Immunization with a MOMP-Based Vaccine Pfrotects Mice against a Pulmonary Chlamydia Challenge and Identifies a Disconnection between Infection and Pathology

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  O'Meara, Connor P ^a   Armitage, Charles W ^a   Harvie, Marina C G ^a   Timms, Peter ^a   Lycke, Nils Y ^b   Beagley, Kenneth W ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; CHOLERA TOXIN; CPG OLIGODEOXYNUCLEOTIDE; CTA1 DD; GAMMA INTERFERON; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 17; RECOMBINANT CHLAMYDIAL OUTER MEMBRANE PROTEIN VACCINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL LOAD; CHLAMYDIAL PNEUMONIA; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; DRUG EFFECT; IMMUNOREACTIVITY; INFECTION CONTROL; INFECTION PREVENTION; LYMPHOCYTE PROLIFERATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; SPLEEN CELL; VACCINATION; WEIGHT REDUCTION;

ANIMALS; CHLAMYDIA; CHLAMYDIA INFECTIONS; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; TUMOR NECROSIS FACTOR-ALPHA; VACCINATION;

ANIMALIA; BACTERIA (MICROORGANISMS); CHLAMYDIA; CHLAMYDIA MURIDARUM; CHLAMYDOPHILA PNEUMONIAE; MUS;

EID: 84876165228     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061962     Document Type: Article

References (75)

1. Grayston JT, (2000) Background and current knowledge of Chlamydia pneumoniae and atherosclerosis. J Infect Dis 181Suppl 3: S402-410.
2. Clementsen P, Permin H, Norn S, (2002) Chlamydia pneumoniae infection and its role in asthma and chronic obstructive pulmonary disease. J Investig Allergol Clin Immunol 12: 73-79.
3. Kuo CC, Shor A, Campbell LA, Fukushi H, Patton DL, et al. (1993) Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J Infect Dis 167: 841-849.
4. Villegas E, Sorlozano A, Gutierrez J, (2010) Serological diagnosis of Chlamydia pneumoniae infection: limitations and perspectives. J Med Microbiol 59: 1267-1274.
5. Hammerschlag MR, Chirgwin K, Roblin PM, Gelling M, Dumornay W, et al. (1992) Persistent infection with Chlamydia pneumoniae following acute respiratory illness. Clin Infect Dis 14: 178-182.
6. Aldous MB, Grayston JT, Wang SP, Foy HM, (1992) Seroepidemiology of Chlamydia pneumoniae TWAR infection in Seattle families, 1966-1979. J Infect Dis 166: 646-649.
7. Penttila JM, Anttila M, Puolakkainen M, Laurila A, Varkila K, et al. (1998) Local immune responses to Chlamydia pneumoniae in the lungs of BALB/c mice during primary infection and reinfection. Infect Immun 66: 5113-5118.
8. Mutsch M, Zhou W, Rhodes P, Bopp M, Chen RT, et al. (2004) Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 350: 896-903.
9. Frech SA, Dupont HL, Bourgeois AL, McKenzie R, Belkind-Gerson J, et al. (2008) Use of a patch containing heat-labile toxin from Escherichia coli against travellers' diarrhoea: a phase II, randomised, double-blind, placebo-controlled field trial. Lancet 371: 2019-2025.
10. Agren LC, Ekman L, Lowenadler B, Lycke NY, (1997) Genetically engineered nontoxic vaccine adjuvant that combines B cell targeting with immunomodulation by cholera toxin A1 subunit. J Immunol 158: 3936-3946.
11. Eriksson AM, Schon KM, Lycke NY, (2004) The cholera toxin-derived CTA1-DD vaccine adjuvant administered intranasally does not cause inflammation or accumulate in the nervous tissues. J Immunol 173: 3310-3319.
12. Sundling C, Schon K, Morner A, Forsell MN, Wyatt RT, et al. (2008) CTA1-DD adjuvant promotes strong immunity against human immunodeficiency virus type 1 envelope glycoproteins following mucosal immunization. J Gen Virol 89: 2954-2964.
13. De Filette M, Ramne A, Birkett A, Lycke N, Lowenadler B, et al. (2006) The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine 24: 544-551.
14. Akhiani AA, Stensson A, Schon K, Lycke N, (2006) The nontoxic CTA1-DD adjuvant enhances protective immunity against Helicobacter pylori infection following mucosal immunization. Scand J Immunol 63: 97-105.
15. Andersen CS, Dietrich J, Agger EM, Lycke NY, Lovgren K, et al. (2007) The combined CTA1-DD/ISCOMs vector is an effective intranasal adjuvant for boosting prior Mycobacterium bovis BCG immunity to Mycobacterium tuberculosis. Infect Immun 75: 408-416.
16. McNeal MM, Basu M, Bean JA, Clements JD, Lycke NY, et al. (2007) Intrarectal immunization of mice with VP6 and either LT(R192G) or CTA1-DD as adjuvant protects against fecal rotavirus shedding after EDIM challenge. Vaccine 25: 6224-6231.
17. Choi AH, McNeal MM, Flint JA, Basu M, Lycke NY, et al. (2002) The level of protection against rotavirus shedding in mice following immunization with a chimeric VP6 protein is dependent on the route and the coadministered adjuvant. Vaccine 20: 1733-1740.
18. 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.
19. 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.
20. Cuburu N, Kweon MN, Song JH, Hervouet C, Luci C, et al. (2007) Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine 25: 8598-8610.
21. Czerkinsky C, Holmgren J, (2010) Mucosal Delivery Routes for Optimal Immunization: Targeting Immunity to the Right Tissues. Curr Top Microbiol Immunol.
22. Caldwell HD, Kromhout J, Schachter J, (1981) Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 31: 1161-1176.
23. 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.
24. Hickey DK, Aldwell FE, Beagley KW, (2009) Transcutaneous immunization with a novel lipid-based adjuvant protects against Chlamydia genital and respiratory infections. Vaccine 27: 6217-6225.
25. Hickey DK, Bao S, Ikeda LT, Carey AJ, Beagley KW, (2005) Induction of anti-chlamydial mucosal immunity by transcutaneous immunization is enhanced by topical application of GM-CSF. Curr Mol Med 5: 599-605.
26. Karande P, Arora A, Pham TK, Stevens D, Wojicki A, et al. (2009) Transcutaneous immunization using common chemicals. J Control Release.
27. Yang X, HayGlass KT, Brunham RC, (1996) Genetically determined differences in IL-10 and IFN-gamma responses correlate with clearance of Chlamydia trachomatis mouse pneumonitis infection. J Immunol 156: 4338-4344.
28. Williams DM, Grubbs BG, Pack E, Kelly K, Rank RG, (1997) Humoral and cellular immunity in secondary infection due to murine Chlamydia trachomatis. Infect Immun 65: 2876-2882.
29. Yang X, Brunham RC, (1998) Gene knockout B cell-deficient mice demonstrate that B cells play an important role in the initiation of T cell responses to Chlamydia trachomatis (mouse pneumonitis) lung infection. J Immunol 161: 1439-1446.
30. Wagner H, (2004) The immunobiology of the TLR9 subfamily. Trends Immunol 25: 381-386.
31. Sanchez J, Holmgren J, (2010) Cholera toxin- a foe & a friend. Indian J Med Res 133: 153-163.
32. Mattsson J, Yrlid U, Stensson A, Schon K, Karlsson MC, et al. (2011) Complement activation and complement receptors on follicular dendritic cells are critical for the function of a targeted adjuvant. J Immunol 187: 3641-3652.
33. Agren LC, Ekman L, Lowenadler B, Nedrud JG, Lycke NY, (1999) Adjuvanticity of the cholera toxin A1-based gene fusion protein, CTA1-DD, is critically dependent on the ADP-ribosyltransferase and Ig-binding activity. J Immunol 162: 2432-2440.
34. Mascarell L, Lombardi V, Zimmer A, Louise A, Tourdot S, et al. (2009) Mapping of the lingual immune system reveals the presence of both regulatory and effector CD4+ T cells. Clin Exp Allergy 39: 1910-1919.
35. Bos JD (2005) Skin Immune System (SIS). Skin Immune System: Cutaneous Immunology and Clinical Immunodermatology 3-13.
36. Pal S, Bravo J, Peterson EM, de la Maza LM, (2008) Protection of wild-type and severe combined immunodeficiency mice against an intranasal challenge by passive immunization with monoclonal antibodies to the Chlamydia trachomatis mouse pneumonitis major outer membrane protein. Infect Immun 76: 5581-5587.
37. Murthy AK, Sharma J, Coalson JJ, Zhong G, Arulanandam BP, (2004) Chlamydia trachomatis pulmonary infection induces greater inflammatory pathology in immunoglobulin A deficient mice. Cell Immunol 230: 56-64.
38. Bai Y, Ye L, Tesar DB, Song H, Zhao D, et al. (2011) Intracellular neutralization of viral infection in polarized epithelial cells by neonatal Fc receptor (FcRn)-mediated IgG transport. Proc Natl Acad Sci U S A 108: 18406-18411.
39. Moore T, Ananaba GA, Bolier J, Bowers S, Belay T, et al. (2002) Fc receptor regulation of protective immunity against Chlamydia trachomatis. Immunology 105: 213-221.
40. Cunningham KA, Carey AJ, Hafner L, Timms P, Beagley KW, (2011) Chlamydia muridarum major outer membrane protein-specific antibodies inhibit in vitro infection but enhance pathology in vivo. Am J Reprod Immunol 65: 118-126.
41. Fox JD, Kapust RB, Waugh DS, (2001) Single amino acid substitutions on the surface of Escherichia coli maltose-binding protein can have a profound impact on the solubility of fusion proteins. Protein Sci 10: 622-630.
42. Su H, Raymond L, Rockey DD, Fischer E, Hackstadt T, et al. (1996) A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc Natl Acad Sci U S A 93: 11143-11148.
43. Sun G, Pal S, Weiland J, Peterson EM, de la Maza LM, (2009) Protection against an intranasal challenge by vaccines formulated with native and recombinant preparations of the Chlamydia trachomatis major outer membrane protein. Vaccine 27: 5020-5025.
44. Fernandez S, Palmer DR, Simmons M, Sun P, Bisbing J, et al. (2007) Potential role for Toll-like receptor 4 in mediating Escherichia coli maltose-binding protein activation of dendritic cells. Infect Immun 75: 1359-1363.
45. Yuzawa S, Kurita-Ochiai T, Hashizume T, Kobayashi R, Abiko Y, et al. (2012) Sublingual vaccination with fusion protein consisting of the functional domain of hemagglutinin A of Porphyromonas gingivalis and Escherichia coli maltose-binding protein elicits protective immunity in the oral cavity. FEMS Immunol Med Microbiol.
46. Simmons M, Murphy GS, Hayes CG, (2001) Short report: Antibody responses of mice immunized with a tetravalent dengue recombinant protein subunit vaccine. Am J Trop Med Hyg 65: 159-161.
47. Simmons M, Murphy GS, Kochel T, Raviprakash K, Hayes CG, (2001) Characterization of antibody responses to combinations of a dengue-2 DNA and dengue-2 recombinant subunit vaccine. Am J Trop Med Hyg 65: 420-426.
48. Kushwaha A, Rao PP, Suresh RP, Chauhan VS, (2001) Immunogenicity of recombinant fragments of Plasmodium falciparum acidic basic repeat antigen produced in Escherichia coli. Parasite Immunol 23: 435-444.
49. Czerkinsky C, Anjuere F, McGhee JR, George-Chandy A, Holmgren J, et al. (1999) Mucosal immunity and tolerance: relevance to vaccine development. Immunol Rev 170: 197-222.
50. Fujihashi K, McGhee JR, (2004) Mucosal immunity and tolerance in the elderly. Mech Ageing Dev 125: 889-898.
51. Zygmunt BM, Rharbaoui F, Groebe L, Guzman CA, (2009) Intranasal immunization promotes th17 immune responses. J Immunol 183: 6933-6938.
52. Yang X, Gartner J, Zhu L, Wang S, Brunham RC, (1999) IL-10 gene knockout mice show enhanced Th1-like protective immunity and absent granuloma formation following Chlamydia trachomatis lung infection. J Immunol 162: 1010-1017.
53. Lu H, Zhong G, (1999) Interleukin-12 production is required for chlamydial antigen-pulsed dendritic cells to induce protection against live Chlamydia trachomatis infection. Infect Immun 67: 1763-1769.
54. Jupelli M, Guentzel MN, Meier PA, Zhong G, Murthy AK, et al. (2008) Endogenous IFN-gamma production is induced and required for protective immunity against pulmonary chlamydial infection in neonatal mice. J Immunol 180: 4148-4155.
55. 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.
56. Summersgill JT, Sahney NN, Gaydos CA, Quinn TC, Ramirez JA, (1995) Inhibition of Chlamydia pneumoniae growth in HEp-2 cells pretreated with gamma interferon and tumor necrosis factor alpha. Infect Immun 63: 2801-2803.
57. Robinson CM, Shirey KA, Carlin JM, (2003) Synergistic transcriptional activation of indoleamine dioxygenase by IFN-gamma and tumor necrosis factor-alpha. J Interferon Cytokine Res 23: 413-421.
58. Perry LL, Su H, Feilzer K, Messer R, Hughes S, et al. (1999) Differential sensitivity of distinct Chlamydia trachomatis isolates to IFN-gamma-mediated inhibition. J Immunol 162: 3541-3548.
59. Gabr MA, Jing L, Helbling AR, Sinclair SM, Allen KD, et al. (2011) Interleukin-17 synergizes with IFNgamma or TNFalpha to promote inflammatory mediator release and intercellular adhesion molecule-1 (ICAM-1) expression in human intervertebral disc cells. J Orthop Res 29: 1-7.
60. Fichorova RN, Anderson DJ, (1999) Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol Reprod 60: 508-514.
61. Igietseme JU, Ananaba GA, Bolier J, Bowers S, Moore T, et al. (1999) The intercellular adhesion molecule type-1 is required for rapid activation of T helper type 1 lymphocytes that control early acute phase of genital chlamydial infection in mice. Immunology 98: 510-519.
62. Igietseme JU, Uriri IM, Hawkins R, Rank RG, (1996) Integrin-mediated epithelial-T cell interaction enhances nitric oxide production and increased intracellular inhibition of Chlamydia. J Leukoc Biol 59: 656-662.
63. Igietseme JU, Ramsey KH, Magee DM, Williams DM, Kincy TJ, et al. (1993) Resolution of murine chlamydial genital infection by the adoptive transfer of a biovar-specific, Th1 lymphocyte clone. Reg Immunol 5: 317-324.
64. 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.
65. Iezzi G, Karjalainen K, Lanzavecchia A, (1998) The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95.
66. Steinman RM, Hemmi H, (2006) Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311: 17-58.
67. O'Garra A, (1998) Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8: 275-283.
68. Zhao X, Deak E, Soderberg K, Linehan M, Spezzano D, et al. (2003) Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J Exp Med 197: 153-162.
69. Han Q, Bagheri N, Bradshaw EM, Hafler DA, Lauffenburger DA, et al. (2011) Polyfunctional responses by human T cells result from sequential release of cytokines. Proc Natl Acad Sci U S A.
70. Atamas SP, White B, (2003) Cytokine regulation of pulmonary fibrosis in scleroderma. Cytokine Growth Factor Rev 14: 537-550.
71. Lawrence CW, Braciale TJ, (2004) Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J Immunol 173: 1209-1218.
72. Lund FE, Partida-Sanchez S, Lee BO, Kusser KL, Hartson L, et al. (2002) Lymphotoxin-alpha-deficient mice make delayed, but effective, T and B cell responses to influenza. J Immunol 169: 5236-5243.
73. Lu C, Zeng H, Li Z, Lei L, Yeh IT, et al. (2011) 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.
74. Visweswaraiah A, Novotny LA, Hjemdahl-Monsen EJ, Bakaletz LO, Thanavala Y, (2002) Tracking the tissue distribution of marker dye following intranasal delivery in mice and chinchillas: a multifactorial analysis of parameters affecting nasal retention. Vaccine 20: 3209-3220.
75. Miyairi I, Ziebarth J, Laxton JD, Wang X, van Rooijen N, et al. (2012) Host genetics and Chlamydia disease: prediction and validation of disease severity mechanisms. PLoS One 7: e33781.