Recruited macrophages control dissemination of group A Streptococcus from infected soft tissues

Journal of Immunology

Volumn 187, Issue 11, 2011, Pages 6022-6031

  Mishalian, Inbal ^a   Ordan, Merav ^a   Peled, Amnon ^b   Maly, Alexander ^b   Eichenbaum, Miriam B ^c   Ravins, Miriam ^a   Aychek, Tegest ^d   Jung, Steffen ^d   Hanski, Emanuel ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CELL INTERACTION; CONTROLLED STUDY; GROUP A STREPTOCOCCAL INFECTION; INFECTION CONTROL; INFECTION SENSITIVITY; MACROPHAGE FUNCTION; MACROPHAGE MIGRATION; MICROBIAL ACTIVITY; MONOCYTE; MOUSE; NECROTIZING FASCIITIS; NEUTROPHIL COUNT; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN DEPLETION; STREPTOCOCCUS GROUP A;

ANIMALS; CELL SEPARATION; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FASCIITIS, NECROTIZING; FLOW CYTOMETRY; MACROPHAGES; MICE; MICE, INBRED C57BL; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

EID: 82755189237     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101385     Document Type: Article

References (48)

1. Carapetis, J. R., A. C. Steer, E. K. Mulholland, and M. Weber. 2005. The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5: 685-694. (Pubitemid 41505357)
2. O'Loughlin, R. E., A. Roberson, P. R. Cieslak, R. Lynfield, K. Gershman, A. Craig, B. A. Albanese, M. M. Farley, N. L. Barrett, N. L. Spina, et al. Active Bacterial Core Surveillance Team. 2007. The epidemiology of invasive group A streptococcal infection and potential vaccine implications: United States, 2000- 2004. Clin. Infect. Dis. 45: 853-862. (Pubitemid 47580376)
3. Wong, C. H., A. K. Yam, A. B. Tan, and C. Song. 2008. Approach to debridement in necrotizing fasciitis. Am. J. Surg. 196: e19-e24.
4. Sharkawy, A., D. E. Low, R. Saginur, D. Gregson, B. Schwartz, P. Jessamine, K. Green, A. McGeer; Ontario Group A Streptococcal Study Group. 2002. Severe group a streptococcal soft-tissue infections in Ontario: 1992-1996. Clin. Infect. Dis. 34: 454-460. (Pubitemid 34112265)
5. Nestle, F. O., P. Di Meglio, J. Z. Qin, and B. J. Nickoloff. 2009. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 9: 679-691.
6. Medzhitov, R., and C. Janeway, Jr. 2000. Innate immunity. N. Engl. J. Med. 343: 338-344.
7. Aggarwal, B. B. 2003. Signalling pathways of the TNF superfamily: a doubleedged sword. Nat. Rev. Immunol. 3: 745-756. (Pubitemid 41070815)
8. Brinkmann, V., U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D. S. Weiss, Y. Weinrauch, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535. (Pubitemid 38314426)
9. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182. (Pubitemid 43290987)
10. Segal, A.W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23: 197-223. (Pubitemid 40563169)
11. Mishalian, I., M. Ravins, M. Baruch, M. Persky, I. Belotserkovsky, and E. Hanski. 2010. Host-pathogen relationship in skin and soft-tissue infections caused by group A Streptococcus and Staphylococcus aureus. In Bacterial Virulence: Basic principles, Models and Global Approaches. P. Sansonetti, ed. Wiley-VCH, Weinheim, Germany. DOI: 10.1002/9783527629664.ch4.
12. Nizet, V. 2007. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120: 13-22. (Pubitemid 46990514)
13. Olsen, R. J., and J. M. Musser. 2010. Molecular pathogenesis of necrotizing fasciitis. Annu. Rev. Pathol. 5: 1-31.
14. Voyich, J. M., J. M. Musser, and F. R. DeLeo. 2004. Streptococcus pyogenes and human neutrophils: a paradigm for evasion of innate host defense by bacterial pathogens. Microbes Infect. 6: 1117-1123. (Pubitemid 39233684)
15. Thulin, P., L. Johansson, D. E. Low, B. S. Gan, M. Kotb, A. McGeer, and A. Norrby-Teglund. 2006. Viable group A streptococci in macrophages during acute soft tissue infection. PLoS Med. 3: e53.
16. Goldmann, O., M. Rohde, G. S. Chhatwal, and E. Medina. 2004. Role of macrophages in host resistance to group A streptococci. Infect. Immun. 72: 2956-2963. (Pubitemid 38542426)
17. Auffray, C., M. H. Sieweke, and F. Geissmann. 2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27: 669-692.
18. Serbina, N. V., T. Jia, T. M. Hohl, and E. G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26: 421-452. (Pubitemid 351600381)
19. Geissmann, F., M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, and K. Ley. 2010. Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661.
20. Yona, S., and S. Jung. 2010. Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17: 53-59.
21. Hidalgo-Grass, C., M. Ravins, M. Dan-Goor, J. Jaffe, A. E. Moses, and E. Hanski. 2002. A locus of group A Streptococcus involved in invasive disease and DNA transfer. Mol. Microbiol. 46: 87-99. (Pubitemid 35231949)
22. Aziz, R. K., M. J. Pabst, A. Jeng, R. Kansal, D. E. Low, V. Nizet, and M. Kotb. 2004. Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol. Microbiol. 51: 123-134. (Pubitemid 38031076)
23. Hohl, T. M., A. Rivera, L. Lipuma, A. Gallegos, C. Shi, M. Mack, and E. G. Pamer. 2009. Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6: 470-481.
24. Hidalgo-Grass, C., M. Dan-Goor, A. Maly, Y. Eran, L. A. Kwinn, V. Nizet, M. Ravins, J. Jaffe, A. Peyser, A. E. Moses, and E. Hanski. 2004. Effect of a bacterial pheromone peptide on host chemokine degradation in group A streptococcal necrotising soft-tissue infections. Lancet 363: 696-703. (Pubitemid 38296556)
25. Hidalgo-Grass, C., I. Mishalian, M. Dan-Goor, I. Belotserkovsky, Y. Eran, V. Nizet, A. Peled, and E. Hanski. 2006. A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues. EMBO J. 25: 4628-4637. (Pubitemid 44498135)
26. Kumagai, K., K. Itoh, S. Hinuma, and M. Tada. 1979. Pretreatment of plastic Petri dishes with fetal calf serum. A simple method for macrophage isolation. J. Immunol. Methods 29: 17-25. (Pubitemid 9244611)
27. Fournier, B., and D. J. Philpott. 2005. Recognition of Staphylococcus aureus by the innate immune system. Clin. Microbiol. Rev. 18: 521-540. (Pubitemid 40995114)
28. 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. (Pubitemid 43077202)
29. Ashbaugh, C. D., H. B. Warren, V. J. Carey, and M. R. Wessels. 1998. Molecular analysis of the role of the group A streptococcal cysteine protease, hyaluronic acid capsule, and M protein in a murine model of human invasive soft-tissue infection. J. Clin. Invest. 102: 550-560. (Pubitemid 28376158)
30. Walker, M. J., A. Hollands, M. L. Sanderson-Smith, J. N. Cole, J. K. Kirk, A. Henningham, J. D. McArthur, K. Dinkla, R. K. Aziz, R. G. Kansal, et al. 2007. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat. Med. 13: 981-985. (Pubitemid 47222039)
31. Chan, A. T., V. Cleeve, and T. J. Daymond. 2002. Necrotising fasciitis in a patient receiving infliximab for rheumatoid arthritis. Postgrad. Med. J. 78: 47-48. (Pubitemid 34074917)
32. Choi, K. H., and W. H. Yoo. 2009. Necrotizing fasciitis in a patient treated with etanercept for dermatomyositis. Rheumatol. Int. 29: 463-466.
33. Goldmann, O., S. Lehne, and E. Medina. 2010. Age-related susceptibility to Streptococcus pyogenes infection in mice: underlying immune dysfunction and strategy to enhance immunity. J. Pathol. 220: 521-529.
34. Medina, E., and A. Lengeling. 2005. Genetic regulation of host responses to group A streptococcus in mice. Brief. Funct. Genomics Proteomics 4: 248-257. (Pubitemid 43055806)
35. Sedgwick, J. D., D. S. Riminton, J. G. Cyster, and H. Körner. 2000. Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol. Today 21: 110-113. (Pubitemid 30122696)
36. Imai, T., K. Hieshima, C. Haskell, M. Baba, M. Nagira, M. Nishimura, M. Kakizaki, S. Takagi, H. Nomiyama, T. J. Schall, and O. Yoshie. 1997. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 91: 521-530. (Pubitemid 27508241)
37. Paludan, S. R. 2000. Synergistic action of pro-inflammatory agents: cellular and molecular aspects. J. Leukoc. Biol. 67: 18-25. (Pubitemid 30046813)
38. Tessier, P. A., P. H. Naccache, I. Clark-Lewis, R. P. Gladue, K. S. Neote, and S. R. McColl. 1997. Chemokine networks in vivo: involvement of C-X-C and CC chemokines in neutrophil extravasation in vivo in response to TNF-alpha. J. Immunol. 159: 3595-3602. (Pubitemid 127482119)
39. Casola, A., A. Henderson, T. Liu, R. P. Garofalo, and A. R. Brasier. 2002. Regulation of RANTES promoter activation in alveolar epithelial cells after cytokine stimulation. Am. J. Physiol. Lung Cell. Mol. Physiol. 283: L1280-L1290. (Pubitemid 35385615)
40. Stratis, A., M. Pasparakis, R. A. Rupec, D. Markur, K. Hartmann, K. Scharffetter-Kochanek, T. Peters, N. van Rooijen, T. Krieg, and I. Haase. 2006. Pathogenic role for skin macrophages in a mouse model of keratinocyteinduced psoriasis-like skin inflammation. J. Clin. Invest. 116: 2094-2104. (Pubitemid 44162318)
41. van Rooijen, N., J. Bakker, and A. Sanders. 1997. Transient suppression of macrophage functions by liposome-encapsulated drugs. Trends Biotechnol. 15: 178-185. (Pubitemid 27219576)
42. van Rooijen, N., and E. Hendrikx. 2010. Liposomes for specific depletion of macrophages from organs and tissues. Methods Mol. Biol. 605: 189-203.
43. Buchanan, J. T., A. J. Simpson, R. K. Aziz, G. Y. Liu, S. A. Kristian, M. Kotb, J. Feramisco, and V. Nizet. 2006. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16: 396-400. (Pubitemid 43259350)
44. Zinkernagel, A. S., A. M. Timmer, M. A. Pence, J. B. Locke, J. T. Buchanan, C. E. Turner, I. Mishalian, S. Sriskandan, E. Hanski, and V. Nizet. 2008. The IL- 8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell Host Microbe 4: 170-178.
45. Serbina, N. V., and E. G. Pamer. 2006. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7: 311-317.
46. Montecucco, F., S. Steffens, F. Burger, A. Da Costa, G. Bianchi, M. Bertolotto, F. Mach, F. Dallegri, and L. Ottonello. 2008. Tumor necrosis factor-alpha (TNFalpha) induces integrin CD11b/CD18 (Mac-1) up-regulation and migration to the CC chemokine CCL3 (MIP-1alpha) on human neutrophils through defined signalling pathways. Cell. Signal. 20: 557-568.
47. Takahashi, H., T. Tashiro, M. Miyazaki, M. Kobayashi, R. B. Pollard, and F. Suzuki. 2002. An essential role of macrophage inflammatory protein 1alpha/ CCL3 on the expression of host's innate immunities against infectious complications. J. Leukoc. Biol. 72: 1190-1197. (Pubitemid 36008890)
48. Loof, T. G., O. Goldmann, A. Gessner, H. Herwald, and E. Medina. 2010. Aberrant inflammatory response to Streptococcus pyogenes in mice lacking myeloid differentiation factor 88. Am. J. Pathol. 176: 754-763.