Collaborative Interferon-γ and Interleukin-17 Signaling Protects the Oral Mucosa from Staphylococcus aureus

American Journal of Pathology

Volumn 186, Issue 9, 2016, Pages 2337-2352

  Barin, Jobert G ^a   Talor, Monica V ^a   Schaub, Julie A ^a   Diny, Nicola L ^b   Hou, Xuezhou ^b   Hoyer, Matthew ^a   Archer, Nathan K ^a   Gebremariam, Elizabeth S ^a   Davis, Meghan F ^b   Miller, Lloyd S ^a   Rose, Noel R ^a,b   Čiháková, Daniela ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CLODRONIC ACID; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 17 RECEPTOR A; LIPOSOME; UNCLASSIFIED DRUG;

ABSCESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; HOST RESISTANCE; IN VIVO STUDY; LYMPH NODE; MACROPHAGE; MONOCYTE; MOUSE; MOUTH ABSCESS; MOUTH MUCOSA; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MOUTH MUCOSA; SIGNAL TRANSDUCTION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84995579569     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2016.07.001     Document Type: Article

References (74)

1. 1 Barin, J.G., Baldeviano, G.C., Talor, M.V., Wu, L., Ong, S., Fairweather, D., Bedja, D., Stickel, N.R., Fontes, J.A., Cardamone, A.B., Zheng, D., Gabrielson, K.L., Rose, N.R., Cihakova, D., Fatal eosinophilic myocarditis develops in the absence of IFN-gamma and IL-17A. J Immunol 191 (2013), 4038–4047.
2. 2 Lowy, F.D., Staphylococcus aureus infections. N Engl J Med 339 (1998), 520–532.
3. 3 Tong, S.Y., Davis, J.S., Eichenberger, E., Holland, T.L., Fowler, V.G. Jr., Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 28 (2015), 603–661.
4. 4 Miller, L.S., Cho, J.S., Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol 11 (2011), 505–518.
5. 5 Cho, J.S., Pietras, E.M., Garcia, N.C., Ramos, R.I., Farzam, D.M., Monroe, H.R., Magorien, J.E., Blauvelt, A., Kolls, J.K., Cheung, A.L., Cheng, G., Modlin, R.L., Miller, L.S., IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120 (2010), 1762–1773.
6. 6 Cho, J.S., Guo, Y., Ramos, R.I., Hebroni, F., Plaisier, S.B., Xuan, C., Granick, J.L., Matsushima, H., Takashima, A., Iwakura, Y., Cheung, A.L., Cheng, G., Lee, D.J., Simon, S.I., Miller, L.S., Neutrophil-derived IL-1beta is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog, 8, 2012, e1003047.
7. 7 Nakane, A., Okamoto, M., Asano, M., Kohanawa, M., Minagawa, T., Endogenous gamma interferon, tumor necrosis factor, and interleukin-6 in Staphylococcus aureus infection in mice. Infect Immun 63 (1995), 1165–1172.
8. 8 Sasaki, S., Nishikawa, S., Miura, T., Mizuki, M., Yamada, K., Madarame, H., Tagawa, Y.I., Iwakura, Y., Nakane, A., Interleukin-4 and interleukin-10 are involved in host resistance to Staphylococcus aureus infection through regulation of gamma interferon. Infect Immun 68 (2000), 2424–2430.
9. 9 Sasaki, S., Tagawa, Y., Iwakura, Y., Nakane, A., The role of gamma interferon in acquired host resistance against Staphylococcus aureus infection in mice. FEMS Immunol Med Microbiol 46 (2006), 367–374.
10. 10 Zhao, Y.X., Tarkowski, A., Impact of interferon-gamma receptor deficiency on experimental Staphylococcus aureus septicemia and arthritis. J Immunol 155 (1995), 5736–5742.
11. 11 Committee for the Update of the Guide for the Care and Use of Laboratory Animals; National Research Council. Guide for the Care and Use of Laboratory Animals: Eighth Edition, 2011, National Academies Press, Washington, DC.
12. 12 Davis, M.F., Baron, P., Price, L.B., Williams, D.L., Jeyaseelan, S., Hambleton, I.R., Diette, G.B., Breysse, P.N., McCormack, M.C., Dry collection and culture methods for recovery of methicillin-susceptible and methicillin-resistant Staphylococcus aureus strains from indoor home environments. Appl Environ Microbiol 78 (2012), 2474–2476.
13. 13 Garcia-Alvarez, L., Holden, M.T., Lindsay, H., Webb, C.R., Brown, D.F., Curran, M.D., Walpole, E., Brooks, K., Pickard, D.J., Teale, C., Parkhill, J., Bentley, S.D., Edwards, G.F., Girvan, E.K., Kearns, A.M., Pichon, B., Hill, R.L., Larsen, A.R., Skov, R.L., Peacock, S.J., Maskell, D.J., Holmes, M.A., Methicillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11 (2011), 595–603.
14. 14 Shopsin, B., Gomez, M., Montgomery, S.O., Smith, D.H., Waddington, M., Dodge, D.E., Bost, D.A., Riehman, M., Naidich, S., Kreiswirth, B.N., Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37 (1999), 3556–3563.
15. 15 Sasaki, T., Tsubakishita, S., Tanaka, Y., Sakusabe, A., Ohtsuka, M., Hirotaki, S., Kawakami, T., Fukata, T., Hiramatsu, K., Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 48 (2010), 765–769.
16. 16 Zhang, K., McClure, J.A., Elsayed, S., Louie, T., Conly, J.M., Novel multiplex PCR assay for simultaneous identification of community-associated methicillin-resistant Staphylococcus aureus strains USA300 and USA400 and detection of mecA and Panton-Valentine leukocidin genes, with discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 46 (2008), 1118–1122.
17. 17 Poyart, C., Quesne, G., Boumaila, C., Trieu-Cuot, P., Rapid and accurate species-level identification of coagulase-negative staphylococci by using the sodA gene as a target. J Clin Microbiol 39 (2001), 4296–4301.
18. 18 Puel, A., Cypowyj, S., Bustamante, J., Wright, J.F., Liu, L., Lim, H.K., 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, N.M., Al-Muhsen, S., Galicchio, M., Abel, L., Picard, C., Casanova, J.L., Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332 (2011), 65–68.
19. 19 Boisson, B., Wang, C., Pedergnana, V., Wu, L., Cypowyj, S., Rybojad, M., Belkadi, A., Picard, C., Abel, L., Fieschi, C., Puel, A., Li, X., Casanova, J.L., An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 39 (2013), 676–686.
20. 20 Bae, I.G., Tonthat, G.T., Stryjewski, M.E., Rude, T.H., Reilly, L.F., Barriere, S.L., Genter, F.C., Corey, G.R., Fowler, V.G. Jr., Presence of genes encoding the panton-valentine leukocidin exotoxin is not the primary determinant of outcome in patients with complicated skin and skin structure infections due to methicillin-resistant Staphylococcus aureus: results of a multinational trial. J Clin Microbiol 47 (2009), 3952–3957.
21. 21 Holtfreter, S., Radcliff, F.J., Grumann, D., Read, H., Johnson, S., Monecke, S., Ritchie, S., Clow, F., Goerke, C., Broker, B.M., Fraser, J.D., Wiles, S., Characterization of a mouse-adapted Staphylococcus aureus strain. PLoS One, 8, 2013, e71142.
22. 22 Kim, M.H., Granick, J.L., Kwok, C., Walker, N.J., Borjesson, D.L., Curry, F.R., Miller, L.S., Simon, S.I., Neutrophil survival and c-kit(+)-progenitor proliferation in Staphylococcus aureus-infected skin wounds promote resolution. Blood 117 (2011), 3343–3352.
23. 23 Mohan, K., Cordeiro, E., Vaci, M., McMaster, C., Issekutz, T.B., CXCR3 is required for migration to dermal inflammation by normal and in vivo activated T cells: differential requirements by CD4 and CD8 memory subsets. Eur J Immunol 35 (2005), 1702–1711.
24. 24 Rivino, L., Messi, M., Jarrossay, D., Lanzavecchia, A., Sallusto, F., Geginat, J., Chemokine receptor expression identifies Pre-T helper (Th)1, Pre-Th2, and nonpolarized cells among human CD4+ central memory T cells. J Exp Med 200 (2004), 725–735.
25. 25 Song, K., Rabin, R.L., Hill, B.J., De Rosa, S.C., Perfetto, S.P., Zhang, H.H., Foley, J.F., Reiner, J.S., Liu, J., Mattapallil, J.J., Douek, D.C., Roederer, M., Farber, J.M., Characterization of subsets of CD4+ memory T cells reveals early branched pathways of T cell differentiation in humans. Proc Natl Acad Sci U S A 102 (2005), 7916–7921.
26. 26 Mosser, D.M., The many faces of macrophage activation. J Leukoc Biol 73 (2003), 209–212.
27. 27 Martinez, F.O., Helming, L., Gordon, S., Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27 (2009), 451–483.
28. 28 Geissmann, F., Jung, S., Littman, D.R., Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 (2003), 71–82.
29. 29 van Rooijen, N., van Kesteren-Hendrikx, E., “In vivo” depletion of macrophages by liposome-mediated “suicide”. Methods Enzymol 373 (2003), 3–16.
30. 30 Liao, F., Rabin, R.L., Yannelli, J.R., Koniaris, L.G., Vanguri, P., Farber, J.M., Human Mig chemokine: biochemical and functional characterization. J Exp Med 182 (1995), 1301–1314.
31. 31 Teruya-Feldstein, J., Jaffe, E.S., Burd, P.R., Kanegane, H., Kingma, D.W., Wilson, W.H., Longo, D.L., Tosato, G., The role of Mig, the monokine induced by interferon-gamma, and IP-10, the interferon-gamma-inducible protein-10, in tissue necrosis and vascular damage associated with Epstein-Barr virus-positive lymphoproliferative disease. Blood 90 (1997), 4099–4105.
32. 32 Eck, M., Schmausser, B., Scheller, K., Toksoy, A., Kraus, M., Menzel, T., Muller-Hermelink, H.K., Gillitzer, R., CXC chemokines Gro(alpha)/IL-8 and IP-10/MIG in Helicobacter pylori gastritis. Clin Exp Immunol 122 (2000), 192–199.
33. 33 Ciccia, F., Alessandro, R., Rizzo, A., Accardo-Palumbo, A., Raimondo, S., Raiata, F., Guggino, G., Giardina, A., De Leo, G., Sireci, G., Triolo, G., Macrophage phenotype in the subclinical gut inflammation of patients with ankylosing spondylitis. Rheumatology 53 (2014), 104–113.
34. 34 Schwarzenberger, P., Kolls, J.K., Interleukin 17: an example for gene therapy as a tool to study cytokine mediated regulation of hematopoiesis. J Cell Biochem Suppl 38 (2002), 88–95.
35. 35 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., Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30 (2009), 108–119.
36. 36 Gaffen, S.L., Jain, R., Garg, A.V., Cua, D.J., The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol 14 (2014), 585–600.
37. 37 Gaffen, S.L., Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 9 (2009), 556–567.
38. 38 Lin, L., Ibrahim, A.S., Xu, X., Farber, J.M., Avanesian, V., Baquir, B., Fu, Y., French, S.W., Edwards, J.E. Jr., Spellberg, B., Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog, 5, 2009, e1000703.
39. 39 Conti, H.R., Whibley, N., Coleman, B.M., Garg, A.V., Jaycox, J.R., Gaffen, S.L., Signaling through IL-17C/IL-17RE is dispensable for immunity to systemic, oral and cutaneous candidiasis. PLoS One, 10, 2015, e0122807.
40. 40 Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T.B., Oukka, M., Weiner, H.L., Kuchroo, V.K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006), 235–238.
41. 41 Harrington, L.E., Hatton, R.D., Mangan, P.R., Turner, H., Murphy, T.L., Murphy, K.M., Weaver, C.T., Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6 (2005), 1123–1132.
42. 42 Damsker, J.M., Hansen, A.M., Caspi, R.R., Th1 and Th17 cells: adversaries and collaborators. Ann N Y Acad Sci 1183 (2010), 211–221.
43. 43 Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M., Stockinger, B., TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006), 179–189.
44. 44 Lee, Y.K., Mukasa, R., Hatton, R.D., Weaver, C.T., Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 21 (2009), 274–280.
45. 45 Kebir, H., Ifergan, I., Alvarez, J.I., Bernard, M., Poirier, J., Arbour, N., Duquette, P., Prat, A., Preferential recruitment of interferon-gamma-expressing TH17 cells in multiple sclerosis. Ann Neurol 66 (2009), 390–402.
46. 46 Hirota, K., Duarte, J.H., Veldhoen, M., Hornsby, E., Li, Y., Cua, D.J., Ahlfors, H., Wilhelm, C., Tolaini, M., Menzel, U., Garefalaki, A., Potocnik, A.J., Stockinger, B., Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 12 (2011), 255–263.
47. 47 Sallusto, F., Zielinski, C.E., Lanzavecchia, A., Human Th17 subsets. Eur J Immunol 42 (2012), 2215–2220.
48. 48 Peters, A., Lee, Y., Kuchroo, V.K., The many faces of Th17 cells. Curr Opin Immunol 23 (2011), 702–706.
49. 49 Picard, C., Puel, A., Bonnet, M., Ku, C.L., Bustamante, J., Yang, K., Soudais, C., Dupuis, S., Feinberg, J., Fieschi, C., Elbim, C., Hitchcock, R., Lammas, D., Davies, G., Al-Ghonaium, A., Al-Rayes, H., Al-Jumaah, S., Al-Hajjar, S., Al-Mohsen, I.Z., Frayha, H.H., Rucker, R., Hawn, T.R., Aderem, A., Tufenkeji, H., Haraguchi, S., Day, N.K., Good, R.A., Gougerot-Pocidalo, M.A., Ozinsky, A., Casanova, J.L., Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299 (2003), 2076–2079.
50. 50 Picard, C., von Bernuth, H., Ghandil, P., Chrabieh, M., Levy, O., Arkwright, P.D., et al. Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency. Medicine 89 (2010), 403–425.
51. 51 von Bernuth, H., Picard, C., Jin, Z., Pankla, R., Xiao, H., Ku, C.L., et al. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321 (2008), 691–696.
52. 52 Gonzalez-Barca, E., Carratala, J., Mykietiuk, A., Fernandez-Sevilla, A., Gudiol, F., Predisposing factors and outcome of Staphylococcus aureus bacteremia in neutropenic patients with cancer. Eur J Clin Microbiol Infect Dis 20 (2001), 117–119.
53. 53 Andrews, T., Sullivan, K.E., Infections in patients with inherited defects in phagocytic function. Clin Microbiol Rev 16 (2003), 597–621.
54. 54 Winterbourn, C.C., Kettle, A.J., Hampton, M.B., Reactive Oxygen Species and Neutrophil Function. Annu Rev Biochem 85 (2016), 765–792.
55. 55 Gordon, S., Taylor, P.R., Monocyte and macrophage heterogeneity. Nat Rev Immunol 5 (2005), 953–964.
56. 56 Hamza, T., Li, B., Differential responses of osteoblasts and macrophages upon Staphylococcus aureus infection. BMC Microbiol, 14, 2014, 207.
57. 57 Dey, S., Bishayi, B., Killing of Staphylococcus aureus in murine macrophages by chloroquine used alone and in combination with ciprofloxacin or azithromycin. J Inflamm Res 8 (2015), 29–47.
58. 58 Das, D., Bishayi, B., Staphylococcal catalase protects intracellularly survived bacteria by destroying H2O2 produced by the murine peritoneal macrophages. Microb Pathog 47 (2009), 57–67.
59. 59 Das, D., Bishayi, B., Contribution of Catalase and Superoxide Dismutase to the Intracellular Survival of Clinical Isolates of Staphylococcus aureus in Murine Macrophages. Indian J Microbiol 50 (2010), 375–384.
60. 60 Smith, R.P., Baltch, A.L., Ritz, W.J., Michelsen, P.B., Bopp, L.H., IFN-gamma enhances killing of methicillin-resistant Staphylococcus aureus by human monocytes more effectively than GM-CSF in the presence of daptomycin and other antibiotics. Cytokine 51 (2010), 274–277.
61. 61 Wu, L., Ong, S., Talor, M.V., Barin, J.G., Baldeviano, G.C., Kass, D.A., Bedja, D., Zhang, H., Sheikh, A., Margolick, J.B., Iwakura, Y., Rose, N.R., Cihakova, D., Cardiac fibroblasts mediate IL-17A-driven inflammatory dilated cardiomyopathy. J Exp Med 211 (2014), 1449–1464.
62. 62 Groom, J.R., Luster, A.D., CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 89 (2011), 207–215.
63. 63 Farber, J.M., Mig and IP-10: CXC chemokines that target lymphocytes. J Leukoc Biol 61 (1997), 246–257.
64. 64 Martin, F.J., Parker, D., Harfenist, B.S., Soong, G., Prince, A., Participation of CD11c(+) leukocytes in methicillin-resistant Staphylococcus aureus clearance from the lung. Infect Immun 79 (2011), 1898–1904.
65. 65 Qin, S., Rottman, J.B., Myers, P., Kassam, N., Weinblatt, M., Loetscher, M., Koch, A.E., Moser, B., Mackay, C.R., The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 101 (1998), 746–754.
66. 66 Sallusto, F., Lenig, D., Mackay, C.R., Lanzavecchia, A., Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med 187 (1998), 875–883.
67. 67 Holland, S.M., DeLeo, F.R., Elloumi, H.Z., Hsu, A.P., Uzel, G., Brodsky, N., Freeman, A.F., Demidowich, A., Davis, J., Turner, M.L., Anderson, V.L., Darnell, D.N., Welch, P.A., Kuhns, D.B., Frucht, D.M., Malech, H.L., Gallin, J.I., Kobayashi, S.D., Whitney, A.R., Voyich, J.M., Musser, J.M., Woellner, C., Schaffer, A.A., Puck, J.M., Grimbacher, B., STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 357 (2007), 1608–1619.
68. 68 Minegishi, Y., Saito, M., Tsuchiya, S., Tsuge, I., Takada, H., Hara, T., Kawamura, N., Ariga, T., Pasic, S., Stojkovic, O., Metin, A., Karasuyama, H., Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 448 (2007), 1058–1062.
69. 69 Puel, A., Cypowyj, S., Marodi, L., Abel, L., Picard, C., Casanova, J.L., Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr Opin Allergy Clin Immunol 12 (2012), 616–622.
70. 70 Paulson, M.L., Freeman, A.F., Holland, S.M., Hyper IgE syndrome: an update on clinical aspects and the role of signal transducer and activator of transcription 3. Curr Opin Allergy Clin Immunol 8 (2008), 527–533.
71. 71 Ito, R., Mori, M., Katakura, S., Kobayashi, N., Naruto, T., Osamura, Y., Aihara, Y., Yokota, S., Selective insufficiency of IFN-gamma secretion in patients with hyper-IgE syndrome. Allergy 58 (2003), 329–336.
72. 72 Paganelli, R., Scala, E., Capobianchi, M.R., Fanales-Belasio, E., D'Offizi, G., Fiorilli, M., Aiuti, F., Selective deficiency of interferon-gamma production in the hyper-IgE syndrome. Relationship to in vitro IgE synthesis. Clin Exp Immunol 84 (1991), 28–33.
73. 73 Del Prete, G., Tiri, A., Maggi, E., De Carli, M., Macchia, D., Parronchi, P., Rossi, M.E., Pietrogrande, M.C., Ricci, M., Romagnani, S., Defective in vitro production of gamma-interferon and tumor necrosis factor-alpha by circulating T cells from patients with the hyper-immunoglobulin E syndrome. J Clin Invest 84 (1989), 1830–1835.
74. 74 Thammavongsa, V., Missiakas, D.M., Schneewind, O., Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 342 (2013), 863–866.