The impact of α toxin on host cell plasma membrane permeability and cytokine expression during human blood infection by CA-MRSA USA300

Journal of Leukocyte Biology

Volumn 94, Issue 5, 2013, Pages 971-979

  Nygaard, Tyler K ^a   Pallister, Kyler B ^a   Zurek, Oliwia W ^a   Voyich, Jovanka M ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Chemokine; Monocyte; Pathogenesis; Staphylococcus aureus; T cell; Virulence

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALPHA TOXIN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BLOODSTREAM INFECTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MONOCYTE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

CHEMOKINE; MONOCYTE; PATHOGENESIS; STAPHYLOCOCCUS AUREUS; T CELL; VIRULENCE;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANTIGENS, CD14; BACTEREMIA; BACTERIAL TOXINS; CELL MEMBRANE PERMEABILITY; CYTOKINES; HEMOLYSIN PROTEINS; HUMANS; MEMBRANE PROTEINS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCAL INFECTIONS;

EID: 84887004573     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0213080     Document Type: Article

References (57)

1. Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., Harrison, L. H., Lynfield, R., Dumyati, G., Townes, J. M., Craig, A. S., Zell, E. R., Fosheim, G. E., McDougal, L. K., Carey, R. B., Fridkin, S. K., Active Bacterial Core Surveillance (ABCs) MRSA Investigators (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763-1771.
2. Nygaard, T. K., DeLeo, F. R., Voyich, J. M. (2008) Community-associated methicillin-resistant Staphylococcus aureus skin infections: advances toward identifying the key virulence factors. Curr. Opin. Infect. Dis. 21, 147-152.
3. Moran, G. J., Krishnadasan, A., Gorwitz, R. J., Fosheim, G. E., McDougal, L. K., Carey, R. B., Talan, D. A., EMERGEncy ID Net Study Group (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N. Engl. J. Med. 355, 666-674.
4. Li, M., Cheung, G. Y., Hu, J., Wang, D., Joo, H. S., Deleo, F. R., Otto, M. (2010) Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J. Infect. Dis. 202, 1866-1876.
5. Voyich, J. M., Braughton, K. R., Sturdevant, D. E., Whitney, A. R., Said Salim, B., Porcella, S. F., Long, R. D., Dorward, D. W., Gardner, D. J., Kreiswirth, B. N., Musser, J. M., DeLeo, F. R. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175, 3907-3919.
6. Seybold, U., Kourbatova, E. V., Johnson, J. G., Halvosa, S. J., Wang, Y. F., King, M. D., Ray, S. M., Blumberg, H. M. (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin. Infect. Dis. 42, 647-656.
7. Nygaard, T. K., Pallister, K. B., Dumont, A. L., Dewald, M., Watkins, R. L., Pallister, E. Q., Malone, C., Griffith, S., Horswill, A. R., Torres, V. J., Voyich, J. M. (2012)-Toxin induces programmed cell death of human T cells, B cells, and monocytes during USA300 infection. PLoS One 7, e36532.
8. Prince, L. R., Graham, K. J., Connolly, J., Anwar, S., Ridley, R., Sabroe, I., Foster, S. J., Whyte, M. K. (2012) Staphylococcus aureus induces eosinophil cell death mediated by-hemolysin. PLoS One 7, e31506.
9. Bubeck Wardenburg, J., Schneewind, O. (2008) Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205, 287-294.
10. Kennedy, A. D., Bubeck Wardenburg, J., Gardner, D. J., Long, D., Whitney, A. R., Braughton, K. R., Schneewind, O., DeLeo, F. R. (2010) Targeting of-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 202, 1050-1058.
11. Nygaard, T. K., Pallister, K. B., Ruzevich, P., Griffith, S., Vuong, C., Voyich, J. M. (2010) SaeR binds a consensus sequence within virulence gene promoters to advance USA300 pathogenesis. J. Infect. Dis. 201, 241-254.
12. Montgomery, C. P., Boyle-Vavra, S., Daum, R. S. (2010) Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5, e15177.
13. Loughman, J. A., Fritz, S. A., Storch, G. A., Hunstad, D. A. (2009) Virulence gene expression in human community-acquired Staphylococcus aureus infection. J. Infect. Dis. 199, 294-301.
14. Malachowa, N., Whitney, A. R., Kobayashi, S. D., Sturdevant, D. E., Kennedy, A. D., Braughton, K. R., Shabb, D. W., Diep, B. A., Chambers, H. F., Otto, M., DeLeo, F. R. (2011) Global changes in Staphylococcus aureus gene expression in human blood. PLoS One 6, e18617.
15. Palazzolo-Ballance, A. M., Reniere, M. L., Braughton, K. R., Sturdevant, D. E., Otto, M., Kreiswirth, B. N., Skaar, E. P., DeLeo, F. R. (2008) Neutrophil microbicides induce a pathogen survival response in communityassociated methicillin-resistant Staphylococcus aureus. J. Immunol. 180, 500-509.
16. Montgomery, C. P., Boyle-Vavra, S., Adem, P. V., Lee, J. C., Husain, A. N., Clasen, J., Daum, R. S. (2008) Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J. Infect. Dis. 198, 561-570.
17. Inoshima, I., Inoshima, N., Wilke, G. A., Powers, M. E., Frank, K. M., Wang, Y., Bubeck Wardenburg, J. (2011) A Staphylococcus aureus poreforming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 17, 1310-1314.
18. Wilke, G. A., and Bubeck Wardenburg, J. (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus-hemolysin-mediated cellular injury. Proc. Natl. Acad. Sci. USA 107, 13473-13478.
19. Diep, B. A., Gill, S. R., Chang, R. F., Phan, T. H., Chen, J. H., Davidson, M. G., Lin, F., Lin, J., Carleton, H. A., Mongodin, E. F., Sensabaugh, G. F., Perdreau-Remington, F. (2006) Complete genome sequence of USA300, an epidemic clone of ommunity-acquired meticillin-resistant Staphylococcus aureus. Lancet 367, 731-739.
20. Boyum, A. (1968) Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab. Invest. Suppl. 97, 77-89.
21. Voyich, J. M., DeLeo, F. R. (2002) Host-pathogen interactions: leukocyte phagocytosis and associated sequelae. Methods Cell. Sci. 24, 79-90.
22. Graves, S. F., Kobayashi, S. D., Braughton, K. R., Diep, B. A., Chambers, H. F., Otto, M., Deleo, F. R. (2010) Relative contribution of PantonValentine leukocidin to PMN plasma membrane permeability and lysis caused by USA300 and USA400 culture supernatants. Microbes Infect. 12, 446-456.
23. Kobayashi, S. D., Braughton, K. R., Palazzolo-Ballance, A. M., Kennedy, A. D., Sampaio, E., Kristosturyan, E., Whitney, A. R., Sturdevant, D. E., Dorward, D. W., Holland, S. M., Kreiswirth, B. N., Musser, J. M., DeLeo, F. R. (2010) Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus. J. Innate Immun. 2, 560-575.
24. Bhakdi, S., Muhly, M., Korom, S., Hugo, F. (1989) Release of interleukin-1 associated with potent cytocidal action of Staphylococcaltoxin on human monocytes. Infect. Immun. 57, 3512-3519.
25. Frank, K. M., Zhou, T., Moreno-Vinasco, L., Hollett, B., Garcia, J. G., Bubeck Wardenburg, J. (2012) Host response signature to Staphylococcus aureus-hemolysin implicates pulmonary Th17 response. Infect. Immun. 80, 3161-3169.
26. Hruz, P., Zinkernagel, A. S., Jenikova, G., Botwin, G. J., Hugot, J. P., Karin, M., Nizet, V., Eckmann, L. (2009) NOD2 contributes to cutaneous defense against Staphylococcus aureus through -toxin-dependent innate immune activation. Proc. Natl. Acad. Sci. USA 106, 12873-12878.
27. Munoz-Planillo, R., Franchi, L., Miller, L. S., Nunez, G. (2009) A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureusinduced activation of the Nlrp3 inflammasome. J. Immunol. 183, 3942-3948.
28. Niebuhr, M., Gathmann, M., Scharonow, H., Mamerow, D., Mommert, S., Balaji, H., Werfel, T. (2011) Staphylococcal -toxin is a strong inducer of interleukin-17 in humans. Infect. Immun. 79, 1615-1622.
29. Walev, I., Weller, U., Strauch, S., Foster, T., Bhakdi, S. (1996) Selective killing of human monocytes and cytokine release provoked by sphingomyelinase (-toxin) of Staphylococcus aureus. Infect. Immun. 64, 2974-2979.
30. Montgomery, C. P., Daum, R. S. (2009) Transcription of inflammatory genes in the lung after infection with community-associated methicillinresistant Staphylococcus aureus: a role for Panton-Valentine leukocidin? Infect. Immun. 77, 2159-2167.
31. Kielian, T., Bearden, E. D., Baldwin, A. C., Esen, N. (2004) IL-1 and TNFplay a pivotal role in the host immune response in a mouse model of Staphylococcus aureus-induced experimental brain abscess. J. Neuropathol. Exp. Neurol. 63, 381-396.
32. Auffray, C., Sieweke, M. H., Geissmann, F. (2009) Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669-692.
33. Menten, P., Wuyts, A., Van Damme, J. (2002) Macrophage inflammatory protein-1. Cytokine Growth Factor Rev. 13, 455-481.
34. Schutyser, E., Richmond, A., Van Damme, J. (2005) Involvement of CC chemokine ligand 18 (CCL18) in normal and pathological processes. J. Leukoc. Biol. 78, 14-26.
35. Schutyser, E., Struyf, S., Van Damme, J. (2003) The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 14, 409-426.
36. Kebaier, C., Chamberland, R. R., Allen, I. C., Gao, X., Broglie, P. M., Hall, J. D., Jania, C., Doerschuk, C. M., Tilley, S. L., Duncan, J. A. (2012) Staphylococcus aureus-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J. Infect. Dis. 205, 807-817.
37. Gresham, H. D., Lowrance, J. H., Caver, T. E., Wilson, B. S., Cheung, A. L., Lindberg, F. P. (2000) Survival of Staphylococcus aureus inside neutrophils contributes to infection. J. Immunol. 164, 3713-3722.
38. Kubica, M., Guzik, K., Koziel, J., Zarebski, M., Richter, W., Gajkowska, B., Golda, A., Maciag-Gudowska, A., Brix, K., Shaw, L., Foster, T., Potempa, J. (2008) A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS One 3, e1409.
39. Prajsnar, T. K., Hamilton, R., Garcia-Lara, J., McVicker, G., Williams, A., Boots, M., Foster, S. J., Renshaw, S. A. (2012) A privileged intraphagocyte niche is responsible for disseminated infection of Staphylococcus aureus in a zebrafish model. Cell. Microbiol. 14, 1600-1619.
40. Thwaites, G. E., Gant, V. (2011) Are bloodstream leukocytes Trojan Horses for the metastasis of Staphylococcus aureus? Nat. Rev. Microbiol. 9, 215-222.
41. Koziel, J., Maciag-Gudowska, A., Mikolajczyk, T., Bzowska, M., Sturdevant, D. E., Whitney, A. R., Shaw, L. N., DeLeo, F. R., Potempa, J. (2009) Phagocytosis of Staphylococcus aureus by macrophages exerts cytoprotective effects manifested by the upregulation of antiapoptotic factors. PLoS One 4, e5210.
42. Miller, L. S., Cho, J. S. (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat. Rev. Immunol. 11, 505-518.
43. Wang, J. E., Jorgensen, P. F., Almlof, M., Thiemermann, C., Foster, S. J., Aasen, A. O., Solberg, R. (2000) Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect. Immun. 68, 3965-3970.
44. Frodermann, V., Chau, T. A., Sayedyahossein, S., Toth, J. M., Heinrichs, D. E., Madrenas, J. (2011) A modulatory interleukin-10 response to Staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. J. Infect. Dis. 204, 253-262.
45. Van Beelen, A. J., Zelinkova, Z., Taanman-Kueter, E. W., Muller, F. J., Hommes, D. W., Zaat, S. A., Kapsenberg, M. L., de Jong, E. C. (2007) Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity 27, 660-669.
46. Shimada, T., Park, B. G., Wolf, A. J., Brikos, C., Goodridge, H. S., Becker, C. A., Reyes, C. N., Miao, E. A., Aderem, A., Gotz, F., Liu, G. Y., Underhill, D. M. (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1 secretion. Cell Host Microbe 7, 38-49.
47. Watkins, R. L., Pallister, K. B., Voyich, J. M. (2011) The SaeR/S gene regulatory system induces a pro-inflammatory cytokine response during Staphylococcus aureus infection. PLoS One 6, e19939.
48. Holzinger, D., Gieldon, L., Mysore, V., Nippe, N., Taxman, D. J., Duncan, J. A., Broglie, P. M., Marketon, K., Austermann, J., Vogl, T., Foell, D., Niemann, S., Peters, G., Roth, J., Löffler, B. (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J. Leukoc. Biol. 92, 1069-1081.
49. Reynolds, J. M., Angkasekwinai, P., Dong, C. (2010) IL-17 family member cytokines: regulation and function in innate immunity. Cytokine Growth Factor Rev. 21, 413-423.
50. Wilson, N. J., Boniface, K., Chan, J. R., McKenzie, B. S., Blumenschein, W. M., Mattson, J. D., Basham, B., Smith, K., Chen, T., Morel, F., Lecron, J. C., Kastelein, R. A., Cua, D. J., McClanahan, T. K., Bowman, E. P., de Waal Malefyt, R. (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8, 950-957.
51. Zielinski, C. E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., Monticelli, S., Lanzavecchia, A., Sallusto, F. (2012) Pathogen-induced human TH17 cells produce IFN-÷ or IL-10 and are regulated by IL-1. Nature 484, 514-518.
52. Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A., Sallusto, F. (2007) Interleukins 1 and 6 but not transforming growth factorare essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8, 942-949.
53. 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. (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 120, 1762-1773.
54. Ma, C. S., Chew, G. Y., Simpson, N., Priyadarshi, A., Wong, M., Grimbacher, B., Fulcher, D. A., Tangye, S. G., Cook, M. C. (2008) Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 205, 1551-1557.
55. Schmaler, M., Jann, N. J., 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, 443-452.
56. Ardura, M. I., Banchereau, R., Mejias, A., Di Pucchio, T., Glaser, C., Allantaz, F., Pascual, V., Banchereau, J., Chaussabel, D., Ramilo, O. (2009) Enhanced monocyte response and decreased central memory T cells in children with invasive Staphylococcus aureus infections. PLoS One 4, e5446.
57. Szkaradkiewicz, A., Karpinski, T. M., Zeidler, A., Szkaradkiewicz, A. K., Masiuk, H., Giedrys-Kalemba, S. (2012) Cytokine response in patients with chronic infections caused by Staphylococcus aureus strains and diversification of their Agr system classes. Eur. J. Clin. Microbiol. Infect. Dis. 31, 2809-2815.