Interleukin-10 production by myeloid-derived suppressor cells contributes to bacterial persistence during staphylococcus aureus orthopedic biofilm infection

Journal of Leukocyte Biology

Volumn 98, Issue 6, 2015, Pages 1003-1013

  Heim, Cortney E ^a   Vidlak, Debbie ^a   Kielian, Tammy ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

IL 10; Macrophage; MDSC

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GREEN FLUORESCENT PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 9; PROTEIN; PROTEIN ARG 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IL10 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BIOFILM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEVICE INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMUR; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; KIRSCHNER WIRE; KNEE; KNOCKOUT MOUSE; MACROPHAGE; MALE; MONOCYTE; MOUSE; MOUSE MODEL; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; ORTHOPEDIC IMPLANT BIOFILM INFECTION; PRIORITY JOURNAL; SOFT TISSUE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; ANIMAL; BONE MARROW CELL; IMMUNOLOGY; KNEE ARTHROPLASTY; KNEE PROSTHESIS; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ARTHROPLASTY, REPLACEMENT, KNEE; BIOFILMS; INTERLEUKIN-10; KNEE PROSTHESIS; MALE; MICE; MICE, KNOCKOUT; MYELOID CELLS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84948951226     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4VMA0315-125RR     Document Type: Article

References (59)

1. Boucher, H., Miller, L. G., Razonable, R. R. (2010) Serious infections caused by methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 51 (Suppl 2), S183–S197.
2. Grundmann, H., Hellriegel, B. (2006) Mathematical modelling: a tool for hospital infection control. Lancet Infect. Dis. 6, 39–45.
3. Shorr, A. F. (2007) Epidemiology and economic impact of meticillinresistant Staphylococcus aureus: review and analysis of the literature. Pharmacoeconomics 25, 751–768.
4. Parry, M. C., Duncan, C. P. (2014) The challenge of methicillin resistant staphylococcal infection after total hip replacement: overlooked or overstated? Bone Joint J. 96-B(11:, Suppl A)60–65.
5. Otto, M. (2008) Staphylococcal biofilms. Curr. Top. Microbiol. Immunol. 322, 207–228.
6. Fitzsimmons, K., Bamber, A. I., Smalley, H. B. (2010) Infective endocarditis: changing aetiology of disease. Br. J. Biomed. Sci. 67, 35–41.
7. Del Pozo, J. L., Patel, R. (2009) Clinical practice. Infection associated with prosthetic joints. N. Engl. J. Med. 361, 787–794.
8. Zimmerli, W., Trampuz, A., Ochsner, P. E. (2004) Prosthetic-joint infections. N. Engl. J. Med. 351, 1645–1654.
9. Cho, J. S., Guo, Y., Ramos, R. I., Hebroni, F., Plaisier, S. B., Xuan, C., Granick, J. L., Matsushima, H., Takashima, A., Iwakura, Y., Cheung, A. L., Cheng, G., Lee, D. J., Simon, S. I., Miller, L. S. (2012) Neutrophil-derived IL-1b is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog. 8, e1003047.
10. Feuerstein, R., Seidl, M., Prinz, M., Henneke, P. (2015) MyD88 in macrophages is critical for abscess resolution in staphylococcal skin infection. J. Immunol. 194, 2735–2745.
11. Heim, C. E., Vidlak, D., Scherr, T. D., Kozel, J. A., Holzapfel, M., Muirhead, D. E., Kielian, T. (2014) Myeloid-derived suppressor cells contribute to Staphylococcus aureus orthopedic biofilm infection. J. Immunol. 192, 3778–3792.
12. Dai, J., El Gazzar, M., Li, G. Y., Moorman, J. P., Yao, Z. Q. (2015) Myeloidderived suppressor cells: paradoxical roles in infection and immunity. J. Innate Immun. 7, 116–126.
13. Gabrilovich, D. I., Nagaraj, S. (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162–174.
14. Sica, A., Bronte, V. (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 117, 1155–1166.
15. Youn, J. I., Collazo, M., Shalova, I. N., Biswas, S. K., Gabrilovich, D. I. (2012) Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J. Leukoc. Biol. 91, 167–181.
16. Brudecki, L., Ferguson, D. A., McCall, C. E., El Gazzar, M. (2012) Myeloid-derived suppressor cells evolve during sepsis and can enhance or attenuate the systemic inflammatory response. Infect. Immun. 80, 2026–2034.
17. Ostrand-Rosenberg, S., Sinha, P. (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182, 4499–4506.
18. Condamine, T., Gabrilovich, D. I. (2011) Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 32, 19–25.
19. Heim, C. E., Vidlak, D., Scherr, T. D., Hartman, C. W., Garvin, K. L., Kielian, T. (2015) IL-12 Promotes Myeloid-Derived Suppressor Cell Recruitment and Bacterial Persistence during Staphylococcus aureus orthopedic implant infection. J. Immunol. 194, 3861–3872.
20. Murray, P. J. (2005) The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. U. S. A. 102, 8686–8691.
21. Couper, K. N., Blount, D. G., Riley, E. M. (2008) IL-10: the master regulator of immunity to infection. J. Immunol. 180, 5771–5777.
22. Bunt, S. K., Clements, V. K., Hanson, E. M., Sinha, P., Ostrand-Rosenberg, S. (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J. Leukoc. Biol. 85, 996–1004.
23. Perrin, G. Q., Johnson, H. M., Subramaniam, P. S. (1999) Mechanism of interleukin-10 inhibition of T-helper cell activation by superantigen at the level of the cell cycle. Blood 93, 208–216.
24. Taga, K., Mostowski, H., Tosato, G. (1993) Human interleukin-10 can directly inhibit T-cell growth. Blood 81, 2964–2971.
25. Letterio, J. J., Roberts, A. B. (1998) Regulation of immune responses by TGF-b. Annu. Rev. Immunol. 16, 137–161.
26. Sinha, P., Clements, V. K., Bunt, S. K., Albelda, S. M., Ostrand-Rosenberg, S. (2007) Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179, 977–983.
27. Thurlow, L. R., Hanke, M. L., Fritz, T., Angle, A., Aldrich, A., Williams, S. H., Engebretsen, I. L., Bayles, K. W., Horswill, A. R., Kielian, T. (2011) Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol. 186, 6585–6596.
28. Bernthal, N. M., Stavrakis, A. I., Billi, F., Cho, J. S., Kremen, T. J., Simon, S. I., Cheung, A. L., Finerman, G. A., Lieberman, J. R., Adams, J. S., Miller, L. S. (2010) A mouse model of post-arthroplasty Staphylococcus aureus joint infection to evaluate in vivo the efficacy of antimicrobial implant coatings. PLoS One 5, e12580.
29. Waight, J. D., Hu, Q., Miller, A., Liu, S., Abrams, S. I. (2011) Tumorderived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism. PLoS One 6, e27690.
30. Sawanobori, Y., Ueha, S., Kurachi, M., Shimaoka, T., Talmadge, J. E., Abe, J., Shono, Y., Kitabatake, M., Kakimi, K., Mukaida, N., Matsushima, K. (2008) Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 111, 5457–5466.
31. Tebartz, C., Horst, S. A., Sparwasser, T., Huehn, J., Beineke, A., Peters, G., Medina, E. (2015) A major role for myeloid-derived suppressor cells and a minor role for regulatory T cells in immunosuppression during Staphylococcus aureus infection. J. Immunol. 194, 1100–1111.
32. Skabytska, Y., Wölbing, F., Günther, C., Köberle, M., Kaesler, S., Chen, K. M., Guenova, E., Demircioglu, D., Kempf, W. E., Volz, T., Rammensee, H. G., Schaller, M., Röcken, M., Götz, F., Biedermann, T. (2014) Cutaneous innate immune sensing of Toll-like receptor 2-6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. Immunity 41, 762–775.
33. Hanke, M. L., Heim, C. E., Angle, A., Sanderson, S. D., Kielian, T. (2013) Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections. J. Immunol. 190, 2159–2168.
34. Prabhakara, R., Harro, J. M., Leid, J. G., Keegan, A. D., Prior, M. L., Shirtliff, M. E. (2011) Suppression of the inflammatory immune response prevents the development of chronic biofilm infection due to methicillinresistant Staphylococcus aureus. Infect. Immun. 79, 5010–5018.
35. regs) and myeloid derived suppressor cells (MDSCs) during melanoma growth. Oncoimmunology 1, 1433–1434.
36. Corsetti, P. P., de Almeida, L. A., Carvalho, N. B., Azevedo, V., Silva, T. M., Teixeira, H. C., Faria, A. C., Oliveira, S. C. (2013) Lack of endogenous IL-10 enhances production of proinflammatory cytokines and leads to Brucella abortus clearance in mice. PLoS One 8, e74729.
37. Wang, J., Roderiquez, G., Norcross, M. A. (2012) Control of adaptive immune responses by Staphylococcus aureus through IL-10, PD-L1, and TLR 2. Sci. Rep. 2, 606.
38. Sasaki, H., Hou, L., Belani, A., Wang, C. Y., Uchiyama, T., Müller, R., Stashenko, P. (2000) IL-10, but not IL-4, suppresses infection-stimulated bone resorption in vivo. J. Immunol. 165, 3626–3630.
39. García-Alvarez, F., Monzón, M., Grasa, J. M., Laclériga, A., Amorena, B., García-Alvarez, I., Navarro-Zorraquino, M., Alvarez, F. G. (2006) Interleukin-1, interleukin-6, and interleukin-10 responses after antibiotic treatment in experimental chronic Staphylococcus aureus osteomyelitis. J. Orthop. Sci. 11, 370–374.
40. Gjertsson, I., Jonsson, I. M., Peschel, A., Tarkowski, A., Lindholm, C. (2012) Formylated peptides are important virulence factors in Staphylococcus aureus arthritis in mice. J. Infect. Dis. 205, 305–311.
41. Ritchlin, C., Haas-Smith, S. A. (2001) Expression of interleukin 10 mRNA and protein by synovial fibroblastoid cells. J. Rheumatol. 28, 698–705.
42. Redford, P. S., Murray, P. J., O’Garra, A. (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol. 4, 261–270.
43. Frodermann, V., Chau, T. A., Sayedyahossein, S., Toth, J. M., Heinrichs, D. E., Madrenas, J. (2011) A modulatory interleukin-10 response to staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. J. Infect. Dis. 204, 253–262.
44. Peres, A. G. and Madrenas, J. (2013) The broad landscape of immune interactions with Staphylococcus aureus: from commensalism to lethal infections. Burns 39, 380–388.
45. Ray, A., Chakraborty, K., Ray, P. (2013) Immunosuppressive MDSCs induced by TLR signaling during infection and role in resolution of inflammation. Front. Cell. Infect. Microbiol. 3, 52.
46. + population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 204, 1463–1474.
47. Nagaraj, S., Gabrilovich, D. I. (2007) Myeloid-derived suppressor cells. Adv. Exp. Med. Biol. 601, 213–223.
48. Maruyama, A., Shime, H., Takeda, Y., Azuma, M., Matsumoto, M., Seya, T. (2015) Pam2 lipopeptides systemically increase myeloid-derived suppressor cells through TLR2 signaling. Biochem. Biophys. Res. Commun. 457, 445–450.
49. Bromberg, J. (2002) Stat proteins and oncogenesis. J. Clin. Invest. 109, 1139–1142.
50. Nefedova, Y., Nagaraj, S., Rosenbauer, A., Muro-Cacho, C., Sebti, S. M., Gabrilovich, D. I. (2005) Regulation of dendritic cell differentiation and antitumor immune response in cancer by pharmacologic-selective inhibition of the Janus-activated kinase 2/signal transducers and activators of transcription 3 pathway. Cancer Res. 65, 9525–9535.
51. Nefedova, Y., Huang, M., Kusmartsev, S., Bhattacharya, R., Cheng, P., Salup, R., Jove, R., Gabrilovich, D. (2004) Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 172, 464–474.
52. Yu, H., Kortylewski, M., Pardoll, D. (2007) Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7, 41–51.
53. Chakraborty, A., Tweardy, D. J. (1998) Stat3 and G-CSF-induced myeloid differentiation. Leuk. Lymphoma 30, 433–442.
54. Hedrich, C. M., Bream, J. H. (2010) Cell type-specific regulation of IL-10 expression in inflammation and disease. Immunol. Res. 47, 185–206.
55. Townsend, J. M., Fallon, G. P., Matthews, J. D., Smith, P., Jolin, E. H., McKenzie, N. A. (2000) IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13, 573–583.
56. Matsuzawa, S., Sakashita, K., Kinoshita, T., Ito, S., Yamashita, T., Koike, K. (2003) IL-9 enhances the growth of human mast cell progenitors under stimulation with stem cell factor. J. Immunol. 170, 3461–3467.
57. Goswami, R., Kaplan, M. H. (2011) A brief history of IL-9. J. Immunol. 186, 3283–3288.
58. Renoux, M., Hilliquin, P., Galoppin, L., Florentin, I., Menkes, C. J. (1996) Release of mast cell mediators and nitrites into knee joint fluid in osteoarthritis–comparison with articular chondrocalcinosis and rheumatoid arthritis. Osteoarthritis Cartilage 4, 175–179.
59. Freeman, T. A., Parvizi, J., Dela Valle, C. J., Steinbeck, M. J. (2010) Mast cells and hypoxia drive tissue metaplasia and heterotopic ossification in idiopathic arthrofibrosis after total knee arthroplasty. Fibrogenesis Tissue Repair 3, 17.