The fall of a Dogma? Unexpected high T-cell memory response to staphylococcus aureus in humans

Journal of Infectious Diseases

Volumn 212, Issue 5, 2015, Pages 830-838

  Kolata, Julia B ^a   Kühbandner, Iris ^a   Link, Christopher ^a   Normann, Nicole ^a   Vu, Chi Hai ^a   Steil, Leif ^b   Weidenmaier, Christopher ^c   Bröker, Barbara M ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cytokines; Human T cells; Memory response; Proliferation; S. aureus

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CYTOKINE;

ADULT; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DNA SYNTHESIS; FLOW CYTOMETRY; HELPER CELL; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TH17 CELL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; ISOTOPE LABELING; MONONUCLEAR CELL; SECRETION (PROCESS); T LYMPHOCYTE;

ADULT; ANTIGENS, BACTERIAL; CELL PROLIFERATION; CYTOKINES; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC MEMORY; ISOTOPE LABELING; LEUKOCYTES, MONONUCLEAR; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTES;

EID: 84943248536     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv128     Document Type: Article

References (50)

1. Concia E, Prandini N, Massari L, et al. Osteomyelitis: clinical update for practical guidelines. Nucl Med Commun 2006; 27:645-60.
2. Dryden MS. Skin and soft tissue infection: microbiology and epidemiology. Int J Antimicrob Agents 2009; 34(suppl 1):S2-7.
3. Fernández Guerrero ML, González López JJ, Goyenechea A, Fraile J, de Górgolas M. Endocarditis caused by Staphylococcus aureus: a reappraisal of the epidemiologic, clinical, and pathologic manifestations with analysis of factors determining outcome. Medicine (Baltimore) 2009; 88:1-22.
4. Gillet Y, Vanhems P, Lina G, et al. Factors predicting mortality in necrotizing community-acquired pneumonia caused by Staphylococcus aureus containing panton-valentine leukocidin. Clin Infect Dis 2007; 45:315-21.
5. Wertheim HFL, Vos MC, Ott A, et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 2004; 364:703-5.
6. Boucher HW, Corey GR. Epidemiology of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 2008; 46(suppl 5):S344-9.
7. Robert-Koch-Institut. Community acquired MRSA weltweit und in Deutschland. Epidemiol Bull 2004; 5:33-6.
8. Fattom A, Fuller S, Propst M, et al. Safety and immunogenicity of a booster dose of Staphylococcus aureus types 5 and 8 capsular polysaccharide conjugate vaccine (StaphVAX) in hemodialysis patients. Vaccine 2004; 23:656-63.
9. Fowler VG, Allen KB, Moreira ED, et al. Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA 2013; 309:1368-78.
10. Garcia-Lara J, Foster SJ. Anti-Staphylococcus aureus immunotherapy: current status and prospects. Curr Opin Pharmacol 2009; 9:552-7.
11. Proctor RA. Challenges for a universal Staphylococcus aureus vaccine. Clin Infect Dis 2012; 54:1179-86.
12. Schaffer AC, Lee JC. Staphylococcal vaccines and immunotherapies. Infect Dis Clin North Am 2009; 23:153-71.
13. Colque-Navarro P, Jacobsson G, Andersson R, Flock JI, Mollby R. Antibody levels against eleven Staphylococcus aureus antigens in a healthy population. Clin Vaccine Immunol 2010; 17:1117-23.
14. Dryla A, Prustomersky S, Gelbmann D, et al. Comparison of antibody repertoires against Staphylococcus aureus in healthy individuals and in acutely infected patients. Clin Diagn Lab Immunol 2005; 12:387-98.
15. Holtfreter S, Kolata J, Bröker BM. Towards the immune proteome of Staphylococcus aureus-the anti-S. aureus antibody response. Int J Med Microbiol IJMM 2010; 300:176-92.
16. Holtfreter S, Nguyen TT, Wertheim H, et al. Human immune proteome in experimental colonization with Staphylococcus aureus. Clin Vaccine Immunol 2009; 16:1607-14.
17. Holtfreter S, Roschack K, Eichler P, et al. Staphylococcus aureus carriers neutralize superantigens by antibodies specific for their colonizing strain: a potential explanation for their improved prognosis in severe sepsis. J Infect Dis 2006; 193:1275-8.
18. Verkaik NJ, de Vogel CP, Boelens HA, et al. Anti-staphylococcal humoral immune response in persistent nasal carriers and noncarriers of Staphylococcus aureus. J Infect Dis 2009; 199:625-32.
19. Ohlsen K, Lorenz U. Immunotherapeutic strategies to combat staphylococcal infections. Int J Med Microbiol IJMM 2010; 300:402-10.
20. Verkaik NJ, van Wamel WJB, van Belkum A. Immunotherapeutic approaches against Staphylococcus aureus. Immunotherapy 2011; 3: 1063-73.
21. Bröker BM, van Belkum A. Immune proteomics of Staphylococcus aureus. Proteomics 2011; 11:3221-31.
22. Cho JS, Pietras EM, Garcia NC, et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 2010; 120:1762-73.
23. Joshi A, Pancari G, Cope L, et al. Immunization with Staphylococcus aureus iron regulated surface determinant B (IsdB) confers protection via Th17/IL17 pathway in a murine sepsis model. Hum Vaccines Immunother 2012; 8:336-46.
24. Lin L, Ibrahim AS, Xu X, et al. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLOS Pathog 2009; 5:e1000703.
25. Manfredi R, Calza L, Chiodo F. Epidemiology and microbiology of cellulitis and bacterial soft tissue infection during HIV disease: a 10-year survey. J Cutan Pathol 2002; 29:168-72.
26. Minegishi Y, Saito M, Nagasawa M, et al. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 2009; 206:1291-301.
27. Alonzo F, Kozhaya L, Rawlings SA, et al. CCR5 is a receptor for Staphylococcus aureus leukotoxin ED. Nature 2013; 493:51-5.
28. Grumann D, Nübel U, Bröker BM. Staphylococcus aureus toxins-their functions and genetics. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 2014; 21:583-92.
29. Nygaard TK, Pallister KB, DuMont AL, et al. Alpha-toxin induces programmed cell death of human T cells, B cells, and monocytes during USA300 infection. PLOS One 2012; 7:e36532.
30. Zielinski CE, Corti D, Mele F, Pinto D, Lanzavecchia A, Sallusto F. Dissecting the human immunologic memory for pathogens. Immunol Rev 2011; 240:40-51.
31. Zielinski CE, Mele F, Aschenbrenner D, et al. Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature 2012; 484:514-8.
32. Kolata J, Bode LGM, Holtfreter S, et al. Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 2011; 11:3914-27.
33. Weidenmaier C, McLoughlin RM, Lee JC. The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4+ T-cell-dependent mechanism. PLOS One 2010; 5:e13227.
34. Jenkins MK, Chu HH, McLachlan JB, Moon JJ. On the composition of the preimmune repertoire of T cells specific for peptide-major histocompatibility complex ligands. Annu Rev Immunol 2010; 28:275-94.
35. Rowe J, Macaubas C, Monger TM, et al. Antigen-specific responses to diphtheria-tetanus-acellular pertussis vaccine in human infants are initially Th2 polarized. Infect Immun 2000; 68:3873-7.
36. Holtfreter S, Bauer K, Thomas D, et al. egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect Immun 2004; 72:4061-71.
37. Kappler J, Kotzin B, Herron L, et al. V-beta-specific stimulation of human T cells by staphylococcal toxins. Science 1989; 244:811-3.
38. Lewis AL, Lewis WG. Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 2012; 14:1174-82.
39. Spellberg B, Ibrahim AS, Yeaman MR, et al. The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect Immun 2008; 76:4574-80.
40. Schmidt CS, White CJ, Ibrahim AS, et al. NDV-3, a recombinant alum-adjuvanted vaccine for Candida and Staphylococcus aureus, is safe and immunogenic in healthy adults. Vaccine 2012; 30: 7594-600.
41. Zorman JK, Esser M, Raedler M, et al. Naturally occurring IgG antibody levels to the Staphylococcus aureus protein IsdB in humans. Hum Vaccines Immunother 2013; 9:1857-64.
42. Mazmanian SK, Liu G, Jensen ER, Lenoy E, Schneewind O. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci USA 2000; 97:5510-5.
43. Reed SB, Wesson CA, Liou LE, et al. Molecular characterization of a novel Staphylococcus aureus serine protease operon. Infect Immun 2001; 69:1521-7.
44. Zdzalik M, Karim AY, Wolski K, et al. Prevalence of genes encoding extracellular proteases in Staphylococcus aureus-important targets triggering immune response in vivo. FEMS Immunol Med Microbiol 2012; 66:220-9.
45. Ravipaty S, Reilly JP. Comprehensive characterization of methicillinresistant Staphylococcus aureus subsp. aureus COL secretome by twodimensional liquid chromatography and mass spectrometry. Mol Cell Proteomics MCP 2010; 9:1898-919.
46. Mazmanian SK, Kasper DL. The love-hate relationship between bacterial polysaccharides and the host immune system. Nat Rev Immunol 2006; 6:849-58.
47. Yanagisawa C, Hanaki H, Natae T, Sunakawa K. Neutralization of staphylococcal exotoxins in vitro by human-origin intravenous immunoglobulin. J Infect Chemother Off J Jpn Soc Chemother 2007; 13:368-72.
48. Grumann D, Scharf SS, Holtfreter S, et al. Immune cell activation by enterotoxin gene cluster (egc)-encoded and non-egc superantigens from Staphylococcus aureus. J Immunol 2008; 181:5054-61.
49. Weidenmaier C, Kokai-Kun JF, Kristian SA, et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 2004; 10:243-5.
50. Carneiro J, Duarte L, Padovan E. Limiting dilution analysis of antigenspecific T cells. Methods Mol Biol Clifton NJ 2009; 514:95-105.