Tissue-specific patterning of host innate immune responses by staphylococcus aureus α-Toxin

Journal of Innate Immunity

Volumn 6, Issue 5, 2014, Pages 619-631

  Becker, Russell E N ^a   Berube, Bryan J ^a   Sampedro, Georgia R ^a   Dedent, Andrea C ^a   Bubeck Wardenburg, Juliane ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

ADAM10; Innate immunity; Myeloid lineage specific knockout; Pathogenesis; Staphylococcus aureus; Toxin

Indexed keywords

INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MYELOID DIFFERENTIATION FACTOR 88; STAPHYLOCOCCUS ALPHA TOXIN; TOLL LIKE RECEPTOR 2; ADAM10 ENDOPEPTIDASE; ADAM PROTEIN; ADAM10 PROTEIN, MOUSE; BACTERIAL TOXIN; HEMOLYSIN; MEMBRANE PROTEIN; SECRETASE; STAPHYLOCOCCAL ALPHA-TOXIN; VIRULENCE FACTOR;

ADULT; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HOST RESISTANCE; IMMUNE RESPONSE; INNATE IMMUNITY; KNOCKOUT MOUSE; LUNG ALVEOLUS EPITHELIUM; MALE; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; OUTCOME ASSESSMENT; PNEUMONIA; PRIORITY JOURNAL; PROTECTION; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; TISSUE SPECIFICITY; BONE MARROW CELL; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; MICROENVIRONMENT; PROTEIN EXPRESSION; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION PROFILING; GENETICS; HUMAN; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SKIN; STAPHYLOCOCCUS INFECTION; TRANSMISSION; TUMOR MICROENVIRONMENT;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BACTERIAL TOXINS; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; GENE EXPRESSION PROFILING; HEMOLYSIN PROTEINS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-1BETA; LUNG; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY; SKIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84906939947     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000360006     Document Type: Article

References (51)

1. Lowy FD: Staphylococcus aureus infections. N Engl J Med 1998; 339: 520-532.
2. Otto M: Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus . Annu Rev Microbiol 2010; 64: 143-162.
3. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK: Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007; 298: 1763-1771.
4. Antibiotic Resistance Threats in the United States. Washington, US Department of Health and Human Services, 2013.
5. Alonzo F 3rd, Torres VJ: Ba cterial survival amidst an immune onslaught: the contribution of the Staphylococcus aureus leukotoxins. PLoS Pathog 2013; 9:e1003143.
6. Berube BJ, Bubeck Wardenburg J: Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins 2013; 5: 1140-1166.
7. Wilke GA, Bubeck Wardenburg J: Role of a disintegrin and metalloprotease in Staphylococcus aureus alpha-hemoly sin-mediated cellular injury. Proc Natl Acad Sci USA 2010; 107: 13473-13478.
8. Inoshima I, Inoshima N, Wilke GA, Powers ME, Frank KM, Wang Y, Bubeck Wardenburg J: A Staphylococcus au reus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat Med 2011; 17: 1310-1314.
9. Inoshima N, Wang Y, Wardenburg JB: Genetic requirement for ADAM10 in severe Staphylococcus aureus skin infection. J Invest Dermatol 2012; 132: 1513-1516.
10. Powers ME, Kim HK, Wang Y, Bubeck Wardenburg J: ADAM10 mediates vascular injury induced by Staphylococcus aureus alpha-hemolysin. J Infect Dis 2012; 206: 352-356.
11. Bubeck Wardenburg J, Schneewind O: Vaccine protection against Staphylococcus aureus pneumonia. J Exp Med 2008; 205: 287-294.
12. Brady RA, Mocca CP, Prabhakara R, Plaut RD, Shirtliff ME, Merkel TJ, Burns DL: Evaluation of genetically inactivated alpha toxin for protection in multiple mouse models of Staphylococcus aureus infection. PLoS One 2013; 8:e63040.
13. Molne L, Verdrengh M, Tarkowski A: Role of neutrophil leukocytes in cutaneous infection caused by Staphylococcus aureus . Infect Immun 2000; 68: 6162-6167.
14. Bubeck Wardenburg J, Patel RJ, Schneewind O: Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 2007; 75: 1040-1044.
15. Valeva A,Walev I,Pinkernell M,Walker B,Bayley H,Palmer M,Bhakdi S: Transmembrane beta-barrel of staphylococcal alphatoxin forms in sensitive but not in resistant cells. Proc Natl Acad Sci USA. 1997; 94: 11607-11611.
16. Nygaard TK, Pallister KB, DuMont AL, De-Wald M, Watkins RL, Pallister EQ, Malone C, Griffith S, Horswill AR, Torres VJ, Voyich JM: Alpha-toxin induces programmed cell death of human T cells, B cells, and monocytes during USA300 infection. PLoS One 2012; 7:e36532.
17. McGee MP, Kreger A, Leake ES, Harshman S: Toxicity of staphylococcal alpha toxin for rabbit alveolar macrophages. Infect Immun 1983; 39: 439-444.
18. Nygaard TK, Pallister KB, Zurek OW, Voyich JM: The impact of alpha-toxin on host cell plasma membrane permeability and cytokine expression during human blood infection by CA-MRSA USA300. J Leukoc Biol 2013; 94: 971-979.
19. Bhakdi S, Muhly M, Korom S, Hugo F: Release of interleukin-1 beta associated with potent cytocidal action of staphylococcal alphatoxin on human monocytes. Infect Immun 1989; 57: 3512-3519.
20. Munoz-Planillo R, Franchi L, Miller LS, Nunez G: A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J Immunol 2009; 183: 3942-3948.
21. Cho JS, Guo Y, Ramos RI, Hebroni F, Plaisier SB, Xuan C, Granick JL, Matsushima H, Takashima A, Iwakura Y, Cheung AL, Cheng G, Lee DJ, Simon SI, Miller LS: Neutrophil-derived IL-1beta is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog 2012; 8:e1003047.
22. Hruz P, Zinkernagel AS, Jenikov a G, Botwin GJ, Hugot JP, Karin M, Nizet V, Eckmann L: NOD2 contributes to cutaneous defense against Staphylococcus aureus through alphatoxin-dependent innate immune activation. Proc Natl Acad Sci USA 2009; 106: 12873-12878.
23. Craven RR, Gao X, Allen IC, Gris D, Bubeck Wardenburg J, McElvania-Tekippe E, Ting JP, Duncan JA: Staphylococcus aureus alphahemolysin activates the NLRP3-inflammasome in human and m ouse monocytic cells. PloS One 2009; 4:e7446.
24. Kebaier C, Chamberland RR, Allen IC, Gao X, Broglie PM, Hall JD, Jania C, Doerschuk CM, Tilley SL, Duncan JA: Staphylococc us aureus alpha-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J Infect Dis 2012; 205: 807-817.
25. Bartlett AH, Foster TJ, Hayashida A, Park PW: ǧlpha-toxin facilitates the generation of CXC chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J Infect Dis 2008; 198: 1529-1535.
26. Patel AH, N owlan P, Weavers ED, Foster T: Virulence of protein A-deficient and alphatoxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect Immun 1987; 55: 3103-3110.
27. Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, Braughton KR, Schneewind O, De Leo FR: Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 2010; 202: 1050-1058.
28. Frank KM, Zhou T, Moreno-Vinasco L, Hollett B, Garcia JG, Bubeck Wardenburg J: Host response signature to Staphylococcus a ureus alpha-hemolysin implicates pulmonary Th17 response. Infect Immun 2012; 80: 3161-3169.
29. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O: Poring over pores: alphahemolysin a nd Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 2007; 13: 1405-1406.
30. Neutrophil Methods and Protocols. Totowa, Humana, 2007.
31. Clausen BE, Bu rkhardt C, Reith W, Renkawitz R, Forster I: Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999; 8: 265-277.
32. Tian L, Wu X, Chi C, Han M, Xu T, Zhuang Y: ADAM10 is essential for proteolytic activation of Notch during thymocyte development. Int Immunol 2008; 20: 1181-1187.
33. Ragle BE, Bubeck Wardenburg J: Anti-alphahemolysin monoclonal antibodies mediate protection against Staphylococcus aureus pneumonia. Infect Immun 2009; 77: 2712-2718.
34. Chaimowitz NS, Martin RK, Cichy J, Gibb DR, Patil P, Kang DJ, Farn sworth J, Butcher EC, McCright B, Conrad DH: A disintegrin and metalloproteinase 10 regulates antibody production and maintenance of lymphoid architecture. J Immunol 2011; 187: 5114-5122.
35. Yod a M, Kimura T, Tohmonda T, Uchikawa S, Koba T, Takito J, Morioka H, Matsumoto M, Link DC, Chiba K, Okada Y, Toyama Y, Horiuchi K: Dual functions of cell-autonomous and non-cell-autonomous ADAM10 activit y in granulopoiesis. Blood 2011; 118: 6939-6942.
36. Weber S, Wetzel S, Prox J, Lehmann T, Schneppenheim J, Donners M, Saftig P: Regulation of adult hematopoiesis by the a disintegrin and metalloproteinase 10 (ADAM10). Biochem Biophys Res Commun 2013; 442: 234-241.
37. Holland SM: Chronic granulomatous disease. Clin Rev Allergy Immunol 2010; 38: 3-10.
38. Matthay MA, Zemans RL: The acute respiratory distress syndrome: pathogenesis and treatment. Annu Rev Pathol 2011; 6: 147-163.
39. Miller LS, O'Connell RM, Gutierrez MA, Pietras EM, Shahangian A, Gross CE, Thirumala A, Cheung AL, Cheng G, Modlin RL: MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus . Immunity 2006; 24: 79-91.
40. Miller LS, Pietras EM, Uricchio LH, Hirano K, Rao S, Lin H, O'Connell RM, Iwakura Y, Cheung AL, Cheng G, Modlin RL: Inflammasome-mediated production of IL-1beta is require d for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol 2007; 179: 6933-6942.
41. Spaan AN, Henry T, van Rooijen WJ, Perret M, Badiou C, Aerts PC, Kemmink J, de Ha as CJ, van Kessel KP, Vandenesch F, Lina G, van Strijp JA: The staphylococcal toxin Panton-Valentine leukocidin targets human C5a receptors. Cell Host Microbe 2013; 13: 584-594.
42. Dumont AL, Yoong P, Day CJ, Alonzo F 3rd, McDonald WH, Jennings MP, Torres VJ: Staphylococcus aureus LukAB cytotoxin kills human neutrophils by targeting the CD11b subunit of the integrin Mac-1. Proc Nat l Acad Sci USA 2013; 110: 10794-10799.
43. Alonzo F 3rd, Kozhaya L, Rawlings SA, Reyes-Robles T, DuMont AL, Myszka DG, Landau NR, Unutmaz D, Torres VJ: CCR5 is a receptor for Staph ylococcus aureus leukotoxin ED. Nature 2013; 493: 51-55.
44. Chatterjee SS, Joo HS, Duong AC, Dieringer TD, Tan VY, Song Y, Fischer ER, Cheung GY, Li M, Otto M: Essential Staphylococ cus aureus toxin export system. Nat Med 2013; 19: 364-367.
45. Montgomery CP, Daniels MD, Zhao F, Spellberg B, Chong AS, Daum RS: Local inflammation exacerbates the severity of Staphyloco ccus aureus skin infection. PLoS One 2013; 8: e69508.
46. Abtin A, Jain R, Mitchell AJ, Roediger B, Brzoska AJ, Tikoo S, Cheng Q, Ng LG, Cavanagh LL, von Andrian UH, Hickey MJ, Firth N, Weninger W: Perivascular macrophages mediate neutrophil recruitment during bacterial skin infection. Nat Immunol 2014; 15: 45-53.
47. Inoshima N, Wang Y, Bubeck Wardenburg J: Genetic requirement for ADAM10 in severe Staphylococcus aureus skin infection. J Invest Dermatol 2012; 132: 1513-1516.
48. Cohen TS, Prince AS: Activation of inflammasome signaling mediates pathology of acute P. aeruginosa pneumonia. J Clin Invest 2013; 123: 1630-1637.
49. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K: Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 2005; 32: 311-318.
50. Martin FJ, Parker D, Harfenist BS, Soong G, Prince A: Participation of CD11c(+) leukocytes in methicillin-resistant Staphylococcus aureus clearance from the lung. Infect Immun 2011; 79: 1898- 1904.
51. Casadevall A, Pirofski LA: The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 2003; 1: 17-24.