The Duration of Chlamydia muridarum Genital Tract Infection and Associated Chronic Pathological Changes Are Reduced in IL-17 Knockout Mice but Protection Is Not Increased Further by Immunization

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Andrew, Dean W ^a   Cochrane, Melanie ^a   Schripsema, Justin H ^b   Ramsey, Kyle H ^b   Dando, Samantha J ^a   O'Meara, Connor P ^a   Timms, Peter ^a   Beagley, Kenneth W ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b MIDWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; GAMMA INTERFERON; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 17; MAJOR OUTER MEMBRANE PROTEIN; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ACTIVE IMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CHLAMYDIASIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE DURATION; FEMALE; GENITAL TRACT INFECTION; HISTOPATHOLOGY; HYDROSALPINX; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; IN VIVO STUDY; INFECTION RESISTANCE; LYMPHOCYTE PROLIFERATION; MACROPHAGE MIGRATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE;

ADMINISTRATION, INTRANASAL; ANIMALS; BACTERIAL VACCINES; CELL PROLIFERATION; CELLS, CULTURED; CHLAMYDIA INFECTIONS; CHLAMYDIA MURIDARUM; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNIZATION; INTERFERON-GAMMA; INTERLEUKIN-17; MACROPHAGES; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEUTROPHILS; OVIDUCTS; REPRODUCTIVE TRACT INFECTIONS; TIME FACTORS; VAGINA;

EID: 84884481545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076664     Document Type: Article

References (73)

1. Beagley KW, Timms P, (2000) Chlamydia trachomatis infection: incidence, health costs and prospects for vaccine development. J Reprod Immunol 48: 47-68. doi:10.1016/S0165-0378(00)00069-3. PubMed: 10996382.
2. Morrison RP, Caldwell HD, (2002) Immunity to murine chlamydial genital infection. Infect Immun 70: 2741-2751. doi:10.1128/IAI.70.6.2741-2751.2002. PubMed: 12010958.
3. Cochrane M, Armitage CW, O'Meara CP, Beagley KW, (2010) Towards a Chlamydia trachomatis vaccine: how close are we? Future Microbiol 5: 1833-1856. doi:10.2217/fmb.10.148. PubMed: 21155665.
4. Morrison SG, Morrison RP, (2005) A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J Immunol 175: 7536-7542. PubMed: 16301662.
5. Fling SP, Sutherland RA, Steele LN, Hess B, D'Orazio SE, et al. (2001) CD8+ T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis. Proc Natl Acad Sci U S A 98: 1160-1165. doi:10.1073/pnas.98.3.1160. PubMed: 11158611.
6. Lampe MF, Wilson CB, Bevan MJ, Starnbach MN, (1998) Gamma interferon production by cytotoxic T lymphocytes is required for resolution of Chlamydia trachomatis infection. Infect Immun 66: 5457-5461. PubMed: 9784557.
7. Mosmann TR, Coffman RL, (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 7: 145-173. doi:10.1146/annurev.iy.07.040189.001045. PubMed: 2523712.
8. Zhu J, Paul WE, (2008) CD4 T cells: fates, functions, and faults. Blood 112: 1557-1569. doi:10.1182/blood-2008-05-078154. PubMed: 18725574.
9. Infante-Duarte C, Horton HF, Byrne MC, Kamradt T, (2000) Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol 165: 6107-6115. PubMed: 11086043.
10. Kimura A, Naka T, Kishimoto T, (2007) IL-6-dependent and-independent pathways in the development of interleukin 17-producing T helper cells. Proc Natl Acad Sci U S A 104: 12099-12104. doi:10.1073/pnas.0705268104. PubMed: 17623780.
11. Ouyang W, Kolls JK, Zheng Y, (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467. doi:10.1016/j.immuni.2008.03.004. PubMed: 18400188.
12. Marwaha AK, Leung NJ, McMurchy AN, Levings MK, (2012) TH17 Cells in Autoimmunity and Immunodeficiency: Protective or Pathogenic? Front Immunol 3: 129. PubMed: 22675324.
13. Rudner XL, Happel KI, Young EA, Shellito JE, (2007) Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect Immun 75: 3055-3061. doi:10.1128/IAI.01329-06. PubMed: 17403873.
14. Huang W, Na L, Fidel PL, Schwarzenberger P, (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190: 624-631. doi:10.1086/422329. PubMed: 15243941.
15. Kohyama S, Ohno S, Isoda A, Moriya O, Belladonna ML, et al. (2007) IL-23 enhances host defense against vaccinia virus infection via a mechanism partly involving IL-17. J Immunol 179: 3917-3925.
16. Happel KI, Dubin PJ, Zheng M, Ghilardi N, Lockhart C, et al. (2005) Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J Exp Med 202: 761-769. doi:10.1084/jem.20050193. PubMed: 16157683.
17. Matsuzaki G, Umemura M, (2007) Interleukin-17 as an Effector Molecule of Innate and Acquired Immunity against Infections. Microbiol Immunol 51: 1139-1147. PubMed: 18094532.
18. Curtis MM, Way SS, (2009) Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126: 177-185. doi:10.1111/j.1365-2567.2008.03017.x. PubMed: 19125888.
19. Khader SA, Gopal R, (2010) IL-17 in protective immunity to intracellular pathogens. Virulence 1: 423-427. doi:10.4161/viru.1.5.12862. PubMed: 21178483.
20. Chen Z, O'Shea JJ, (2008) Regulation of IL-17 production in human lymphocytes. Cytokine 41: 71-78. doi:10.1016/j.cyto.2007.09.009. PubMed: 17981475.
21. Porter E, Yang H, Yavagal S, Preza GC, Murillo O, et al. (2005) Distinct defensin profiles in Neisseria gonorrhoeae and Chlamydia trachomatis urethritis reveal novel epithelial cell-neutrophil interactions. Infect Immun 73: 4823-4833. doi:10.1128/IAI.73.8.4823-4833.2005. PubMed: 16040996.
22. Scurlock AM, Frazer LC, Andrews CW Jr., O'Connell CM, Foote IP, et al. (2011) Interleukin-17 contributes to generation of Th1 immunity and neutrophil recruitment during Chlamydia muridarum genital tract infection but is not required for macrophage influx or normal resolution of infection. Infect Immun 79: 1349-1362. doi:10.1128/IAI.00984-10. PubMed: 21149587.
23. Imtiaz MT, Schripsema JH, Sigar IM, Kasimos JN, Ramsey KH, (2006) Inhibition of matrix metalloproteinases protects mice from ascending infection and chronic disease manifestations resulting from urogenital Chlamydia muridarum infection. Infect Immun 74: 5513-5521. doi:10.1128/IAI.00730-06. PubMed: 16988226.
24. Imtiaz MT, Distelhorst JT, Schripsema JH, Sigar IM, Kasimos JN, et al. (2007) A role for matrix metalloproteinase-9 in pathogenesis of urogenital Chlamydia muridarum infection in mice. Microbes Infect 9: 1561-1566. doi:10.1016/j.micinf.2007.08.010. PubMed: 18023394.
25. Prause O, Bozinovski S, Anderson GP, Lindén A, (2004) Increased matrix metalloproteinase-9 concentration and activity after stimulation with interleukin-17 in mouse airways. Thorax 59: 313-317. doi:10.1136/thx.2003.008854. PubMed: 15047951.
26. Koenders MI, Marijnissen RJ, Devesa I, Lubberts E, Joosten LA, et al. (2011) Tumor necrosis factor-interleukin-17 interplay induces S100A8, interleukin-1beta, and matrix metalloproteinases, and drives irreversible cartilage destruction in murine arthritis: rationale for combination treatment during arthritis. Arthritis Rheum 63: 2329-2339. doi:10.1002/art.30418. PubMed: 21520013.
27. Sadik CD, Kim ND, Alekseeva E, Luster AD, (2011) IL-17RA signaling amplifies antibody-induced arthritis. PLOS ONE 6: e26342. doi:10.1371/journal.pone.0026342. PubMed: 22028860.
28. Li J, Lau GK, Chen L, Dong SS, Lan HY, et al. (2011) Interleukin 17A promotes hepatocellular carcinoma metastasis via NF-kB induced matrix metalloproteinases 2 and 9 expression. PLOS ONE 6: e21816. doi:10.1371/journal.pone.0021816. PubMed: 21760911.
29. Benagiano M, Munari F, Ciervo A, Amedei A, Paccani SR, et al. (2012) Chlamydophila pneumoniae phospholipase D (CpPLD) drives Th17 inflammation in human atherosclerosis. Proc Natl Acad Sci U S A 109: 1222-1227. doi:10.1073/pnas.1111833109. PubMed: 22232679.
30. Fazio G, Giovino M, Gullotti A, Bacarella D, Novo G, et al. (2009) Atherosclerosis, inflammation and Chlamydia pneumoniae. World. J Cardiol 1: 31-40.
31. Barker CJ, Beagley KW, Hafner LM, Timms P, (2008) In silico identification and in vivo analysis of a novel T-cell antigen from Chlamydia, NrdB. Vaccine 26: 1285-1296. doi:10.1016/j.vaccine.2007.12.048. PubMed: 18261829.
32. Cunningham KA, Carey AJ, Lycke N, Timms P, Beagley KW, (2009) CTA1-DD is an effective adjuvant for targeting anti-chlamydial immunity to the murine genital mucosa. J Reprod Immunol 81: 34-38. doi:10.1016/j.jri.2009.04.002. PubMed: 19501917.
33. Andrew DW, Hafner LM, Beagley KW, Timms P, (2011) Partial protection against chlamydial reproductive tract infection by a recombinant major outer membrane protein/CpG/cholera toxin intranasal vaccine in the guinea pig Chlamydia caviae model. J Reprod Immunol 91: 9-16. doi:10.1016/j.jri.2011.06.100. PubMed: 21856018.
34. Carey A, Cunningham K, Andrew D, Hafner L, Timms P, et al. (2011) A comparison of the effects of a chlamydial vaccine administered during or after a C. muridarum urogenital infection of female mice. Vaccine 29: 6505-6513. doi:10.1016/j.vaccine.2011.07.012. PubMed: 21767592.
35. Zygmunt BM, Rharbaoui F, Groebe L, Guzman CA, (2009) Intranasal immunization promotes th17 immune responses. J Immunol 183: 6933-6938. doi:10.4049/jimmunol.0901144. PubMed: 19890060.
36. Lu C, Zeng H, Li Z, Lei L, Yeh IT, et al. (2012) Protective immunity against mouse upper genital tract pathology correlates with high IFNgamma but low IL-17 T cell and anti-secretion protein antibody responses induced by replicating chlamydial organisms in the airway. Vaccine 30: 475-485. doi:10.1016/j.vaccine.2011.10.059. PubMed: 22079265.
37. Yu H, Jiang X, Shen C, Karunakaran KP, Jiang J, et al. (2010) Chlamydia muridarum T-cell antigens formulated with the adjuvant DDA/TDB induce immunity against infection that correlates with a high frequency of gamma interferon (IFN-gamma)/tumor necrosis factor alpha and IFN-gamma/interleukin-17 double-positive CD4+ T cells. Infect Immun 78: 2272-2282. doi:10.1128/IAI.01374-09. PubMed: 20231405.
38. Zhang X, Gao L, Lei L, Zhong Y, Dube P, et al. (2009) A MyD88-dependent early IL-17 production protects mice against airway infection with the obligate intracellular pathogen Chlamydia muridarum. J Immunol 183: 1291-1300. doi:10.4049/jimmunol.0803075. PubMed: 19542374.
39. Pal S, Fielder TJ, Peterson EM, de la Maza LM, (1994) Protection against infertility in a BALB/c mouse salpingitis model by intranasal immunization with the mouse pneumonitis biovar of Chlamydia trachomatis. Infect Immun 62: 3354-3362. PubMed: 8039906.
40. Skelding KA, Hickey DK, Horvat JC, Bao S, Roberts KG, et al. (2006) Comparison of intranasal and transcutaneous immunization for induction of protective immunity against Chlamydia muridarum respiratory tract infection. Vaccine 24: 355-366. doi:10.1016/j.vaccine.2005.07.104. PubMed: 16153755.
41. Berry LJ, Hickey DK, Skelding KA, Bao S, Rendina AM, et al. (2004) Transcutaneous Immunization with Combined Cholera Toxin and CpG Adjuvant Protects against Chlamydia muridarum Genital Tract Infection. Infect Immun 72: 1019-1028. doi:10.1128/IAI.72.2.1019-1028.2004. PubMed: 14742549.
42. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387. doi:10.1016/S1074-7613(02)00391-6. PubMed: 12354389.
43. Carey AJ, Cunningham KA, Hafner LM, Timms P, Beagley KW, (2009) Effects of inoculating dose on the kinetics of Chlamydia muridarum genital infection in female mice. Immunol Cell Biol 87: 337-343. doi:10.1038/icb.2009.3. PubMed: 19204735.
44. Shah AA, Schripsema JH, Imtiaz MT, Sigar IM, Kasimos J, et al. (2005) Histopathologic changes related to fibrotic oviduct occlusion after genital tract infection of mice with Chlamydia muridarum. Sex Transm Dis 32: 49-56. doi:10.1097/01.olq.0000148299.14513.11. PubMed: 15614121.
45. Ramsey KH, Sigar IM, Schripsema JH, Shaba N, Cohoon KP, (2005) Expression of matrix metalloproteinases subsequent to urogenital Chlamydia muridarum infection of mice. Infect Immun 73: 6962-6973. doi:10.1128/IAI.73.10.6962-6973.2005. PubMed: 16177376.
46. Beagley KW, Timms P, Debattista J, Wilson DP, (2009) Time to rethink the expectations for a chlamydial vaccine. Mucosal Immunol 2: 278. doi:10.1038/mi.2009.11.
47. Hickey DK, Aldwell FE, Tan ZY, Bao S, Beagley KW, (2009) Transcutaneous immunization with novel lipid-based adjuvants induces protection against gastric Helicobacter pylori infection. Vaccine, 27: 6983-90. PubMed: 19800441.
48. Beklen A, Ainola M, Hukkanen M, Gürgan C, Sorsa T, et al. (2007) MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis. J Dent Res 86: 347-351. doi:10.1177/154405910708600409. PubMed: 17384030.
49. Prantner D, Darville T, Sikes JD, Andrews CW Jr., Brade H, et al. (2009) Critical role for interleukin-1beta (IL-1beta) during Chlamydia muridarum genital infection and bacterial replication-independent secretion of IL-1beta in mouse macrophages. Infect Immun 77: 5334-5346. doi:10.1128/IAI.00883-09. PubMed: 19805535.
50. Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, et al. (2007) Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia trachomatis infection. Cell Microbiol 9: 2795-2803. doi:10.1111/j.1462-5822.2007.00996.x. PubMed: 17614966.
51. Lee HY, Schripsema JH, Sigar IM, Murray CM, Lacy SR, et al. (2010) A link between neutrophils and chronic disease manifestations of Chlamydia muridarum urogenital infection of mice. FEMS Immunol Med Microbiol 59: 108-116. doi:10.1111/j.1574-695X.2010.00668.x. PubMed: 20370824.
52. Frazer LC, O'Connell CM, Andrews CW Jr., Zurenski MA, Darville T, (2011) Enhanced neutrophil longevity and recruitment contribute to the severity of oviduct pathology during Chlamydia muridarum infection. Infect Immun 79: 4029-4041. doi:10.1128/IAI.05535-11. PubMed: 21825059.
53. van Zandbergen G, Gieffers J, Kothe H, Rupp J, Bollinger A, et al. (2004) Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J Immunol 172: 1768-1776. PubMed: 14734760.
54. Rupp J, Pfleiderer L, Jugert C, Moeller S, Klinger M, et al. (2009) Chlamydia pneumoniae hides inside apoptotic neutrophils to silently infect and propagate in macrophages. PLOS ONE 4: e6020. doi:10.1371/journal.pone.0006020. PubMed: 19547701.
55. Zhang Y, Wang H, Ren J, Tang X, Jing Y, et al. (2012) IL-17A synergizes with IFN-gamma to upregulate iNOS and NO production and inhibit chlamydial growth. PLOS ONE 7: e39214. doi:10.1371/journal.pone.0039214. PubMed: 22745717.
56. Mitsdoerffer M, Lee Y, Jäger A, Kim HJ, Korn T, et al. (2010) Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc Natl Acad Sci U S A 107: 14292-14297. doi:10.1073/pnas.1009234107. PubMed: 20660725.
57. Hirota K, Turner JE, Villa M, Duarte JH, Demengeot J, et al. (2013) Plasticity of TH17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol 14: 372-379. doi:10.1038/ni.2552. PubMed: 23475182.
58. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498. doi:10.1016/j.cell.2009.09.033. PubMed: 19836068.
59. Feng T, Qin H, Wang L, Benveniste EN, Elson CO, et al. (2011) Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J Immunol 186: 6313-6318. doi:10.4049/jimmunol.1001454. PubMed: 21531892.
60. Gopal R, Lin Y, Obermajer N, Slight S, Nuthalapati N, et al. (2012) IL-23-dependent IL-17 drives Th1-cell responses following Mycobacterium bovis BCG vaccination. Eur J Immunol 42: 364-373. doi:10.1002/eji.201141569. PubMed: 22101830.
61. Lee YK, Turner H, Maynard CL, Oliver JR, Chen D, et al. (2009) Late developmental plasticity in the T helper 17 lineage. Immunity 30: 92-107. doi:10.1016/j.immuni.2008.11.005. PubMed: 19119024.
62. Basu R, Hatton RD, Weaver CT, (2013) The Th17 family: flexibility follows function. Immunol Rev 252: 89-103. doi:10.1111/imr.12035. PubMed: 23405897.
63. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, et al. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 178: 3786-3796. PubMed: 17339477.
64. Gaffen SL, (2009) Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 9: 556-567. doi:10.1038/nri2586. PubMed: 19575028.
65. Haudenschild D, Moseley T, Rose L, Reddi AH, (2002) Soluble and transmembrane isoforms of novel interleukin-17 receptor-like protein by RNA splicing and expression in prostate cancer. J Biol Chem 277: 4309-4316. doi:10.1074/jbc.M109372200. PubMed: 11706037.
66. Zhang Q, Atsuta I, Liu S, Chen C, Shi S, et al. (2013) IL-17-mediated M1/M2 Macrophage Alteration Contributes to Pathogenesis of Bisphosphonate-related Osteonecrosis of the Jaws. Clin Cancer Res, 19: 3176-88. PubMed: 23616636.
67. Raes G, De Baetselier P, Noël W, Beschin A, Brombacher F, et al. (2002) Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol 71: 597-602. PubMed: 11927645.
68. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, et al. (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29: 13435-13444. doi:10.1523/JNEUROSCI.3257-09.2009. PubMed: 19864556.
69. Schulte S, Sukhova GK, Libby P, (2008) Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis. Am J Pathol 172: 1500-1508. doi:10.2353/ajpath.2008.070776. PubMed: 18467709.
70. de la Maza LM, Pal S, Khamesipour A, Peterson EM, (1994) Intravaginal inoculation of mice with the Chlamydia trachomatis mouse pneumonitis biovar results in infertility. Infect Immun 62: 2094-2097. PubMed: 8168974.
71. Darville T, Andrews CW Jr., Laffoon KK, Shymasani W, Kishen LR, et al. (1997) Mouse strain-dependent variation in the course and outcome of chlamydial genital tract infection is associated with differences in host response. Infect Immun 65: 3065-3073. PubMed: 9234755.
72. Jiang X, Shen C, Yu H, Karunakaran KP, Brunham RC, (2010) Differences in innate immune responses correlate with differences in murine susceptibility to Chlamydia muridarum pulmonary infection. Immunology 129: 556-566. doi:10.1111/j.1365-2567.2009.03157.x. PubMed: 20102413.
73. Bai H, Cheng J, Gao X, Joyee AG, Fan Y, et al. (2009) IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J Immunol 183: 5886-5895. doi:10.4049/jimmunol.0901584. PubMed: 19812198.