b   Liu, Yan ^a   Xiao, Hui ^c   Leng, Qibin ^c   Jiang, Xinquan ^a   Zhang, Zhiyuan ^a   Sun, Shuyang ^a   Duan, Sheng Zhong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE PASTEUR OF SHANGHAI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIGITAL STORAGE; IMMUNE SYSTEM; MACROPHAGES; MAMMALS; NUCLEIC ACIDS; SODIUM CHLORIDE; VIRUSES;

ANTIVIRAL RESISTANCE; ENVIRONMENTAL FACTORS; INNATE IMMUNE RESPONSE; NUCLEIC ACID ANALOGUES; PHARMACOLOGICAL INHIBITORS; RNA INTERFERENCE; SIGNALING PATHWAYS; TYPE I INTERFERONS;

SIGNALING;

2',5' OLIGOADENYLATE SYNTHETASE; ACTIVATING TRANSCRIPTION FACTOR 2; BETA INTERFERON; BETA1 INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; SODIUM CHLORIDE; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; ANTIVIRUS AGENT; INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; BRAIN; CONTROLLED STUDY; CXCL10 GENE; CYTOKINE PRODUCTION; GENE; GENE EXPRESSION; HOST RESISTANCE; HUMAN; HUMAN CELL; IFI27 GENE; IFI44L GENE; IFIT2 GENE; IFNB1 GENE; IN VITRO STUDY; IN VIVO STUDY; IRF7 GENE; ISG15 GENE; LUNG; MACROPHAGE; MOUSE; MX2 GENE; NONHUMAN; OAS3 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SURVIVAL; UPREGULATION; VESICULAR STOMATITIS; VIRUS GENE; VIRUS LOAD; VIRUS REPLICATION; VIRUS RESISTANCE; ANIMAL; ANTIVIRAL RESISTANCE; C57BL MOUSE; DRUG EFFECT; GENETICS; INNATE IMMUNITY; KNOCKOUT MOUSE; METABOLISM; WESTERN BLOTTING;

ANIMALS; ANTIVIRAL AGENTS; BLOTTING, WESTERN; DRUG RESISTANCE, VIRAL; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

EID: 85040807307     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.805093     Document Type: Article

References (33)

1. Ivashkiv, L. B., and Donlin, L. T. (2014) Regulation of type I interferon responses. Nat. Rev. Immunol. 14, 36-49 Medline.
2. Schneider, W. M., Chevillotte, M. D., and Rice, C. M. (2014) Interferonstimulated genes: A complex web of host defenses. Annu. Rev. Immunol. 32, 513-545 CrossRef Medline.
3. Liu, S. Y., Sanchez, D. J., and Cheng, G. (2011) New developments in the induction and antiviral effectors of type I interferon. Curr. Opin. Immunol. 23, 57-64 CrossRef Medline.
4. Karupiah, G., Buller, R. M., Van Rooijen, N., Duarte, C. J., and Chen, J. (1996) Different roles for CD4+ and CD8+ T lymphocytes and macrophage subsets in the control of a generalized virus infection. J. Virol. 70, 8301-8309 Medline.
5. Züst, R., Toh, Y. X., Valdés, I., Cerny, D., Heinrich, J., Hermida, L., Marcos, E., Guillén, G., Kalinke, U., Shi, P. Y., and Fink, K. (2014) Type I interferon signals in macrophages and dendritic cells control dengue virus infection: implications for a new mouse model to test dengue vaccines. J. Virol. 88, 7276-7285 CrossRef Medline.
6. Carroll, E. C., Jin, L., Mori, A., Muñoz-Wolf, N., Oleszycka, E., Moran, H. B. T., Mansouri, S., McEntee, C. P., Lambe, E., Agger, E. M., Andersen, P., Cunningham, C., Hertzog, P., Fitzgerald, K. A., Bowie, A. G., and Lavelle, E. C. (2016) The vaccine adjuvant chitosan promotes cellular immunity via DNA sensor cGAS-STING-dependent induction of type I interferons. Immunity 44, 597-608 CrossRef Medline.
7. Hafner, A. M., Corthésy, B., and Merkle, H. P. (2013) Particulate formulations for the delivery of poly(I:C) as vaccine adjuvant. Adv. Drug Deliv. Rev. 65, 1386-1399 CrossRef Medline.
8. Chang, C. J., Sun, B., and Robertsen, B. (2015) Adjuvant activity of fish type I interferon shown in a virus DNA vaccination model. Vaccine 33, 2442-2448 CrossRef Medline.
9. Martínez-Gil, L., Goff, P. H., Hai, R., García-Sastre, A., Shaw, M. L., and Palese, P. (2013) A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. J. Virol. 87, 1290-1300 CrossRef Medline.
10. Schiwon, M., Weisheit, C., Franken, L., Gutweiler, S., Dixit, A., Meyer- Schwesinger, C., Pohl, J. M., Maurice, N. J., Thiebes, S., Lorenz, K., Quast, T., Fuhrmann, M., Baumgarten, G., Lohse, M. J., Opdenakker, G., et al. (2014) Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156, 456-468 CrossRef Medline.
11. Lehmann, M. H., Price, P. J., Brandmüller, C., and Sutter, G. (2015) Modified vaccinia virus Ankara but not vaccinia virus induces chemokine expression in cells of the monocyte/macrophage lineage. Virol. J. 12, 21 CrossRef Medline.
12. Long, L., Deng, Y., Yao, F., Guan, D., Feng, Y., Jiang, H., Li, X., Hu, P., Lu, X., Wang, H., Li, J., Gao, X., and Xie, D. (2014) Recruitment of phosphatase PP2A by RACK1 adaptor protein deactivates transcription factor IRF3 and limits type I interferon signaling. Immunity 40, 515-529 CrossRef Medline.
13. Wang, Q., Liu, X., Cui, Y., Tang, Y., Chen, W., Li, S., Yu, H., Pan, Y., and Wang, C. (2014) The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41, 919-933 CrossRef Medline.
14. Powles, J., Fahimi, S., Micha, R., Khatibzadeh, S., Shi, P., Ezzati, M., Engell, R. E., Lim, S. S., Danaei, G., Mozaffarian, D., Global Burden of Diseases Nutrition and Chronic Diseases Expert Group. (2013) Global, regional and national sodium intakes in 1990 and 2010: A systematic analysis of 24 h urinary sodium excretion and dietary surveys worldwide. BMJ Open 3, e003733 CrossRef Medline.
15. Wiig, H., Schröder, A., Neuhofer, W., Jantsch, J., Kopp, C., Karlsen, T. V., Boschmann, M., Goss, J., Bry, M., Rakova, N., Dahlmann, A., Brenner, S., Tenstad, O., Nurmi, H., Mervaala, E., et al. (2013) Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J. Clin. Investig. 123, 2803-2815 CrossRef Medline.
16. Zhao, Y., Gao, P., Sun, F., Li, Q., Chen, J., Yu, H., Li, L., Wei, X., He, H., Lu, Z., Wei, X., Wang, B., Cui, Y., Xiong, S., Shang, Q., Xu, A., Huang, Y., Liu, D., and Zhu, Z. (2016) Sodium intake regulates glucose homeostasis through the PPARδ/adiponectin-mediated SGLT2 pathway. Cell Metab. 23, 699-711 CrossRef Medline.
17. Zhang, W. C., Zheng, X. J., Du, L. J., Sun, J. Y., Shen, Z. X., Shi, C., Sun, S., Zhang, Z., Chen, X. Q., Qin, M., Liu, X., Tao, J., Jia, L., Fan, H. Y., Zhou, B., et al. (2015) High salt primes a specific activation state of macrophages, M(Na). Cell Res. 25, 893-910 CrossRef Medline.
18. Binger, K. J., Gebhardt, M., Heinig, M., Rintisch, C., Schroeder, A., Neuhofer, W., Hilgers, K., Manzel, A., Schwartz, C., Kleinewietfeld, M., Voelkl, J., Schatz, V., Linker, R. A., Lang, F., Voehringer, D., et al. (2015) High salt reduces the activation of IL-4-And IL-13-stimulated macrophages. J. Clin. Investig. 125, 4223-4238 CrossRef Medline.
19. + storage strengthens the antimicrobial barrier function of the skin and boosts macrophage-driven host defense. Cell Metab. 21, 493-501 CrossRef Medline.
20. Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R. A., Muller, D. N., and Hafler, D. A. (2013) Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522 CrossRef Medline.
21. Wu, C., Yosef, N., Thalhamer, T., Zhu, C., Xiao, S., Kishi, Y., Regev, A., and Kuchroo, V. K. (2013) Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496, 513-517 CrossRef Medline.
22. Hernandez, A. L., Kitz, A., Wu, C., Lowther, D. E., Rodriguez, D. M., Vudattu, N., Deng, S., Herold, K. C., Kuchroo, V. K., Kleinewietfeld, M., and Hafler, D. A. (2015) Sodium chloride inhibits the suppressive function of FOXP3+ regulatory T cells. J. Clin. Investig. 125, 4212-4222 CrossRef Medline.
23. Safa, K., Ohori, S., Borges, T. J., Uehara, M., Batal, I., Shimizu, T., Magee, C. N., Belizaire, R., Abdi, R., Wu, C., Chandraker, A., and Riella, L. V. (2015) Salt accelerates allograft rejection through serum-And glucocorticoid- regulated kinase-1-dependent inhibition of regulatory T cells. J. Am. Soc. Nephrol. 26, 2341-2347 CrossRef Medline.
24. Luo, M., Shao, B., Yu, J. Y., Liu, T., Liang, X., Lu, L., Ye, T. H., He, Z. Y., Xiao, H. Y., and Wei, X. W. (2017) Simultaneous enhancement of cellular and humoral immunity by the high salt formulation of Al(OH)3 adjuvant. Cell Res.
25. Bonjardim, C. A., Ferreira, P. C., and Kroon, E. G. (2009) Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122, 1-11 CrossRef Medline.
26. Honda, K., Takaoka, A., and Taniguchi, T. (2006) Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349-360 CrossRef Medline.
27. Hornung, V. (2014) SnapShot: nucleic acid immune sensors, part 1. Immunity 41, 868 CrossRef Medline.
28. Ouwens, D. M., de Ruiter, N. D., van der Zon, G. C., Carter, A. P., Schouten, J., van der Burgt, C., Kooistra, K., Bos, J. L., Maassen, J. A., and van Dam, H. (2002) Growth factors can activate ATF2 via a two-step mechanism: phosphorylation of Thr71 through the Ras-MEK-ERK pathway and of Thr69 through RalGDS-Src-p38. EMBO J. 21, 3782-3793 CrossRef Medline.
29. McNab, F., Mayer-Barber, K., Sher, A., Wack, A., and O'Garra, A. (2015) Type I interferons in infectious disease. Nat. Rev. Immunol. 15, 87-103 CrossRef Medline.
30. Wu, H., Huang, X., Qiu, H., Zhao, M., Liao, W., Yuan, S., Xie, Y., Dai, Y., Chang, C., Yoshimura, A., and Lu, Q. (2016) High salt promotes autoimmunity by TET2-induced DNA demethylation and driving the differentiation of Tfh cells. Sci. Rep. 6, 28065 CrossRef Medline.
31. Alfieri, R. R., and Petronini, P. G. (2007) Hyperosmotic stress response: comparison with other cellular stresses. Pflugers Arch. 454, 173-185 CrossRef.
32. Uhlik, M. T., Abell, A. N., Johnson, N. L., Sun, W., Cuevas, B. D., Lobel- Rice, K. E., Horne, E. A., Dell'Acqua, M. L., and Johnson, G. L. (2003) Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat. Cell Biol. 5, 1104-1110 CrossRef Medline.
33. Yang, J., Yang, C., Guo, N., Zhu, K., Luo, K., Zhang, N., Zhao, H., Cui, Y., Chen, L., Wang, H., Gu, J., Ge, B., Qin, C. F., and Leng, Q. (2015) Type I interferons triggered through the Toll-like receptor 3-TRIF pathway control coxsackievirus A16 infection in young mice. J. Virol. 89, 10860-10867 CrossRef Medline.