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Research Paper

Staphylococcus aureus planktonic but not biofilm environment induces an IFN-β macrophage immune response via the STING/IRF3 pathway

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Article: 2254599 | Received 01 Jun 2023, Accepted 28 Aug 2023, Published online: 11 Sep 2023

References

  • Arciola CR, Campoccia D, Montanaro L. Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol. 2018;16(7):397–16. doi: 10.1038/s41579-018-0019-y
  • Seebach E, Kubatzky KF. Chronic implant-related bone infections-can immune modulation be a therapeutic strategy? Front Immunol. 2019;10:1724. doi: 10.3389/fimmu.2019.01724
  • Gries CM, Kielian T. Staphylococcal biofilms and immune polarization during prosthetic joint infection. J Am Acad Orthop Surg. 2017;25(Suppl 1):S20–S4. doi: 10.5435/JAAOS-D-16-00636
  • Yamada KJ, Kielian T. Biofilm-leukocyte cross-talk: impact on immune polarization and immunometabolism. J Innate Immun. 2018;11(3):1–9. doi: 10.1159/000492680
  • Resch A, Leicht S, Saric M, et al. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics. 2006;6(6):1867–1877. doi: 10.1002/pmic.200500531
  • Seebach E, Elschner T, Kraus FV, et al. Bacterial and metabolic factors of staphylococcal planktonic and biofilm environments differentially regulate macrophage immune activation. Inflammation. 2023;46(4):1512–1530. doi: 10.1007/s10753-023-01824-3
  • Seebach E, Kraus FV, Elschner T, et al. Staphylococci planktonic and biofilm environments differentially affect osteoclast formation. Inflamm Res. 2023;72(7):1465–1484. doi: 10.1007/s00011-023-01745-9
  • Honda K, Taniguchi T. Irfs: master regulators of signalling by toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol. 2006;6(9):644–658. doi: 10.1038/nri1900
  • Rehwinkel J, Gack MU. RIG-I-like receptors: their regulation and roles in RNA sensing. Nat Rev Immunol. 2020;20(9):537–551. doi: 10.1038/s41577-020-0288-3
  • Liu S, Cai X, Wu J, et al. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science. 2015;347(6227):aaa2630. doi: 10.1126/science.aaa2630
  • Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 2008;455(7213):674–678. doi: 10.1038/nature07317
  • Marinho FV, Benmerzoug S, Oliveira SC, et al. The Emerging roles of STING in bacterial infections. Trends Microbiol. 2017;25(11):906–918. doi: 10.1016/j.tim.2017.05.008
  • Burdette DL, Monroe KM, Sotelo-Troha K, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature. 2011;478(7370):515–518. doi: 10.1038/nature10429
  • Krasteva PV, Sondermann H. Versatile modes of cellular regulation via cyclic dinucleotides. Nat Chem Biol. 2017;13(4):350–359. doi: 10.1038/nchembio.2337
  • Valentini M, Filloux A. Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem. 2016;291(24):12547–12555. doi: 10.1074/jbc.R115.711507
  • Park S, Sauer K. Controlling biofilm development through cyclic di-GMP signaling. Adv Exp Med Biol. 2022;1386:69–94. doi: 10.1007/978-3-031-08491-1_3
  • Sun L, Wu J, Du F, et al. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 2013;339(6121):786–791. doi: 10.1126/science.1232458
  • Wu J, Sun L, Chen X, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science. 2013;339(6121):826–830. doi: 10.1126/science.1229963
  • Motwani M, Pesiridis S, Fitzgerald KA. DNA sensing by the cGAS–STING pathway in health and disease. Nat Rev Genet. 2019;20(11):657–674. doi: 10.1038/s41576-019-0151-1
  • Tanaka Y, Chen ZJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal. 2012;5(214):ra20. doi: 10.1126/scisignal.2002521
  • Hopfner KP, Hornung V. Molecular mechanisms and cellular functions of cGAS–STING signalling. Nat Rev Mol Cell Biol. 2020;21(9):501–521. doi: 10.1038/s41580-020-0244-x
  • Barber GN. STING: infection, inflammation and cancer. Nat Rev Immunol. 2015;15(12):760–770. doi: 10.1038/nri3921
  • Ahn J, Barber GN. STING signaling and host defense against microbial infection. Exp Mol Med. 2019;51(12):1–10. doi: 10.1038/s12276-019-0333-0
  • Zhang Z, Zhou H, Ouyang X, et al. Multifaceted functions of STING in human health and disease: from molecular mechanism to targeted strategy. Signal Transduct Target Ther. 2022;7(1):394. doi: 10.1038/s41392-022-01252-z
  • Liu N, Pang X, Zhang H, et al. The cGAS-STING pathway in bacterial infection and bacterial immunity. Front Immunol. 2021;12:814709. doi: 10.3389/fimmu.2021.814709
  • Liu ZZ, Chen W, Zhou CK, et al. Stimulator of interferon genes (STING) promotes staphylococcus aureus-induced extracellular traps formation via the ROS-ERK signaling pathway. Front Cell Dev Biol. 2022;10:836880. doi: 10.3389/fcell.2022.836880
  • Liu ZZ, Yang YJ, Zhou CK, et al. STING contributes to host defense against Staphylococcus aureus pneumonia through suppressing necroptosis. Front Immunol. 2021;12:636861. doi: 10.3389/fimmu.2021.636861
  • Scumpia PO, Botten GA, Norman JS, et al. Opposing roles of toll-like receptor and cytosolic DNA-STING signaling pathways for Staphylococcus aureus cutaneous host defense. PLOS Pathog. 2017;13(7):e1006496. doi: 10.1371/journal.ppat.1006496
  • Yamada KJ, Kielian T. Biofilm-leukocyte cross-talk: impact on immune polarization and immunometabolism. J Innate Immun. 2019;11(3):280–288. doi: 10.1159/000492680
  • Heim CE, Bosch ME, Yamada KJ, et al. Lactate production by Staphylococcus aureus biofilm inhibits HDAC11 to reprogramme the host immune response during persistent infection. Nat Microbiol. 2020;5(10):1271–1284. doi: 10.1038/s41564-020-0756-3
  • Gries CM, Bruger EL, Moormeier DE, et al. Cyclic di-AMP released from Staphylococcus aureus biofilm induces a macrophage type I interferon response. Infect Immun. 2016;84(12):3564–3574. doi: 10.1128/IAI.00447-16
  • Gillaspy AF, Hickmon SG, Skinner RA, et al. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun. 1995;63(9):3373–3380. doi: 10.1128/IAI.63.9.3373-3380.1995
  • Raschke WC, Baird S, Ralph P, et al. Functional macrophage cell lines transformed by Abelson leukemia virus. Cell. 1978;15(1):261–267. doi: 10.1016/0092-8674(78)90101-0
  • Ishihara Y, Hyodo M, Hayakawa Y, et al. Effect of cyclic bis(3â?²â??5â?²)diguanylic acid and its analogs on bacterial biofilm formation. FEMS Microbiol Lett. 2009;301(2):193–200. doi: 10.1111/j.1574-6968.2009.01825.x
  • Gundogdu MS, Liu H, Metzdorf D, et al. The haematopoietic GTPase RhoH modulates IL3 signalling through regulation of STAT activity and IL3 receptor expression. Mol Cancer. 2010;9(1):225. doi: 10.1186/1476-4598-9-225
  • Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12(1):547–569. doi: 10.1080/21505594.2021.1878688
  • Archer NK, Mazaitis MJ, Costerton JW, et al. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence. 2011;2(5):445–459. doi: 10.4161/viru.2.5.17724
  • Cheung AL, Schmidt K, Bateman B, et al. SarS, a SarA homolog repressible by agr, is an activator of protein a synthesis in Staphylococcus aureus. Infect Immun. 2001;69(4):2448–2455. doi: 10.1128/IAI.69.4.2448-2455.2001
  • Zhou Y, Zhao S, Gao X, et al. Staphylococcus aureus induces IFN-β production via a CARMA3-independent mechanism. Pathogens. 2021;10(3):300. doi: 10.3390/pathogens10030300
  • Valle J, Solano C, Garcia B, et al. Biofilm switch and immune response determinants at early stages of infection. Trends Microbiol. 2013;21(8):364–371. doi: 10.1016/j.tim.2013.05.008
  • Beenken KE, Dunman PM, McAleese F, et al. Global gene expression in Staphylococcus aureus biofilms. J Bacteriol. 2004;186(14):4665–4684. doi: 10.1128/JB.186.14.4665-4684.2004
  • Tamayo R, Pratt JT, Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol. 2007;61(1):131–148. doi: 10.1146/annurev.micro.61.080706.093426
  • Martin FJ, Gomez MI, Wetzel DM, et al. Staphylococcus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J Clin Invest. 2009;119:1931–1939. doi: 10.1172/jci35879
  • Parker D, Planet PJ, Soong G, et al. Induction of type I interferon signaling determines the relative pathogenicity of Staphylococcus aureus strains. PLOS Pathog. 2014;10(2):e1003951. doi: 10.1371/journal.ppat.1003951
  • Zhou CM, Wang B, Wu Q, et al. Identification of cGAS as an innate immune sensor of extracellular bacterium Pseudomonas aeruginosa. iScience. 2021;24(1):101928. doi: 10.1016/j.isci.2020.101928
  • Mosallanejad K, Kagan JC. Control of innate immunity by the cGAS-STING pathway. Immunol Cell Biol. 2022;100(6):409–423. doi: 10.1111/imcb.12555
  • Dalpke A, Frank J, Peter M, et al. Activation of toll-like receptor 9 by DNA from different bacterial species. Infect Immun. 2006;74(2):940–946. doi: 10.1128/IAI.74.2.940-946.2006
  • Hacker H, Mischak H, Miethke T, et al. CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 1998;17(21):6230–6240. doi: 10.1093/emboj/17.21.6230
  • Lee HC, Chathuranga K, Lee JS. Intracellular sensing of viral genomes and viral evasion. Exp Mol Med. 2019;51(12):1–13. doi: 10.1038/s12276-019-0299-y
  • Yu L, Liu P. Cytosolic DNA sensing by cGAS: regulation, function, and human diseases. Signal Transduct Target Ther. 2021;6(1):170. doi: 10.1038/s41392-021-00554-y
  • Kovarik P, Castiglia V, Ivin M, et al. Type I Interferons in bacterial infections: a balancing act. Front Immunol. 2016;7:652. doi: 10.3389/fimmu.2016.00652
  • Boxx GM, Cheng G. The roles of type I interferon in bacterial infection. Cell Host Microbe. 2016;19(6):760–769. doi: 10.1016/j.chom.2016.05.016
  • Kaplan A, Ma J, Kyme P, et al. Failure to induce IFN-β production during Staphylococcus aureus infection contributes to pathogenicity. J Immunol. 2012;189(9):4537–4545. doi: 10.4049/jimmunol.1201111
  • Xiong Q, Zhang L, Ge W, et al. The roles of interferons in osteoclasts and osteoclastogenesis. Joint Bone Spine. 2016;83(3):276–281. doi: 10.1016/j.jbspin.2015.07.010
  • Heim CE, Vidlak D, Kielian T. Interleukin-10 production by myeloid-derived suppressor cells contributes to bacterial persistence during Staphylococcus aureus orthopedic biofilm infection. J Leukocyte Biol. 2015;98(6):1003–1013. doi: 10.1189/jlb.4VMA0315-125RR