Microarray-based identification of human antibodies against Staphylococcus aureus antigens

Proteomics - Clinical Applications

Volumn 9, Issue 11-12, 2015, Pages 1003-1011

  Kloppot, Peggy ^a   Selle, Martina ^b   Kohler, Christian ^a   Stentzel, Sebastian ^c   Fuchs, Stephan ^a   Liebscher, Volkmar ^a   Müller, Elke ^d   Kale, Devika ^e   Ohlsen, Knut ^b   Bröker, Barbara M ^c   Zipfel, Peter F ^f,g   Kahl, Barbara C ^e   Ehricht, Ralf ^d   Hecker, Michael ^a   Engelmann, Susanne ^a,h,i  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^d Alere Technologies GmbH   (Germany)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^f Infektionsbiologie   (Germany)

^g FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^h TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

ⁱ Helmholtzzentrum für Infektionsforschung   (Germany)

Author keywords

Humoral immunity; Protein microarray; Staphylococcus aureus; Vaccines

Indexed keywords

BACTERIAL ANTIGEN; IMMUNOGLOBULIN G ANTIBODY; ISAA PROTEIN; SACOL0479 PROTEIN; SACOL0480 PROTEIN; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY; IMMUNOGLOBULIN G;

ANTIBODY DETECTION; ANTIBODY RESPONSE; ARTICLE; BACTERIUM CARRIER; HUMAN; PRIORITY JOURNAL; PROTEIN MICROARRAY; STAPHYLOCOCCUS AUREUS; HUMORAL IMMUNITY; IMMUNOLOGY; NORMAL HUMAN; SPECIES DIFFERENCE;

ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; HEALTHY VOLUNTEERS; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; PROTEIN ARRAY ANALYSIS; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

EID: 84954383824     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201400123     Document Type: Article

References (51)

1. Foster, T. J., Immune evasion by staphylococci. Nat. Rev. Microbiol. 2005, 3, 948-958.
2. Wertheim, H. F., Melles, D. C., Vos, M. C., vanLeeuwen, W. et al., The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005, 5, 751-762.
3. vonEiff, C., Becker, K., Machka, K., Stammer, H., Peters, G., Nasal carriage as a source of Staphylococcus aureus bacteremia. Study group. New Eng. J. Med. 2001, 344, 11-16.
4. Wertheim, H. F., Vos, M. C., Ott, A., vanBelkum, A. et al., Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 2004, 364, 703-705.
5. Nygaard, T. K., DeLeo, F. R., Voyich, J. M., Community-associated methicillin-resistant Staphylococcus aureus skin infections: advances toward identifying the key virulence factors. Curr. Opin. Infect. Dis. 2008, 21, 147-152.
6. David, M. Z., Daum, R. S., Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 2010, 23, 616-687.
7. Moran, G. J., Krishnadasan, A., Gorwitz, R. J., Fosheim, G. E. et al., Prevalence of methicillin-resistant Staphylococcus aureus as an etiology of community-acquired pneumonia. Clin. Infect. Dis. 2012, 54, 1126-1133.
8. Diep, B. A., Gill, S. R., Chang, R. F., Phan, T. H. et al., Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367, 731-739.
9. Lindsay, J. A., Moore, C. E., Day, N. P., Peacock, S. J. et al., Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J. Bacteriol. 2006, 188, 669-676.
10. Rogasch, K., Rühmling, V., Pane-Farre, J., Höper, D. et al., Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J. Bacteriol. 2006, 188, 7742-7758.
11. Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H. T. et al., Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J. Clin. Microbiol. 2007, 45, 2669-2680.
12. Ziebandt, A. K., Kusch, H., Degner, M., Jaglitz, S. et al., Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation. Proteomics 2010, 10, 1634-1644.
13. Dreisbach, A., Hempel, K., Buist, G., Hecker, M. et al., Profiling the surfacome of Staphylococcus aureus. Proteomics 2010, 10, 3082-3096.
14. Kusch, H., Engelmann, S., Secrets of the secretome in Staphylococcus aureus. Int. J. Med. Microbiol. 2014, 304, 133-141.
15. Lowy, F. D., Staphylococcus aureus infections. New Eng. J. Med. 1998, 339, 520-532.
16. Verkaik, N. J., Boelens, H. A., deVogel, C. P., Tavakol, M. et al., Heterogeneity of the humoral immune response following Staphylococcus aureus bacteremia. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29, 509-518.
17. Verkaik, N. J., deVogel, C. P., Boelens, H. A., Grumann, D. et al., Anti-staphylococcal humoral immune response in persistent nasal carriers and noncarriers of Staphylococcus aureus. J. Infect. Dis. 2009, 199, 625-632.
18. Verkaik, N. J., Lebon, A., deVogel, C. P., Hooijkaas, H. et al., Induction of antibodies by Staphylococcus aureus nasal colonization in young children. Clin. Microbiol. Infect. 2010, 16, 1312-1317.
19. den Reijer, P. M., Lemmens-den Toom, N., Kant, S., Snijders, S. V. et al., Characterization of the humoral immune response during Staphylococcus aureus bacteremia and global gene expression by Staphylococcus aureus in human blood. PloS One 2013, 8, e53391.
20. Holtfreter, S., Kolata, J., Bröker, B. M., Towards the immune proteome of Staphylococcus aureus-the anti-S. aureus antibody response. Int. J. Med. Microbiol. 2010, 300, 176-192.
21. Lebon, A., Verkaik, N. J., deVogel, C. P., Hooijkaas, H. et al., The inverse correlation between Staphylococcus aureus and Streptococcus pneumoniae colonization in infants is not explained by differences in serum antibody levels in the Generation R Study. Clin. Vac. Immunol. 2011, 18, 180-183.
22. Prevaes, S. M., vanWamel, W. J., deVogel, C. P., Veenhoven, R. H. et al., Nasopharyngeal colonization elicits antibody responses to staphylococcal and pneumococcal proteins that are not associated with a reduced risk of subsequent carriage. Infect. Immun. 2012, 80, 2186-2193.
23. Holtfreter, S., Roschack, K., Eichler, P., Eske, K. 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, 1275-1278.
24. Nouwen, J., Boelens, H., vanBelkum, A., Verbrugh, H., Human factor in Staphylococcus aureus nasal carriage. Infect. Immun. 2004, 72, 6685-6688.
25. Lueong, S. S., Hoheisel, J. D., Alhamdani, M. S. S., Protein microarrays as tools for functional proteomics: achievements, promises and challenges. J. Proteomics Bioinform. 2013, S7, 004.
26. Starcher, B., A ninhydrin-based assay to quantitate the total protein content of tissue samples. Anal. Biochem. 2001, 292, 125-129.
27. Monecke, S., Jatzwauk, L., Weber, S., Slickers, P., Ehricht, R., DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony. Clin. Microbiol. Infect. 2008, 14, 534-545.
28. Monecke, S., Slickers, P., Ehricht, R., Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol. Med. Microbiol. 2008, 53, 237-251.
29. Ehricht, R., Adelhelm, K., Monecke, S., Huelseweh, B., Application of protein arraytubes to bacteria, toxin, and biological warfare agent detection. Meth. Mol. Biol. 2009, 509, 85-105.
30. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. B 1995, 57, 289-300.
31. Zhou, M., Boekhorst, J., Francke, C., Siezen, R. J., LocateP: genome-scale subcellular-location predictor for bacterial proteins. BMC Bioinform. 2008, 9, 173.
32. Holtfreter, S., Jursa-Kulesza, J., Masiuk, H., Verkaik, N. J. et al., Antibody responses in furunculosis patients vaccinated with autologous formalin-killed Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30, 707-717.
33. Hansenova Manaskova, S., Bikker, F. J., Veerman, E. C., vanBelkum, A., vanWamel, W. J., Rapid detection and semi-quantification of IgG-accessible Staphylococcus aureus surface-associated antigens using a multiplex competitive Luminex assay. J. Immunol. Meth. 2013, 397, 18-27.
34. Crombe, F., Vanderhaeghen, W., deVogel, C. P., VanWamel, W. J. et al., Serological profiles in nursery piglets colonized with Staphylococcus aureus. Vet. Res. 2013, 44, 4.
35. Holtfreter, S., Nguyen, T. T., Wertheim, H., Steil, L. et al., Human immune proteome in experimental colonization with Staphylococcus aureus. Clin. Vac. Immunol. 2009, 16, 1607-1614.
36. Colque-Navarro, P., Palma, M., Soderquist, B., Flock, J. I., Mollby, R., Antibody responses in patients with staphylococcal septicemia against two Staphylococcus aureus fibrinogen binding proteins: clumping factor and an extracellular fibrinogen binding protein. Clin. Diagnostic Lab. Immunol. 2000, 7, 14-20.
37. Colque-Navarro, P., Soderquist, B., Holmberg, H., Blomqvist, L. et al., Antibody response in Staphylococcus aureus septicaemia-a prospective study. J. Med. Microbiol. 1998, 47, 217-225.
38. Jacobsson, G., Colque-Navarro, P., Gustafsson, E., Andersson, R., Mollby, R., Antibody responses in patients with invasive Staphylococcus aureus infections. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29, 715-725.
39. Kolata, J., Bode, L. G., Holtfreter, S., Steil, L. et al., Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 2011, 11, 3914-3927.
40. Bröker, B. M., Holtfreter, S., Bekeredjian-Ding, I., Immune control of Staphylococcus aureus-regulation and counter-regulation of the adaptive immune response. Int. J. Med. Microbiol. 2014, 304, 204-214.
41. Ritz, H. L., Kirkland, J. J., Bond, G. G., Warner, E. K., Petty, G. P., Association of high levels of serum antibody to staphylococcal toxic shock antigen with nasal carriage of toxic shock antigen-producing strains of Staphylococcus aureus. Infec. Immun. 1984, 43, 954-958.
42. Grumann, D., Ruotsalainen, E., Kolata, J., Kuusela, P. et al., Characterization of infecting strains and superantigen-neutralizing antibodies in Staphylococcus aureus bacteremia. Clin. Vac. Immunol. 2011, 18, 487-493.
43. Bavari, S., Ulrich, R. G., LeClaire, R. D., Cross-reactive antibodies prevent the lethal effects of Staphylococcus aureus superantigens. J. Infect. Dis. 1999, 180, 1365-1369.
44. Bröker, B. M., vanBelkum, A., Immune proteomics of Staphylococcus aureus. Proteomics 2011, 11, 3221-3231.
45. vander Kooi-Pol, M. M., deVogel, C. P., Westerhout-Pluister, G. N., Veenstra-Kyuchukova, Y. K. et al., High anti-staphylococcal antibody titers in patients with epidermolysis bullosa relate to long-term colonization with alternating types of Staphylococcus aureus. J. Invest. Dermatol. 2013, 133, 847-850.
46. Adhikari, R. P., Ajao, A. O., Aman, M. J., Karauzum, H. et al., Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S. aureus infections. J. Infect. Dis. 2012, 206, 915-923.
47. Ohlsen, K., Lorenz, U., Immunotherapeutic strategies to combat staphylococcal infections. Int. J. Med. Microbiol. 2010, 300, 402-410.
48. Salgado-Pabon, W., Schlievert, P. M., Models matter: the search for an effective Staphylococcus aureus vaccine. Nat. Rev. Microbiol. 2014, 12, 585-591.
49. Fowler, V. G., Allen, K. B., Moreira, E. D., Moustafa, M. et al., Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA 2013, 309, 1368-1378.
50. Spaulding, A. R., Salgado-Pabon, W., Merriman, J. A., Stach, C. S. et al., Vaccination against Staphylococcus aureus pneumonia. J. Infect. Dis. 2014, 209, 1955-1962.
51. Oesterreich, B., Lorenz, B., Schmitter, T., Kontermann, R. et al., Characterization of the biological anti-staphylococcal functionality of hUK-66 IgG1, a humanized monoclonal antibody as substantial component for an immunotherapeutic approach. Hum. Vac. Immunother. 2014, 10, 926-937.