Skip to main content
SpringerLink
Log in

The Innate Immune Response Against Staphylococcus aureus

  • Chapter
  • First Online:
Staphylococcus aureus

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 409))

Abstract

The innate immune system harbors a multitude of different receptor systems and cells that are constantly prepared to sense and eliminate invading microbial pathogens. Staphylococcus aureus enters the body on its exposed epithelial surfaces, e.g., on skin and mucosa. The initial interaction with epithelial cells is governed by Toll-like receptor (TLR)-2-mediated local production of soluble mediators, including cytokines, chemokines, and antimicrobial peptides. The overall goal is to achieve a steady state of immune mediators and colonizing bacteria. Following cell and tissue invasion clearance of bacteria depends on intracellular microbial sensors and subsequent activation of the inflammasomes. Tissue-resident mast cells and macrophages recruit neutrophils, macrophages, and NK cells. This inflammatory response supports the generation of IL-17 producing NKT, γδ T cells, and T helper cells. Local dendritic cells migrate to the lymph nodes and fine-tune the adaptive immune response. The scope of this chapter is to provide an overview on the major cell types and receptors involved in innate immune defense against S. aureus. By segregating the different stages of infection from epithelial barrier to intracellular and systemic infection, this chapter highlights the different qualities of the innate immune response to S. aureus at different stages of invasiveness.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Abel J, Goldmann O, Ziegler C, Holtje C, Smeltzer MS, Cheung AL, Bruhn D, Rohde M, Medina E (2011) Staphylococcus aureus evades the extracellular antimicrobial activity of mast cells by promoting its own uptake. J Innate Immun 3(5):495–507. doi:10.1159/000327714

    Article  CAS  PubMed  Google Scholar 

  • Accarias S, Lugo-Villarino G, Foucras G, Neyrolles O, Boullier S, Tabouret G (2015) Pyroptosis of resident macrophages differentially orchestrates inflammatory responses to Staphylococcus aureus in resistant and susceptible mice. Eur J Immunol 45(3):794–806. doi:10.1002/eji.201445098

    Article  CAS  PubMed  Google Scholar 

  • Achouiti A, Vogl T, Van der Meer AJ, Stroo I, Florquin S, de Boer OJ, Roth J, Zeerleder S, van’t Veer C, de Vos AF, van der Poll T (2015) Myeloid-related protein-14 deficiency promotes inflammation in staphylococcal pneumonia. Eur Respir J. doi:10.1183/09031936.00183814

  • Ahn KB, Jeon JH, Baik JE, Park OJ, Kang SS, Yun CH, Park JH, Han SH (2014) Muramyl dipeptide potentiates staphylococcal lipoteichoic acid induction of cyclooxygenase-2 expression in macrophages. Microbes Infect 16(2):153–160. doi:10.1016/j.micinf.2013.10.018

    Article  CAS  PubMed  Google Scholar 

  • Amiel E, Alonso A, Uematsu S, Akira S, Poynter ME, Berwin B (2009) Pivotal advance: Toll-like receptor regulation of scavenger receptor-A-mediated phagocytosis. J Leukoc Biol 85(4):595–605. doi:10.1189/jlb.1008631

    Article  CAS  PubMed  Google Scholar 

  • Arlehamn CS, Petrilli V, Gross O, Tschopp J, Evans TJ (2010) The role of potassium in inflammasome activation by bacteria. J Biol Chem 285(14):10508–10518. doi:10.1074/jbc.M109.067298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atilano ML, Pereira PM, Vaz F, Catalao MJ, Reed P, Grilo IR, Sobral RG, Ligoxygakis P, Pinho MG, Filipe SR (2014) Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the Drosophila innate immune system. Elife 3:e02277. doi:10.7554/eLife.02277

  • Atilano ML, Yates J, Glittenberg M, Filipe SR, Ligoxygakis P (2011) Wall teichoic acids of Staphylococcus aureus limit recognition by the drosophila peptidoglycan recognition protein-SA to promote pathogenicity. PLoS Pathog 7(12):e1002421. doi:10.1371/journal.ppat.1002421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K (2006) A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 188(8):2761–2773. doi:188/8/2761 [pii] 10.1128/JB.188.8.2761-2773.2006

  • Banerjee A, Stevenaert F, Pande K, Haghjoo E, Antonenko S, Gorman DM, Sathe M, McClanahan TK, Pierce R, Turner SP, Bigler ME, Phillips JH, Heyworth PG (2010) Modulation of paired immunoglobulin-like type 2 receptor signaling alters the host response to Staphylococcus aureus-induced pneumonia. Infect Immun 78(3):1353–1363. doi:10.1128/iai.00969-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, Remaley AT, Csako G, Patterson AP, Eggerman TL (2008) Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J Immunol 181(10):7147–7156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bekeredjian-Ding I, Greil J, Ammann S, Parcina M (2014) Plasmacytoid dendritic cells: neglected regulators of the immune response to Staphylococcus aureus. Front Immunol 5:238. doi:10.3389/fimmu.2014.00238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bekeredjian-Ding I, Inamura S, Giese T, Moll H, Endres S, Sing A, Zahringer U, Hartmann G (2007) Staphylococcus aureus protein A triggers T cell-independent B cell proliferation by sensitizing B cells for TLR2 ligands. J Immunol 178(5):2803–2812

    Article  CAS  PubMed  Google Scholar 

  • Bekeredjian-Ding I, Schafer M, Hartmann E, Pries R, Parcina M, Schneider P, Giese T, Endres S, Wollenberg B, Hartmann G (2009) Tumour-derived prostaglandin E and transforming growth factor-beta synergize to inhibit plasmacytoid dendritic cell-derived interferon-alpha. Immunology 128(3):439–450. doi:10.1111/j.1365-2567.2009.03134.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bera A, Biswas R, Herbert S, Kulauzovic E, Weidenmaier C, Peschel A, Gotz F (2007) Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J Bacteriol 189(1):280–283. doi:JB.01221-06 [pii] 10.1128/JB.01221-06

  • Bergstrom B, Aune MH, Awuh JA, Kojen JF, Blix KJ, Ryan L, Flo TH, Mollnes TE, Espevik T, Stenvik J (2015) TLR8 senses Staphylococcus aureus RNA in human primary monocytes and macrophages and induces IFN-beta production via a TAK1-IKKbeta-IRF5 signaling pathway. J Immunol. doi:10.4049/jimmunol.1403176

    PubMed  Google Scholar 

  • Bernard JJ, Gallo RL (2010) Cyclooxygenase-2 enhances antimicrobial peptide expression and killing of Staphylococcus aureus. J Immunol 185(11):6535–6544. doi:10.4049/jimmunol.1002009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhalla A, Aron DC, Donskey CJ (2007) Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis 7:105. doi:10.1186/1471-2334-7-105

    Article  PubMed  PubMed Central  Google Scholar 

  • Birjandi SZ, Ippolito JA, Ramadorai AK, Witte PL (2011) Alterations in marginal zone macrophages and marginal zone B cells in old mice. J Immunol 186(6):3441–3451. doi:10.4049/jimmunol.1001271 jimmunol.1001271 [pii]

  • Bishayi B, Bandyopadhyay D, Majhi A, Adhikary R (2014) Possible role of Toll-like receptor-2 in the intracellular survival of Staphylococcus aureus in murine peritoneal macrophages: involvement of cytokines and anti-oxidant enzymes. Scand J Immunol 80(2):127–143. doi:10.1111/sji.12195

    Article  CAS  PubMed  Google Scholar 

  • Blanchet C, Jouvion G, Fitting C, Cavaillon JM, Adib-Conquy M (2014) Protective or deleterious role of scavenger receptors SR-A and CD36 on host resistance to Staphylococcus aureus depends on the site of infection. PLoS ONE 9(1):e87927. doi:10.1371/journal.pone.0087927

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bocker U, Manigold T, Watson JM, Singer MV, Rossol S (2001) Regulation of Staphylococcus aureus-mediated activation of interleukin-18 in peripheral blood mononuclear cells. Eur Cytokine Netw 12(4):631–638

    CAS  PubMed  Google Scholar 

  • Braff MH, Jones AL, Skerrett SJ, Rubens CE (2007) Staphylococcus aureus exploits cathelicidin antimicrobial peptides produced during early pneumonia to promote staphylokinase-dependent fibrinolysis. J Infect Dis 195(9):1365–1372. doi:10.1086/513277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broker BM, Holtfreter S, Bekeredjian-Ding I (2014) Immune control of Staphylococcus aureus—regulation and counter-regulation of the adaptive immune response. Int J Med Microbiol 304(2):204–214. doi:10.1016/j.ijmm.2013.11.008

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Zhang R, Zhang W, Zhu C, Yu Y, Song Y, Wang Q, Bai L, Liu Y, Wu K, Wu J (2014) IL-27, a cytokine, and IFN-lambda1, a type III IFN, are coordinated to regulate virus replication through type I IFN. J Immunol 192(2):691–703. doi:10.4049/jimmunol.1300252

    Article  CAS  PubMed  Google Scholar 

  • Cardot-Martin E, Casalegno JS, Badiou C, Dauwalder O, Keller D, Prevost G, Rieg S, Kern WV, Cuerq C, Etienne J, Vandenesch F, Lina G, Dumitrescu O (2015) alpha-Defensins partially protect human neutrophils against Panton-Valentine leukocidin produced by Staphylococcus aureus. Lett Appl Microbiol. doi:10.1111/lam.12438

    PubMed  Google Scholar 

  • Chaly YV, Paleolog EM, Kolesnikova TS, Tikhonov II, Petratchenko EV, Voitenok NN (2000) Neutrophil alpha-defensin human neutrophil peptide modulates cytokine production in human monocytes and adhesion molecule expression in endothelial cells. Eur Cytokine Netw 11(2):257–266

    CAS  PubMed  Google Scholar 

  • Chau TA, McCully ML, Brintnell W, An G, Kasper KJ, Vines ED, Kubes P, Haeryfar SM, McCormick JK, Cairns E, Heinrichs DE, Madrenas J (2009) Toll-like receptor 2 ligands on the staphylococcal cell wall downregulate superantigen-induced T cell activation and prevent toxic shock syndrome. Nat Med 15(6):641–648

    Article  CAS  PubMed  Google Scholar 

  • Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, Flock JI, Herrmann M, Preissner KT (2002) Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 8(7):687–693. doi:10.1038/nm728

    Article  CAS  PubMed  Google Scholar 

  • Chi CY, Lin CC, Liao IC, Yao YC, Shen FC, Liu CC, Lin CF (2014) Panton-Valentine leukocidin facilitates the escape of Staphylococcus aureus from human keratinocyte endosomes and induces apoptosis. J Infect Dis 209(2):224–235. doi:10.1093/infdis/jit445

    Article  CAS  PubMed  Google Scholar 

  • Cho JS, Guo Y, Ramos RI, Hebroni F, Plaisier SB, Xuan C, Granick JL, Matsushima H, Takashima A, Iwakura Y, Cheung AL, Cheng G, Lee DJ, Simon SI, Miller LS (2012) Neutrophil-derived IL-1beta is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog 8(11):e1003047. doi:10.1371/journal.ppat.1003047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins LV, Kristian SA, Weidenmaier C, Faigle M, Van Kessel KP, Van Strijp JA, Gotz F, Neumeister B, Peschel A (2002) Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J Infect Dis 186(2):214–219. doi:10.1086/341454

    Article  CAS  PubMed  Google Scholar 

  • Contractor N, Louten J, Kim L, Biron CA, Kelsall BL (2007) Cutting edge: Peyer’s patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: possible role for IL-10, TGFbeta, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J Immunol 179(5):2690–2694

    Article  CAS  PubMed  Google Scholar 

  • Craven RR, Gao X, Allen IC, Gris D, Bubeck Wardenburg J, McElvania-Tekippe E, Ting JP, Duncan JA (2009) Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS ONE 4(10):e7446. doi:10.1371/journal.pone.0007446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui F, Meng J, Luo P, Chen P (2014) IFN- alpha blocks IL-17 production by peripheral blood mononuclear cells in patients with chronic active hepatitis B Infection. BMC Infect Dis 14:55. doi:10.1186/1471-2334-14-55

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davis BK, Roberts RA, Huang MT, Willingham SB, Conti BJ, Brickey WJ, Barker BR, Kwan M, Taxman DJ, Accavitti-Loper MA, Duncan JA, Ting JP (2011) Cutting edge: NLRC5-dependent activation of the inflammasome. J Immunol 186(3):1333–1337. doi:10.4049/jimmunol.1003111

    Article  CAS  PubMed  Google Scholar 

  • De Marzi MC, Todone M, Ganem MB, Wang Q, Mariuzza RA, Fernandez MM, Malchiodi EL (2015) Peptidoglycan recognition protein-peptidoglycan complexes increase monocyte/macrophage activation and enhance the inflammatory response. Immunology. doi:10.1111/imm.12460

    PubMed  PubMed Central  Google Scholar 

  • den Dunnen J, Vogelpoel LT, Wypych T, Muller FJ, de Boer L, Kuijpers TW, Zaat SA, Kapsenberg ML, de Jong EC (2012) IgG opsonization of bacteria promotes Th17 responses via synergy between TLRs and FcgammaRIIa in human dendritic cells. Blood 120(1):112–121. doi:10.1182/blood-2011-12-399931

    Article  CAS  Google Scholar 

  • Diefenbach A, Colonna M, Koyasu S (2014) Development, differentiation, and diversity of innate lymphoid cells. Immunity 41(3):354–365. doi:10.1016/j.immuni.2014.09.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doisne JM, Soulard V, Becourt C, Amniai L, Henrot P, Havenar-Daughton C, Blanchet C, Zitvogel L, Ryffel B, Cavaillon JM, Marie JC, Couillin I, Benlagha K (2011) Cutting edge: crucial role of IL-1 and IL-23 in the innate IL-17 response of peripheral lymph node NK1.1- invariant NKT cells to bacteria. J Immunol 186(2):662–666. doi:10.4049/jimmunol.1002725

    Article  CAS  PubMed  Google Scholar 

  • DuMont AL, Torres VJ (2014) Cell targeting by the Staphylococcus aureus pore-forming toxins: it’s not just about lipids. Trends Microbiol 22(1):21–27. doi:10.1016/j.tim.2013.10.004 S0966-842X(13)00202-3 [pii]

  • El-Helou O, Berbari EF, Brown RA, Gralewski JH, Osmon DR, Razonable RR (2011) Functional assessment of Toll-like receptor 2 and its relevance in patients with Staphylococcus aureus infection of joint prosthesis. Hum Immunol 72(1):47–53. doi:10.1016/j.humimm.2010.10.001

    Article  CAS  PubMed  Google Scholar 

  • Fadok VA, Warner ML, Bratton DL, Henson PM (1998) CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3). J Immunol 161(11):6250–6257

    CAS  PubMed  Google Scholar 

  • Feuerstein R, Seidl M, Prinz M, Henneke P (2015) MyD88 in macrophages is critical for abscess resolution in staphylococcal skin infection. J Immunol 194(6):2735–2745. doi:10.4049/jimmunol.1402566 jimmunol.1402566 [pii]

  • Franchi L, Kanneganti TD, Dubyak GR, Nunez G (2007) Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J Biol Chem 282(26):18810–18818. doi:10.1074/jbc.M610762200

    Article  CAS  PubMed  Google Scholar 

  • Frodermann V, Chau TA, Sayedyahossein S, Toth JM, Heinrichs DE, Madrenas J (2011) A modulatory interleukin-10 response to staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. J Infect Dis 204(2):253–262. doi:10.1093/infdis/jir276

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Ma X, Gu W, Fu M, An J, Xing Y, Gao T, Li W, Liu Y (2012) Novel functions of murine B1 cells: active phagocytic and microbicidal abilities. Eur J Immunol 42(4):982–992. doi:10.1002/eji.201141519

    Article  CAS  PubMed  Google Scholar 

  • Garver LS, Wu J, Wu LP (2006) The peptidoglycan recognition protein PGRP-SC1a is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila. Proc Natl Acad Sci U S A 103(3):660–665. doi:10.1073/pnas.0506182103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278(11):8869–8872. doi:10.1074/jbc.C200651200

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Zorn B, Senna JP, Fiette L, Shorte S, Testard A, Chignard M, Courvalin P, Grillot-Courvalin C (2005) Bacterial and host factors implicated in nasal carriage of methicillin-resistant Staphylococcus aureus in mice. Infect Immun 73(3):1847–1851. doi:73/3/1847 [pii] 10.1128/IAI.73.3.1847-1851.2005

  • Goodyear CS, Silverman GJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci U S A 101(31):11392–11397. doi:10.1073/pnas.0404382101 0404382101 [pii]

  • Goriely S, Cavoy R, Goldman M (2009) Interleukin-12 family members and type I interferons in Th17-mediated inflammatory disorders. Allergy 64(5):702–709. doi:10.1111/j.1398-9995.2009.02039.x

    Article  CAS  PubMed  Google Scholar 

  • Goubier A, Dubois B, Gheit H, Joubert G, Villard-Truc F, Asselin-Paturel C, Trinchieri G, Kaiserlian D (2008) Plasmacytoid dendritic cells mediate oral tolerance. Immunity 29(3):464–475. doi:S1074-7613(08)00372-5 [pii] 10.1016/j.immuni.2008.06.017

  • Greenlee-Wacker M, DeLeo FR, Nauseef WM (2015) How methicillin-resistant Staphylococcus aureus evade neutrophil killing. Curr Opin Hematol 22(1):30–35. doi:10.1097/moh.0000000000000096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenlee-Wacker MC, Rigby KM, Kobayashi SD, Porter AR, DeLeo FR, Nauseef WM (2014) Phagocytosis of Staphylococcus aureus by human neutrophils prevents macrophage efferocytosis and induces programmed necrosis. J Immunol 192(10):4709–4717. doi:10.4049/jimmunol.1302692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gries DM, Pultz NJ, Donskey CJ (2005) Growth in cecal mucus facilitates colonization of the mouse intestinal tract by methicillin-resistant Staphylococcus aureus. J Infect Dis 192(9):1621–1627. doi:JID34054 [pii] 10.1086/491737

  • Guo B, Chang EY, Cheng G (2008) The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J Clin Invest 118(5):1680–1690. doi:10.1172/jci33342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126(6):1135–1145. doi:10.1016/j.cell.2006.07.033

    Article  CAS  PubMed  Google Scholar 

  • Haller D, Serrant P, Granato D, Schiffrin EJ, Blum S (2002) Activation of human NK cells by staphylococci and lactobacilli requires cell contact-dependent costimulation by autologous monocytes. Clin Diagn Lab Immunol 9(3):649–657

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hanamsagar R, Aldrich A, Kielian T (2014) Critical role for the AIM2 inflammasome during acute CNS bacterial infection. J Neurochem 129(4):704–711. doi:10.1111/jnc.12669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl D, Lehmann N, Hoffmann F, Jansson A, Hector A, Notheis G, Roos D, Belohradsky BH, Wintergerst U (2008) Dysregulation of innate immune receptors on neutrophils in chronic granulomatous disease. J Allergy Clin Immunol 121(2):375–382 e379. doi:10.1016/j.jaci.2007.10.037

  • Hashimoto M, Tawaratsumida K, Kariya H, Kiyohara A, Suda Y, Krikae F, Kirikae T, Gotz F (2006) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J Immunol 177(5):3162–3169

    Article  CAS  PubMed  Google Scholar 

  • Hayes SM, Howlin R, Johnston DA, Webb JS, Clarke SC, Stoodley P, Harries PG, Wilson SJ, Pender SL, Faust SN, Hall-Stoodley L, Salib RJ (2015) Intracellular residency of Staphylococcus aureus within mast cells in nasal polyps: a novel observation. J Allergy Clin Immunol. doi:10.1016/j.jaci.2014.12.1929

    PubMed  Google Scholar 

  • Heim CE, Vidlak D, Scherr TD, Kozel JA, Holzapfel M, Muirhead DE, Kielian T (2014) Myeloid-derived suppressor cells contribute to Staphylococcus aureus orthopedic biofilm infection. J Immunol 192(8):3778–3792. doi:10.4049/jimmunol.1303408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilmi D, Parcina M, Stollewerk D, Ostrop J, Josten M, Meilaender A, Zaehringer U, Wichelhaus TA, Bierbaum G, Heeg K, Wolz C, Bekeredjian-Ding I (2014) Heterogeneity of host TLR2 stimulation by Staphylocoocus aureus isolates. PLoS One 9(5):e96416. doi:10.1371/journal.pone.0096416 PONE-D-13-55098 [pii]

  • Hirohata S, Shibuya H, Tejima S (2010) Suppressive influences of IFN-alpha on IL-17 expression in human CD4+ T cells. Clin Immunol 134(3):340–344. doi:10.1016/j.clim.2009.11.012

    Article  CAS  PubMed  Google Scholar 

  • Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U, Beutler B (2005) CD36 is a sensor of diacylglycerides. Nature 433(7025):523–527. doi:nature03253 [pii] 10.1038/nature03253

  • Holzinger D, Gieldon L, Mysore V, Nippe N, Taxman DJ, Duncan JA, Broglie PM, Marketon K, Austermann J, Vogl T, Foell D, Niemann S, Peters G, Roth J, Loffler B (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 92(5):1069–1081. doi:10.1189/jlb.0112014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, Endres S, Hartmann G (2002) Quantitative expression of toll-like receptor 1–10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 168(9):4531–4537

    Article  CAS  PubMed  Google Scholar 

  • Hruz P, Zinkernagel AS, Jenikova G, Botwin GJ, Hugot JP, Karin M, Nizet V, Eckmann L (2009) NOD2 contributes to cutaneous defense against Staphylococcus aureus through alpha-toxin-dependent innate immune activation. Proc Natl Acad Sci U S A 106(31):12873–12878. doi:10.1073/pnas.0904958106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain M, Haggar A, Peters G, Chhatwal GS, Herrmann M, Flock JI, Sinha B (2008) More than one tandem repeat domain of the extracellular adherence protein of Staphylococcus aureus is required for aggregation, adherence, and host cell invasion but not for leukocyte activation. Infect Immun 76(12):5615–5623. doi:10.1128/iai.00480-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ip WK, Sokolovska A, Charriere GM, Boyer L, Dejardin S, Cappillino MP, Yantosca LM, Takahashi K, Moore KJ, Lacy-Hulbert A, Stuart LM (2010) Phagocytosis and phagosome acidification are required for pathogen processing and MyD88-dependent responses to Staphylococcus aureus. J Immunol 184(12):7071–7081. doi:10.4049/jimmunol.1000110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ip WK, Takahashi K, Moore KJ, Stuart LM, Ezekowitz RA (2008) Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 205(1):169–181. doi:10.1084/jem.20071164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jann NJ, Schmaler M, Kristian SA, Radek KA, Gallo RL, Nizet V, Peschel A, Landmann R (2009) Neutrophil antimicrobial defense against Staphylococcus aureus is mediated by phagolysosomal but not extracellular trap-associated cathelicidin. J Leukoc Biol 86(5):1159–1169. doi:10.1189/jlb.0209053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jawdat DM, Rowden G, Marshall JS (2006) Mast cells have a pivotal role in TNF-independent lymph node hypertrophy and the mobilization of Langerhans cells in response to bacterial peptidoglycan. J Immunol 177(3):1755–1762

    Article  CAS  PubMed  Google Scholar 

  • Jin T, Bokarewa M, Foster T, Mitchell J, Higgins J, Tarkowski A (2004) Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol 172(2):1169–1176

    Article  CAS  PubMed  Google Scholar 

  • Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik SG, Lee H, Lee JO (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130(6):1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Jin JO, Zhang W, Du JY, Yu Q (2014) BDCA1-positive dendritic cells (DCs) represent a unique human myeloid DC subset that induces innate and adaptive immune responses to Staphylococcus aureus Infection. Infect Immun 82(11):4466–4476. doi:10.1128/iai.01851-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Josefsson E, Tarkowski A (1999) Staphylococcus aureus-induced inflammation and bone destruction in experimental models of septic arthritis. J Periodontal Res 34(7):387–392

    Article  CAS  PubMed  Google Scholar 

  • Jung JY, Roberts LL, Robinson CM (2015) The presence of interleukin-27 during monocyte-derived dendritic cell differentiation promotes improved antigen processing and stimulation of T cells. Immunology 144(4):649–660. doi:10.1111/imm.12417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaesler S, Volz T, Skabytska Y, Koberle M, Hein U, Chen KM, Guenova E, Wolbing F, Rocken M, Biedermann T (2014) Toll-like receptor 2 ligands promote chronic atopic dermatitis through IL-4-mediated suppression of IL-10. J Allergy Clin Immunol 134(1):92–99. doi:10.1016/j.jaci.2014.02.017 S0091-6749(14)00267-X [pii]

  • Kamenyeva O, Boularan C, Kabat J, Cheung GY, Cicala C, Yeh AJ, Chan JL, Periasamy S, Otto M, Kehrl JH (2015) Neutrophil recruitment to lymph nodes limits local humoral response to Staphylococcus aureus. PLoS Pathog 11(4):e1004827. doi:10.1371/journal.ppat.1004827

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang JY, Nan X, Jin MS, Youn SJ, Ryu YH, Mah S, Han SH, Lee H, Paik SG, Lee JO (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31(6):873–884

    Article  CAS  PubMed  Google Scholar 

  • Kang SS, Noh SY, Park OJ, Yun CH, Han SH (2015) Staphylococcus aureus induces IL-8 expression through its lipoproteins in the human intestinal epithelial cell, Caco-2. Cytokine. doi:10.1016/j.cyto.2015.04.017

    Google Scholar 

  • Kapetanovic R, Nahori MA, Balloy V, Fitting C, Philpott DJ, Cavaillon JM, Adib-Conquy M (2007) Contribution of phagocytosis and intracellular sensing for cytokine production by Staphylococcus aureus-activated macrophages. Infect Immun 75(2):830–837. doi:10.1128/iai.01199-06

    Article  CAS  PubMed  Google Scholar 

  • Kaplan A, Ma J, Kyme P, Wolf AJ, Becker CA, Tseng CW, Liu GY, Underhill DM (2012) Failure to induce IFN-beta production during Staphylococcus aureus infection contributes to pathogenicity. J Immunol 189(9):4537–4545. doi:10.4049/jimmunol.1201111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato-Matsunaga N, Okonogi K (1996) Gastrointestinal colonization by methicillin-resistant Staphylococcus aureus in immunosuppressed mice. Infect Immun 64(10):4231–4235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kebaier C, Chamberland RR, Allen IC, Gao X, Broglie PM, Hall JD, Jania C, Doerschuk CM, Tilley SL, Duncan JA (2012) Staphylococcus aureus alpha-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J Infect Dis 205(5):807–817. doi:10.1093/infdis/jir846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kielian T, Haney A, Mayes PM, Garg S, Esen N (2005) Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect Immun 73(11):7428–7435. doi:73/11/7428 [pii] 10.1128/IAI.73.11.7428-7435.2005

  • Kim NJ, Ahn KB, Jeon JH, Yun CH, Finlay BB, Han SH (2015) Lipoprotein in the cell wall of Staphylococcus aureus is a major inducer of nitric oxide production in murine macrophages. Mol Immunol 65(1):17–24. doi:10.1016/j.molimm.2014.12.016 S0161-5890(14)00358-7 [pii]

  • Kinoshita M, Miyazaki H, Ono S, Inatsu A, Nakashima H, Tsujimoto H, Shinomiya N, Saitoh D, Seki S (2011) Enhancement of neutrophil function by interleukin-18 therapy protects burn-injured mice from methicillin-resistant Staphylococcus aureus. Infect Immun 79(7):2670–2680. doi:10.1128/iai.01298-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klotz M, Zimmermann S, Opper S, Heeg K, Mutters R (2005) Possible risk for re-colonization with methicillin-resistant Staphylococcus aureus (MRSA) by faecal transmission. Int J Hyg Environ Health 208(5):401–405. doi:10.1016/j.ijheh.2005.05.004

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi SD, Malachowa N, DeLeo FR (2015) Pathogenesis of Staphylococcus aureus abscesses. Am J Pathol 185(6):1518–1527. doi:10.1016/j.ajpath.2014.11.030

    Article  PubMed  PubMed Central  Google Scholar 

  • Kohler J, Breitbach K, Renner C, Heitsch AK, Bast A, van Rooijen N, Vogelgesang S, Steinmetz I (2011) NADPH-oxidase but not inducible nitric oxide synthase contributes to resistance in a murine Staphylococcus aureus Newman pneumonia model. Microbes Infect 13(11):914–922. doi:10.1016/j.micinf.2011.05.004

    Article  PubMed  CAS  Google Scholar 

  • Kuo IH, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, Gallo RL, Borkowski AW, Yamasaki K, Leung DY, Georas SN, De Benedetto A, Beck LA (2013) Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J Invest Dermatol 133(4):988–998. doi:10.1038/jid.2012.437

    Article  CAS  PubMed  Google Scholar 

  • Kurokawa K, Gong JH, Ryu KH, Zheng L, Chae JH, Kim MS, Lee BL (2011) Biochemical characterization of evasion from peptidoglycan recognition by Staphylococcus aureus D-alanylated wall teichoic acid in insect innate immunity. Dev Comp Immunol 35(8):835–839. doi:10.1016/j.dci.2011.03.001

    Article  CAS  PubMed  Google Scholar 

  • Kwiecinski J, Rhost S, Lofbom L, Blomqvist M, Mansson JE, Cardell SL, Jin T (2013) Sulfatide attenuates experimental Staphylococcus aureus sepsis through a CD1d-dependent pathway. Infect Immun 81(4):1114–1120. doi:10.1128/iai.01334-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labrousse D, Perret M, Hayez D, Da Silva S, Badiou C, Couzon F, Bes M, Chavanet P, Lina G, Vandenesch F, Croisier-Bertin D, Henry T (2014) Kineret(R)/IL-1ra blocks the IL-1/IL-8 inflammatory cascade during recombinant Panton Valentine Leukocidin-triggered pneumonia but not during S. aureus infection. PLoS ONE 9(6):e97546. doi:10.1371/journal.pone.0097546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X, Yang P, Wang C, Li F, Kijlstra A (2011) IFN-alpha blocks IL-17 production by peripheral blood mononuclear cells in Behcet’s disease. Rheumatology (Oxford) 50(2):293–298. doi:10.1093/rheumatology/keq330

    Article  CAS  Google Scholar 

  • Lizak M, Yarovinsky TO (2012) Phospholipid scramblase 1 mediates type i interferon-induced protection against staphylococcal alpha-toxin. Cell Host Microbe 11(1):70–80. doi:10.1016/j.chom.2011.12.004 S1931-3128(11)00405-7 [pii]

  • Maher BM, Mulcahy ME, Murphy AG, Wilk M, O’Keeffe KM, Geoghegan JA, Lavelle EC, McLoughlin RM (2013) Nlrp-3-driven interleukin 17 production by gammadeltaT cells controls infection outcomes during Staphylococcus aureus surgical site infection. Infect Immun 81(12):4478–4489. doi:10.1128/iai.01026-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maresso AW, Schneewind O (2006) Iron acquisition and transport in Staphylococcus aureus. Biometals 19(2):193–203. doi:10.1007/s10534-005-4863-7

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Oliver AM, Kearney JF (2001) Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14(5):617–629. doi:S1074-7613(01)00129-7 [pii]

    Google Scholar 

  • Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6:13. doi:10.12703/p6-13

    Google Scholar 

  • Matsui K, Nishikawa A (2002) Lipoteichoic acid from Staphylococcus aureus induces Th2-prone dermatitis in mice sensitized percutaneously with an allergen. Clin Exp Allergy 32(5):783–788

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Nishikawa A (2005) Percutaneous application of peptidoglycan from Staphylococcus aureus induces an increase in mast cell numbers in the dermis of mice. Clin Exp Allergy 35(3):382–387. doi:10.1111/j.1365-2222.2005.02190.x

    Article  CAS  PubMed  Google Scholar 

  • Mayer AK, Muehmer M, Mages J, Gueinzius K, Hess C, Heeg K, Bals R, Lang R, Dalpke AH (2007) Differential recognition of TLR-dependent microbial ligands in human bronchial epithelial cells. J Immunol 178(5):3134–3142

    Article  CAS  PubMed  Google Scholar 

  • McCurdy JD, Olynych TJ, Maher LH, Marshall JS (2003) Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J Immunol 170(4):1625–1629

    Article  CAS  PubMed  Google Scholar 

  • McGilligan VE, Gregory-Ksander MS, Li D, Moore JE, Hodges RR, Gilmore MS, Moore TC, Dartt DA (2013) Staphylococcus aureus activates the NLRP3 inflammasome in human and rat conjunctival goblet cells. PLoS ONE 8(9):e74010. doi:10.1371/journal.pone.0074010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNeil JC (2014) Staphylococcus aureus—antimicrobial resistance and the immunocompromised child. Infect Drug Resist 7:117–127. doi:10.2147/idr.s39639

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyers JA, Mangini AJ, Nagai T, Roff CF, Sehy D, van Seventer GA, van Seventer JM (2006) Blockade of TLR9 agonist-induced type I interferons promotes inflammatory cytokine IFN-gamma and IL-17 secretion by activated human PBMC. Cytokine 35(5–6):235–246. doi:10.1016/j.cyto.2006.09.001

    Article  CAS  PubMed  Google Scholar 

  • Michea P, Vargas P, Donnadieu MH, Rosemblatt M, Bono MR, Dumenil G, Soumelis V (2013) Epithelial control of the human pDC response to extracellular bacteria. Eur J Immunol 43(5):1264–1273. doi:10.1002/eji.201242990

    Article  CAS  PubMed  Google Scholar 

  • Miller LS, Cho JS (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol 11(8):505–518. doi:10.1038/nri3010

    Article  CAS  PubMed  Google Scholar 

  • Miller LS, O’Connell RM, Gutierrez MA, Pietras EM, Shahangian A, Gross CE, Thirumala A, Cheung AL, Cheng G, Modlin RL (2006) MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 24(1):79–91. doi:10.1016/j.immuni.2005.11.011

    Article  CAS  PubMed  Google Scholar 

  • Miller LS, Pietras EM, Uricchio LH, Hirano K, Rao S, Lin H, O’Connell RM, Iwakura Y, Cheung AL, Cheng G, Modlin RL (2007) Inflammasome-mediated production of IL-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol 179(10):6933–6942

    Article  CAS  PubMed  Google Scholar 

  • Mjosberg J, Eidsmo L (2014) Update on innate lymphoid cells in atopic and non-atopic inflammation in the airways and skin. Clin Exp Allergy 44(8):1033–1043. doi:10.1111/cea.12353

    Article  CAS  PubMed  Google Scholar 

  • Monticelli LA, Sonnenberg GF, Artis D (2012) Innate lymphoid cells: critical regulators of allergic inflammation and tissue repair in the lung. Curr Opin Immunol 24(3):284–289. doi:10.1016/j.coi.2012.03.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore CE, Segal S, Berendt AR, Hill AV, Day NP (2004) Lack of association between Toll-like receptor 2 polymorphisms and susceptibility to severe disease caused by Staphylococcus aureus. Clin Diagn Lab Immunol 11(6):1194–1197. doi:10.1128/cdli.11.6.1194-1197.2004

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mrabet-Dahbi S, Dalpke AH, Niebuhr M, Frey M, Draing C, Brand S, Heeg K, Werfel T, Renz H (2008) The Toll-like receptor 2 R753Q mutation modifies cytokine production and Toll-like receptor expression in atopic dermatitis. J Allergy Clin Immunol 121(4):1013–1019. doi:10.1016/j.jaci.2007.11.029

    Article  CAS  PubMed  Google Scholar 

  • Munoz-Planillo R, Franchi L, Miller LS, Nunez G (2009) A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J Immunol 183(6):3942–3948. doi:jimmunol.0900729 [pii] 10.4049/jimmunol.0900729

  • Nakamura Y, Oscherwitz J, Cease KB, Chan SM, Munoz-Planillo R, Hasegawa M, Villaruz AE, Cheung GY, McGavin MJ, Travers JB, Otto M, Inohara N, Nunez G (2013) Staphylococcus delta-toxin induces allergic skin disease by activating mast cells. Nature 503(7476):397–401. doi:10.1038/nature12655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama M, Kurokawa K, Nakamura K, Lee BL, Sekimizu K, Kubagawa H, Hiramatsu K, Yagita H, Okumura K, Takai T, Underhill DM, Aderem A, Ogasawara K (2012) Inhibitory receptor paired Ig-like receptor B is exploited by Staphylococcus aureus for virulence. J Immunol 189(12):5903–5911. doi:10.4049/jimmunol.1201940

    Article  CAS  PubMed  Google Scholar 

  • Nandi A, Dey S, Biswas J, Jaiswal P, Naaz S, Yasmin T, Bishayi B (2015) Differential induction of inflammatory cytokines and reactive oxygen species in murine peritoneal macrophages and resident fresh bone marrow cells by acute staphylococcus aureus infection: contribution of toll-like receptor 2 (TLR2). Inflammation 38(1):224–244. doi:10.1007/s10753-014-0026-8

    Article  CAS  PubMed  Google Scholar 

  • Negrini TC, Arthur RA, Waeiss RA, Carlosa IZ, Srinivasan M (2014) Salivary epithelial cells as model to study immune response against cutaneous pathogens. Clin Transl Sci 7(1):48–51. doi:10.1111/cts.12113

    Article  CAS  PubMed  Google Scholar 

  • Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW (2000) Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 68(2):688–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neth O, Jack DL, Johnson M, Klein NJ, Turner MW (2002) Enhancement of complement activation and opsonophagocytosis by complexes of mannose-binding lectin with mannose-binding lectin-associated serine protease after binding to Staphylococcus aureus. J Immunol 169(8):4430–4436

    Article  CAS  PubMed  Google Scholar 

  • Neumann A, Berends ET, Nerlich A, Molhoek EM, Gallo RL, Meerloo T, Nizet V, Naim HY, von Kockritz-Blickwede M (2014) The antimicrobial peptide LL-37 facilitates the formation of neutrophil extracellular traps. Biochem J 464(1):3–11. doi:10.1042/bj20140778

    Article  CAS  PubMed  Google Scholar 

  • Nguyen MT, Kraft B, Yu W, Demicrioglu DD, Hertlein T, Burian M, Schmaler M, Boller K, Bekeredjian-Ding I, Ohlsen K, Schittek B, Gotz F (2015) The nuSaalpha specific lipoprotein like cluster (lpl) of S. aureus USA300 contributes to immune stimulation and invasion in human cells. PLoS Pathog 11(6):e1004984. doi:10.1371/journal.ppat.1004984 PPATHOGENS-D-15-00227 [pii]

  • Niebuhr M, Baumert K, Heratizadeh A, Satzger I, Werfel T (2014) Impaired NLRP3 inflammasome expression and function in atopic dermatitis due to Th2 milieu. Allergy 69(8):1058–1067. doi:10.1111/all.12428

    Article  CAS  PubMed  Google Scholar 

  • Niebuhr M, Baumert K, Werfel T (2010a) TLR-2-mediated cytokine and chemokine secretion in human keratinocytes. Exp Dermatol 19(10):873–877. doi:10.1111/j.1600-0625.2010.01140.x

    Article  CAS  PubMed  Google Scholar 

  • Niebuhr M, Langnickel J, Sigel S, Werfel T (2010b) Dysregulation of CD36 upon TLR-2 stimulation in monocytes from patients with atopic dermatitis and the TLR2 R753Q polymorphism. Exp Dermatol 19(8):e296–e298. doi:10.1111/j.1600-0625.2009.00989.x

    Article  PubMed  Google Scholar 

  • Niebuhr M, Heratizadeh A, Wichmann K, Satzger I, Werfel T (2011) Intrinsic alterations of pro-inflammatory mediators in unstimulated and TLR-2 stimulated keratinocytes from atopic dermatitis patients. Exp Dermatol 20(6):468–472. doi:10.1111/j.1600-0625.2011.01277.x

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuis EE, Matsumoto T, Lindenbergh D, Willemsen R, Kaser A, Simons-Oosterhuis Y, Brugman S, Yamaguchi K, Ishikawa H, Aiba Y, Koga Y, Samsom JN, Oshima K, Kikuchi M, Escher JC, Hattori M, Onderdonk AB, Blumberg RS (2009) Cd1d-dependent regulation of bacterial colonization in the intestine of mice. J Clin Invest 119(5):1241–1250. doi:10.1172/jci36509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsen NJ, Deininger S, Nonstad U, Skjeldal F, Husebye H, Rodionov D, von Aulock S, Hartung T, Lien E, Bakke O, Espevik T (2008) Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling: role of CD14 and CD36. J Leukoc Biol 84(1):280–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson N, Bremell T, Tarkowski A, Carlsten H (1999) Protective role of NK1.1+ cells in experimental Staphylococcus aureus arthritis. Clin Exp Immunol 117(1):63–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowrouzian FL, Dauwalder O, Meugnier H, Bes M, Etienne J, Vandenesch F, Lindberg E, Hesselmar B, Saalman R, Strannegard IL, Aberg N, Adlerberth I, Wold AE, Lina G (2011) Adhesin and superantigen genes and the capacity of Staphylococcus aureus to colonize the infantile gut. J Infect Dis 204(5):714–721. doi:10.1093/infdis/jir388

    Article  CAS  PubMed  Google Scholar 

  • Nurjadi D, Herrmann E, Hinderberger I, Zanger P (2013) Impaired beta-defensin expression in human skin links DEFB1 promoter polymorphisms with persistent Staphylococcus aureus nasal carriage. J Infect Dis 207(4):666–674. doi:10.1093/infdis/jis735

    Article  CAS  PubMed  Google Scholar 

  • Olaru F, Jensen LE (2010) Staphylococcus aureus stimulates neutrophil targeting chemokine expression in keratinocytes through an autocrine IL-1alpha signaling loop. J Invest Dermatol 130(7):1866–1876. doi:10.1038/jid.2010.37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldenburg M, Kruger A, Ferstl R, Kaufmann A, Nees G, Sigmund A, Bathke B, Lauterbach H, Suter M, Dreher S, Koedel U, Akira S, Kawai T, Buer J, Wagner H, Bauer S, Hochrein H, Kirschning CJ (2012) TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 337(6098):1111–1115. doi:10.1126/science.1220363 science.1220363 [pii]

  • Ono K, Nishitani C, Mitsuzawa H, Shimizu T, Sano H, Suzuki H, Kodama T, Fujii N, Fukase K, Hirata K, Kuroki Y (2006) Mannose-binding lectin augments the uptake of lipid A, Staphylococcus aureus, and Escherichia coli by Kupffer cells through increased cell surface expression of scavenger receptor A. J Immunol 177(8):5517–5523

    Article  CAS  PubMed  Google Scholar 

  • Over B, Ziegler S, Foermer S, Weber AN, Bode KA, Heeg K, Bekeredjian-Ding I (2013) IRAK4 turns IL-10+ phospho-FOXO+ monocytes into pro-inflammatory cells by suppression of protein kinase B. Eur J Immunol 43(6):1630–1642. doi:10.1002/eji.201243217

    Article  CAS  PubMed  Google Scholar 

  • Palecanda A, Paulauskis J, Al-Mutairi E, Imrich A, Qin G, Suzuki H, Kodama T, Tryggvason K, Koziel H, Kobzik L (1999) Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J Exp Med 189(9):1497–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parcina M, Miranda-Garcia MA, Durlanik S, Ziegler S, Over B, Georg P, Foermer S, Ammann S, Hilmi D, Weber KJ, Schiller M, Heeg K, Schneider-Brachert W, Gotz F, Bekeredjian-Ding I (2013) Pathogen-triggered activation of plasmacytoid dendritic cells induces IL-10-producing B cells in response to Staphylococcus aureus. J Immunol 190(4):1591–1602. doi:10.4049/jimmunol.1201222

  • Parcina M, Wendt C, Goetz F, Zawatzky R, Zahringer U, Heeg K, Bekeredjian-Ding I (2008) Staphylococcus aureus-induced plasmacytoid dendritic cell activation is based on an IgG-mediated memory response. J Immunol 181(6):3823–3833. doi:181/6/3823 [pii]

    Google Scholar 

  • Parker D, Prince A (2012) Staphylococcus aureus induces type I IFN signaling in dendritic cells via TLR9. J Immunol 189(8):4040–4046. doi:10.4049/jimmunol.1201055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perret M, Badiou C, Lina G, Burbaud S, Benito Y, Bes M, Cottin V, Couzon F, Juruj C, Dauwalder O, Goutagny N, Diep BA, Vandenesch F, Henry T (2012) Cross-talk between Staphylococcus aureus leukocidins-intoxicated macrophages and lung epithelial cells triggers chemokine secretion in an inflammasome-dependent manner. Cell Microbiol 14(7):1019–1036. doi:10.1111/j.1462-5822.2012.01772.x

    Article  CAS  PubMed  Google Scholar 

  • Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Gotz F (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274(13):8405–8410

    Article  CAS  PubMed  Google Scholar 

  • Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J (2007) Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ 14(9):1583–1589. doi:10.1038/sj.cdd.4402195

    Article  CAS  PubMed  Google Scholar 

  • Philip NH, Artis D (2013) New friendships and old feuds: relationships between innate lymphoid cells and microbial communities. Immunol Cell Biol 91(3):225–231. doi:10.1038/icb.2013.2

    Article  CAS  PubMed  Google Scholar 

  • Pizzolla A, Hultqvist M, Nilson B, Grimm MJ, Eneljung T, Jonsson IM, Verdrengh M, Kelkka T, Gjertsson I, Segal BH, Holmdahl R (2012) Reactive oxygen species produced by the NADPH oxidase 2 complex in monocytes protect mice from bacterial infections. J Immunol 188(10):5003–5011. doi:10.4049/jimmunol.1103430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Queck SY, Jameson-Lee M, Villaruz AE, Bach TH, Khan BA, Sturdevant DE, Ricklefs SM, Li M, Otto M (2008) RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol Cell 32(1):150–158. doi:10.1016/j.molcel.2008.08.005 S1097-2765(08)00537-6 [pii]

  • Quinn GA, Cole AM (2007) Suppression of innate immunity by a nasal carriage strain of Staphylococcus aureus increases its colonization on nasal epithelium. Immunology 122(1):80–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed P, Atilano ML, Alves R, Hoiczyk E, Sher X, Reichmann NT, Pereira PM, Roemer T, Filipe SR, Pereira-Leal JB, Ligoxygakis P, Pinho MG (2015) Staphylococcus aureus survives with a minimal peptidoglycan synthesis machine but sacrifices virulence and antibiotic resistance. PLoS Pathog 11(5):e1004891. doi:10.1371/journal.ppat.1004891

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reis e Sousa C, Stahl PD, Austyn JM (1993) Phagocytosis of antigens by Langerhans cells in vitro. J Exp Med 178(2):509–519

    Google Scholar 

  • Rigby KM, DeLeo FR (2012) Neutrophils in innate host defense against Staphylococcus aureus infections. Semin Immunopathol 34(2):237–259. doi:10.1007/s00281-011-0295-3

    Article  CAS  PubMed  Google Scholar 

  • Robertson CM, Perrone EE, McConnell KW, Dunne WM, Boody B, Brahmbhatt T, Diacovo MJ, Van Rooijen N, Hogue LA, Cannon CL, Buchman TG, Hotchkiss RS, Coopersmith CM (2008) Neutrophil depletion causes a fatal defect in murine pulmonary Staphylococcus aureus clearance. J Surg Res 150(2):278–285. doi:10.1016/j.jss.2008.02.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinette ML, Fuchs A, Cortez VS, Lee JS, Wang Y, Durum SK, Gilfillan S, Colonna M (2015) Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat Immunol 16(3):306–317. doi:10.1038/ni.3094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson KM, Lee B, Scheller EV, Mandalapu S, Enelow RI, Kolls JK, Alcorn JF (2015) The role of IL-27 in susceptibility to post-influenza Staphylococcus aureus pneumonia. Respir Res 16(1):10. doi:10.1186/s12931-015-0168-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha-de-Souza CM, Berent-Maoz B, Mankuta D, Moses AE, Levi-Schaffer F (2008) Human mast cell activation by Staphylococcus aureus: interleukin-8 and tumor necrosis factor alpha release and the role of Toll-like receptor 2 and CD48 molecules. Infect Immun 76(10):4489–4497. doi:10.1128/iai.00270-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronnberg E, Johnzon CF, Calounova G, Garcia Faroldi G, Grujic M, Hartmann K, Roers A, Guss B, Lundequist A, Pejler G (2014) Mast cells are activated by Staphylococcus aureus in vitro but do not influence the outcome of intraperitoneal S. aureus infection in vivo. Immunology 143(2):155–163. doi:10.1111/imm.12297

  • Roquilly A, Gautreau L, Segain JP, de Coppet P, Sebille V, Jacqueline C, Caillon J, Potel G, Lejus C, Josien R, Asehnoune K (2010) CpG-ODN and MPLA prevent mortality in a murine model of post-hemorrhage-Staphyloccocus aureus pneumonia. PLoS One 5(10):e13228. doi:10.1371/journal.pone.0013228 e13228 [pii]

  • Ryu S, Song PI, Seo CH, Cheong H, Park Y (2014) Colonization and infection of the skin by S. aureus: immune system evasion and the response to cationic antimicrobial peptides. Int J Mol Sci 15(5):8753–8772. doi:10.3390/ijms15058753 ijms15058753 [pii]

  • Sachse F, Becker K, Rudack C (2010) Incidence of staphylococcal colonization and of the 753Q Toll-like receptor 2 variant in nasal polyposis. Am J Rhinol Allergy 24(1):e10–e13. doi:10.2500/ajra.2010.24.3416

    Article  PubMed  Google Scholar 

  • Sakiniene E, Bremell T, Tarkowski A (1999) Complement depletion aggravates Staphylococcus aureus septicaemia and septic arthritis. Clin Exp Immunol 115(1):95–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvi V, Scutera S, Rossi S, Zucca M, Alessandria M, Greco D, Bosisio D, Sozzani S, Musso T (2013) Dual regulation of osteopontin production by TLR stimulation in dendritic cells. J Leukoc Biol 94(1):147–158. doi:10.1189/jlb.0412194

    Article  CAS  PubMed  Google Scholar 

  • Sankaran K, Gupta SD, Wu HC (1995) Modification of bacterial lipoproteins. Methods Enzymol 250:683–697. doi:0076-6879(95)50105-3 [pii]

    Google Scholar 

  • Sankaran K, Wu HC (1995) Bacterial prolipoprotein signal peptidase. Methods Enzymol 248:169–180

    Article  CAS  PubMed  Google Scholar 

  • Schaffler H, Demircioglu DD, Kuhner D, Menz S, Bender A, Autenrieth IB, Bodammer P, Lamprecht G, Gotz F, Frick JS (2014) NOD2 stimulation by Staphylococcus aureus-derived peptidoglycan is boosted by Toll-like receptor 2 costimulation with lipoproteins in dendritic cells. Infect Immun 82(11):4681–4688. doi:10.1128/iai.02043-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schindler D, Gutierrez MG, Beineke A, Rauter Y, Rohde M, Foster S, Goldmann O, Medina E (2012) Dendritic cells are central coordinators of the host immune response to Staphylococcus aureus bloodstream infection. Am J Pathol 181(4):1327–1337. doi:10.1016/j.ajpath.2012.06.039

    Article  CAS  PubMed  Google Scholar 

  • Schmaler M, Jann NJ, Ferracin F, Landolt LZ, Biswas L, Götz F, Landmann R (2009) Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J Immunol 182(11):7110–7118. doi:182/11/7110 [pii] 10.4049/jimmunol.0804292

  • Schmaler M, Jann NJ, Ferracin F, Landmann R (2011) T and B cells are not required for clearing Staphylococcus aureus in systemic infection despite a strong TLR2-MyD88-dependent T cell activation. J Immunol 186(1):443–452. doi:10.4049/jimmunol.1001407

    Article  CAS  PubMed  Google Scholar 

  • Schmaler M, Jann NJ, Gotz F, Landmann R (2010) Staphylococcal lipoproteins and their role in bacterial survival in mice. IntJMedMicrobiol 300(2–3):155–160. doi:S1438-4221(09)00111-8 [pii]; 10.1016/j.ijmm.2009.08.018 [doi]

  • Schreiner J, Kretschmer D, Klenk J, Otto M, Buhring HJ, Stevanovic S, Wang JM, Beer-Hammer S, Peschel A, Autenrieth SE (2013) Staphylococcus aureus phenol-soluble modulin peptides modulate dendritic cell functions and increase in vitro priming of regulatory T cells. J Immunol 190(7):3417–3426. doi:10.4049/jimmunol.1202563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang SQ, Chen GX, Shen J, Yu XH, Wang KY (2005) The binding of MBL to common bacteria in infectious diseases of children. J Zhejiang Univ Sci B 6(1):53–56. doi:10.1631/jzus.2005.B0053

    Article  PubMed  Google Scholar 

  • Shi L, Takahashi K, Dundee J, Shahroor-Karni S, Thiel S, Jensenius JC, Gad F, Hamblin MR, Sastry KN, Ezekowitz RA (2004) Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 199(10):1379–1390. doi:10.1084/jem.20032207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibuya A, Honda S (2006) Molecular and functional characteristics of the Fcalpha/muR, a novel Fc receptor for IgM and IgA. Springer Semin Immunopathol 28(4):377–382. doi:10.1007/s00281-006-0050-3

    Article  CAS  PubMed  Google Scholar 

  • Shimada T, Park BG, Wolf AJ, Brikos C, Goodridge HS, Becker CA, Reyes CN, Miao EA, Aderem A, Gotz F, Liu GY, Underhill DM (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7(1):38–49. doi:10.1016/j.chom.2009.12.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimaoka T, Kume N, Minami M, Hayashida K, Sawamura T, Kita T, Yonehara S (2001) LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J Immunol 166(8):5108–5114

    Article  CAS  PubMed  Google Scholar 

  • Shinohara ML, Kim JH, Garcia VA, Cantor H (2008) Engagement of the type I interferon receptor on dendritic cells inhibits T helper 17 cell development: role of intracellular osteopontin. Immunity 29(1):68–78. doi:10.1016/j.immuni.2008.05.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sieprawska-Lupa M, Mydel P, Krawczyk K, Wojcik K, Puklo M, Lupa B, Suder P, Silberring J, Reed M, Pohl J, Shafer W, McAleese F, Foster T, Travis J, Potempa J (2004) Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48(12):4673–4679. doi:48/12/4673 [pii] 10.1128/AAC.48.12.4673-4679.2004

  • Simanski M, Glaser R, Koten B, Meyer-Hoffert U, Wanner S, Weidenmaier C, Peschel A, Harder J (2013) Staphylococcus aureus subverts cutaneous defense by D-alanylation of teichoic acids. Exp Dermatol 22(4):294–296. doi:10.1111/exd.12114

    Article  CAS  PubMed  Google Scholar 

  • Skabytska Y, Wolbing F, Gunther C, Koberle M, Kaesler S, Chen KM, Guenova E, Demircioglu D, Kempf WE, Volz T, Rammensee HG, Schaller M, Rocken M, Gotz F, Biedermann T (2014) Cutaneous innate immune sensing of Toll-like receptor 2-6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. Immunity 41(5):762–775. doi:10.1016/j.immuni.2014.10.009

    Article  CAS  PubMed  Google Scholar 

  • Small CL, McCormick S, Gill N, Kugathasan K, Santosuosso M, Donaldson N, Heinrichs DE, Ashkar A, Xing Z (2008) NK cells play a critical protective role in host defense against acute extracellular Staphylococcus aureus bacterial infection in the lung. J Immunol 180(8):5558–5568

    Article  CAS  PubMed  Google Scholar 

  • Sokolovska A, Becker CE, Ip WK, Rathinam VA, Brudner M, Paquette N, Tanne A, Vanaja SK, Moore KJ, Fitzgerald KA, Lacy-Hulbert A, Stuart LM (2013) Activation of caspase-1 by the NLRP3 inflammasome regulates the NADPH oxidase NOX2 to control phagosome function. Nat Immunol 14(6):543–553. doi:10.1038/ni.2595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soong G, Paulino F, Wachtel S, Parker D, Wickersham M, Zhang D, Brown A, Lauren C, Dowd M, West E, Horst B, Planet P, Prince A (2015) Methicillin-resistant Staphylococcus aureus adaptation to human keratinocytes. MBio 6(2). doi:10.1128/mBio.00289-15

  • Stoll H, Dengjel J, Nerz C, Gotz F (2005) Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect Immun 73(4):2411–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, Hennessy EJ, Ezekowitz RA, Moore KJ (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170(3):477–485. doi:jcb.200501113 [pii] 10.1083/jcb.200501113

  • Subramaniam R, Barnes PF, Fletcher K, Boggaram V, Hillberry Z, Neuenschwander P, Shams H (2014) Protecting against post-influenza bacterial pneumonia by increasing phagocyte recruitment and ROS production. J Infect Dis 209(11):1827–1836. doi:10.1093/infdis/jit830

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Suzuki S, Duncan GS, Millar DG, Wada T, Mirtsos C, Takada H, Wakeham A, Itie A, Li S, Penninger JM, Wesche H, Ohashi PS, Mak TW, Yeh WC (2002) Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 416(6882):750–756. doi:10.1038/nature736

    Article  CAS  PubMed  Google Scholar 

  • Tait Wojno ED, Artis D (2012) Innate lymphoid cells: balancing immunity, inflammation, and tissue repair in the intestine. Cell Host Microbe 12(4):445–457. doi:10.1016/j.chom.2012.10.003

    Article  CAS  PubMed  Google Scholar 

  • Takai T, Chen X, Xie Y, Vu AT, Le TA, Kinoshita H, Kawasaki J, Kamijo S, Hara M, Ushio H, Baba T, Hiramatsu K, Ikeda S, Ogawa H, Okumura K (2014) TSLP expression induced via Toll-like receptor pathways in human keratinocytes. Methods Enzymol 535:371–387. doi:10.1016/b978-0-12-397925-4.00021-3

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi O, Hoshino K, Akira S (2000) Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165(10):5392–5396

    Article  CAS  PubMed  Google Scholar 

  • Tebartz C, Horst SA, Sparwasser T, Huehn J, Beineke A, Peters G, Medina E (2015) A major role for myeloid-derived suppressor cells and a minor role for regulatory T cells in immunosuppression during Staphylococcus aureus infection. J Immunol 194(3):1100–1111. doi:10.4049/jimmunol.1400196

    Article  CAS  PubMed  Google Scholar 

  • Terada M, Tsutsui H, Imai Y, Yasuda K, Mizutani H, Yamanishi K, Kubo M, Matsui K, Sano H, Nakanishi K (2006) Contribution of IL-18 to atopic-dermatitis-like skin inflammation induced by Staphylococcus aureus product in mice. Proc Natl Acad Sci U S A 103(23):8816–8821. doi:10.1073/pnas.0602900103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tewfik MA, Bosse Y, Hudson TJ, Vallee-Smejda S, Al-Shemari H, Desrosiers M (2008) Assessment of Toll-like receptor 2 gene polymorphisms in severe chronic rhinosinusitis. J Otolaryngol Head Neck Surg 37(4):552–558

    PubMed  Google Scholar 

  • Urb M, Sheppard DC (2012) The role of mast cells in the defence against pathogens. PLoS Pathog 8(4):e1002619. doi:10.1371/journal.ppat.1002619 PPATHOGENS-D-12-00120 [pii]

  • Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, Bassetti M, Aderem A (1999) The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401(6755):811–815. doi:10.1038/44605

    Article  CAS  PubMed  Google Scholar 

  • van der Laan LJ, Dopp EA, Haworth R, Pikkarainen T, Kangas M, Elomaa O, Dijkstra CD, Gordon S, Tryggvason K, Kraal G (1999) Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol 162(2):939–947

    PubMed  Google Scholar 

  • Verdrengh M, Tarkowski A (1997) Role of neutrophils in experimental septicemia and septic arthritis induced by Staphylococcus aureus. Infect Immun 65(7):2517–2521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verkaik NJ, de Vogel CP, Boelens HA, Grumann D, Hoogenboezem T, Vink C, Hooijkaas H, Foster TJ, Verbrugh HA, van Belkum A, van Wamel WJ (2009) Anti-staphylococcal humoral immune response in persistent nasal carriers and noncarriers of Staphylococcus aureus. J Infect Dis 199(5):625–632

    Article  PubMed  Google Scholar 

  • Viau M, Longo NS, Lipsky PE, Zouali M (2005) Staphylococcal protein a deletes B-1a and marginal zone B lymphocytes expressing human immunoglobulins: an immune evasion mechanism. J Immunol 175(11):7719–7727

    Article  CAS  PubMed  Google Scholar 

  • Volz T, Nega M, Buschmann J, Kaesler S, Guenova E, Peschel A, Rocken M, Gotz F, Biedermann T (2010) Natural Staphylococcus aureus-derived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals. FASEB J 24(10):4089–4102. doi:10.1096/fj.09-151001

    Article  CAS  PubMed  Google Scholar 

  • von Bernuth H, Picard C, Puel A, Casanova JL (2012) Experimental and natural infections in MyD88- and IRAK-4-deficient mice and humans. Eur J Immunol 42(12):3126–3135. doi:10.1002/eji.201242683

    Article  CAS  Google Scholar 

  • von Kockritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M, Medina E (2008a) Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111(6):3070–3080. doi:10.1182/blood-2007-07-104018

    Article  CAS  Google Scholar 

  • von Kockritz-Blickwede M, Rohde M, Oehmcke S, Miller LS, Cheung AL, Herwald H, Foster S, Medina E (2008b) Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am J Pathol 173(6):1657–1668. doi:10.2353/ajpath.2008.080337

    Article  CAS  Google Scholar 

  • Vu AT, Baba T, Chen X, Le TA, Kinoshita H, Xie Y, Kamijo S, Hiramatsu K, Ikeda S, Ogawa H, Okumura K, Takai T (2010) Staphylococcus aureus membrane and diacylated lipopeptide induce thymic stromal lymphopoietin in keratinocytes through the Toll-like receptor 2-Toll-like receptor 6 pathway. J Allergy Clin Immunol 126(5):985–993, 993 e981-983. doi:10.1016/j.jaci.2010.09.002

  • Vultaggio A, Nencini F, Pratesi S, Maggi L, Guarna A, Annunziato F, Romagnani S, Parronchi P, Maggi E (2011) The TLR7 ligand 9-benzyl-2-butoxy-8-hydroxy adenine inhibits IL-17 response by eliciting IL-10 and IL-10-inducing cytokines. J Immunol 186(8):4707–4715. doi:10.4049/jimmunol.1002398

    Article  CAS  PubMed  Google Scholar 

  • Wagner C, Iking-Konert C, Hug F, Stegmaier S, Heppert V, Wentzensen A, Hansch GM (2006) Cellular inflammatory response to persistent localized Staphylococcus aureus infection: phenotypical and functional characterization of polymorphonuclear neutrophils (PMN). Clin Exp Immunol 143(1):70–77. doi:10.1111/j.1365-2249.2005.02963.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanke I, Steffen H, Christ C, Krismer B, Gotz F, Peschel A, Schaller M, Schittek B (2011) Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J Invest Dermatol 131(2):382–390. doi:10.1038/jid.2010.328

    Article  CAS  PubMed  Google Scholar 

  • Westerberg LS, de la Fuente MA, Wermeling F, Ochs HD, Karlsson MC, Snapper SB, Notarangelo LD (2008) WASP confers selective advantage for specific hematopoietic cell populations and serves a unique role in marginal zone B-cell homeostasis and function. Blood 112(10):4139–4147. doi:10.1182/blood-2008-02-140715 blood-2008-02-140715 [pii]

  • Wolf AJ, Arruda A, Reyes CN, Kaplan AT, Shimada T, Shimada K, Arditi M, Liu G, Underhill DM (2011) Phagosomal degradation increases TLR access to bacterial ligands and enhances macrophage sensitivity to bacteria. J Immunol 187(11):6002–6010. doi:10.4049/jimmunol.1100232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang D, Chertov O, Oppenheim JJ (2001) Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). J Leukoc Biol 69(5):691–697

    CAS  PubMed  Google Scholar 

  • Yimin Kohanawa M, Zhao S, Ozaki M, Haga S, Nan G, Kuge Y, Tamaki N (2013) Contribution of toll-like receptor 2 to the innate response against Staphylococcus aureus infection in mice. PLoS ONE 8(9):e74287. doi:10.1371/journal.pone.0074287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaidman-Remy A, Herve M, Poidevin M, Pili-Floury S, Kim MS, Blanot D, Oh BH, Ueda R, Mengin-Lecreulx D, Lemaitre B (2006) The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24(4):463–473

    Article  CAS  PubMed  Google Scholar 

  • Zanger P, Nurjadi D, Vath B, Kremsner PG (2011) Persistent nasal carriage of Staphylococcus aureus is associated with deficient induction of human beta-defensin 3 after sterile wounding of healthy skin in vivo. Infect Immun 79(7):2658–2662. doi:10.1128/iai.00101-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Li W, Gao Y, Li J, Wang H (2014) Exposure to particular matter increases susceptibility to respiratory Staphylococcus aureus infection in rats via reducing pulmonary natural killer cells. Toxicology 325:180–188. doi:10.1016/j.tox.2014.09.006

    Article  CAS  PubMed  Google Scholar 

  • Ziegler SF, Roan F, Bell BD, Stoklasek TA, Kitajima M, Han H (2013) The biology of thymic stromal lymphopoietin (TSLP). Adv Pharmacol 66:129–155. doi:10.1016/b978-0-12-404717-4.00004-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Microbiology, Paul-Ehrlich-Institute, Paul-Ehrlich-Str. 51-59, 63225, Langen, Germany

    Isabelle Bekeredjian-Ding

  2. Division of EU Cooperation/Microbiology, Paul-Ehrlich-Institute, Paul-Ehrlich-Str. 51-59, 63225, Langen, Germany

    Christoph Stein & Julia Uebele

Authors
  1. Isabelle Bekeredjian-Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christoph Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julia Uebele
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Bekeredjian-Ding .

Editor information

Editors and Affiliations

  1. GSK Vaccines, Siena, Italy

    Fabio Bagnoli

  2. GSK Vaccines, Siena, Italy

    Rino Rappuoli

  3. Center for Integrative Biology (CIBIO), University of Trento, Trento, Italy

    Guido Grandi

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Bekeredjian-Ding, I., Stein, C., Uebele, J. (2015). The Innate Immune Response Against Staphylococcus aureus . In: Bagnoli, F., Rappuoli, R., Grandi, G. (eds) Staphylococcus aureus. Current Topics in Microbiology and Immunology, vol 409. Springer, Cham. https://doi.org/10.1007/82_2015_5004

Download citation

Publish with us

Policies and ethics

Search

Navigation