A major role for myeloid-derived suppressor cells and a minor role for regulatory T cells in immunosuppression during Staphylococcus aureus infection

Journal of Immunology

Volumn 194, Issue 3, 2015, Pages 1100-1111

  Tebartz, Christina ^a   Horst, Sarah Anita ^a   Sparwasser, Tim ^b   Huehn, Jochen ^a   Beineke, Andreas ^c   Peters, Georg ^d   Medina, Eva ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL ASSAY; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MOLECULAR DYNAMICS; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPLEEN CELL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; SUPPRESSOR CELL; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; BONE MARROW CELL; CELL COMMUNICATION; COCULTURE; CYTOLOGY; DENDRITIC CELL; DISEASE MODEL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOPHENOTYPING; METABOLISM; PHENOTYPE; SEVERITY OF ILLNESS INDEX; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; B-LYMPHOCYTES, REGULATORY; CELL COMMUNICATION; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNE TOLERANCE; IMMUNOMODULATION; IMMUNOPHENOTYPING; MICE; MICE, TRANSGENIC; MYELOID CELLS; PHENOTYPE; SEVERITY OF ILLNESS INDEX; SPLEEN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84921451497     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400196     Document Type: Article

References (60)

1. Chambers, H. F., and F. R. Deleo. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7: 629-641.
2. Peacock, S. J., I. de Silva, and F. D. Lowy. 2001. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol. 9: 605-610.
3. Foster, T. J. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3: 948-958.
4. Kim, H. K., V. Thammavongsa, O. Schneewind, and D. Missiakas. 2012. Recurrent infections and immune evasion strategies of Staphylococcus aureus. Curr. Opin. Microbiol. 15: 92-99.
5. Fedtke, I., F. Götz, and A. Peschel. 2004. Bacterial evasion of innate host defenses - the Staphylococcus aureus lesson. Int. J. Med. Microbiol. 294: 189-194.
6. Rooijakkers, S. H., K. P. van Kessel, and J. A. van Strijp. 2005. Staphylococcal innate immune evasion. Trends Microbiol. 13: 596-601.
7. Kappler, J., B. Kotzin, L. Herron, E. W. Gelfand, R. D. Bigler, A. Boylston, S. Carrel, D. N. Posnett, Y. Choi, and P. Marrack. 1989. V beta-specific stimulation of human T cells by staphylococcal toxins. Science 244: 811-813.
8. Watson, A. R., J. N. Mittler, and W. T. Lee. 2003. Staphylococcal enterotoxin B induces anergy to conventional peptide in memory T cells. Cell. Immunol. 222: 144-155.
9. Silverman, G. J., S. P. Cary, D. C. Dwyer, L. Luo, R. Wagenknecht, and V. E. Curtiss. 2000. A B cell superantigen-induced persistent "Hole" in the B-1 repertoire. J. Exp. Med. 192: 87-98.
10. Lee, L. Y., Y. J. Miyamoto, B. W. McIntyre, M. Höök, K. W. McCrea, D. McDevitt, and E. L. Brown. 2002. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J. Clin. Invest. 110: 1461-1471.
11. Sendi, P., and R. A. Proctor. 2009. Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol. 17: 54-58.
12. Tuchscherr, L., E. Medina, M. Hussain, W. Völker, V. Heitmann, S. Niemann, D. Holzinger, J. Roth, R. A. Proctor, K. Becker, et al. 2011. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 3: 129-141.
13. Ziegler, C., O. Goldmann, E. Hobeika, R. Geffers, G. Peters, and E. Medina. 2011. The dynamics of T cells during persistent Staphylococcus aureus infection: from antigen-reactivity to in vivo anergy. EMBO Mol. Med. 3: 652-666.
14. Belkaid, Y. 2007. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7: 875-888.
15. Majlessi, L., R. Lo-Man, and C. Leclerc. 2008. Regulatory B and T cells in infections. Microbes Infect. 10: 1030-1035.
16. Mauri, C., and M. R. Ehrenstein. 2008. The 'short' history of regulatory B cells. Trends Immunol. 29: 34-40.
17. Torres-Aguilar, H., S. R. Aguilar-Ruiz, G. González-Pérez, R. Munguía, S. Bajaña, M. A. Meraz-Ríos, and C. Sánchez-Torres. 2010. Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J. Immunol. 184: 1765-1775.
18. Gabrilovich, D. I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9: 162-174.
19. Condamine, T., and D. I. Gabrilovich. 2011. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 32: 19-25.
20. Iwashiro, M., R. J. Messer, K. E. Peterson, I. M. Stromnes, T. Sugie, and K. J. Hasenkrug. 2001. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc. Natl. Acad. Sci. USA 98: 9226-9230.
21. Suvas, S., U. Kumaraguru, C. D. Pack, S. Lee, and B. T. Rouse. 2003. CD4 +CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J. Exp. Med. 198: 889-901.
22. Zelinskyy, G., K. Dietze, T. Sparwasser, and U. Dittmer. 2009. Regulatory T cells suppress antiviral immune responses and increase viral loads during acute infection with a lymphotropic retrovirus. PLoS Pathog. 5: e1000406.
23. Belkaid, Y., C. A. Piccirillo, S. Mendez, E. M. Shevach, and D. L. Sacks. 2002. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
24. Kursar, M., M. Koch, H. W. Mittrücker, G. Nouailles, K. Bonhagen, T. Kamradt, and S. H. Kaufmann. 2007. Cutting Edge: Regulatory T cells prevent efficient clearance of Mycobacterium tuberculosis. J. Immunol. 178: 2661-2665.
25. Oertli, M., and A. Müller. 2012. Helicobacter pylori targets dendritic cells to induce immune tolerance, promote persistence and confer protection against allergic asthma. Gut Microbes 3: 566-571.
26. Horikawa, M., E. T. Weimer, D. J. DiLillo, G. M. Venturi, R. Spolski, W. J. Leonard, M. T. Heise, and T. F. Tedder. 2013. Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice. J. Immunol. 190: 1158-1168.
27. Rieber, N., A. Brand, A. Hector, U. Graepler-Mainka, M. Ost, I. Schäfer, I. Wecker, D. Neri, A. Wirth, L. Mays, et al. 2013. Flagellin induces myeloidderived suppressor cells: implications for Pseudomonas aeruginosa infection in cystic fibrosis lung disease. J. Immunol. 190: 1276-1284.
28. Hisaeda, H., Y. Maekawa, D. Iwakawa, H. Okada, K. Himeno, K. Kishihara, S. Tsukumo, and K. Yasutomo. 2004. Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat. Med. 10: 29-30.
29. Taylor, M. D., A. Harris, S. A. Babayan, O. Bain, A. Culshaw, J. E. Allen, and R. M. Maizels. 2007. CTLA-4 and CD4+ CD25+ regulatory T cells inhibit protective immunity to filarial parasites in vivo. J. Immunol. 179: 4626-4634.
30. Jonsson, I. M., S. Arvidson, S. Foster, and A. Tarkowski. 2004. Sigma factor B and RsbU are required for virulence in Staphylococcus aureus-induced arthritis and sepsis. Infect. Immun. 72: 6106-6111.
31. Vann, J. M., and R. A. Proctor. 1987. Ingestion of Staphylococcus aureus by bovine endothelial cells results in time- and inoculum-dependent damage to endothelial cell monolayers. Infect. Immun. 55: 2155-2163.
32. Fontenot, J. D., J. P. Rasmussen, L. M. Williams, J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22: 329-341.
33. Lahl, K., C. Loddenkemper, C. Drouin, J. Freyer, J. Arnason, G. Eberl, A. Hamann, H. Wagner, J. Huehn, and T. Sparwasser. 2007. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 204: 57-63.
34. Horst, S. A., V. Hoerr, A. Beineke, C. Kreis, L. Tuchscherr, J. Kalinka, S. Lehne, I. Schleicher, G. Köhler, T. Fuchs, et al. 2012. A novel mouse model of Staphylococcus aureus chronic osteomyelitis that closely mimics the human infection: an integrated view of disease pathogenesis. Am. J. Pathol. 181: 1206-1214.
35. Taga, K., H. Mostowski, and G. Tosato. 1993. Human interleukin-10 can directly inhibit T-cell growth. Blood 81: 2964-2971.
36. Letterio, J. J., and A. B. Roberts. 1998. Regulation of immune responses by TGF-beta. Annu. Rev. Immunol. 16: 137-161.
37. Sakaguchi, S. 2005. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6: 345-352.
38. + phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650.
39. Mauri, C., and A. Bosma. 2012. Immune regulatory function of B cells. Annu. Rev. Immunol. 30: 221-241.
40. Schreiner, J., D. Kretschmer, J. Klenk, M. Otto, H. J. Bühring, S. Stevanovic, J. M. Wang, S. Beer-Hammer, A. Peschel, and S. E. Autenrieth. 2013. Staphylococcus aureus phenol-soluble modulin peptides modulate dendritic cell functions and increase in vitro priming of regulatory T cells. J. Immunol. 190: 3417-3426.
41. Youn, J. I., S. Nagaraj, M. Collazo, and D. I. Gabrilovich. 2008. Subsets of myeloidderived suppressor cells in tumor-bearing mice. J. Immunol. 181: 5791-5802.
42. Suzuki, E., V. Kapoor, A. S. Jassar, L. R. Kaiser, and S. M. Albelda. 2005. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11: 6713-6721.
43. Le, H. K., L. Graham, E. Cha, J. K. Morales, M. H. Manjili, and H. D. Bear. 2009. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int. Immunopharmacol. 9: 900-909.
44. Heim, C. E., D. Vidlak, T. D. Scherr, J. A. Kozel, M. Holzapfel, D. E. Muirhead, and T. Kielian. 2014. Myeloid-derived suppressor cells contribute to Staphylococcus aureus orthopedic biofilm infection. J. Immunol. 192: 3778-3792.
45. Goh, C., S. Narayanan, and Y. S. Hahn. 2013. Myeloid-derived suppressor cells: the dark knight or the joker in viral infections? Immunol. Rev. 255: 210-221.
46. du Plessis, N., L. Loebenberg, M. Kriel, F. von Groote-Bidlingmaier, E. Ribechini, A. G. Loxton, P. D. van Helden, M. B. Lutz, and G. Walzl. 2013. Increased frequency of myeloid-derived suppressor cells during active tuberculosis and after recent mycobacterium tuberculosis infection suppresses T-cell function. Am. J. Respir. Crit. Care Med. 188: 724-732.
47. Goñi, O., P. Alcaide, and M. Fresno. 2002. Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+)immature myeloid suppressor cells. Int. Immunol. 14: 1125-1134.
48. Voisin, M. B., D. Buzoni-Gatel, D. Bout, and F. Velge-Roussel. 2004. Both expansion of regulatory GR1+ CD11b+ myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect. Immun. 72: 5487-5492.
49. Terrazas, L. I., K. L. Walsh, D. Piskorska, E. McGuire, and D. A. Harn, Jr. 2001. The schistosome oligosaccharide lacto-N-neotetraose expands Gr1(+) cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4(+) cells: a potential mechanism for immune polarization in helminth infections. J. Immunol. 167: 5294-5303.
50. Brys, L., A. Beschin, G. Raes, G. H. Ghassabeh, W. Noël, J. Brandt, F. Brombacher, and P. De Baetselier. 2005. Reactive oxygen species and 12/15-lipoxygenase contribute to the antiproliferative capacity of alternatively activated myeloid cells elicited during helminth infection. J. Immunol. 174: 6095-6104.
51. Mencacci, A., C. Montagnoli, A. Bacci, E. Cenci, L. Pitzurra, A. Spreca, M. Kopf, A. H. Sharpe, and L. Romani. 2002. CD80+Gr-1+ myeloid cells inhibit development of antifungal Th1 immunity in mice with candidiasis. J. Immunol. 169: 3180-3190.
52. Youn, J. I., and D. I. Gabrilovich. 2010. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur. J. Immunol. 40: 2969-2975.
53. Mundy-Bosse, B. L., G. B. Lesinski, A. C. Jaime-Ramirez, K. Benninger, M. Khan, P. Kuppusamy, K. Guenterberg, S. V. Kondadasula, A. R. Chaudhury, K. M. La Perle, et al. 2011. Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res. 71: 5101-5110.
54. Li, H., Y. Han, Q. Guo, M. Zhang, and X. Cao. 2009. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J. Immunol. 182: 240-249.
55. Ribechini, E., P. J. Leenen, and M. B. Lutz. 2009. Gr-1 antibody induces STAT signaling, macrophage marker expression and abrogation of myeloid-derived suppressor cell activity in BM cells. Eur. J. Immunol. 39: 3538-3551.
56. Ma, C., T. Kapanadze, J. Gamrekelashvili, M. P. Manns, F. Korangy, and T. F. Greten. 2012. Anti-Gr-1 antibody depletion fails to eliminate hepatic myeloid-derived suppressor cells in tumor-bearing mice. J. Leukoc. Biol. 92: 1199-1206.
57. Talmadge, J. E., and D. I. Gabrilovich. 2013. History of myeloid-derived suppressor cells. Nat. Rev. Cancer 13: 739-752.
58. Kusmartsev, S., Y. Nefedova, D. Yoder, and D. I. Gabrilovich. 2004. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172: 989-999.
59. Mazzoni, A., V. Bronte, A. Visintin, J. H. Spitzer, E. Apolloni, P. Serafini, P. Zanovello, and D. M. Segal. 2002. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 168: 689-695.
60. Schmielau, J., and O. J. Finn. 2001. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res. 61: 4756-4760.