Staphylococcal serine protease–like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus

Journal of Allergy and Clinical Immunology

Volumn 139, Issue 2, 2017, Pages 492-500.e8

  Stentzel, Sebastian ^a   Teufelberger, Andrea ^b   Nordengrün, Maria ^a   Kolata, Julia ^a,c   Schmidt, Frank ^a   van Crombruggen, Koen ^b   Michalik, Stephan ^a   Kumpfmüller, Jana ^d,h   Tischer, Sebastian ^a   Schweder, Thomas ^d   Hecker, Michael ^d   Engelmann, Susanne ^d,e,f   Völker, Uwe ^a   Krysko, Olga ^b   Bachert, Claus ^b,g   Bröker, Barbara M ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^f HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^g KAROLINSKA INSTITUTE   (Sweden)

^h HANS KNÖLL INSTITUTE   (Germany)

Author keywords

Asthma; IgE; serine protease like proteins; Staphylococcus aureus; type 2 inflammation

Indexed keywords

ALPHA HEMOLYSIN; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CYTOKINE; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G4; RECOMBINANT PROTEIN; STAPHYLOCOCCAL SERINE PROTEASE LIKE PROTEIN; UNCLASSIFIED DRUG; ALLERGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; PROTEIN BINDING; SERINE PROTEINASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; ASTHMA; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; IMMUNOBLOTTING; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; STAPHYLOCOCCUS INFECTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; AGED; ANIMAL; C57BL MOUSE; CELL CULTURE; HYPERSENSITIVITY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MIDDLE AGED; STAPHYLOCOCCUS AUREUS; YOUNG ADULT;

ADULT; AGED; ALLERGENS; ANIMALS; ASTHMA; BACTERIAL PROTEINS; CELLS, CULTURED; FEMALE; HUMANS; HYPERSENSITIVITY; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; PROTEIN BINDING; SERINE PROTEASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TH2 CELLS; YOUNG ADULT;

EID: 85006488917     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.03.045     Document Type: Article

References (73)

1. 1 Masoli, M., Fabian, D., Holt, S., Beasley, R., The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 59 (2004), 469–478.
2. 2 Barnes, P.J., Intrinsic asthma: not so different from allergic asthma but driven by superantigens?. Clin Exp Allergy 39 (2009), 1145–1151.
3. 3 Barnes, P.J., Severe asthma: advances in current management and future therapy. J Allergy Clin Immunol 129 (2012), 48–59.
4. 4 Jarvis, D., Newson, R., Lotvall, J., Hastan, D., Tomassen, P., Keil, T., et al. Asthma in adults and its association with chronic rhinosinusitis: the GA2LEN survey in Europe. Allergy 67 (2012), 91–98.
5. 5 Lowy, F., Staphylococcus aureus infections. N Engl J Med 339 (1998), 520–529.
6. 6 Wertheim, H.F.L., Melles, D.C., Vos, M.C., van Leeuwen, W., van Belkum, A., Verbrugh, H.A., et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5 (2005), 751–762.
7. 7 Bachert, C., Zhang, N., Chronic rhinosinusitis and asthma: novel understanding of the role of IgE ‘above atopy’. J Intern Med 272 (2012), 133–143.
8. 8 Davis, M.F., Peng, R.D., McCormack, M.C., Matsui, E.C., Staphylococcus aureus colonization is associated with wheeze and asthma among US children and young adults. J Allergy Clin Immunol 135 (2015), 811–813.e5.
9. 9 Van Zele, T., Gevaert, P., Watelet, J.B., Claeys, G., Holtappels, G., Claeys, C., et al. Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis. J Allergy Clin Immunol 114 (2004), 981–983.
10. 10 Bachert, C., Zhang, N., Holtappels, G., De Lobel, L., van Cauwenberge, P., Liu, S., et al. Presence of IL-5 protein and IgE antibodies to staphylococcal enterotoxins in nasal polyps is associated with comorbid asthma. J Allergy Clin Immunol 126 (2010), 962–968 e1-6.
11. 11 Bachert, C., van Steen, K., Zhang, N., Holtappels, G., Cattaert, T., Maus, B., et al. Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma. J Allergy Clin Immunol 130 (2012), 376–381.e8.
12. 12 Huvenne, W., Hellings, P.W., Bachert, C., Role of staphylococcal superantigens in airway disease. Int Arch Allergy Immunol 161 (2013), 304–314.
13. 13 Proft, T., Fraser, J., Superantigens: just like peptides, only different. J Exp Med 187 (1998), 819–821.
14. 14 Schlievert, P., Bohach, G., Staphylococcal and streptococcal superantigens: an update. Kotb, M., Fraser, J., (eds.) Superantigens: Molecular basis for their role in human diseases, 2007, ASM Press, Washington (DC), 21–36.
15. 15 Holgate, S.T., Innate and adaptive immune responses in asthma. Nat Med 18 (2012), 673–683.
16. 16 Galli, S.J., Tsai, M., IgE and mast cells in allergic disease. Nat Med 18 (2012), 693–704.
17. 17 Yamane, H., Paul, W.E., Cytokines of the gamma(c) family control CD4+ T cell differentiation and function. Nat Immunol 13 (2012), 1037–1044.
18. 18 McHeyzer-Williams, M., Okitsu, S., Wang, N., McHeyzer-Williams, L., Molecular programming of B cell memory. Nat Rev Immunol 12 (2012), 24–34.
19. 19 Aalberse, R.C., Stapel, S.O., Schuurman, J., Rispens, T., Immunoglobulin G4: an odd antibody. Clin Exp Allergy 39 (2009), 469–477.
20. 20 Oettgen, H.C., Regulation of the IgE isotype switch: new insights on cytokine signals and the functions of epsilon germline transcripts. Curr Opin Immunol 12 (2000), 618–623.
21. 21 Nirula, A., Glaser, S.M., Kalled, S.L., Taylor, F.R., What is IgG4? A review of the biology of a unique immunoglobulin subtype. Curr Opin Rheumatol 23 (2011), 119–124.
22. 22 Davies, J.M., Platts-Mills, T.A., Aalberse, R.C., The enigma of IgE+ B-cell memory in human subjects. J Allergy Clin Immunol 131 (2013), 972–976.
23. 23 Vidarsson, G., Dekkers, G., Rispens, T., IgG subclasses and allotypes: from structure to effector functions. Front Immunol, 5, 2014, 520.
24. 24 Popowicz, G.M., Dubin, G., Stec-Niemczyk, J., Czarny, A., Dubin, A., Potempa, J., et al. Functional and structural characterization of Spl proteases from Staphylococcus aureus. J Mol Biol 358 (2006), 270–279.
25. 25 Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H.T., Eichler, P., Strommenger, B., et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45 (2007), 2669–2680.
26. 26 Stentzel, S., Vu, H.C., Weyrich, A.M., Jehmlich, N., Schmidt, F., Salazar, M.G., et al. Altered immune proteome of Staphylococcus aureus under iron-restricted growth conditions. Proteomics 14 (2014), 1857–1867.
27. 27 Stentzel, S., Sundaramoorthy, N., Michalik, S., Nordengrün, M., Schulz, S., Kolata, J., et al. Specific serum IgG at diagnosis of Staphylococcus aureus blood stream invasion is correlated with disease progression. J Proteomics 128 (2015), 1–7.
28. 28 Krysko, O., Maes, T., Plantinga, M., Holtappels, G., Imiru, R., Vandenabeele, P., et al. The adjuvant-like activity of staphylococcal enterotoxin B in a murine asthma model is independent of IL-1R signaling. Allergy 68 (2013), 446–453.
29. 29 Hudson, Z., Sample size, power and effect size–what all researchers need to know. Phys Ther Sport 10 (2009), 43–44.
30. 30 Huvenne, W., Callebaut, I., Reekmans, K., Hens, G., Bobic, S., Jorissen, M., et al. Staphylococcus aureus enterotoxin B augments granulocyte migration and survival via airway epithelial cell activation. Allergy 65 (2010), 1013–1020.
31. 31 Reed, S.B., Wesson, C.A., Liou, L.E., Trumble, W.R., Schlievert, P.M., Bohach, G.A., et al. Molecular characterization of a novel Staphylococcus aureus serine protease operon. Infect Immun 69 (2001), 1521–1527.
32. 32 Zielinski, C.E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., et al. Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484 (2012), 514–518.
33. 33 Kolata, J., Kühbandner, I., Link, C., Normann, N., Weidenmaier, C., Bröker, B., The fall of a dogma? Unexpectedly high T cell memory response to Staphylococcus aureus in humans. J Infect Dis 212 (2015), 830–838.
34. 34 Stec-Niemczyk, J., Pustelny, K., Kisielewska, M., Bista, M., Boulware, K.T., Stennicke, H.R., et al. Structural and functional characterization of SplA, an exclusively specific protease of Staphylococcus aureus. Biochem J 419 (2009), 555–564.
35. 35 Dubin, G., Stec-Niemczyk, J., Kisielewska, M., Pustelny, K., Popowicz, G.M., Bista, M., et al. Enzymatic activity of the Staphylococcus aureus SplB serine protease is induced by substrates containing the sequence Trp-Glu-Leu-Gln. J Mol Biol 379 (2008), 343–356.
36. 36 Zdzalik, M., Kalinska, M., Wysocka, M., Stec-Niemczyk, J., Cichon, P., Stach, N., et al. Biochemical and structural characterization of SplD protease from Staphylococcus aureus. PLoS One, 8, 2013, e76812.
37. 37 Prescott, S.L., Early-life environmental determinants of allergic diseases and the wider pandemic of inflammatory noncommunicable diseases. J Allergy Clin Immunol 131 (2013), 23–30.
38. 38 Kool, M., Soullie, T., van Nimwegen, M., Willart, M.A., Muskens, F., Jung, S., et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 205 (2008), 869–882.
39. 39 Niebuhr, M., Gathmann, M., Scharonow, H., Mamerow, D., Mommert, S., Balaji, H., et al. Staphylococcal alpha-toxin is a strong inducer of interleukin-17 in humans. Infect Immun 79 (2011), 1615–1622.
40. 40 Frank, K.M., Zhou, T., Moreno-Vinasco, L., Hollett, B., Garcia, J.G.N., Wardenburg, J.B., Host response signature to Staphylococcus aureus alpha-hemolysin implicates pulmonary Th17 response. Infect Immun 80 (2012), 3161–3169.
41. 41 Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30 (2009), 108–119.
42. 42 Lin, L., Ibrahim, A.S., Xu, X., Farber, J.M., Avanesian, V., Baquir, B., et al. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog, 5, 2009, e1000703.
43. 43 Cho, J.S., Pietras, E.M., Garcia, N.C., Ramos, R.I., Farzam, D.M., Monroe, H.R., et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120 (2010), 1762–1773.
44. 44 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 304 (2014), 204–214.
45. 45 Renner, E.D., Rylaarsdam, S., Anover-Sombke, S., Rack, A.L., Reichenbach, J., Carey, J.C., et al. Novel signal transducer and activator of transcription 3 (STAT3) mutations, reduced T(H)17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J Allergy Clin Immunol 122 (2008), 181–187.
46. 46 Milner, J.D., Brenchley, J.M., Laurence, A., Freeman, A.F., Hill, B.J., Elias, K.M., et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452 (2008), 773–776.
47. 47 Cook, M.C., Tangye, S.G., Primary immune deficiencies affecting lymphocyte differentiation: lessons from the spectrum of resulting infections. Int Immunol 21 (2009), 1003–1011.
48. 48 Chandesris, M.O., Melki, I., Natividad, A., Puel, A., Fieschi, C., Yun, L., et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine (Baltimore) 91 (2012), e1–e19.
49. 49 Nakamura, Y., Oscherwitz, J., Cease, K.B., Chan, S.M., Munoz-Planillo, R., Hasegawa, M., et al. Staphylococcus d-toxin induces allergic skin disease by activating mast cells. Nature 503 (2013), 397–401.
50. 50 Fraser, J., Arcus, V., Kong, P., Baker, E., Proft, T., Superantigens–powerful modifiers of the immune system. Mol Med Today 6 (2000), 125–132.
51. 51 Bachert, C., Gevaert, P., van Cauwenberge, P., Staphylococcus aureus enterotoxins: a key in airway disease?. Allergy 57 (2002), 480–487.
52. 52 Berube, B.J., Bubeck Wardenburg, J., Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel) 5 (2013), 1140–1166.
53. 53 Inoshima, I., Inoshima, N., Wilke, G.A., Powers, M.E., Frank, K.M., Wang, Y., et al. A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat Med 17 (2011), 1310–1314.
54. 54 Brauweiler, A.M., Bin, L., Kim, B.E., Oyoshi, M.K., Geha, R.S., Goleva, E., et al. Filaggrin-dependent secretion of sphingomyelinase protects against staphylococcal alpha-toxin-induced keratinocyte death. J Allergy Clin Immunol 131 (2012), 421–427 e1-2.
55. 55 Zdzalik, M., Karim, A.Y., Wolski, K., Buda, P., Wojcik, K., Brueggemann, S., et al. Prevalence of genes encoding extracellular proteases in Staphylococcus aureus–important targets triggering immune response in vivo. FEMS Immunol Med Microbiol 66 (2012), 220–229.
56. 56 Pustelny, K., Stach, N., Wladyka, B., Dubin, A., Dubin, G., Evaluation of P1' substrate specificity of staphylococcal SplB protease. Acta Biochim Pol 61 (2014), 149–152.
57. 57 Balenga, N.A., Klichinsky, M., Xie, Z., Chan, E.C., Zhao, M., Jude, J., et al. A fungal protease allergen provokes airway hyper-responsiveness in asthma. Nat Commun, 6, 2015, 6763.
58. Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H.T., Eichler, P., Strommenger, B., et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45 (2007), 2669–2680.
59. Stentzel, S., Vu, H.C., Weyrich, A.M., Jehmlich, N., Schmidt, F., Salazar, M.G., et al. Altered immune proteome of Staphylococcus aureus under iron-restricted growth conditions. Proteomics 14 (2014), 1857–1867.
60. Holtfreter, S., Nguyen, T.T., Wertheim, H., Steil, L., Kusch, H., Truong, Q.P., et al. Human immune proteome in experimental colonization with Staphylococcus aureus. Clin Vaccine Immunol 16 (2009), 1607–1614.
61. Kolata, J., Bode, L.G., Holtfreter, S., Steil, L., Kusch, H., Holtfreter, B., et al. Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11 (2011), 3914–3927.
62. Jehmlich, N., Dinh, K.H., Gesell-Salazar, M., Hammer, E., Steil, L., Dhople, V.M., et al. Quantitative analysis of the intra- and inter-subject variability of the whole salivary proteome. J Periodontal Res 48 (2013), 392–403.
63. de Souza, G.A., Arntzen, M.O., Wiker, H.G., MSMSpdbb: providing protein databases of closely related organisms to improve proteomic characterization of prokaryotic microbes. Bioinformatics 26 (2010), 698–699.
64. Eichstaedt, S., Gabler, K., Below, S., Muller, C., Kohler, C., Engelmann, S., et al. Effects of Staphylococcus aureus-hemolysin A on calcium signalling in immortalized human airway epithelial cells. Cell Calcium 45 (2009), 165–176.
65. Grumann, D., Scharf, S.S., Holtfreter, S., Kohler, C., Steil, L., Engelmann, S., et al. Immune cell activation by enterotoxin gene cluster (EGC)-encoded and non-EGC superantigens from Staphylococcus aureus. J Immunol 181 (2008), 5054–5061.
66. Silbersack, J., Jurgen, B., Hecker, M., Schneidinger, B., Schmuck, R., Schweder, T., An acetoin-regulated expression system of Bacillus subtilis. Appl Microbiol Biotechnol 73 (2006), 895–903.
67. Li, M.Z., Elledge, S.J., Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat Methods 4 (2007), 251–256.
68. Kabisch, J., Thurmer, A., Hubel, T., Popper, L., Daniel, R., Schweder, T., Characterization and optimization of Bacillus subtilis ATCC 6051 as an expression host. J Biotechnol 163 (2013), 97–104.
69. Zobel, S., Kumpfmuller, J., Sussmuth, R.D., Schweder, T., Bacillus subtilis as heterologous host for the secretory production of the non-ribosomal cyclodepsipeptide enniatin. Appl Microbiol Biotechnol 99 (2015), 681–691.
70. Kolata, J.B., Kuhbandner, I., Link, C., Normann, N., Vu, C.H., Steil, L., et al. The fall of a dogma? Unexpected high T-cell memory response to Staphylococcus aureus in humans. J Infect Dis 212 (2015), 830–838.
71. R Core Team. R: a language and environment for statistical computing. 2013, R Foundation for Statistical Computing, Vienna (Austria).
72. Krysko, O., Maes, T., Plantinga, M., Holtappels, G., Imiru, R., Vandenabeele, P., et al. The adjuvant-like activity of staphylococcal enterotoxin B in a murine asthma model is independent of IL-1R signaling. Allergy 68 (2013), 446–453.
73. Hudson, Z., Sample size, power and effect size—what all researchers need to know. Phys Ther Sport 10 (2009), 43–44.