CD36 is essential for regulation of the host innate response to Staphylococcus aureus α-toxin-mediated dermonecrosis

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2294-2302

  Castleman, Moriah J ^a   Febbraio, Maria ^b   Hall, Pamela R ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; CXCL1 CHEMOKINE; INTERLEUKIN 1BETA; STAPHYLOCOCCUS ALPHA TOXIN; TUMOR NECROSIS FACTOR ALPHA; BACTERIAL TOXIN; HEMOLYSIN; SCAVENGER RECEPTOR; STAPHYLOCOCCAL ALPHA-TOXIN;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE PRODUCTION; HOST RESISTANCE; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN INJURY; SKIN NECROSIS; STAPHYLOCOCCUS AUREUS; WILD TYPE MOUSE; ANIMAL; APOPTOSIS; BACTERIAL SKIN DISEASE; C57BL MOUSE; DISEASE MODEL; FLOW CYTOMETRY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; NEUTROPHIL; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS INFECTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD36; APOPTOSIS; BACTERIAL TOXINS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; HEMOLYSIN PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PHAGOCYTOSIS; RECEPTORS, SCAVENGER; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN DISEASES, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84940121894     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500500     Document Type: Article

References (57)

1. Moran, G. J., A. Krishnadasan, R. J. Gorwitz, G. E. Fosheim, L. K. McDougal, R. B. Carey, and D. A. Talan, EMERGEncy ID Net Study Group. 2006. Methicillin-resistant S. aureus infections among patients in the emergency department. N. Engl. J. Med. 355: 666-674.
2. Talan, D. A., A. Krishnadasan, R. J. Gorwitz, G. E. Fosheim, B. Limbago, V. Albrecht, and G. J. Moran, EMERGEncy ID Net Study Group. 2011. Comparison of Staphylococcus aureus from skin and soft-tissue infections in US emergency department patients, 2004 and 2008. Clin. Infect. Dis. 53: 144-149.
3. Inoshima, N., Y. Wang, and J. Bubeck Wardenburg. 2012. Genetic requirement for ADAM10 in severe Staphylococcus aureus skin infection. J. Invest. Dermatol. 132: 1513-1516.
4. Kennedy, A. D., J. Bubeck Wardenburg, D. J. Gardner, D. Long, A. R. Whitney, K. R. Braughton, O. Schneewind, and F. R. DeLeo. 2010. Targeting of a-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 202: 1050-1058.
5. Sampedro, G. R., A. C. DeDent, R. E. Becker, B. J. Berube, M. J. Gebhardt, H. Cao, and J. Bubeck Wardenburg. 2014. Targeting Staphylococcus aureus a-toxin as a novel approach to reduce severity of recurrent skin and soft-tissue infections. J. Infect. Dis. 210: 1012-1018.
6. Kobayashi, S. D., N. Malachowa, A. R. Whitney, K. R. Braughton, D. J. Gardner, D. Long, J. Bubeck Wardenburg, O. Schneewind, M. Otto, and F. R. Deleo. 2011. Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J. Infect. Dis. 204: 937-941.
7. Tkaczyk, C., M. M. Hamilton, V. Datta, X. P. Yang, J. J. Hilliard, G. L. Stephens, A. Sadowska, L. Hua, T. O'Day, J. Suzich, et al. 2013. Staphylococcus aureus a-toxin suppresses effective innate and adaptive immune responses in a murine dermonecrosis model. PLoS One 8: e75103.
8. Becker, R. E., B. J. Berube, G. R. Sampedro, A. C. DeDent, and J. Bubeck Wardenburg. 2014. Tissue-specific patterning of host innate immune responses by Staphylococcus aureus a-toxin. J. Innate Immun. 6: 619-631.
9. Berube, B. J., and J. Bubeck Wardenburg. 2013. Staphylococcus aureus a-toxin: nearly a century of intrigue. Toxins (Basel) 5: 1140-1166.
10. Inoshima, I., N. Inoshima, G. A. Wilke, M. E. Powers, K. M. Frank, Y. Wang, and J. Bubeck Wardenburg. 2011. A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 17: 1310-1314.
11. Powers, M. E., H. K. Kim, Y.Wang, and J. Bubeck Wardenburg. 2012. ADAM10 mediates vascular injury induced by Staphylococcus aureus a-hemolysin. J. Infect. Dis. 206: 352-356.
12. Wilke, G. A., and J. Bubeck Wardenburg. 2010. Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus a-hemolysin-mediated cellular injury. Proc. Natl. Acad. Sci. USA 107: 13473-13478.
13. Rigby, K. M., and F. R. DeLeo. 2012. Neutrophils in innate host defense against Staphylococcus aureus infections. Semin. Immunopathol. 34: 237-259.
14. Weiss, S. J. 1989. Tissue destruction by neutrophils. N. Engl. J. Med. 320: 365-376.
15. Soehnlein, O., and L. Lindbom. 2010. Phagocyte partnership during the onset and resolution of inflammation. Nat. Rev. Immunol. 10: 427-439.
16. Bartlett, A. H., T. J. Foster, A. Hayashida, and P. W. Park. 2008. α-Toxin facilitates the generation of CXC chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J. Infect. Dis. 198: 1529-1535.
17. Silverstein, R. L., and M. Febbraio. 2009. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2: re3.
18. Park, Y. M. 2014. CD36, a scavenger receptor implicated in atherosclerosis. Exp. Mol. Med. 46: e99.
19. Collot-Teixeira, S., J. Martin, C. McDermott-Roe, R. Poston, and J. L. McGregor. 2007. CD36 and macrophages in atherosclerosis. Cardiovasc. Res. 75: 468-477.
20. Stuart, L. M., J. Deng, J. M. Silver, K. Takahashi, A. A. Tseng, E. J. Hennessy, R. A. Ezekowitz, and K. J. Moore. 2005. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170: 477-485.
21. Hoebe, K., P. Georgel, S. Rutschmann, X. Du, S. Mudd, K. Crozat, S. Sovath, L. Shamel, T. Hartung, U. Zähringer, and B. Beutler. 2005. CD36 is a sensor of diacylglycerides. Nature 433: 523-527.
22. Navazo, M. D., L. Daviet, J. Savill, Y. Ren, L. L. Leung, and J. L. McGregor. 1996. Identification of a domain (155-183) on CD36 implicated in the phagocytosis of apoptotic neutrophils. J. Biol. Chem. 271: 15381-15385.
23. Ren, Y., R. L. Silverstein, J. Allen, and J. Savill. 1995. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181: 1857-1862.
24. Savill, J., N. Hogg, and C. Haslett. 1991. Macrophage vitronectin receptor, CD36, and thrombospondin cooperate in recognition of neutrophils undergoing programmed cell death. Chest 99(3, Suppl)6S-7S.
25. Savill, J., N. Hogg, Y. Ren, and C. Haslett. 1992. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90: 1513-1522.
26. Rothfork, J. M., G. S. Timmins, M. N. Harris, X. Chen, A. J. Lusis, M. Otto, A. L. Cheung, and H. D. Gresham. 2004. Inactivation of a bacterial virulence pheromone by phagocyte-derived oxidants: new role for the NADPH oxidase in host defense. Proc. Natl. Acad. Sci. USA 101: 13867-13872.
27. Malachowa, N., S. D. Kobayashi, K. R. Braughton, and F. R. DeLeo. 2013. Mouse model of Staphylococcus aureus skin infection. Methods Mol. Biol. 1031: 109-116.
28. Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9: 671-675.
29. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
30. Bernheimer, A. W. 1988. Assay of hemolytic toxins. Methods Enzymol. 165: 213-217.
31. Bubeck Wardenburg, J., T. Bae, M. Otto, F. R. Deleo, and O. Schneewind. 2007. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13: 1405-1406.
32. Berube, B. J., G. R. Sampedro, M. Otto, and J. Bubeck Wardenburg. 2014. The psma locus regulates production of Staphylococcus aureus a-toxin during infection. Infect. Immun. 82: 3350-3358.
33. Montgomery, C. P., S. Boyle-Vavra, and R. S. Daum. 2010. Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5: e15177.
34. Cheung, G. Y., R. Wang, B. A. Khan, D. E. Sturdevant, and M. Otto. 2011. Role of the accessory gene regulator agr in community-associated methicillinresistant Staphylococcus aureus pathogenesis. Infect. Immun. 79: 1927-1935.
35. Sully, E. K., N. Malachowa, B. O. Elmore, S. M. Alexander, J. K. Femling, B. M. Gray, F. R. DeLeo, M. Otto, A. L. Cheung, B. S. Edwards, et al. 2014. Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance. PLoS Pathog. 10: e1004174.
36. Daly, S. M., B. O. Elmore, J. S. Kavanaugh, K. D. Triplett, M. Figueroa, H. A. Raja, T. El-Elimat, H. A. Crosby, J. K. Femling, N. B. Cech, et al. 2015. v-Hydroxyemodin limits staphylococcus aureus quorum sensing-mediated pathogenesis and inflammation. Antimicrob. Agents Chemother. 59: 2223-2235.
37. Wang, R., K. R. Braughton, D. Kretschmer, T. H. L. Bach, S. Y. Queck, M. Li, A. D. Kennedy, D. W. Dorward, S. J. Klebanoff, A. Peschel, et al. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 13: 1510-1514.
38. Peterson, M. M., J. L. Mack, P. R. Hall, A. A. Alsup, S. M. Alexander, E. K. Sully, Y. S. Sawires, A. L. Cheung, M. Otto, and H. D. Gresham. 2008. Apolipoprotein B Is an innate barrier against invasive Staphylococcus aureus infection. Cell Host Microbe 4: 555-566.
39. Wright, J. S., III, R. Jin, and R. P. Novick. 2005. Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc. Natl. Acad. Sci. USA 102: 1691-1696.
40. Jursch, R., A. Hildebrand, G. Hobom, J. Tranum-Jensen, R. Ward, M. Kehoe, and S. Bhakdi. 1994. Histidine residues near the N terminus of staphylococcal a-toxin as reporters of regions that are critical for oligomerization and pore formation. Infect. Immun. 62: 2249-2256.
41. Bubeck Wardenburg, J., and O. Schneewind. 2008. Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205: 287-294.
42. Muñoz-Planillo, R., L. Franchi, L. S. Miller, and G. Núñez. 2009. A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J. Immunol. 183: 3942-3948.
43. Craven, R. R., X. Gao, I. C. Allen, D. Gris, J. Bubeck Wardenburg, E. McElvania-Tekippe, J. P. Ting, and J. A. Duncan. 2009. Staphylococcus aureus a-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS One 4: e7446.
44. Sutterwala, F. S., S. Haasken, and S. L. Cassel. 2014. Mechanism of NLRP3 inflammasome activation. Ann. N. Y. Acad. Sci. 1319: 82-95.
45. Cho, J. S., Y. Guo, R. I. Ramos, F. Hebroni, S. B. Plaisier, C. Xuan, J. L. Granick, H. Matsushima, A. Takashima, Y. Iwakura, et al. 2012. Neutrophil-derived IL-1β is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog. 8: e1003047.
46. Ford, C. W., J. C. Hamel, D. Stapert, and R. J. Yancey. 1989. Establishment of an experimental model of a Staphylococcus aureus abscess in mice by use of dextran and gelatin microcarriers. J. Med. Microbiol. 28: 259-266.
47. Nygaard, T. K., K. B. Pallister, A. L. DuMont, M. DeWald, R. L. Watkins, E. Q. Pallister, C. Malone, S. Griffith, A. R. Horswill, V. J. Torres, and J. M. Voyich. 2012. α-Toxin induces programmed cell death of human T cells, B cells, and monocytes during USA300 infection. PLoS One 7: e36532.
48. Miller, L. S., R. M. O'Connell, M. A. Gutierrez, E. M. Pietras, A. Shahangian, C. E. Gross, A. Thirumala, A. L. Cheung, G. Cheng, and R. L. Modlin. 2006. MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 24: 79-91.
49. Miller, L. S., E. M. Pietras, L. H. Uricchio, K. Hirano, S. Rao, H. Lin, R. M. O'Connell, Y. Iwakura, A. L. Cheung, G. Cheng, and R. L. Modlin. 2007. Inflammasome-mediated production of IL-1β is required for neutrophil recruitment against Staphylococcus aureus in vivo. J. Immunol. 179: 6933-6942.
50. Alonzo, F., III, and V. J. Torres. 2013. Bacterial survival amidst an immune onslaught: the contribution of the Staphylococcus aureus leukotoxins. PLoS Pathog. 9: e1003143.
51. Surewaard, B. G., C. J. de Haas, F. Vervoort, K. M. Rigby, F. R. DeLeo, M. Otto, J. A. van Strijp, and R. Nijland. 2013. Staphylococcal a-phenol soluble modulins contribute to neutrophil lysis after phagocytosis. Cell. Microbiol. 15: 1427-1437.
52. Henson, P. M., and R. B. Johnston, Jr. 1987. Tissue injury in inflammation: oxidants, proteinases, and cationic proteins. J. Clin. Invest. 79: 669-674.
53. Raucci, A., R. Palumbo, and M. E. Bianchi. 2007. HMGB1: a signal of necrosis. Autoimmunity 40: 285-289.
54. Sheedy, F. J., A. Grebe, K. J. Rayner, P. Kalantari, B. Ramkhelawon, S. B. Carpenter, C. E. Becker, H. N. Ediriweera, A. E. Mullick, D. T. Golenbock, et al. 2013. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat. Immunol. 14: 812-820.
55. Stewart, C. R., L. M. Stuart, K. Wilkinson, J. M. van Gils, J. Deng, A. Halle, K. J. Rayner, L. Boyer, R. Zhong, W. A. Frazier, et al. 2010. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11: 155-161.
56. Grange, P. A., C. Chéreau, J. Raingeaud, C. Nicco, B. Weill, N. Dupin, and F. Batteux. 2009. Production of superoxide anions by keratinocytes initiates P. acnes-induced inflammation of the skin. PLoS Pathog. 5: e1000527.
57. Sharif, O., U. Matt, S. Saluzzo, K. Lakovits, I. Haslinger, T. Furtner, B. Doninger, and S. Knapp. 2013. The scavenger receptor CD36 downmodulates the early inflammatory response while enhancing bacterial phagocytosis during pneumococcal pneumonia. J. Immunol. 190: 5640-5648.