Phagocytosis of staphylococcus aureus by human neutrophils prevents macrophage efferocytosis and induces programmed necrosis

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4709-4717

  Greenlee Wacker, Mallary C ^a   Rigby, Kevin M ^b   Kobayashi, Scott D ^c   Porter, Adeline R ^c   DeLeo, Frank R ^c   Nauseef, William M ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; CRYOPYRIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; PHOSPHATIDYLSERINE; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BINDING AFFINITY; CELL MEMBRANE DEPOLARIZATION; CELL PROLIFERATION; COMMUNITY ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MACROPHAGE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MITOCHONDRIAL MEMBRANE; NECROPTOSIS; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STAPHYLOCOCCUS AUREUS;

ANTIGENS, CD47; APOPTOSIS; CASPASE 1; COCULTURE TECHNIQUES; FEMALE; HUMANS; INTERLEUKIN-1BETA; MACROPHAGES; MALE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; NECROSIS; NEUTROPHILS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901253655     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302692     Document Type: Article

References (41)

1. DeLeo, F. R., M. Otto, B. N. Kreiswirth, and H. F. Chambers. 2010. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
2. Rigby, K. M., and F. R. DeLeo. 2012. Neutrophils in innate host defense against Staphylococcus aureus infections. Semin. Immunopathol. 34: 237-259.
3. Nauseef, W. M. 2007. How human neutrophils kill and degrade microbes: an integrated view. Immunol. Rev. 219: 88-102.
4. Klebanoff, S. J., A. J. Kettle, H. Rosen, C. C. Winterbourn, and W. M. Nauseef. 2013. Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J. Leukoc. Biol. 93: 185-198.
5. Voyich, J. M., K. R. Braughton, D. E. Sturdevant, A. R. Whitney, B. Saïd-Salim, S. F. Porcella, R. D. Long, D. W. Dorward, D. J. Gardner, B. N. Kreiswirth, et al. 2005. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175: 3907-3919.
6. Rogers, D. E., and R. Tompsett. 1952. The survival of staphylococci within human leukocytes. J. Exp. Med. 95: 209-230.
7. Kobayashi, S. D., K. R. Braughton, A. M. Palazzolo-Ballance, A. D. Kennedy, E. Sampaio, E. Kristosturyan, A. R. Whitney, D. E. Sturdevant, D. W. Dorward, S. M. Holland, et al. 2010. Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus. J. Innate Immun. 2: 560-575.
8. Boles, B. R., M. Thoendel, A. J. Roth, and A. R. Horswill. 2010. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS ONE 5: e10146.
9. Pang, Y. Y., J. Schwartz, M. Thoendel, L. W. Ackermann, A. R. Horswill, and W. M. Nauseef. 2010. agr-Dependent interactions of Staphylococcus aureus USA300 with human polymorphonuclear neutrophils. J. Innate Immun. 2: 546-559.
10. Nauseef, W. M. 2007. Isolation of human neutrophils from venous blood. Methods Mol. Biol. 412: 15-20.
11. Decleva, E., R. Menegazzi, S. Busetto, P. Patriarca, and P. Dri. 2006. Common methodology is inadequate for studies on the microbicidal activity of neutrophils. J. Leukoc. Biol. 79: 87-94.
12. Schwartz, J., K. G. Leidal, J. K. Femling, J. P. Weiss, and W. M. Nauseef. 2009. Neutrophil bleaching of GFP-expressing staphylococci: probing the intraphagosomal fate of individual bacteria. J. Immunol. 183: 2632-2641.
13. Lillis, A. P., M. C. Greenlee, I. Mikhailenko, S. V. Pizzo, A. J. Tenner, D. K. Strickland, and S. S. Bohlson. 2008. Murine low-density lipoprotein receptor-related protein 1 (LRP) is required for phagocytosis of targets bearing LRP ligands but is not required for C1q-triggered enhancement of phagocytosis. J. Immunol. 181: 364-373.
14. Schulert, G. S., and L. A. Allen. 2006. Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J. Leukoc. Biol. 80: 563-571.
15. Andrew, S. M., and J. A. Titus. 2003. Fragmentation of immunoglobulin G. Curr. Protoc. Cell Biol. Chapter 16: Unit 16.14.
16. Schwartz, J. T., J. H. Barker, J. Kaufman, D. C. Fayram, J. M. McCracken, and L. A. Allen. 2012. Francisella tularensis inhibits the intrinsic and extrinsic pathways to delay constitutive apoptosis and prolong human neutrophil lifespan. J. Immunol. 188: 3351-3363.
17. Gardai, S. J., K. A. McPhillips, S. C. Frasch, W. J. Janssen, A. Starefeldt, J. E. Murphy-Ullrich, D. L. Bratton, P. A. Oldenborg, M. Michalak, and P. M. Henson. 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334.
18. Gardai, S. J., Y. Q. Xiao, M. Dickinson, J. A. Nick, D. R. Voelker, K. E. Greene, and P. M. Henson. 2003. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115: 13-23.
19. Fadok, V. A., D. L. Bratton, A. Konowal, P. W. Freed, J. Y. Westcott, and P. M. Henson. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101: 890-898.
20. Krishna, S., and L. S. Miller. 2012. Host-pathogen interactions between the skin and Staphylococcus aureus. Curr. Opin. Microbiol. 15: 28-35.
21. Sutterwala, F. S., Y. Ogura, and R. A. Flavell. 2007. The inflammasome in pathogen recognition and inflammation. J. Leukoc. Biol. 82: 259-264.
22. 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.
23. Ventura, C. L., N. Malachowa, C. H. Hammer, G. A. Nardone, M. A. Robinson, S. D. Kobayashi, and F. R. DeLeo. 2010. Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE 5: e11634.
24. Witko-Sarsat, V., J. Mocek, D. Bouayad, N. Tamassia, J. A. Ribeil, C. Candalh, N. Davezac, N. Reuter, L. Mouthon, O. Hermine, et al. 2010. Proliferating cell nuclear antigen acts as a cytoplasmic platform controlling human neutrophil survival. J. Exp. Med. 207: 2631-2645.
25. Watson, R. W., A. O'Neill, A. E. Brannigan, R. Coffey, J. C. Marshall, H. R. Brady, and J. M. Fitzpatrick. 1999. Regulation of Fas antibody induced neutrophil apoptosis is both caspase and mitochondrial dependent. FEBS Lett. 453: 67-71.
26. [Published erratum appears in 2006 FEBS Lett. 580: 996.]
27. He, S., L. Wang, L. Miao, T. Wang, F. Du, L. Zhao, and X. Wang. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNFalpha. Cell 137: 1100-1111.
28. Kaczmarek, A., P. Vandenabeele, and D. V. Krysko. 2013. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38: 209-223.
29. DeLeo, F. R., and H. F. Chambers. 2009. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 119: 2464-2474.
30. Gresham, H. D., J. H. Lowrance, T. E. Caver, B. S. Wilson, A. L. Cheung, and F. P. Lindberg. 2000. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J. Immunol. 164: 3713-3722.
31. Rogers, D. E. 1956. Studies on bacteriemia. I. Mechanisms relating to the persistence of bacteriemia in rabbits following the intravenous injection of staphylococci. J. Exp. Med. 103: 713-742.
32. Brown, S., I. Heinisch, E. Ross, K. Shaw, C. D. Buckley, and J. Savill. 2002. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 418: 200-203.
33. Park, Y. J., G. Liu, Y. Tsuruta, E. Lorne, and E. Abraham. 2009. Participation of the urokinase receptor in neutrophil efferocytosis. Blood 114: 860-870.
34. Park, Y. J., G. Liu, E. F. Lorne, X. Zhao, J. Wang, Y. Tsuruta, J. Zmijewski, and E. Abraham. 2008. PAI-1 inhibits neutrophil efferocytosis. Proc. Natl. Acad. Sci. USA 105: 11784-11789.
35. Hammond, M. E., G. R. Lapointe, P. H. Feucht, S. Hilt, C. A. Gallegos, C. A. Gordon, M. A. Giedlin, G. Mullenbach, and P. Tekamp-Olson. 1995. IL-8 induces neutrophil chemotaxis predominantly via type I IL-8 receptors. J. Immunol. 155: 1428-1433.
36. 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.
37. 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-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J. Immunol. 179: 6933-6942.
38. 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-1b is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog. 8: e1003047.
39. Feoktistova, M., P. Geserick, D. Panayotova-Dimitrova, and M. Leverkus. 2012. Pick your poison: the Ripoptosome, a cell death platform regulating apoptosis and necroptosis. Cell Cycle 11: 460-467.
40. Vandenabeele, P., W. Declercq, F. Van Herreweghe, and T. Vanden Berghe. 2010. The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal. 3: re4.
41. Long, J. S., and K. M. Ryan. 2012. New frontiers in promoting tumour cell death: targeting apoptosis, necroptosis and autophagy. Oncogene 31: 5045-5060.