Role and plasticity of Th1 and Th17 responses in immunity to Staphylococcus aureus

References

• Chan LC, Rossetti M, Miller LS, Filler SG, Johnson CW, Lee HK, Wang H, Gjertson D, Fowler VG Jr., Reed EF, et al. Protective immunity in recurrent Staphylococcus aureus infection reflects localized immune signatures and macrophage-conferred memory. Proc Natl Acad Sci U S A. 2018;115(47):E11111–E11119. doi:10.1073/pnas.1808353115.
   PubMed Web of Science ®Google Scholar
• Clowry J, Irvine AD, McLoughlin RM. Next-generation anti-Staphylococcus aureus vaccines: A potential new therapeutic option for atopic dermatitis? J Allergy Clin Immunol. 2019;143(1):78–81. doi:10.1016/j.jaci.2018.08.038.
   PubMed Web of Science ®Google Scholar
• Pozzi C, Olaniyi R, Liljeroos L, Galgani I, Rappuoli R, Bagnoli F. Vaccines for Staphylococcus aureus and target populations. Curr Top Microbiol Immunol. 2017;409:491–528. doi:10.1007/82_2016_54.
   PubMed Web of Science ®Google Scholar
• Stentzel S, Hagl B, Abel F, Kahl BC, Rack-Hoch A, Bröker BM, Renner ED. Reduced immunoglobulin (Ig) G response to Staphylococcus aureus in STAT3 hyper-IgE syndrome. Clin Infect Dis. 2017;64(9):1279–82. doi:10.1093/cid/cix140.
   PubMed Web of Science ®Google Scholar
• Monaci E, Mancini F, Lofano G, Bacconi M, Tavarini S, Sammicheli C, Arcidiacono L, Giraldi M, Galletti B, Rossi Paccani S, et al. MF59- and Al(OH)3-adjuvanted Staphylococcus aureus (4C-Staph) vaccines induce sustained protective humoral and cellular immune responses, with a critical role for effector CD4 T cells at low antibody titers. Front Immunol. 2015;6:439. doi:10.3389/fimmu.2015.00439.
   PubMed Web of Science ®Google Scholar
• Mancini F, Monaci E, Lofano G, Torre A, Bacconi M, Tavarini S, Sammicheli C, Arcidiacono L, Galletti B, Laera D, et al. One dose of Staphylococcus aureus 4C-Staph vaccine formulated with a novel TLR7-dependent adjuvant rapidly protects mice through antibodies, effector CD4+ T Cells, and IL-17A. PLoS One. 2016;11(1):e0147767. doi:10.1371/journal.pone.0147767.
   PubMed Web of Science ®Google Scholar
• Brown AF, Murphy AG, Lalor SJ, Leech JM, O‘Keeffe KM, Mac Aogáin M, O‘Halloran DP, Lacey KA, Tavakol M, Hearnden CH, et al. Memory Th1 cells are protective in invasive Staphylococcus aureus infection. PLoS Pathog. 2015;11(11):e1005226. doi:10.1371/journal.ppat.1005226.
   PubMed Web of Science ®Google Scholar
• Li Z, Peres AG, Damian AC, Madrenas J. Immunomodulation and disease tolerance to Staphylococcus aureus. Pathogens. 2015;4(4):793–815. doi:10.3390/pathogens4040793.
   PubMed Web of Science ®Google Scholar
• Kolata JB, Kühbandner I, Link C, Normann N, Vu CH, Steil L, Weidenmaier C, Bröker BM. The fall of a dogma? Unexpected high T-cell memory response to Staphylococcus aureus in humans. J Infect Dis. 2015;212(5):830–38. doi:10.1093/infdis/jiv128.
   PubMed Web of Science ®Google Scholar
• Salgado-Pabón W, Schlievert PM. Models matter: the search for an effective Staphylococcus aureus vaccine. Nat Rev Microbiol. 2014;12(8):585–91. doi:10.1038/nrmicro3308.
   PubMed Web of Science ®Google Scholar
• Watts A, Ke D, Wang Q, Pillay A, Nicholson-Weller A, Lee JC. Staphylococcus aureus strains that express serotype 5 or serotype 8 capsular polysaccharides differ in virulence. Infect Immun. 2005;73(6):3502–11. doi:10.1128/IAI.73.6.3502-3511.2005.
   PubMed Web of Science ®Google Scholar
• Pancari G, Fan H, Smith S, Joshi A, Haimbach R, Clark D, Li Y, Hua J, McKelvey T, Ou Y, et al. Characterization of the mechanism of protection mediated by CS-D7, a monoclonal antibody to Staphylococcus aureus iron regulated surface determinant B (IsdB). Front Cell Infect Microbiol. 2012;2:36. doi:10.3389/fcimb.2012.00036.
   PubMed Web of Science ®Google Scholar
• Fattom A, Matalon A, Buerkert J, Taylor K, Damaso S, Boutriau D. Efficacy profile of a bivalent Staphylococcus aureus glycoconjugated vaccine in adults on hemodialysis: phase III randomized study. Hum Vaccin Immunother. 2015;11(3):632–41. doi:10.4161/hv.34414.
   PubMed Web of Science ®Google Scholar
• Fowler VG, Allen KB, Moreira ED, Moustafa M, Isgro F, Boucher HW, Corey GR, Carmeli Y, Betts R, Hartzel JS, et al. Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA. 2013;309(13):1368–78. doi:10.1001/jama.2013.3010.
   PubMed Web of Science ®Google Scholar
• Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R, et al. Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med. 2002;346(7):491–96. doi:10.1056/NEJMoa011297.
   PubMed Web of Science ®Google Scholar
• Schmidt CS, White CJ, Ibrahim AS, Filler SG, Fu Y, Yeaman MR, Edwards JE Jr., Hennessey JP Jr. NDV-3, a recombinant alum-adjuvanted vaccine for Candida and Staphylococcus aureus, is safe and immunogenic in healthy adults. Vaccine. 2012;30(52):7594–600. doi:10.1016/j.vaccine.2012.10.038.
   PubMed Web of Science ®Google Scholar
• Creech CB, Frenck RW Jr., Sheldon EA, Seiden DJ, Kankam MK, Zito ET, Girgenti D, Severs JM, Immermann FW, McNeil LK, et al. Safety, tolerability, and immunogenicity of a single dose 4-antigen or 3-antigen Staphylococcus aureus vaccine in healthy older adults: results of a randomised trial. Vaccine. 2017;35(2):385–94. doi:10.1016/j.vaccine.2016.11.032.
   PubMed Web of Science ®Google Scholar
• von Köckritz-Blickwede M, Rohde M, Oehmcke S, Miller LS, Cheung AL, Herwald H, Foster S, Medina E. Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am J Pathol. 2008;173(6):1657–68. doi:10.2353/ajpath.2008.080337.
   PubMed Web of Science ®Google Scholar
• Montgomery CP, Daniels M, Zhao F, Alegre ML, Chong AS, Daum RS. Protective immunity against recurrent Staphylococcus aureus skin infection requires antibody and interleukin-17A. Infect Immun. 2014;82(5):2125–34. doi:10.1128/IAI.01491-14.
   PubMed Web of Science ®Google Scholar
• Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, Monroe HR, Magorien JE, Blauvelt A, Kolls JK, Cheung AL, et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest. 2010;120(5):1762–73. doi:10.1172/JCI40891.
   PubMed Web of Science ®Google Scholar
• Lin L, Ibrahim AS, Xu X, Farber JM, Avanesian V, Baquir B, Fu Y, French SW, Edwards JE Jr., Spellberg B. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog. 2009;5(12):e1000703. doi:10.1371/journal.ppat.1000706.
   PubMed Web of Science ®Google Scholar
• Amatya N, Garg AV, Gaffen SL. IL-17 signaling: the Yin and the Yang. Trends Immunol. 2017;38(5):310–22. doi:10.1016/j.it.2017.01.006.
   PubMed Web of Science ®Google Scholar
• Dayan GH, Mohamed N, Scully IL, Cooper D, Begier E, Eiden J, Jansen KU, Gurtman A, Anderson AS. Staphylococcus aureus: the current state of disease, pathophysiology and strategies for prevention. Expert Rev Vaccines. 2016;15(11):1373–92. doi:10.1080/14760584.2016.1179583.
   PubMed Web of Science ®Google Scholar
• Miller LS, Cho JS. Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol. 2011;11(8):505–18. doi:10.1038/nri3010.
   PubMed Web of Science ®Google Scholar
• Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity. 2009;30(5):646–55. doi:10.1016/j.immuni.2009.05.001.
   PubMed Web of Science ®Google Scholar
• Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, Gattorno M, Monticelli S, Lanzavecchia A, Sallusto F. Pathogen-induced human TH17 cells produce IFN-, or IL-10 and are regulated by IL-1β. Nature. 2012;484(7395):514–18. doi:10.1038/nature10957.
   PubMed Web of Science ®Google Scholar
• Wang J, Roderiquez G, Norcross MA. Control of adaptive immune responses by Staphylococcus aureus through IL-10, PD-L1, and TLR2. Sci Rep. 2012;2:606. doi:10.1038/srep00386.
   PubMed Web of Science ®Google Scholar
• Frodermann V, Chau TA, Sayedyahossein S, Toth JM, Heinrichs DE, Madrenas J. A modulatory interleukin-10 response to staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. J Infect Dis. 2011;204(2):253–62. doi:10.1093/infdis/jir276.
   PubMed Web of Science ®Google Scholar
• Rose WE, Eickhoff JC, Shukla SK, Pantrangi M, Rooijakkers S, Cosgrove SE, Nizet V, Sakoulas G. Elevated serum interleukin-10 at time of hospital admission is predictive of mortality in patients with Staphylococcus aureus bacteremia. J Infect Dis. 2012;206(10):1604–11. doi:10.1093/infdis/jis552.
   PubMed Web of Science ®Google Scholar
• Levy J, Licini L, Haelterman E, Moris P, Lestrate P, Damaso S, Van Belle P, Boutriau D. Safety and immunogenicity of an investigational 4-component Staphylococcus aureus vaccine with or without AS03B adjuvant: results of a randomized phase I trial. Hum Vaccin Immunother. 2015;11(3):620–31. doi:10.1080/21645515.2015.1011021.
   PubMed Web of Science ®Google Scholar
• Etz H, Minh DB, Henics T, Dryla A, Winkler B, Triska C, Boyd AP, Söllner J, Schmidt W, von Ahsen U, et al. Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc Natl Acad Sci U S A. 2002;99(10):6573–78. doi:10.1073/pnas.092569199.
   PubMed Web of Science ®Google Scholar
• Roche FM, Massey R, Peacock SJ, Day NP, Visai L, Speziale P, Lam A, Pallen M, Foster TJ. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology. 2003;149(Pt 3):643–54. doi:10.1099/mic.0.25996-0.
   PubMed Web of Science ®Google Scholar
• Vytvytska O, Nagy E, Blüggel M, Meyer HE, Kurzbauer R, Huber LA, Klade CS. Identification of vaccine candidate antigens of Staphylococcus aureus by serological proteome analysis. Proteomics. 2002;2(5):580–90. doi:10.1002/1615-9861(200205)2:5<580::AID-PROT580>3.0.CO;2-G.
   PubMed Web of Science ®Google Scholar
• Weichhart T, Horky M, Söllner J, Gangl S, Henics T, Nagy E, Meinke A, von Gabain A, Fraser CM, Gill SR, et al. Functional selection of vaccine candidate peptides from Staphylococcus aureus whole-genome expression libraries in vitro. Infect Immun. 2003;71(8):4633–41. doi:10.1128/iai.71.8.4633-4641.2003.
   PubMed Web of Science ®Google Scholar
• Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, Acevedo J, Read RC, Day NP, Peacock SJ, et al. Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis. 2006;193(8):1098–108. doi:10.1086/501471.
   PubMed Web of Science ®Google Scholar
• Nair SP, Williams RJ, Henderson B. Advances in our understanding of the bone and joint pathology caused by Staphylococcus aureus infection. Rheumatology (Oxford). 2000;39:821–34.
   PubMed Web of Science ®Google Scholar
• El-Mezayen RE, Matsumoto T. In vitro responsiveness to IL-18 in combination with IL-12 or IL-2 by PBMC from patients with bronchial asthma and atopic dermatitis. Clin Immunol. 2004;111(1):61–68. doi:10.1016/j.clim.2003.12.006.
   PubMed Web of Science ®Google Scholar
• Shikano H, Kato Z, Kaneko H, Watanabe M, Inoue R, Kasahara K, Takemura M, Kondo N. IFN-, production in response to IL-18 or IL-12 stimulation by peripheral blood mononuclear cells of atopic patients. Clin Exp Allergy. 2001;31:1263–70.
   PubMed Web of Science ®Google Scholar
• Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol. 2010;10(7):479–89. doi:10.1038/nri2800.
   PubMed Web of Science ®Google Scholar
• Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol. 2009;27:485–517. doi:10.1146/annurev.immunol.021908.132710.
   PubMed Web of Science ®Google Scholar
• McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ. TGF-β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nat Immunol. 2007;8(12):1390–97. doi:10.1038/ni1539.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Hunter CA. The immunobiology of interleukin-27. Annu Rev Immunol. 2015;33:417–43. doi:10.1146/annurev-immunol-032414-112134.
   PubMed Web of Science ®Google Scholar
• Chu CC, Ali N, Karagiannis P, Di Meglio P, Skowera A, Napolitano L, Barinaga G, Grys K, Sharif-Paghaleh E, Karagiannis SN, et al. Resident CD141 (BDCA3)+ dendritic cells in human skin produce IL-10 and induce regulatory T cells that suppress skin inflammation. J Exp Med. 2012;209(5):935–45. doi:10.1084/jem.20112583.
   PubMed Web of Science ®Google Scholar
• Morel S, Didierlaurent A, Bourguignon P, Delhaye S, Baras B, Jacob V, Planty C, Elouahabi A, Harvengt P, Carlsen H, et al. Adjuvant System AS03 containing α-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine. 2011;29(13):2461–73. doi:10.1016/j.vaccine.2011.01.011.
   PubMed Web of Science ®Google Scholar
• Daum RS, Spellberg B. Progress toward a Staphylococcus aureus vaccine. Clin Infect Dis. 2012;54(4):560–67. doi:10.1093/cid/cir828.
   PubMed Web of Science ®Google Scholar
• Bagnoli F, Bertholet S, Grandi G. Inferring reasons for the failure of Staphylococcus aureus vaccines in clinical trials. Front Cell Inf Microbio. 2012;2(16):1–4. doi:10.3389/fcimb.2012.00016.
   PubMed Web of Science ®Google Scholar
• Breuer K, Wittmann M, Kempe K, Kapp A, Mai U, Dittrich-Breiholz O, Kracht M, Mrabet-Dahbi S, Werfel T. Alpha-toxin is produced by skin colonizing Staphylococcus aureus and induces a T helper type 1 response in atopic dermatitis. Clin Exp Allergy. 2005;35(8):1088–95. doi:10.1111/j.1365-2222.2005.02295.x.
   PubMed Web of Science ®Google Scholar
• Niebuhr M, Gathmann M, Scharonow H, Mamerow D, Mommert S, Balaji H, Werfel T. Staphylococcal alpha-toxin is a strong inducer of interleukin-17 in humans. Infect Immun. 2011;79(4):1615–22. doi:10.1128/IAI.00958-10.
   PubMed Web of Science ®Google Scholar
• Mulcahy ME, Leech JM, Renauld JC, Mills KH, McLoughlin RM. Interleukin-22 regulates antimicrobial peptide expression and keratinocyte differentiation to control Staphylococcus aureus colonization of the nasal mucosa. Mucosal Immunol. 2016;9(6):1429–41. doi:10.1038/mi.2016.24.
   PubMed Web of Science ®Google Scholar
• Cosmi L, Maggi L, Santarlasci V, Liotta F, Annunziato F. T helper cells plasticity in inflammation. Cytometry A. 2014;85(1):36–42. doi:10.1002/cyto.a.22348.
   PubMed Web of Science ®Google Scholar
• Nakahira M, Ahn HJ, Park WR, Gao P, Tomura M, Park CS, Hamaoka T, Ohta T, Kurimoto M, Fujiwara H. Synergy of IL-12 and IL-18 for IFN-, gene expression: IL-12-induced STAT4 contributes to IFN-, promoter activation by up-regulating the binding activity of IL-18-induced Activator Protein 1. J Immunol. 2002;168:1146–53.
   PubMed Web of Science ®Google Scholar
• van de Veerdonk FL, Plantinga TS, Hoischen A, Smeekens SP, Joosten LA, Gilissen C, Arts P, Rosentul DC, Carmichael AJ, Smits-van der Graaf CA, et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N Engl J Med. 2011;365(1):54–61. doi:10.1056/NEJMoa1100102.
   PubMed Web of Science ®Google Scholar
• Murugaiyan G, Mittal A, Lopez-Diego R, Maier LM, Anderson DE, Weiner HL. IL-27 is a key regulator of IL-10 and IL-17 production by human CD4+ T cells. J Immunol. 2009;183(4):2435–43. doi:10.4049/jimmunol.0900568.
   PubMed Web of Science ®Google Scholar
• Rose WE, Shukla SK, Berti AD, Hayney MS, Henriquez KM, Ranzoni A, Cooper MA, Proctor RA, Nizet V, Sakoulas G. Increased endovascular Staphylococcus aureus inoculum is the link between elevated serum interleukin 10 concentrations and mortality in patients with bacteremia. Clin Infect Dis. 2017;64(10):1406–12. doi:10.1093/cid/cix157.
   PubMed Web of Science ®Google Scholar
• McNeely TB, Shah NA, Fridman A, Joshi A, Hartzel JS, Keshari RS, Lupu F, DiNubile MJ. Mortality among recipients of the Merck V710 Staphylococcus aureus vaccine after postoperative S. aureus infections: an analysis of possible contributing host factors. Hum Vaccin Immunother. 2014;10(12):3513–16. doi:10.4161/hv.34407.
   PubMed Web of Science ®Google Scholar
• Roman F, Clement F, Dewé W, Walravens K, Maes C, Willekens J, De Boever F, Hanon E, Leroux-Roels G. Effect on cellular and humoral immune responses of the AS03 Adjuvant System in an A/H1N1/2009 influenza virus vaccine administered to adults during two randomized controlled trials. Clin Vaccine Immunol. 2011;18(5):835–43. doi:10.1128/CVI.00480-10.
   PubMed Web of Science ®Google Scholar
• Burny W, Callegaro A, Bechtold V, Clement F, Delhaye S, Fissette L, Janssens M, Leroux-Roels G, Marchant A, van Den Berg RA, et al. Different adjuvants induce common innate pathways that are associated with enhanced adaptive responses against a model antigen in humans. Front Immunol. 2017;8:943. doi:10.3389/fimmu.2017.00943.
   PubMed Web of Science ®Google Scholar
• Berglund J, Vink P, Tavares Da Silva F, Lestrate P, Boutriau D. Safety, immunogenicity, and antibody persistence following an investigational Streptococcus pneumoniae and Haemophilus influenzae triple-protein vaccine in a Phase 1 randomized controlled study in healthy adults. Clin Vaccine Immunol. 2014;21(1):56–65. doi:10.1128/CVI.00430-13.
   PubMed Web of Science ®Google Scholar
• Duechting A, Przybyla A, Kuerten S, Lehmann PV. Delayed activation kinetics of Th2- and Th17 cells compared to Th1 cells. Cells. 2017;6(3):29. doi:10.3390/cells6030029.
   Web of Science ®Google Scholar
• Brown AF, Leech JM, Rogers TR, McLoughlin RM. Staphylococcus aureus colonization: modulation of host immune response and impact on human vaccine design. Front Immunol. 2014;4:507. doi:10.3389/fimmu.2013.00507.
   PubMed Web of Science ®Google Scholar
• Moris P, van der Most R, Leroux-Roels I, Clement F, Dramé M, Hanon E, Leroux-Roels GG, Van Mechelen M. H5N1 influenza vaccine formulated with AS03A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J Clin Immunol. 2011;31(3):443–54. doi:10.1007/s10875-010-9490-6.
   PubMed Web of Science ®Google Scholar