Extracellular Cold Shock Protein YB-1 Induces Tolerance to GMDP and LPS in Mouse Macrophage Cell Line J774

L. G. Alekseeva; Алексеева Л. Г.; A. G. Laman; Ламан А. Г.; E. A. Meshcherykova; Мещерякова Е. А.; A. O. Shepelyakovskaya; Шепеляковская А. О.; F. A. Brovko; Бровко Ф. А.; V. T. Ivanov; Иванов В. Т.

doi:10.31857/S013234232303003X

Extracellular Cold Shock Protein YB-1 Induces Tolerance to GMDP and LPS in Mouse Macrophage Cell Line J774

Authors: Alekseeva L.G.¹, Laman A.G.², Meshcherykova E.A.¹, Shepelyakovskaya A.O.², Brovko F.A.², Ivanov V.T.¹
Affiliations:
1. Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
2. Branch of Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Issue: Vol 49, No 4 (2023)
Pages: 384-391
Section: Articles
URL: https://rjmseer.com/0132-3423/article/view/670583
DOI: https://doi.org/10.31857/S013234232303003X
EDN: https://elibrary.ru/PDIGUQ
ID: 670583

Cite item

Full Text

Open Access
Restricted Access

Access granted
Restricted Access

Subscription Access

Abstract
About the authors
References
Supplementary files
Statistics

Abstract

Cold shock protein YB-1 is involved in the regulation of a huge number of fundamental biological processes. Previously, we showed that YB-1 is also involved in the process of recognition of muramylpeptide GMDP by the innate immune receptor NOD2 and is able upon preliminary administration to protect mice from death in a model of septic shock induced by Escherichia coli bacteria. We hypothesized that its protective effect may be associated with the development of a state of tolerance (“nonresponsiveness”). Changes in the cellular response were assessed by the level of mRNA expression of the target molecules by quantitative PCR analysis combined with reverse transcription. We tested the possibility of tolerance induction by the YB-1 protein in a model system on the J774 mouse macrophage cell line with the participation of E. coli bacterial cell wall components, immunostimulants GMDP (NOD2 receptor agonist) and LPS (TLR4 receptor agonist). Pretreatment of cells with YB-1 resulted in a significant decrease in the level of mRNA expression of pro-inflammatory cytokines IL-1β, TNF-α, and IL-6 in response to further stimulation with GMDP and LPS, as well as significant changes in the expression of mRNA of RIP2 and MyD88 adapter molecules and components of transcriptional factor NF-κB. Our data show that YB-1 is able to induce tolerance to such as GMDP and LPS immunostimulants, apparently by increasing the production of the anti-inflammatory cytokine IL-1Ra and the SOCS1 inhibitor. A more precise characterization of the features of the YB-1-induced tolerogenic immune response requires further research.

Keywords

innate immunity, GMDP, LPS, transcription factor YB-1, tolerance

References

Lindquist J.A., Mertens P.R. // Cell Commun. Signal. 2018. V. 16. P. 63. https://doi.org/10.1186/s12964-018-0274-6
Laman A.G., Lathe R., Shepelyakovskaya A.O., Gartseva A., Brovko F.A., Guryanova S.V., Alekseeva L.G., Meshcheryakova E.A., Ivanov V.T. // Innate Immun. 2016. V. 22. P. 666–673. https://doi.org/10.1177/1753425916668982
Laman A.G., Lathe R., Savinov G.V., Shepelyakovskaya A.O., Boziev Kh.M., Baidakova L.K., Chulin A.N., Brovko F.A., Svirshchevskaya E.V., Kotelevtsev Y., Eliseeva I.A., Guryanov S.G., Lyabin D.N., Ovchinnikov L.P., Ivanov V.T. // FEBS Lett. 2015. V. 589. P. 1819–1824. https://doi.org/10.1016/j.febslet.2015.05.028
Weichart D., Gobom J., Klopfleisch S., Häsler R., Gustavsson N., Billmann S., Lehrach H., Seegert D., Schreiber S., Rosenstiel P. // J. Biol. Chem. 2006. V. 281. P. 2380–2389. https://doi.org/10.1074/jbc.M505986200
Алексеева Л.Г., Ламан А.Г., Щепеляковская А.О., Плеханова Н.С., Иванов В.Т. // Биоорг. химия. 2019. Т. 45. С. 404–411. [Alekseeva L.G., Plekhanova N.S., Ivanov V.T., Laman A.G., Shepelyakovskaya A.O. // Russ. J. Bioorg. Chem. 2019. V. 45. P. 285–291.] https://doi.org/10.1134/S1068162019040022
Shepelyakovskaya A.O., Alekseeva L.G., Meshcheryakova E.A., Boziev Kh., Tsitrina A., Ivanov V.T., Brovko F.A., Kotelevtsev Y., Lathe R., Laman A.G. // bioRxiv preprinthttps://doi.org/10.1101/2022.11.09.515841
Hayden M.S., Ghosh S. // Cell. 2008. V. 132. P. 344–362. https://doi.org/10.1016/j.cell.2008.01.020
Nomura F., Akashi S., Sakao Y., Sato S., Kawai T., Matsumoto M., Nakanishi K., Kimoto M., Miyake K., Takeda K., Akira S. // J. Immunol. 2000. V. 164. P. 3476–3479. https://doi.org/10.4049/jimmunol.164.7.3476
Mizel S.B., Snipes J.A. // J. Biol. Chem. 2002. V. 277. P. 22414–22420. https://doi.org/10.1074/jbc.M201762200
Hedl M., Li J., Cho J.H., Abraham C. // Proc. Natl. Acad. Sci. USA. 2007. V. 104. P. 19440–19445. https://doi.org/10.1073/pnas.0706097104
Meshcheryakova E., Guryanova S., Makarov E., Alekseeva L., Andronova T., Ivanov V. // Int. Immunopharmacol. 2001. V. 9–10. P. 1857–1865. https://doi.org/10.1016/s1567-5769(01)00111-4
O’Brien G.C., Wang J.H., Redmond H.P. // J. Immunol. 2005. V. 174. P. 1020–1026. https://doi.org/10.4049/jimmunol.174.2.1020
Huber R., Bikker R., Welz B., Christmann M., Brand K. // J. Immunol. Res. 2017. P. 9570129. https://doi.org/10.1155/2017/9570129
Aneja R., Odoms K., Dunsmore K., Shanley T.P., Wong H.R. // J. Immunol. 2006. V. 177. P. 7184–7192. https://doi.org/10.4049/jimmunol.177.10.7184
Coveney A.P., Wang W., Kelly J., Liu J.H., Blankson S., Wu Q.D., Redmond H.P., Wang J.H. // Sci. Rep. 2015. V. 5. P. 13694. https://doi.org/10.1038/srep13694
Bolhassani A., Rafati S. // Exp. Rev. Vaccines. 2008. V. 8. P. 1185–1199. https://doi.org/10.1586/14760584.7.8.1185
Hsu J.H., Yang R.C., Lin S.J., Liou S.F., Dai Z.K., Yeh J.L., Wu J.R. // Shock. 2014. V. 42. P. 540–547. https://doi.org/10.1097/SHK.0000000000000254
Butcher S.K., O’Carroll C.E., Wells C.A., Carmody R.J. // Front. Immunol. 2018. V. 9. P. 933. https://doi.org/10.3389/fimmu.2018.00933
Fritz J.H., Girardin S.E., Fitting C., Werts C., Mengin-Lecreulx D., Caroff M., Cavaillon J.M., Philpott D.J., Adib-Conquy M. // Eur. J. Immunol. 2005. V. 35. P. 2459–2470. https://doi.org/10.1002/eji.200526286
Wang J., Djudjaj S., Gibbert L., Lennartz V., Breitkopf D.M., Rauen T., Hermert D., Martin I.V., Boor P., Braun G.S., Floege J., Ostendorf T., Raffetseder U. // J. Cell. Mol. Med. 2017. V. 12. P. 3494–3505. https://doi.org/10.1111/jcmm.13260
Hu J., Wang G., Liu X., Zhou L., Jiang M., Yang L. // PLoS One. 2014. V. 9. e87528. https://doi.org/10.1371/journal.pone.0087528
Xiong Y., Medvedev A.E. // J. Leukoc. Biol. 2011. V. 90. P. 1141–1148. https://doi.org/10.1189/jlb.0611273
Savinov G.V., Shepelyakovskaya A.O., Boziev Kh.M., Brovko F.A., Laman A.G. // Biochemistry (Moscow). 2014. V. 79. P. 131–138. https://doi.org/10.1134/S0006297914020060
Livak K.J., Schmittgen T.D. // Methods. 2001. V. 25. P. 402–408. https://doi.org/10.1006/meth.2001.1262