Interleukin-23 (IL-23) deficiency disrupts Th17 and Th1-related defenses against Streptococcus pneumoniae infection

Cytokine

Volumn 64, Issue 1, 2013, Pages 375-381

  Kim, Byung Jin ^a   Lee, Suheung ^a   Berg, Rance E ^a   Simecka, Jerry W ^a   Jones, Harlan P ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Interleukin 17; Interlukin 23; Neutrophils; Streptococcus pneumoniae

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; LEUKOCYTE; LUNG FLUID; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; TH1 CELL; TH17 CELL;

BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS PNEUMONIAE;

INTERLEUKIN-17; INTERLUKIN-23; NEUTROPHILS; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; FEMALE; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-23 SUBUNIT P19; INTERLEUKIN-6; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; TH1 CELLS; TH17 CELLS;

EID: 84883553675     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2013.05.013     Document Type: Article

References (70)

1. Chenoweth C.E., Saint S., Martinez F., Lynch J.P., Fendrick A.M. Antimicrobial resistance in streptococcus pneumoniae: implications for patients with community-acquired pneumonia. Mayo Clin Proc 2000, 75(11):1161-1168.
2. Dengler T.J., Strnad N., Buhring I., Zimmermann R., Girgsdies O., Kubler W.E., et al. Differential immune response to influenza and pneumococcal vaccination in immunosuppressed patients after heart transplantation. Transplantation 1998, 66(10):1340-1347.
3. Musher D.M. Infections caused by streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin Infect Dis 1992, 14(4):801-807.
4. Curtis M.M., Way S.S., Wilson C.B. IL-23 promotes the production of IL-17 by antigen-specific CD8 T cells in the absence of IL-12 and type-I interferons. J Immunol 2009, 183(1):381-387.
5. Kleinschek M.A., Muller U., Brodie S.J., Stenzel W., Kohler G., Blumenschein W.M., et al. IL-23 enhances the inflammatory cell response in cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J Immunol 2006, 176(2):1098-1106.
6. Kleinschek M.A., Muller U., Schutze N., Sabat R., Straubinger R.K., Blumenschein W.M., et al. Administration of IL-23 engages innate and adaptive immune mechanisms during fungal infection. Int Immunol 2010, 22(2):81-90.
7. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005, 201(2):233-240.
8. Munoz M., Heimesaat M.M., Danker K., Struck D., Lohmann U., Plickert R., et al. Interleukin (IL)-23 mediates toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 2009, 206(13):3047-3059.
9. Langrish C.L., McKenzie B.S., Wilson N.J., de Waal Malefyt R., Kastelein R.A., Cua D.J. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 2004, 202:96-105.
10. Stritesky G.L., Yeh N., Kaplan M.H. IL-23 promotes maintenance but not commitment to the Th17 lineage. J Immunol 2008, 181(9):5948-5955.
11. Laan M., Cui Z.H., Hoshino H., Lotvall J., Sjostrand M., Gruenert D.C., et al. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 1999, 162(4):2347-2352.
12. Linden A., Laan M., Anderson G.P. Neutrophils, interleukin-17A and lung disease. Eur Respir J 2005, 25(1):159-172.
13. Sun K., Salmon S.L., Lotz S.A., Metzger D.W. Interleukin-12 promotes gamma interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect Immun 2007, 75(3):1196-1202.
14. Olafsdottir T.A., Lingau K., Nagy E., Jonsfottir I. Novel protein-based pneumococcal vaccines administered with the Th1-promoting adjuvant IC31 induce protective immunity against pneumococcal disease in neonatal mice. Infect Immun 2012, 80(1):461-468.
15. Abraham C., Cho J.H. IL-23 and autoimmunity: new insights into the pathogenesis of inflammatory bowel disease. Annu Rev Med 2009, 60:97-110.
16. Chen Y., Langrish C.L., McKenzie B., Joyce-Shaikh B., Stumhofer J.S., McClanahan T., et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 2006, 116(5):1317-1326.
17. Gyulveszi G., Haak S., Becher B. IL-23-driven encephalo-tropism and Th17 polarization during CNS-inflammation in vivo. Eur J Immunol 2009, 39(7):1864-1869.
18. Kroenke M.A., Carlson T.J., Andjelkovic A.V., Segal B.M. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J Exp Med 2008, 205(7):1535-1541.
19. Li Y., Chu N., Hu A., Gran B., Rostami A., Zhang G.X. Increased IL-23p19 expression in multiple sclerosis lesions and its induction in microglia. Brain 2007, 130(Pt 2):490-501.
20. Thakker P., Leach M.W., Kuang W., Benoit S.E., Leonard J.P., Marusic S. IL-23 is critical in the induction but not in the effector phase of experimental autoimmune encephalomyelitis. J Immunol 2007, 178(4):2589-2598.
21. Meeks K.D., Sieve A.N., Kolls J.K., Ghilardi N., Berg R.E. IL-23 is required for protection against systemic infection with Listeria monocytogenes. J Immunol 2009, 183(12):8026-8034.
22. Awoniyi M., Miller S.I., Wilson C.B., Hajjar A.M., Smith K.D. Homeostatic regulation of salmonella-induced mucosal inflammation and injury by IL-23. PLoS One 2012, 7(5):e37311.
23. Zarbock A., Ley K. Neutrophil adhesion and activation under flow. Microcirculation 2009, 16(1):31-42.
24. Garvy B.A., Harmsen A.G. The importance of neutrophils in resistance to pneumococcal pneumonia in adult and neonatal mice. Inflammation 1996, 20(5):499-512.
25. Roger T., Calandra T. TLR2-mediated neutrophil depletion exacerbates bacterial sepsis. Proc Natl Acad Sci USA 2009, 106(17):6889-6890.
26. van Faassen H., KuoLee R., Harris G., Zhao X., Conlan J.W., Chen W. Neutrophils play an important role in host resistance to respiratory infection with acinetobacter baumannii in mice. Infect Immun 2007, 75(12):5597-5608.
27. Carr K.D., Sieve A.N., Indramohan M., Break T.J., Lee S., Berg R.E. Specific depletion reveals a novel role for neutrophil-mediated protection in the liver during Listeria monocytogenes infection. Eur J Immunol 2011, 41(9):2666-2676.
28. Christopher M.J., Link D.C. Regulation of neutrophil homeostasis. Curr Opin Hematol 2007, 14(1):3-8.
29. DiStasi M.R., Ley K. Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability. Trends Immunol 2009, 30(11):547-556.
30. Lu Y.J., Gross J., Bogaert D., Finn A., Bagrade L., Zhang Q., et al. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog 2008, 4(9):e1000159.
31. Zhang Z., Clarke T.B., Weiser J.N. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 2009, 119(7):1899-1909.
32. Ma J., Wang J., Wan J., Charboneau R., Chang Y., Barke R.A., et al. Morphine disrupts interleukin-23 (IL-23)/IL-17-mediated pulmonary mucosal host defense against streptococcus pneumoniae infection. Infect Immun 2010, 78(2):830-837.
33. Jones H.P., Hodge L.M., Fujihashi K., Kiyono H., McGhee J.R., Simecka J.W. The pulmonary environment promotes Th2 cell responses after nasal-pulmonary immunization with antigen alone, but Th1 responses are induced during instances of intense immune stimulation. J Immunol 2001, 167(8):4518-4526.
34. Jones H.P., Tabor L., Sun X., Woolard M.D., Simecka J.W. Depletion of CD8+ T cells exacerbates CD4+ th cell-associated inflammatory lesions during murine mycoplasma respiratory disease. J Immunol 2002, 168(7):3493-3501.
35. Kruisbeek A.M. Isolation of mouse mononuclear cells. Curr Protoc Immunol 2001, Chapter 3:Unit 3.1.
36. Costa V.S., Mattana T.C., da Silva M.E. Unregulated IL-23/IL-17 immune response in autoimmune diseases. Diabetes Res Clin Pract 2010.
37. Kim B.J., Jones H.P. Epinephrine-primed murine bone marrow-derived dendritic cells facilitate production of IL-17A and IL-4 but not IFN-gamma by CD4+ T cells. Brain Behav Immun 2010, 24(7):1126-1136.
38. Lin Y., Ritchea S., Logar A., Slight S., Messmer M., Rangel-Moreno J., et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009, 31(5):799-810.
39. Godinez I., Raffatellu M., Chu H., Paixao T.A., Haneda T., Santos R.L., et al. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype typhimurium in the intestine. Infect Immun 2009, 77(1):387-398.
40. Himer L., Balog A., Szebeni B., Szakal D.N., Sziksz E., Reusz G., et al. Th17 cells in rheumatoid arthritis. Orv Hetil 2010, 151(25):1003-1010.
41. Miossec P. IL-17 and Th17 cells in human inflammatory diseases. Microbes Infect 2009, 11(5):625-630.
42. Garcia-Rey C., Martin-Herrero J.E., Baquero F. Antibiotic consumption and generation of resistance in streptococcus pneumoniae: the paradoxical impact of quinolones in a complex selective landscape. Clin Microbiol Infect 2006, 12(Suppl. 3):55-66.
43. Karchmer A.W. Increased antibiotic resistance in respiratory tract pathogens: PROTEKT US - an update. Clin Infect Dis 2004, 39(Suppl. 3):S142-S150.
44. Aujla S.J., Dubin P.J., Kolls J.K. Th17 cells and mucosal host defense. Semin Immunol 2007, 19(6):377-382.
45. Dubin P.J., Kolls J.K. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 2007, 292(2):L519-L528.
46. Kawaguchi M., Kokubu F., Kuga H., Tomita T., Matsukura S., Hoshino H., et al. Effect of IL-17 on ICAM-1 expression of human bronchial epithelial cells, NCI-H 292. Arerugi 1999, 48(10):1184-1187.
47. Lee J.W., Wang P., Kattah M.G., Youssef S., Steinman L., DeFea K., et al. Differential regulation of chemokines by IL-17 in colonic epithelial cells. J Immunol 2008, 181(9):6536-6545.
48. Albanesi C., Cavani A., Girolomoni G. IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: Synergistic or antagonist effects with IFN-gamma and TNF-alpha. J Immunol 1999, 162(1):494-502.
49. Ruddy M.J., Shen F., Smith J.B., Sharma A., Gaffen S.L. Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment. J Leukocyte Biol 2004, 76(1):135-144.
50. Xu S., Cao X. Interleukin-17 and its expanding biological functions. Cell Mol Immunol 2010, 7(3):164-174.
51. Brown C.R., Blaho V.A., Loiacono C.M. Treatment of mice with the neutrophil-depleting antibody RB6-8C5 results in early development of experimental lyme arthritis via the recruitment of gr-1-polymorphonuclear leukocyte-like cells. Infect Immun 2004, 72(9):4956-4965.
52. Liu Z.X., Han D., Gunawan B., Kaplowitz N. Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 2006, 43(6):1220-1230.
53. Sitia G., Isogawa M., Kakimi K., Wieland S.F., Chisari F.V., Guidotti L.G. Depletion of neutrophils blocks the recruitment of antigen-nonspecific cells into the liver without affecting the antiviral activity of hepatitis B virus-specific cytotoxic T lymphocytes. Proc Natl Acad Sci USA 2002, 99(21):13717-13722.
54. Daley J.M., Thomay A.A., Connolly M.D., Reichner J.S., Albina J.E. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 2008, 83(1):64-70.
55. Mayer-Scholl A., Averhoff P., Zychlinsky A. How do neutrophils and pathogens interact?. Curr Opin Microbiol 2004, 7(1):62-66.
56. Belizario J.E., Dinarello C.A. Interleukin 1, interleukin 6, tumor necrosis factor, and transforming growth factor beta increase cell resistance to tumor necrosis factor cytotoxicity by growth arrest in the G1 phase of the cell cycle. Cancer Res 1991, 51(9):2379-2385.
57. Czuprynski C.J., Haak-Frendscho M., Maroushek N., Brown J.F. Effects of recombinant human interleukin-6 alone and in combination with recombinant interleukin-1 alpha and tumor necrosis factor alpha on antibacterial resistance in mice. Antimicrob Agents Chemother 1992, 36(1):68-70.
58. Dann S.M., Spehlmann M.E., Hammond D.C., Iimura M., Hase K., Choi L.J., et al. IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 2008, 180(10):6816-6826.
59. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007, 8(12):1390-1397.
60. McGeachy M.J., Cua D.J. Th17 cell differentiation: the long and winding road. Immunity 2008, 28(4):445-453.
61. Neurath M.F., Finotto S., Glimcher L.H. The role of Th1/Th2 polarization in mucosal immunity. Nat Med 2002, 8(6):567-573.
62. Shan B.E., Hao J.S., Li Q.X., Tagawa M. Antitumor activity and immune enhancement of murine interleukin-23 expressed in murine colon carcinoma cells. Cell Mol Immunol 2006, 3(1):47-52.
63. Moreno S.E., Alves-Filho J.C., Alfaya T.M., da Silva J.S., Ferreira S.H., Liew F.Y. IL-12, but not IL-18, is critical to neutrophil activation and resistance to polymicrobial sepsis induced by cecal ligation and puncture. J Immunol 2006, 177(5):3218-3224.
64. Winter C., Herbold W., Maus R., Langer F., Briles D.E., Paton J.C., et al. Important role for CC chemokine ligand 2-dependent lung mononuclear phagocyte recruitment to inhibit sepsis in mice infected with streptococcus pneumoniae. J Immunol 2009, 182(8):4931-4937.
65. Shahrara S., Pickens S.R., Dorfleutner A., Pope R.M. IL-17 induces monocyte migration in rheumatoid arthritis. J Immunol 2009, 182(6):3884-3891.
66. van de Wetering D., de Paus R.A., van Dissel J.T., van de Vosse E. Salmonella induced IL-23 and IL-1beta allow for IL-12 production by monocytes and Mphi1 through induction of IFN-gamma in CD56 NK/NK-like T cells. PLoS One 2009, 4(12):e8396.
67. Marks M., Burns T., Abadi M., Seyoum B., Thornton J., Tuomanen E., et al. Influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice. Infect Immun 2007, 75(4):1586-1597.
68. Indramohan M., Sieve A.N., Break T.J., Berg R.E. Inflammatory monocyte recruitment is regulated by interleukin-23 during systemic bacterial infection. Infect Immun 2012, 80(12):4099-4105.
69. O'Dwyer M.J., Mankan A.K., White M., Lawless M.W., Stordeur P., O'Connell B., et al. The human response to infection is associated with distinct patterns of interleukin 23 and interleukin 27 expression. Intens Care Med 2008, 34(4):683-691.
70. Langowski J.L., Kastelein R.A., Oft M. Swords into plowshares: IL-23 repurposes tumor immune surveillance. Trends Immunol 2007, 28(5):207-212.