Abstract
A complex interplay between host and bacterial factors allows Staphylococcus aureus to occupy its niche as a human commensal and a major human pathogen. The role of neutrophils as a critical component of the innate immune response against S. aureus, particularly for control of systemic infection, has been established in both animal models and in humans with acquired and congenital neutrophil dysfunction. The role of the adaptive immune system is less clear. Although deficiencies in adaptive immunity do not result in the marked susceptibility to S. aureus infection that neutrophil dysfunction imparts, emerging evidence suggests both T cell- and B cell-mediated adaptive immunity can influence host susceptibility and control of S. aureus. The contribution of adaptive immunity depends on the context and site of infection and can be either beneficial or detrimental to the host. Furthermore, S. aureus has evolved mechanisms to manipulate adaptive immune responses to its advantage. In this chapter, we will review the evidence for the role of adaptive immunity during S. aureus infections. Further elucidation of this role will be important to understand how it influences susceptibility to infection and to appropriately design vaccines that elicit adaptive immune responses to protect against subsequent infections.
References
Abdelnour A, Bremell T, Holmdahl R, Tarkowski A (1994) Role of T lymphocytes in experimental Staphylococcus aureus arthritis. Scand J Immunol 39(4):403–408
Adhikari RP, Ajao AO, Aman MJ, Karauzum H, Sarwar J, Lydecker AD, Johnson JK, Nguyen C, Chen WH, Roghmann MC (2012a) Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S. aureus infections. J Infect Dis 206(6):915–923. doi:10.1093/infdis/jis462
Adhikari RP, Karauzum H, Sarwar J, Abaandou L, Mahmoudieh M, Boroun AR, Vu H, Nguyen T, Devi VS, Shulenin S, Warfield KL, Aman MJ (2012b) Novel structurally designed vaccine for S. aureus alpha-hemolysin: protection against bacteremia and pneumonia. PLoS One 7(6):e38567. doi:10.1371/journal.pone.0038567
Allen JE, Sutherland TE (2014) Host protective roles of type 2 immunity: parasite killing and tissue repair, flip sides of the same coin. Semin Immunol 26(4):329–340. doi:10.1016/j.smim.2014.06.003
Bagnoli F, Fontana MR, Soldaini E, Mishra RP, Fiaschi L, Cartocci E, Nardi-Dei V, Ruggiero P, Nosari S, De Falco MG, Lofano G, Marchi S, Galletti B, Mariotti P, Bacconi M, Torre A, Maccari S, Scarselli M, Rinaudo CD, Inoshima N, Savino S, Mori E, Rossi-Paccani S, Baudner B, Pallaoro M, Swennen E, Petracca R, Brettoni C, Liberatori S, Norais N, Monaci E, Bubeck Wardenburg J, Schneewind O, O’Hagan DT, Valiante NM, Bensi G, Bertholet S, De Gregorio E, Rappuoli R, Grandi G (2015) Vaccine composition formulated with a novel TLR7-dependent adjuvant induces high and broad protection against Staphylococcus aureus. Proc Natl Acad Sci USA 112(12):3680–3685. doi:10.1073/pnas.1424924112
Bavari S, Dyas B, Ulrich RG (1996) Superantigen vaccines: a comparative study of genetically attenuated receptor-binding mutants of staphylococcal enterotoxin A. J Infect Dis 174(2):338–345
Boguniewicz M, Leung DY (2011) Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol Rev 242(1):233–246. doi:10.1111/j.1600-065X.2011.01027.x
Boles JW, Pitt ML, LeClaire RD, Gibbs PH, Torres E, Dyas B, Ulrich RG, Bavari S (2003) Generation of protective immunity by inactivated recombinant staphylococcal enterotoxin B vaccine in nonhuman primates and identification of correlates of immunity. Clin Immunol 108(1):51–59
Brauweiler AM, Goleva E, Leung DY (2014) Th2 cytokines increase Staphylococcus aureus alpha toxin-induced keratinocyte death through the signal transducer and activator of transcription 6 (STAT6). J Invest Dermatol 134(8):2114–2121. doi:10.1038/jid.2014.43
Bruton OC (1952) Agammaglobulinemia. Pediatrics 9(6):722–728
Bubeck Wardenburg J, Schneewind O (2008) Vaccine protection against Staphylococcus aureus pneumonia. J Exp Med 205(2):287–294. doi:10.1084/jem.20072208
Burbelo PD, Browne SK, Sampaio EP, Giaccone G, Zaman R, Kristosturyan E, Rajan A, Ding L, Ching KH, Berman A, Oliveira JB, Hsu AP, Klimavicz CM, Iadarola MJ, Holland SM (2010) Anti-cytokine autoantibodies are associated with opportunistic infection in patients with thymic neoplasia. Blood 116(23):4848–4858. doi:10.1182/blood-2010-05-286161
Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7(9):629–641. doi:10.1038/nrmicro2200
Chan LC, Chaili S, Filler SG, Barr K, Wang H, Kupferwasser D, Edwards JE Jr, Xiong YQ, Ibrahim AS, Miller LS, Schmidt CS, Hennessey JP Jr, Yeaman MR (2015) Non-redundant roles of IL-17A and IL-22 in murine host defense against cutaneous and hematogenous infection due to methicillin-resistant Staphylococcus aureus. Infect Immun. doi:10.1128/IAI.01061-15
Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, Monroe HR, Magorien JE, Blauvelt A, Kolls JK, Cheung AL, Cheng G, Modlin RL, Miller LS (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120(5):1762–1773. doi:10.1172/JCI40891
Choi SM, McAleer JP, Zheng M, Pociask DA, Kaplan MH, Qin S, Reinhart TA, Kolls JK (2013) Innate Stat3-mediated induction of the antimicrobial protein Reg3gamma is required for host defense against MRSA pneumonia. J Exp Med 210(3):551–561. doi:10.1084/jem.20120260
Choi SJ, Kim MH, Jeon J, Kim OY, Choi Y, Seo J, Hong SW, Lee WH, Jeon SG, Gho YS, Jee YK, Kim YK (2015) Active immunization with extracellular vesicles derived from Staphylococcus aureus effectively protects against staphylococcal lung infections, mainly via Th1 cell-mediated immunity. PLoS ONE 10(9):e0136021. doi:10.1371/journal.pone.0136021
Chung Y, Yang X, Chang SH, Ma L, Tian Q, Dong C (2006) Expression and regulation of IL-22 in the IL-17-producing CD4+ T lymphocytes. Cell Res 16(11):902–907. doi:10.1038/sj.cr.7310106
Conley ME, Howard VC (1993) X-linked agammaglobulinemia. In: Pagon RA, Adam MP, Ardinger HH et al (eds) GeneReviews. University of Washington, Seattle
Cook MC, Tangye SG (2009) Primary immune deficiencies affecting lymphocyte differentiation: lessons from the spectrum of resulting infections. Int Immunol 21(9):1003–1011. doi:10.1093/intimm/dxp076
Domanski PJ, Patel PR, Bayer AS, Zhang L, Hall AE, Syribeys PJ, Gorovits EL, Bryant D, Vernachio JH, Hutchins JT, Patti JM (2005) Characterization of a humanized monoclonal antibody recognizing clumping factor A expressed by Staphylococcus aureus. Infect Immun 73(8):5229–5232. doi:10.1128/IAI.73.8.5229-5232.2005
Etz H, Minh DB, Henics T, Dryla A, Winkler B, Triska C, Boyd AP, Sollner J, Schmidt W, von Ahsen U, Buschle M, Gill SR, Kolonay J, Khalak H, Fraser CM, von Gabain A, Nagy E, Meinke A (2002) Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc Natl Acad Sci USA 99(10):6573–6578. doi:10.1073/pnas.092569199
Falugi F, Kim HK, Missiakas DM, Schneewind O (2013) Role of protein A in the evasion of host adaptive immune responses by Staphylococcus aureus. MBio 4(5):e00575–e00513. doi:10.1128/mBio.00575-13
Fattom A, Schneerson R, Szu SC, Vann WF, Shiloach J, Karakawa WW, Robbins JB (1990) Synthesis and immunologic properties in mice of vaccines composed of Staphylococcus aureus type 5 and type 8 capsular polysaccharides conjugated to Pseudomonas aeruginosa exotoxin A. Infect Immun 58(7):2367–2374
Fattom AI, Sarwar J, Ortiz A, Naso R (1996) A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect Immun 64(5):1659–1665
Fattom A, Fuller S, Propst M, Winston S, Muenz L, He D, Naso R, Horwith G (2004) Safety and immunogenicity of a booster dose of Staphylococcus aureus types 5 and 8 capsular polysaccharide conjugate vaccine (StaphVAX) in hemodialysis patients. Vaccine 23(5):656–663. doi:10.1016/j.vaccine.2004.06.043
Feldmann M, Brennan FM, Maini R (1998) Cytokines in autoimmune disorders. Int Rev Immunol 17(1–4):217–228
Fowler VG, Allen KB, Moreira ED, Moustafa M, Isgro F, Boucher HW, Corey GR, Carmeli Y, Betts R, Hartzel JS, Chan IS, McNeely TB, Kartsonis NA, Guris D, Onorato MT, Smugar SS, DiNubile MJ, Sobanjo-ter Meulen A (2013) Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA 309(13):1368–1378. doi:10.1001/jama.2013.3010
Frank KM, Zhou T, Moreno-Vinasco L, Hollett B, Garcia JG, Bubeck Wardenburg J (2012) Host response signature to Staphylococcus aureus alpha-hemolysin implicates pulmonary Th17 response. Infect Immun 80(9):3161–3169. doi:10.1128/IAI.00191-12
Fritz SA, Tiemann KM, Hogan PG, Epplin EK, Rodriguez M, Al-Zubeidi DN, Bubeck Wardenburg J, Hunstad DA (2013) A serologic correlate of protective immunity against community-onset Staphylococcus aureus infection. Clin Infect Dis 56(11):1554–1561. doi:10.1093/cid/cit123
Gaidamakova EK, Myles IA, McDaniel DP, Fowler CJ, Valdez PA, Naik S, Gayen M, Gupta P, Sharma A, Glass PJ, Maheshwari RK, Datta SK, Daly MJ (2012) Preserving immunogenicity of lethally irradiated viral and bacterial vaccine epitopes using a radio-protective Mn2+ -Peptide complex from Deinococcus. Cell Host Microbe 12(1):117–124. doi:10.1016/j.chom.2012.05.011
Geginat J, Paroni M, Facciotti F, Gruarin P, Kastirr I, Caprioli F, Pagani M, Abrignani S (2013) The CD4-centered universe of human T cell subsets. Semin Immunol 25(4):252–262. doi:10.1016/j.smim.2013.10.012
Gjertsson I, Hultgren OH, Stenson M, Holmdahl R, Tarkowski A (2000) Are B lymphocytes of importance in severe Staphylococcus aureus infections? Infect Immun 68(5):2431–2434
Gresham HD, Lowrance JH, Caver TE, Wilson BS, Cheung AL, Lindberg FP (2000) Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol 164(7):3713–3722
Guillen C, McInnes IB, Vaughan DM, Kommajosyula S, Van Berkel PH, Leung BP, Aguila A, Brock JH (2002) Enhanced Th1 response to Staphylococcus aureus infection in human lactoferrin-transgenic mice. J Immunol 168(8):3950–3957
Guttman-Yassky E, Lowes MA, Fuentes-Duculan J, Zaba LC, Cardinale I, Nograles KE, Khatcherian A, Novitskaya I, Carucci JA, Bergman R, Krueger JG (2008) Low expression of the IL-23/Th17 pathway in atopic dermatitis compared to psoriasis. J Immunol 181(10):7420–7427
Hamid Q, Boguniewicz M, Leung DY (1994) Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J Clin Invest 94(2):870–876. doi:10.1172/JCI117408
Harro C, Betts R, Orenstein W, Kwak EJ, Greenberg HE, Onorato MT, Hartzel J, Lipka J, DiNubile MJ, Kartsonis N (2010) Safety and immunogenicity of a novel Staphylococcus aureus vaccine: results from the first study of the vaccine dose range in humans. Clin Vaccine Immunol 17(12):1868–1874. doi:10.1128/CVI.00356-10
Harro CD, Betts RF, Hartzel JS, Onorato MT, Lipka J, Smugar SS, Kartsonis NA (2012) The immunogenicity and safety of different formulations of a novel Staphylococcus aureus vaccine (V710): results of two Phase I studies. Vaccine 30(9):1729–1736. doi:10.1016/j.vaccine.2011.12.045
Henningsson L, Jirholt P, Lindholm C, Eneljung T, Silverpil E, Iwakura Y, Linden A, Gjertsson I (2010) Interleukin-17A during local and systemic Staphylococcus aureus-induced arthritis in mice. Infect Immun 78(9):3783–3790. doi:10.1128/IAI.00385-10
Hidron AI, Kempker R, Moanna A, Rimland D (2010) Methicillin-resistant Staphylococcus aureus in HIV-infected patients. Infect Drug Resist 3:73–86
Holland SM, DeLeo FR, Elloumi HZ, Hsu AP, Uzel G, Brodsky N, Freeman AF, Demidowich A, Davis J, Turner ML, Anderson VL, Darnell DN, Welch PA, Kuhns DB, Frucht DM, Malech HL, Gallin JI, Kobayashi SD, Whitney AR, Voyich JM, Musser JM, Woellner C, Schaffer AA, Puck JM, Grimbacher B (2007) STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 357(16):1608–1619. doi:10.1056/NEJMoa073687
Howell MD, Gallo RL, Boguniewicz M, Jones JF, Wong C, Streib JE, Leung DY (2006) Cytokine milieu of atopic dermatitis skin subverts the innate immune response to vaccinia virus. Immunity 24(3):341–348. doi:10.1016/j.immuni.2006.02.006
Hu DL, Omoe K, Sasaki S, Sashinami H, Sakuraba H, Yokomizo Y, Shinagawa K, Nakane A (2003) Vaccination with nontoxic mutant toxic shock syndrome toxin 1 protects against Staphylococcus aureus infection. J Infect Dis 188(5):743–752. doi:10.1086/377308
Hultgren OH, Verdrengh M, Tarkowski A (2004) T-box transcription-factor-deficient mice display increased joint pathology and failure of infection control during staphylococcal arthritis. Microbes Infect 6(6):529–535. doi:10.1016/j.micinf.2004.02.005
Hume EB, Cole N, Khan S, Garthwaite LL, Aliwarga Y, Schubert TL, Willcox MD (2005) A Staphylococcus aureus mouse keratitis topical infection model: cytokine balance in different strains of mice. Immunol Cell Biol 83(3):294–300. doi:10.1111/j.1440-1711.2005.01326.x
Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, Sudo K, Nakae S, Sasakawa C, Iwakura Y (2009) Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30(1):108–119. doi:10.1016/j.immuni.2008.11.009
Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126(6):1121–1133. doi:10.1016/j.cell.2006.07.035
Joshi A, Pancari G, Cope L, Bowman EP, Cua D, Proctor RA, McNeely T (2012) Immunization with Staphylococcus aureus iron regulated surface determinant B (IsdB) confers protection via Th17/IL17 pathway in a murine sepsis model. Hum Vaccine Immunother 8(3):336–346. doi:10.4161/hv.18946
Karauzum H, Chen G, Abaandou L, Mahmoudieh M, Boroun AR, Shulenin S, Devi VS, Stavale E, Warfield KL, Zeitlin L, Roy CJ, Sidhu SS, Aman MJ (2012) Synthetic human monoclonal antibodies toward staphylococcal enterotoxin B (SEB) protective against toxic shock syndrome. J Biol Chem 287(30):25203–25215. doi:10.1074/jbc.M112.364075
Karauzum H, Adhikari RP, Sarwar J, Devi VS, Abaandou L, Haudenschild C, Mahmoudieh M, Boroun AR, Vu H, Nguyen T, Warfield KL, Shulenin S, Aman MJ (2013) Structurally designed attenuated subunit vaccines for S. aureus LukS-PV and LukF-PV confer protection in a mouse bacteremia model. PLoS ONE 8(6):e65384. doi:10.1371/journal.pone.0065384
Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, Braughton KR, Schneewind O, DeLeo FR (2010) Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 202(7):1050–1058. doi:10.1086/656043
Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F, Missiakas DM, Schneewind O (2010) IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28(38):6382–6392. doi:10.1016/j.vaccine.2010.02.097
Kim HK, Kim HY, Schneewind O, Missiakas D (2011) Identifying protective antigens of Staphylococcus aureus, a pathogen that suppresses host immune responses. FASEB J 25(10):3605–3612. doi:10.1096/fj.11-187963
Kisand K, Boe Wolff AS, Podkrajsek KT, Tserel L, Link M, Kisand KV, Ersvaer E, Perheentupa J, Erichsen MM, Bratanic N, Meloni A, Cetani F, Perniola R, Ergun-Longmire B, Maclaren N, Krohn KJ, Pura M, Schalke B, Strobel P, Leite MI, Battelino T, Husebye ES, Peterson P, Willcox N, Meager A (2010) Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med 207(2):299–308. doi:10.1084/jem.20091669
Kisich KO, Carspecken CW, Fieve S, Boguniewicz M, Leung DY (2008) Defective killing of Staphylococcus aureus in atopic dermatitis is associated with reduced mobilization of human beta-defensin-3. J Allergy Clin Immunol 122(1):62–68. doi:10.1016/j.jaci.2008.04.022
Kobayashi SD, DeLeo FR (2013) Staphylococcus aureus protein A promotes immune suppression. MBio 4(5):e00764–e00713. doi:10.1128/mBio.00764-13
Kolata JB, Kuhbandner I, Link C, Normann N, Vu CH, Steil L, Weidenmaier C, Broker BM (2015) The fall of a dogma? Unexpected high T-cell memory response to Staphylococcus aureus in humans. J Infect Dis 212(5):830–838. doi:10.1093/infdis/jiv128
Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, Slight SR, Khader SA, Dubin PJ, Enelow RI, Kolls JK, Alcorn JF (2011) Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186(3):1666–1674. doi:10.4049/jimmunol.1002194
Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, Noble L, Brown MJ, Zorman JK, Wang XM, Pancari G, Fan H, Isett K, Burgess B, Bryan J, Brownlow M, George H, Meinz M, Liddell ME, Kelly R, Schultz L, Montgomery D, Onishi J, Losada M, Martin M, Ebert T, Tan CY, Schofield TL, Nagy E, Meineke A, Joyce JG, Kurtz MB, Caulfield MJ, Jansen KU, McClements W, Anderson AS (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 74(4):2215–2223. doi:10.1128/IAI.74.4.2215-2223.2006
Larkin EA, Stiles BG, Ulrich RG (2010) Inhibition of toxic shock by human monoclonal antibodies against staphylococcal enterotoxin B. PLoS ONE 5(10):e13253. doi:10.1371/journal.pone.0013253
Lazarevic V, Glimcher LH, Lord GM (2013) T-bet: a bridge between innate and adaptive immunity. Nat Rev Immunol 13(11):777–789. doi:10.1038/nri3536
Leijh PC, van den Barselaar MT, Daha MR, van Furth R (1981) Participation of immunoglobulins and complement components in the intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Infect Immun 33(3):714–724
Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA (2006) Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 203(10):2271–2279. doi:10.1084/jem.20061308
Lin L, Ibrahim AS, Xu X, Farber JM, Avanesian V, Baquir B, Fu Y, French SW, Edwards JE Jr, Spellberg B (2009) Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog 5(12):e1000703. doi:10.1371/journal.ppat.1000703
Lowell GH, Colleton C, Frost D, Kaminski RW, Hughes M, Hatch J, Hooper C, Estep J, Pitt L, Topper M, Hunt RE, Baker W, Baze WB (1996) Immunogenicity and efficacy against lethal aerosol staphylococcal enterotoxin B challenge in monkeys by intramuscular and respiratory delivery of proteosome-toxoid vaccines. Infect Immun 64(11):4686–4693
Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339(8):520–532. doi:10.1056/NEJM199808203390806
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
Matsui K, Nishikawa A (2012) Peptidoglycan from Staphylococcus aureus induces T(H)2 immune response in mice. J Investig Allergol Clin Immunol 22(2):80–86
McLoughlin RM, Solinga RM, Rich J, Zaleski KJ, Cocchiaro JL, Risley A, Tzianabos AO, Lee JC (2006) CD4+ T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc Natl Acad Sci USA 103(27):10408–10413. doi:10.1073/pnas.0508961103
McLoughlin RM, Lee JC, Kasper DL, Tzianabos AO (2008) IFN-gamma regulated chemokine production determines the outcome of Staphylococcus aureus infection. J Immunol 181(2):1323–1332
McNeely TB, Shah NA, Fridman A, Joshi A, Hartzel JS, Keshari RS, Lupu F, DiNubile MJ (2014) Mortality among recipients of the Merck V710 Staphylococcus aureus vaccine after postoperative S. aureus infections: an analysis of possible contributing host factors. Hum Vaccine Immunother 10(12):3513–3516. doi:10.4161/hv.34407
Milner JD, Brenchley JM, Laurence A, Freeman AF, Hill BJ, Elias KM, Kanno Y, Spalding C, Elloumi HZ, Paulson ML, Davis J, Hsu A, Asher AI, O’Shea J, Holland SM, Paul WE, Douek DC (2008) Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452(7188):773–776. doi:10.1038/nature06764
Minegishi Y, Saito M, Tsuchiya S, Tsuge I, Takada H, Hara T, Kawamura N, Ariga T, Pasic S, Stojkovic O, Metin A, Karasuyama H (2007) Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 448(7157):1058–1062. doi:10.1038/nature06096
Minegishi Y, Saito M, Nagasawa M, Takada H, Hara T, Tsuchiya S, Agematsu K, Yamada M, Kawamura N, Ariga T, Tsuge I, Karasuyama H (2009) Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 206(6):1291–1301. doi:10.1084/jem.20082767
Mocca CP, Brady RA, Burns DL (2014) Role of antibodies in protection elicited by active vaccination with genetically inactivated alpha hemolysin in a mouse model of Staphylococcus aureus skin and soft tissue infections. Clin Vaccine Immunol 21(5):622–627. doi:10.1128/CVI.00051-14
Montgomery CP, Daniels M, Zhao F, Alegre ML, Chong AS, Daum RS (2014) Protective immunity against recurrent Staphylococcus aureus skin infection requires antibody and interleukin-17A. Infect Immun 82(5):2125–2134. doi:10.1128/IAI.01491-14
Murphy AG, O’Keeffe KM, Lalor SJ, Maher BM, Mills KH, McLoughlin RM (2014) Staphylococcus aureus infection of mice expands a population of memory gammadelta T cells that are protective against subsequent infection. J Immunol 192(8):3697–3708. doi:10.4049/jimmunol.1303420
Myles IA, Fontecilla NM, Valdez PA, Vithayathil PJ, Naik S, Belkaid Y, Ouyang W, Datta SK (2013) Signaling via the IL-20 receptor inhibits cutaneous production of IL-1beta and IL-17A to promote infection with methicillin-resistant Staphylococcus aureus. Nat Immunol 14(8):804–811. doi:10.1038/ni.2637
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
Narita K, Hu DL, Mori F, Wakabayashi K, Iwakura Y, Nakane A (2010) Role of interleukin-17A in cell-mediated protection against Staphylococcus aureus infection in mice immunized with the fibrinogen-binding domain of clumping factor A. Infect Immun 78(10):4234–4242. doi:10.1128/IAI.00447-10
Nilsson IM, Verdrengh M, Ulrich RG, Bavari S, Tarkowski A (1999) Protection against Staphylococcus aureus sepsis by vaccination with recombinant staphylococcal enterotoxin A devoid of superantigenicity. J Infect Dis 180(4):1370–1373. doi:10.1086/315023
Nippe N, Varga G, Holzinger D, Loffler B, Medina E, Becker K, Roth J, Ehrchen JM, Sunderkotter C (2011) Subcutaneous infection with S. aureus in mice reveals association of resistance with influx of neutrophils and Th2 response. J Invest Dermatol 131(1):125–132. doi:10.1038/jid.2010.282
Nizet V (2007) Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J Allergy Clin Immunol 120(1):13–22. doi:10.1016/j.jaci.2007.06.005
Nomura I, Gao B, Boguniewicz M, Darst MA, Travers JB, Leung DY (2003) Distinct patterns of gene expression in the skin lesions of atopic dermatitis and psoriasis: a gene microarray analysis. J Allergy Clin Immunol 112(6):1195–1202. doi:10.1016/j.jaci.2003.08.049
Ohlsen K, Lorenz U (2010) Immunotherapeutic strategies to combat staphylococcal infections. Int J Med Microbiol 300(6):402–410. doi:10.1016/j.ijmm.2010.04.015
O’Shea JJ, Paul WE (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327(5969):1098–1102. doi:10.1126/science.1178334
Ou LS, Goleva E, Hall C, Leung DY (2004) T regulatory cells in atopic dermatitis and subversion of their activity by superantigens. J Allergy Clin Immunol 113(4):756–763. doi:10.1016/j.jaci.2004.01.772
Ouyang W, Kolls JK, Zheng Y (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28(4):454–467. doi:10.1016/j.immuni.2008.03.004
Parker D, Ryan CL, Alonzo F 3rd, Torres VJ, Planet PJ, Prince AS (2015) CD4+ T cells promote the pathogenesis of Staphylococcus aureus pneumonia. J Infect Dis 211(5):835–845. doi:10.1093/infdis/jiu525
Pauli NT, Kim HK, Falugi F, Huang M, Dulac J, Henry Dunand C, Zheng NY, Kaur K, Andrews SF, Huang Y, DeDent A, Frank KM, Charnot-Katsikas A, Schneewind O, Wilson PC (2014) Staphylococcus aureus infection induces protein A-mediated immune evasion in humans. J Exp Med 211(12):2331–2339. doi:10.1084/jem.20141404
Pozzi C, Wilk K, Lee JC, Gening M, Nifantiev N, Pier GB (2012) Opsonic and protective properties of antibodies raised to conjugate vaccines targeting six Staphylococcus aureus antigens. PLoS ONE 7(10):e46648. doi:10.1371/journal.pone.0046648
Prabhakara R, Harro JM, Leid JG, Keegan AD, Prior ML, Shirtliff ME (2011) Suppression of the inflammatory immune response prevents the development of chronic biofilm infection due to methicillin-resistant Staphylococcus aureus. Infect Immun 79(12):5010–5018. doi:10.1128/IAI.05571-11
Prendergast A, Prado JG, Kang YH, Chen F, Riddell LA, Luzzi G, Goulder P, Klenerman P (2010) HIV-1 infection is characterized by profound depletion of CD161+ Th17 cells and gradual decline in regulatory T cells. AIDS 24(4):491–502. doi:10.1097/QAD.0b013e3283344895
Proctor RA, van Langevelde P, Kristjansson M, Maslow JN, Arbeit RD (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20(1):95–102
Puel A, Doffinger R, Natividad A, Chrabieh M, Barcenas-Morales G, Picard C, Cobat A, Ouachee-Chardin M, Toulon A, Bustamante J, Al-Muhsen S, Al-Owain M, Arkwright PD, Costigan C, McConnell V, Cant AJ, Abinun M, Polak M, Bougneres PF, Kumararatne D, Marodi L, Nahum A, Roifman C, Blanche S, Fischer A, Bodemer C, Abel L, Lilic D, Casanova JL (2010) Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med 207(2):291–297. doi:10.1084/jem.20091983
Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, Lim HK, Migaud M, Israel L, Chrabieh M, Audry M, Gumbleton M, Toulon A, Bodemer C, El-Baghdadi J, Whitters M, Paradis T, Brooks J, Collins M, Wolfman NM, Al-Muhsen S, Galicchio M, Abel L, Picard C, Casanova JL (2011) Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332(6025):65–68. doi:10.1126/science.1200439
Ragle BE, Bubeck Wardenburg J (2009) Anti-alpha-hemolysin monoclonal antibodies mediate protection against Staphylococcus aureus pneumonia. Infect Immun 77(7):2712–2718. doi:10.1128/IAI.00115-09
Raphael I, Nalawade S, Eagar TN, Forsthuber TG (2014) T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine. doi:10.1016/j.cyto.2014.09.011
Rooijakkers SH, van Kessel KP, van Strijp JA (2005) Staphylococcal innate immune evasion. Trends Microbiol 13(12):596–601. doi:10.1016/j.tim.2005.10.002
Rosenzweig SD, Holland SM (2005) Defects in the interferon-gamma and interleukin-12 pathways. Immunol Rev 203:38–47. doi:10.1111/j.0105-2896.2005.00227.x
Schaffer AC, Lee JC (2008) Vaccination and passive immunisation against Staphylococcus aureus. Int J Antimicrob Agents 32(Suppl 1):S71–S78. doi:10.1016/j.ijantimicag.2008.06.009
Schlievert PM, Strandberg KL, Lin YC, Peterson ML, Leung DY (2010) Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 125(1):39–49. doi:10.1016/j.jaci.2009.10.039
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
Schmitt N, Ueno H (2015) Regulation of human helper T cell subset differentiation by cytokines. Curr Opin Immunol 34:130–136. doi:10.1016/j.coi.2015.03.007
Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R, Muenz L, Fuller S, Johnson J, Fireman B, Alcorn H, Naso R (2002) Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 346(7):491–496. doi:10.1056/NEJMoa011297
Skurnik D, Merighi M, Grout M, Gadjeva M, Maira-Litran T, Ericsson M, Goldmann DA, Huang SS, Datta R, Lee JC, Pier GB (2010) Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J Clin Invest 120(9):3220–3233. doi:10.1172/JCI42748
Smith EJ, Visai L, Kerrigan SW, Speziale P, Foster TJ (2011) The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus. Infect Immun 79(9):3801–3809. doi:10.1128/IAI.05075-11
Spaulding AR, Salgado-Pabon W, Kohler PL, Horswill AR, Leung DY, Schlievert PM (2013) Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev 26(3):422–447. doi:10.1128/CMR.00104-12
Spaulding AR, Salgado-Pabon W, Merriman JA, Stach CS, Ji Y, Gillman AN, Peterson ML, Schlievert PM (2014) Vaccination against Staphylococcus aureus pneumonia. J Infect Dis 209(12):1955–1962. doi:10.1093/infdis/jit823
Stephan JL, Vlekova V, Le Deist F, Blanche S, Donadieu J, De Saint-Basile G, Durandy A, Griscelli C, Fischer A (1993) Severe combined immunodeficiency: a retrospective single-center study of clinical presentation and outcome in 117 patients. J Pediatr 123(4):564–572
Stiles BG, Krakauer T, Bonventre PF (1995) Biological activity of toxic shock syndrome toxin 1 and a site-directed mutant, H135A, in a lipopolysaccharide-potentiated mouse lethality model. Infect Immun 63(4):1229–1234
Stranger-Jones YK, Bae T, Schneewind O (2006) Vaccine assembly from surface proteins of Staphylococcus aureus. Proc Natl Acad Sci USA 103(45):16942–16947. doi:10.1073/pnas.0606863103
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
Tkaczyk C, Hua L, Varkey R, Shi Y, Dettinger L, Woods R, Barnes A, MacGill RS, Wilson S, Chowdhury P, Stover CK, Sellman BR (2012) Identification of anti-alpha toxin monoclonal antibodies that reduce the severity of Staphylococcus aureus dermonecrosis and exhibit a correlation between affinity and potency. Clin Vaccine Immunol 19(3):377–385. doi:10.1128/CVI.05589-11
Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr (2015) Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 28(3):603–661. doi:10.1128/CMR.00134-14
Tuchscherr L, Medina E, Hussain M, Volker W, Heitmann V, Niemann S, Holzinger D, Roth J, Proctor RA, Becker K, Peters G, Loffler B (2011) Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med 3(3):129–141. doi:10.1002/emmm.201000115
van Kessel KP, Bestebroer J, van Strijp JA (2014) Neutrophil-mediated phagocytosis of Staphylococcus aureus. Front Immunol 5:467. doi:10.3389/fimmu.2014.00467
Varshney AK, Wang X, MacIntyre J, Zollner RS, Kelleher K, Kovalenko OV, Pechuan X, Byrne FR, Fries BC (2014) Humanized staphylococcal enterotoxin B (SEB)-specific monoclonal antibodies protect from SEB intoxication and Staphylococcus aureus infections alone or as adjunctive therapy with vancomycin. J Infect Dis 210(6):973–981. doi:10.1093/infdis/jiu198
Verbrugh HA, Peterson PK, Nguyen BY, Sisson SP, Kim Y (1982) Opsonization of encapsulated Staphylococcus aureus: the role of specific antibody and complement. J Immunol 129(4):1681–1687
Verhoeven PO, Gagnaire J, Botelho-Nevers E, Grattard F, Carricajo A, Lucht F, Pozzetto B, Berthelot P (2014) Detection and clinical relevance of Staphylococcus aureus nasal carriage: an update. Expert Rev Anti Infect Ther 12(1):75–89. doi:10.1586/14787210.2014.859985
von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001a) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344(1):11–16. doi:10.1056/NEJM200101043440102
von Eiff C, Becker K, Metze D, Lubritz G, Hockmann J, Schwarz T, Peters G (2001b) Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier’s disease. Clin Infect Dis 32(11):1643–1647. doi:10.1086/320519
Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, Porcella SF, Long RD, Dorward DW, Gardner DJ, Kreiswirth BN, Musser JM, DeLeo FR (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175(6):3907–3919
Weisman LE, Fischer GW, Thackray HM, Johnson KE, Schuman RF, Mandy GT, Stratton BE, Adams KM, Kramer WG, Mond JJ (2009) Safety and pharmacokinetics of a chimerized anti-lipoteichoic acid monoclonal antibody in healthy adults. Int Immunopharmacol 9(5):639–644. doi:10.1016/j.intimp.2009.02.008
Weisman LE, Thackray HM, Steinhorn RH, Walsh WF, Lassiter HA, Dhanireddy R, Brozanski BS, Palmer KG, Trautman MS, Escobedo M, Meissner HC, Sasidharan P, Fretz J, Kokai-Kun JF, Kramer WG, Fischer GW, Mond JJ (2011) A randomized study of a monoclonal antibody (pagibaximab) to prevent staphylococcal sepsis. Pediatrics 128(2):271–279. doi:10.1542/peds.2010-3081
Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5(12):751–762. doi:10.1016/S1473-3099(05)70295-4
Yeaman MR, Filler SG, Chaili S, Barr K, Wang H, Kupferwasser D, Hennessey JP Jr, Fu Y, Schmidt CS, Edwards JE Jr, Xiong YQ, Ibrahim AS (2014) Mechanisms of NDV-3 vaccine efficacy in MRSA skin versus invasive infection. Proc Natl Acad Sci USA 111(51):E5555–E5563. doi:10.1073/pnas.1415610111
Yoong P, Pier GB (2010) Antibody-mediated enhancement of community-acquired methicillin-resistant Staphylococcus aureus infection. Proc Natl Acad Sci USA 107(5):2241–2246. doi:10.1073/pnas.0910344107
Yoong P, Torres VJ (2015) Counter inhibition between leukotoxins attenuates Staphylococcus aureus virulence. Nat Commun 6:8125. doi:10.1038/ncomms9125
Zhang L, Jacobsson K, Vasi J, Lindberg M, Frykberg L (1998) A second IgG-binding protein in Staphylococcus aureus. Microbiology 144(Pt 4):985–991
Zhang L, Rosander A, Jacobsson K, Lindberg M, Frykberg L (2000) Expression of staphylococcal protein Sbi is induced by human IgG. FEMS Immunol Med Microbiol 28(3):211–218
Ziegler C, Goldmann O, Hobeika E, Geffers R, Peters G, Medina E (2011) The dynamics of T cells during persistent Staphylococcus aureus infection: from antigen-reactivity to in vivo anergy. EMBO Mol Med 3(11):652–666. doi:10.1002/emmm.201100173
Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, Gattorno M, Monticelli S, Lanzavecchia A, Sallusto F (2012) Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484(7395):514–518. doi:10.1038/nature10957
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This work was supported by the Intramural Research Program of the NIH, NIAID.
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Karauzum, H., Datta, S.K. (2016). Adaptive Immunity 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_2016_1
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