Chlamydia vaccine candidates and tools for chlamydial antigen discovery

Expert Review of Vaccines

Volumn 8, Issue 10, 2009, Pages 1365-1377

  Rockey, Daniel D ^b   Wang, Jie ^a   Lei, Lei ^a   Zhong, Guangming ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Antigen; Chlamydia; Genomics; Sexually transmitted disease; Vaccine

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; CHLAMYDIASIS VACCINE; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN N; PLACEBO; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIBODY DETECTION; ANTIBODY RESPONSE; BACTERIUM ISOLATION; CHLAMYDIA TRACHOMATIS; CHLAMYDIAL PNEUMONIA; CHLAMYDIASIS; CLINICAL TRIAL; DRUG EFFICACY; DRUG SAFETY; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOBLOTTING; INNATE IMMUNITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RADIOIMMUNOPRECIPITATION; REVIEW; SEROTYPE; T LYMPHOCYTE; TRACHOMA; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL VACCINES; CELL LINE; CHLAMYDIA; CHLAMYDIA INFECTIONS; DRUG DISCOVERY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENOMICS; HISTORY, 20TH CENTURY; HUMANS; IMMUNOBLOTTING; IMMUNODOMINANT EPITOPES; PROTEOMICS; RADIOIMMUNOPRECIPITATION ASSAY; T-LYMPHOCYTES;

EID: 70349906776     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.98     Document Type: Review

References (161)

1. Stewart FH, Badir G. Experiments on the cultivation of trachoma virus in the chick embryo. J. Pathol. Bacteriol. 62(3), 457-460 (1950).
2. Tang FF, Chang HL, Huang YT, Wang KC. Studies on the etiology of trachoma with special reference to isolation of the virus in chick embryo. Chin. Med. J. 75(6), 429-447 (1957).
3. Tang FF, Huang YT, Chang HL, Wong KC. Isolation of trachoma virus in chick embryo. J. Hyg. Epidemiol. Microbiol. Immunol. 1(2), 109-120 (1957).
4. Tang FF, Huang YT, Chang HL, Wong KC. Further studies on the isolation of the trachoma virus. Acta Virol. 2(3), 164-170 (1958).
5. Sowa J, Collier LH. Isolation of trachoma virus from patients in West Africa. J. Hyg. (Lond.) 58, 99-108 (1960).
6. Hanna L, Thygeson P, Jawetz E. Elementary-body virus isolated from clinical trachoma in California. Science 130, 1339-1340 (1959).
7. Schachter J, Hill EC, King EB, Coleman VR, Jones P, Meyer KF. Chlamydial infection in women with cervical dysplasia. Am. J. Obstet. Gynecol. 123(7), 753-757 (1975).
8. Collier LH, Duke-Elder S, Jones BR. Experimental trachoma produced by cultured virus. Br. J. Ophthalmol. 42(12), 705-720 (1958).
9. Collier LH, Duke-Elder S, Jones BR. Experimental trachoma produced by cultured virus. Part II. Br. J. Ophthalmol. 44, 65-88 (1960).
10. Jones BR. Human inoculations with trachoma virus. Rev. Int. Trach. 37, 600-608 (1960).
11. Grayston JT, Woolridge RL, Wang S. Trachoma vaccine studies on Taiwan. Ann. NY Acad. Sci. 98, 352-367 (1962).
12. Woolridge RL, Grayston JT, Chang IH, Yang CY, Cheng KH. Long-term follow-up of the initial (1959-1960) trachoma vaccine field trial on Taiwan. Am. J. Ophthalmol. 63(5 Suppl.), 1650-1655 (1967).
13. Bietti GB, Guerra P, Vozza R et al. Results of large-scale vaccination against trachoma in East Africa (Ethiopia) 1960-1965. Am. J. Ophthalmol. 61(5 Pt 2), 1010-1029 (1966).
14. Grayston JT, Wang SP, Woolridge RL, Alexander ER. Prevention of trachoma with vaccine. Arch. Environ. Health 8, 518-526 (1964).
15. Clements C, Dhir SP, Grayston JT, Wang SP. Long term follow-up study of a trachoma vaccine trial in villages of Northern India. Am. J. Ophthalmol. 87(3), 350-353 (1979).
16. Sowa S, Sowa J, Collier LH, Blyth WA. Trachoma vaccine field trials in The Gambia. J. Hyg. (Lond.) 67(4), 699-717 (1969).
17. Morrison RP, Belland RJ, Lyng K, Caldwell HD. Chlamydial disease pathogenesis. The 57-kD chlamydial hypersensitivity antigen is a stress response protein. J. Exp. Med. 170(4), 1271-1283 (1989).
18. Zhong G, Brunham RC. Antibody responses to the chlamydial heat shock proteins hsp60 and hsp70 are H-2 linked. Infect. Immun. 60(8), 3143-3149 (1992).
19. Toye B, Laferriere C, Claman P, Jessamine P, Peeling R. Association between antibody to the chlamydial heat-shock protein and tubal infertility. J. Infect. Dis. 168(5), 1236-1240 (1993).
20. Brunham RC, Rekart ML. The arrested immunity hypothesis and the epidemiology of chlamydia control. Sex. Transm. Dis. 35(1), 53-54 (2008). •• Brief discussion describing how recent epidemiologic data supports the hypothesis that aggressive screening and antibiotic therapy programs may be reducing host immunity provided by chlamydial infection.
21. Longbottom D, Livingstone M. Vaccination against chlamydial infections of man and animals. Vet. J. 171(2), 263-275 (2006). (Pubitemid 43257230)
22. Fields KA, Hackstadt T. The chlamydial inclusion: escape from the endocytic pathway. Annu. Rev. Cell. Dev. Biol. 18, 221-245 (2002).
23. Dautry-Varsat A, Subtil A, Hackstadt T. Recent insights into the mechanisms of chlamydia entry. Cell. Microbiol. 7(12), 1714-1722 (2005).
24. Darville T, O'Neill JM, Andrews CW Jr, Nagarajan UM, Stahl L, Ojcius DM. Toll-like receptor-2, but not Toll-like receptor-4, is essential for development of oviduct pathology in chlamydial genital tract infection. J. Immunol. 171(11), 6187-6197 (2003). (Pubitemid 37467242)
25. Morrison RP, Caldwell HD. Immunity to murine chlamydial genital infection. Infect. Immun. 70(6), 2741-2751 (2002).
26. Loomis WP, Starnbach MN. T cell responses to Chlamydia trachomatis. Curr. Opin. Microbiol. 5(1), 87-91 (2002).
27. Kelly KA. Cellular immunity and Chlamydia genital infection: induction, recruitment, and effector mechanisms. Int. Rev. Immunol. 22(1), 3-41 (2003).
28. Punnonen R, Terho P, Nikkanen V, Meurman O. Chlamydial serology in infertile women by immunofluorescence. Fertil. Steril. 31(6), 656-659 (1979).
29. Brunham RC, Peeling R, Maclean I, Kosseim ML, Paraskevas M. Chlamydia trachomatis-issocmed ectopic pregnancy: serologic and histologic correlates. J. Infect. Dis. 165(6), 1076-1081 (1992).
30. La Verda D, Albanese LN, Ruther PE et al. Seroreactivity to Chlamydia trachomatis Hsp10 correlates with severity of human genital tract disease. Infect. Immun. 68(1), 303-309 (2000).
31. Brunham RC, Kuo CC, Cles L, Holmes KK. Correlation of host immune response with quantitative recovery of Chlamydia trachomatis from the human endocervix. Infect. Immun. 39(3), 1491-1494 (1983).
32. Cotter TW, Meng Q, Shen ZL, Zhang YX, Su H, Cildwell HD. Protective efficacy of major outer membrane protein-specific immunoglobulin A (IgA) and IgG monoclonal antibodies in a murine model of Chlamydia trachomatis genital tract infection. Infect. Immun. 63(12), 4704-4714 (1995).
33. Morrison SG, Morrison RP. A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J. Immunol. 175(11), 7536-7542 (2005).
34. Morrison SG, Morrison RP. The protective effect of antibody in immunity to murine chlamydial genital tract reinfection is independent of immunoglobulin A. Infect. Immun. 73(9), 6183-6186 (2005).
35. Johansson M, Schon K, Ward M, Lycke N. Genital tract infection with Chlamydia trachomatis fails to induce protective immunity in γ interferon receptor-deficient mice despite a strong local immunoglobulin A response. Infect. Immun. 65(3), 1032-1044 (1997).
36. Johansson M, Ward M, Lycke N. B-cell-deficient mice develop complete immune protection against genital tract infection with Chlamydia trachomatis. Immunology 92(4), 422-428 (1997). (Pubitemid 27525212)
37. Su H, Feilzer K, Caldwell HD, Morrison RP. Chlamydia trachomatis genital tract infection of antibody-deficient gene knockout mice. Infect. Immun. 65(6), 1993-1999 (1997).
38. Zhong G, Berry J, Brunham RC. Antibody recognition of a neutralization epitope on the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 62(5), 1576-1583 (1994).
39. Zhang YX, Stewart S, Joseph T, Taylor HR, Caldwell HD. Protective monoclonal antibodies recognize epitopes located on the major outer membrane protein of Chlamydia trachomatis. J. Immunol. 138(2), 575-581 (1987). (Pubitemid 17002223)
40. Pal S, Theodor I, Peterson EM, de la Maza LM. Monoclonal immunoglobulin A antibody to the major outer membrane protein of the Chlamydia trachomatis mouse pneumonitis biovar protects mice against a chlamydial genital challenge. Vaccine 15(5), 575-582 (1997). (Pubitemid 27188626)
41. Peterson EM, Zhong GM, Carlson E, de la Maza LM. Protective role of magnesium in the neutralization by antibodies of Chlamydia trachomatis infectivity. Infect. Immun. 56(4), 885-891 (1988).
42. Peeling RW, Kimani J, Plummer F et al. Antibody to chlamydial Hsp60 predicts an increased risk for chlamydial pelvic inflammatory disease. J. Infect. Dis. 175(5), 1153-1158 (1997).
43. Brunham RC, Peeling RW Chlamydia trachomatis antigens: role in immunity and pathogenesis. Infect. Agents Dis. 3(5), 218-233 (1994).
44. Kimani J, Maclean IW, Bwayo JJ et al. Risk factors for Chlamydia trachomatis pelvic inflammatory disease among sex workers in Nairobi, Kenya. J. Infect. Dis. 173(6), 1437-1444 (1996). (Pubitemid 26286804)
45. Sharma J, Zhong Y, Dong F, Piper JM, Wang G, Zhong G. Profiling of human antibody responses to Chlamydia trachomatis urogenital tract infection using microplates arrayed with 156 chlamydial fusion proteins. Infect. Immun. 74(3), 1490-1499 (2006). • Demonstration of the technique of identifying antigens recognized by infected patients through the use of genomics-based fusion protein production.
46. Williams DM, Grubbs BG, Kelly K, Pack E, Rank RG. Role of γ-δ T cells in murine Chlamydia trachomatis infection. Infect. Immun. 64(9), 3916-3919 (1996).
47. Tseng CT, Rank RG. Role of NK cells in early host response to chlamydial genital infection. Infect. Immun. 66(12), 5867-5875 (1998).
48. Holland MJ, Bailey RL, Conway DJ et al. T helper type-1 (Th1)/Th2 profiles of peripheral blood mononuclear cells (PBMC); responses to antigens of Chlamydia trachomatis in subjects with severe trachomatous scarring. Clin. Exp. Immunol. 105(3), 429-435 (1996).
49. Mabey DC, Holland MJ, Viswalingam ND et al. Lymphocyte proliferative responses to chlamydial antigens in human chlamydial eye infections. Clin. Exp. Immunol. 86(1), 37-42 (1991).
50. + CTLs specific for the major outer membrane protein of Chlamydia trachomatis in human genital tract infections. J. Immunol. 162(11), 6855-6866 (1999).
51. + T cell response. J. Immunol. 171(9), 4742-4749 (2003).
52. + Tcl responses that inhibit intracellular growth of this vacuolar pathogen. J. Immunol. 169(5), 2524-2535 (2002).
53. + T cell responses in humans. J. Immunol. 171(8), 4278-4286 (2003).
54. Morrison RP, Feilzer K, Tumas DB. Gene knockout mice establish a primary protective role for major histocompatibility complex class II-restricted responses in Chlamydia trachomatis genital tract infection. Infect. Immun. 63(12), 4661-4668 (1995).
55. Perry LL, Feilzer K, Hughes S, Caldwell HD. Clearance of Chlamydia trachomatis from the murine genital mucosa does not require perforin-mediated cytolysis or Fas-mediated apoptosis. Infect. Immun. 67(3), 1379-1385 (1999).
56. Perry LL, Feilzer K, Caldwell HD. Immunity to Chlamydia trachomatis is mediated by T helper 1 cells through IFN-γ-dependent and -independent pathways. J. Immunol. 158(7), 3344-3352 (1997). (Pubitemid 127484052)
57. Zhong GM, Peterson EM, Czarniecki CW, de la Maza LM. Recombinant murine γ interferon inhibits Chlamydia trachomatis serovar L1 in vivo. Infect. Immun. 56(1), 283-286 (1988).
58. Zhong GM, Peterson EM, Czarniecki CW, Schreiber RD, de la Maza LM. Role of endogenous γ interferon in host defense against Chlamydia trachomatis infections. Infect. Immun. 57(1), 152-157 (1989).
59. Kinnunen A, Paavonen J, Surcel HM. Heat shock protein 60 specific T-cell response in chlamydial infections. Scand. J. Immunol. 54(1-2), 76-81 (2001).
60. + T cells from humans infected with Chlamydia trachomatis. Clin. Exp. Immunol. 126(3), 488-493 (2001).
61. Gaston JS, Deane KH, Jecock RM, PearceJH. Identification of 2 Chlamydia trachomatis antigens recognized by synovial fluid T cells from patients with Chlamydia induced reactive arthritis. J. Rheumatol. 23(1), 130-136 (1996).
62. Caldwell HD, Kuo CC, Kenny GE. Antigenic analysis of Chlamydiae by two-dimensional immunoelectrophoresis. II. A trachoma-LGV-specific antigen. J. Immunol. 115(4), 969-975 (1975).
63. Sanchez-Campillo M, Bini L, Comanducci M et al. Identification of immunoreactive proteins of Chlamydia trachomatis by western blot analysis of a two-dimensional electrophoresis map with patient sera. Electrophoresis 20(11), 2269-2279 (1999). (Pubitemid 29413316)
64. Shaw AC, Gevaert K, Demol H et al. Comparative proteome analysis of Chlamydia trachomatis serovar A, D and L2. Proteomics 2(2), 164-186 (2002). (Pubitemid 34273086)
65. Wolf K, Fischer E, Mead D et al. Chlamydia pneumoniae major outer membrane protein is a surface-exposed antigen that elicits antibodies primarily directed against conformation-dependent determinants. Infect. Immun. 69(5), 3082-3091 (2001).
66. Bunk S, Susnea I, Rupp J et al. Immunoproteomic identification and serological responses to novel Chlamydia pneumoniae antigens that are associated with persistent C. pneumoniae infections. J. Immunol. 180(8), 5490-5498 (2008).
67. Shaw AC, Vandahl BB, Larsen MR et al. Characterization of a secreted Chlamydia protease. Cell Microbiol. 4(7), 411-424 (2002).
68. + T-cell antigen recognized in the context of chlamydial infection. It is also interesting that the protein identified was present at the inclusion membrane of infected cells.
69. + T cell epitopes in Chlamydia trachomatis infection through use of caged class I MHC tetramers. Proc. Natl Acad. Sci. USA 105(10), 3831-3836 (2008). •• Fascinating report describing the integration of contemporary cellular immunology and genomics technologies to identify otherwise uncharacterized antigens that are important in antichlamydial immune responses.
70. Karunakaran KP, Rey-Ladino J, Stoynov N et al. Immunoproteomic discovery of novel T cell antigens from the obligate intracellular pathogen Chlamydia. J. Immunol. 180(4), 2459-2465 (2008). •• Description of how peptides eluted from antigen-presenting cells can be used to identify important antigens recognized in the context of chlamydial infection.
71. Yu HH, Di Russo EG, Rounds MA, Tan M. Mutational analysis of the promoter recognized by Chlamydia and Escherichia coli σ (28) RNA polymerase. J. Bacteriol. 188(15), 5524-5531 (2006).
72. Kinnunen A, Molander P, Morrison R et al. Chlamydial heat shock protein 60-specific T cells in inflamed salpingeal tissue. Fertil. Steril. 77(1), 162-166 (2002).
73. Patton DL, Sweeney YT, Kuo CC. Demonstration of delayed hypersensitivity in Chlamydia trachomatis salpingitis in monkeys: a pathogenic mechanism of tubal damage. J. Infect. Dis. 169(3), 680-683 (1994).
74. Morrison RP, Lyng K, Caldwell HD. Chlamydial disease pathogenesis. Ocular hypersensitivity elicited by a genus-specific 57-kD protein. J. Exp. Med. 169(3), 663-675 (1989).
75. Hafner L, Beagley K, Timms, P. Chlamydia trachomatis infection: host immune responses and potential vaccines. Mucosal Immunol. 1(2), 116-130 (2008). •• Thorough presentation of antigens used in antichlamydial vaccine trials and their outcomes.
76. Pal S, Peterson EM, de la Maza LM. Vaccination with the Chlamydia trachomatis major outer membrane protein can elicit an immune response as protective as that resulting from inoculation with live bacteria. Infect. Immun. 73(12), 8153-8160 (2005).
77. Byrne GI, Stephens RS, Ada G et al. Workshop on in vitro neutralization of Chlamydia trachomatis: summary of proceedings. J. Infect. Dis. 168(2), 415-420 (1993).
78. Villeneuve A, Brossay L, Paradis G, Hebert J. Determination of neutralizing epitopes in variable domains I and IV of the major outer-membrane protein from Chlamydia trachomatis serovar K. Microbiology 140(Pt 9), 2481-2487 (1994). (Pubitemid 24297056)
79. Batteiger BE. The major outer membrane protein of a single Chlamydia trachomatis serovar can possess more than one serovar-specific epitope. Infect. Immun. 64(2), 542-547 (1996).
80. Fadel S, Eley A. Chlamydia trachomatis OmcB protein is a surface-exposed glycosaminoglycan-dependent adhesin. J. Med. Microbiol. 56(Pt 1), 15-22 (2007).
81. Kawa DE, Schachter J, Stephens RS. Immune response to the Chlamydia trachomatis outer membrane protein PorB. Vaccine 22(31-32), 4282-4286 (2004). (Pubitemid 39330351)
82. Macmillan L, Ifere GO, He Q et al. A recombinant multivalent combination vaccine protects against Chlamydia and genital herpes. FEMS Immunol. Med. Microbiol. 49(1), 46-55 (2007).
83. Crane DD, Carlson JH, Fischer ER et al. Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc. Natl Acad. Sci. USA 103(6), 1894-1899 (2006). • Demonstration that one of the polymorphic membrane proteins of the chlamydiae may be an important antigen, and that this protein may have novel functions on the surface of the bacterium.
84. + T lymphocytes by screening an expression library. Eur. J. Immunol. 31(5), 1513-1522 (2001).
85. Moelleken K, Hegemann JH. The Chlamydia outer membrane protein OmcB is required for adhesion and exhibits biovar-specific differences in glycosaminoglycan binding. Mol. Microbiol. 67(2), 403-419 (2008).
86. Stephens RS, Koshiyama K, Lewis E, Kubo A. Heparin-binding outer membrane protein of chlamydiae. Mol. Microbiol. 40(3), 691-699 (2001).
87. Ting LM, Hsia RC, Haidaris CG, Bavoil PM. Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect. Immun. 63(9), 3600-3608 (1995).
88. + T cells recognize the 60-kDa cysteine-rich outer membrane protein from Chlamydia trachomatis. J. Immunol. 173(11), 6905-6913 (2004). • Demonstration that a surface-exposed and highly conserved chlamydial elementary body protein may serve as an important antigen following chlamydial infection.
89. Frikha-Gargouri O, Gdoura R, Znazen A et al. Evaluation of an in silico predicted specific and immunogenic antigen from the OmcB protein for the serodiagnosis of Chlamydia trachomatis infections. BMC Microbiol. 8, 217 (2008).
90. Swanson KA, Taylor LD, Frank SD et al. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect. Immun. 77(1), 508-516 (2009).
91. Kiselev AO, Stamm WE, Yates JR, Lampe MF. Expression, processing, and localization of PmpD of Chlamydia trachomatis serovar L2 during the chlamydial developmental cycle. PLoS ONE 2(6), e568 (2007).
92. Wehrl W, Brinkmann V, Jungblut PR, Meyer TF, Szczepek, AJ. From the inside out - processing of the chlamydial autotransporter PmpD and its role in bacterial adhesion and activation of human host cells. Mol. Microbiol. 51(2), 319-334 (2004).
93. Murdin AD, Dunn P, Sodoyer R et al. Use of a mouse lung challenge model to identify antigens protective against Chlamydia pneumoniae lung infection. J. Infect. Dis. 181(Suppl. 3), S544-S551 (2000).
94. Stemke-Hale K, Kaltenboeck B, DeGraves FJ et al. Screening the whole genome of a pathogen in vivo for individual protective antigens. Vaccine 23(23), 3016-3025 (2005). • A DNA vaccine approach using a library of the Chlamydia abortus genome to identify candidate antigens that may be protective. (Pubitemid 40462441)
95. Fields KA, Hackstadt T. Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol. Microbiol. 38(5), 1048-1060 (2000).
96. Huang J, Lesser CF, Lory S. The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456(7218), 112-115 (2008).
97. Tammiruusu A, Penttila T, Lahesmaa R, Sarvas M, Puolakkainen M, Vuola JM. Intranasal administration of chlamydial outer protein N (CopN) induces protection against pulmonary Chlamydia pneumoniae infection in a mouse model. Vaccine 25(2), 283-290 (2007). • Demonstration that a conserved chlamydial protein administered via the intranasal route in the presence of a powerful mucosal adjuvant may be useful for protection of hosts against Chlamydia pneumoniae. (Pubitemid 44856072)
98. Thomas NS, Lusher M, Storey CC, Clarke IN. Plasmid diversity in Chlamydia. Microbiology 143(Pt 6), 1847-1854 (1997).
99. Li Z, Chen D, Zhong Y, Wang S, Zhong G. The chlamydial plasmid-encoded protein pgp3 is secreted into the cytosol of Chlamydia-infected cells. Infect. Immun. 76(8), 3415-3428 (2008). • Demonstrates that the chlamydial plasmid encodes a protein secreted to the host cytosol that may be important in chlamydial disease pathogenesis.
100. Li Z, Zhong Y, Lei L, Wu Y, Wang S, Zhong G. Antibodies from women urogenitally infected with C. trachomatis predominantly recognized the plasmid protein pgp3 in a conformation-dependent manner. BMCMicrobiol. 8, 90 (2008). (Pubitemid 351862252)
101. Ghaem-Maghami S, Ratti G, Ghaem-Maghami M et al. Mucosal and systemic immune responses to plasmid protein pgp3 in patients with genital and ocular Chlamydia trachomatis infection. Clin. Exp. Immunol. 132(3), 436-442 (2003).
102. Bas S, Genevay S, Schenkel MC, Vischer TL. Importance of species-specific antigens in the serodiagnosis of Chlamydia trachomatis reactive arthritis. Rheumatology (Oxford) 41(9), 1017-1020 (2002). (Pubitemid 35049931)
103. Donati M, Laroucau K, Storni E et al. Serological response to pgp3 protein in animal and human chlamydial infections. Vet. Microbiol. 135, 181-185 (2008).
104. Donati M, Sambri V, Comanducci M et al. DNA immunization withpgp3 gene of Chlamydia trachomatis inhibits the spread of chlamydial infection from the lower to the upper genital tract in C3H/HeN mice. Vaccine 21(11-12), 1089-1093 (2003). • This and the following reference demonstrate that the plasmid-encoded protein Pgp3 may be important in protection against chlamydial disease. (Pubitemid 36142050)
105. Li Z, Wang S, Wu Y, Zhong G, Chen D. Immunization with chlamydial plasmid protein pORF5 DNA vaccine induces protective immunity against genital chlamydial infection in mice. Sci. China C Life Sci. 51(11), 973-980 (2008). • This and the above reference demonstrate that the plasmid-encoded protein Pgp3 may be important in protection against chlamydial disease.
106. Farencena A, Comanducci M, Donati M, Ratti G, Cevenini R. Characterization of a new isolate of Chlamydia trachomatis which lacks the common plasmid and has properties of biovar trachoma. Infect. Immun. 65(7), 2965-2969 (1997).
107. Ripa T, Nilsson PA. A Chlamydia trachomatis strain with a 377-bp deletion in the cryptic plasmid causing false-negative nucleic acid amplification tests. Sex. Transm. Dis. 34(5), 255-256 (2007).
108. Magbanua JP, Goh BT, Michel CE et al. Chlamydia trachomatis variant not detected by plasmid based nucleic acid amplification tests: molecular characterisation and failure of single dose azithromycin. Sex. Transm. Infect. 83(4), 339-343 (2007).
109. Stothard DR, Williams JA, Van Der Pol B, Jones RB. Identification of a Chlamydia trachomatis serovar E urogenital isolate which lacks the cryptic plasmid. Infect. Immun. 66(12), 6010-6013 (1998).
110. O'Connell CM, Ingalls RR, Andrews CW Jr, Scurlock AM, Darville T. Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease. J. Immunol. 179(6), 4027-4034 (2007). • Discusses the possible role of chlamydial plasmid-encoded proteins in chlamydial biology and disease. This manuscript also discusses the possibility that plasmid-deficient strains may be useful vaccines.
111. Zhong G, Fan P, Ji H, Dong F, Huang Y. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J. Exp. Med. 193(8), 935-942 (2001). •• First example of a chlamydial protein secreted to the cytosol of infected cells, and the beginning of an important line of investigation for chlamydial biology and immunology.
112. Zhong G, Fan T, Liu L. Chlamydia inhibits interferon γ-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J. Exp. Med. 189(12), 1931-1938 (1999).
113. Zhong G, Liu L, Fan T, Fan P, Ji H. Degradation of transcription factor RFX5 during the inhibition of both constitutive and interferon γ-inducible major histocompatibility complex class I expression in chlamydia-infected cells. J. Exp. Med. 191(9), 1525-1534 (2000).
114. Huang Z, Feng Y, Chen D et al. Structural basis for activation and inhibition of the secreted Chlamydia protease CPAF. Cell Host Microbe 4(6), 529-542 (2008). (Pubitemid 352762954)
115. Pirbhai M, Dong F, Zhong Y, Pan KZ, Zhong G. The secreted protease factor CPAF is responsible for degrading. pro-apoptotic BH3-only proteins in Chlamydia trachomatis-infected cells. J. Biol. Chem. 281(42), 31495-31501 (2006).
116. Dong F, Pirbhai M, Xiao Y, Zhong Y, Wu Y, Zhong G. Degradation of the proapoptotic proteins Bik, Puma, and Bim with Bcl-2 domain 3 homology in Chlamydia trachomatis-infected cells. Infect. Immun. 73(3), 1861-1864 (2005).
117. Dong F, Su H, Huang Y, Zhong Y, Zhong G. Cleavage of host keratin 8 by a Chlamydia-secteted protease. Infect. Immun. 72(7), 3863-3868 (2004).
118. Sharma J, Bosnic AM, Piper JM, Zhong G. Human antibody responses to a Chlamydia-secteted protease factor. Infect. Immun. 72(12), 7164-7171 (2004).
119. Sharma J, Dong F, Pirbhai M, Zhong G. Inhibition of proteolytic activity of a chlamydial proteasome/protease-like activity factor by antibodies from humans infected with Chlamydia trachomatis. Infect. Immun. 73(7), 4414-4419 (2005).
120. Murthy AK, Chambers JP, Meier PA, Zhong G, Arulanandam BP. Intranasal vaccination with a secreted chlamydial protein enhances resolution of genital Chlamydia muridarum infection, protects against oviduct pathology, and is highly dependent upon endogenous γ interferon production. Infect. Immun. 75(2), 666-676 (2007).
121. Murthy AK, Cong Y, Murphey C et al. Chlamydial protease-like activity factor induces protective immunity against genital chlamydial infection in transgenic mice that express the human HLA-DR4 allele. Infect. Immun. 74(12), 6722-6729 (2006). •• This and the associated manuscripts demonstrate that chlamydia-secreted protease factor is a potent immunogen that can be used to protect mice from chlamydial infection.
122. + T cells. Cell. Immunol. 242(2), 110-117 (2006). (Pubitemid 46496973)
123. + T cells produce sufficient IFN-γ to mediate robust protective immunity against genital Chlamydia muridarum infection. J. Immunol. 180(5), 3375-3382 (2008).
124. Rockey DD, Heinzen RA, Hackstadt T. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol. Microbiol. 15(4), 617-626 (1995).
125. Bannantine JP, Stamm WE, Suchland RJ, Rockey DD. Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates. Infect. Immun. 66(12), 6017-6021 (1998). • Demonstration that inclusion membrane proteins are produced by human pathogenic chlamydiae, and that humans generate potent antibody responses to chlamydial inclusion membrane proteins.
126. Rockey DD, Scidmore MA, Bannantine JP, Brown WJ. Proteins in the chlamydial inclusion membrane. Microbes Infect. 4(3), 333-340 (2002).
127. Chen C, Chen D, Sharma J et al. The hypothetical protein CT813 is localized in the Chlamydia trachomatis inclusion membrane and is immunogenic in women urogenitally infected with C. trachomatis. Infect. Immun. 74(8), 4826-4840 (2006).
128. Luo J, Liu G, Zhong Y et al. Characterization of hypothetical proteins Cpn0146, 0147, 0284 & 0285 that are predicted to be in the Chlamydia pneumoniae inclusion membrane. BMCMicrobiol. 7, 38 (2007).
129. Dong F, Flores R, Chen D et al. Localization of the hypothetical protein Cpn0797 in the cytoplasm of Chlamydia pneumoniae-infected host cells. Infect. Immun. 74(11), 6479-6486 (2006).
130. Flores R, Luo J, Chen D et al. Characterization of the hypothetical protein Cpn1027, a newly identified inclusion membrane protein unique to Chlamydia pneumoniae. Microbiology 153(Pt 3), 777-786 (2007). (Pubitemid 46444375)
131. Luo J, Jia T, Flores R, Chen D, Zhong G. Hypothetical protein Cpn0308 is localized in the Chlamydia pneumoniae inclusion membrane. Infect. Immun. 75(1), 497-503 (2007).
132. Luo J, Jia T, Zhong Y, Chen D, Flores R, Zhong G. Localization of the hypothetical protein Cpn0585 in the inclusion membrane of Chlamydia pneumoniae-infected cells. Microb. Pathog. 42(2-3), 111-116 (2007).
133. Scidmore-Carlson MA, Shaw EI, Dooley CA, Fischer ER, Hackstadt T. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol. Microbiol. 33(4), 753-765 (1999).
134. Li Z, Chen C, Chen D, Wu Y, Zhong Y, Zhong G. Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect. Immun. 76(6), 2746-2757 (2008). • One of several papers by this group clearly demonstrating that inclusion membrane proteins are important immunogens in human patients.
135. Scidmore MA, Hackstadt T. Mammalian 14-13-3β associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol. Microbiol. 39(6), 1638-1650 (2001).
136. Brumell JH, Scidmore MA. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71(4), 636-652 (2007).
137. Cortes C, Rzomp KA, Tvinnereim A, Scidmore MA, Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect. Immun. 75(12), 5586-5596 (2007).
138. Moorhead AR, Rzomp KA, Scidmore MA. The Rab6 effector Bicaudal D1 associates with Chlamydia trachomatis inclusions in a biovar-specific manner. Infect. Immun. 75(2), 781-791 (2007).
139. Delevoye C, Nilges M, Dautry-Varsat A, Subtil A. Conservation of the biochemical properties of IncA from Chlamydh trachomatis and Chlamydia caviae: oligomerization of IncA mediates interaction between facing membranes. J. Biol. Chem. 279(45), 46896-46906 (2004).
140. Alzhanov D, Barnes J, Hruby DE, Rockey DD. Chlamydial development is blocked in host cells transfected with Chlamydophila caviae incA. BMC Microbiol. 4, 24 (2004). (Pubitemid 39319740)
141. Brown WJ, Skeiky YA, Probst P, Rockey DD. Chlamydial antigens colocalize within IncA-laden fibers extending from the inclusion membrane into the host cytosol. Infect. Immun. 70(10), 5860-5864 (2002).
142. Bannantine JP, Rockey DD, Hackstadt T. Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane. Mol. Microbiol. 28(5), 1017-1026 (1998).
143. Rockey DD, Grosenbach D, Hruby DE, Peacock MG, Heinzen RA, Hackstadt T. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol. Microbiol. 24(1), 217-228 (1997).
144. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell. Microbiol. 1(2), 119-130 (1999).
145. + cells can be protective in animal models of C. pneumoniae infection. (Pubitemid 40593216)
146. + T cell-independent. J. Immunol. 179(6), 3947-3957 (2007).
147. Li W, Guentzel MN, Seshu J, Zhong G, Murthy AK, Arulanandam BP. Induction
148. Brade L, Schramek S, Schade U, Brade H. Chemical, biological, and immunochemical properties of the Chlamydia psittaci lipopolysaccharide. Infect. Immun. 54(2), 568-574 (1986).
149. Taylor HR, Prendergast RA. Attempted oral immunization with chlamydial lipopolysaccharide subunit vaccine. Invest. Ophthalmol. Vis. Sci. 28(10), 1722-1726 (1987).
150. Stuart ES, Wyrick PB, Choong J, Stoler SB, MacDonald AB. Examination of chlamydial glycolipid with monoclonal antibodies: cellular distribution and epitope binding. Immunology 74(4), 740-747 (1991).
151. Whittum-Hudson JA, An LL, Saltzman WM, Prendergast RA, MacDonald AB. Oral immunization with an anti-idiotypic antibody to the exoglycolipid antigen protects against experimental Chlamydia trachomatis infection. Nat. Med. 2(10), 1116-1121 (1996).
152. Whittum-Hudson JA, Rudy D, Gerard H et al. The anti-idiotypic antibody to chlamydial glycolipid exoantigen (GLXA) protects mice against genital infection with a human biovar of Chlamydia trachomatis. Vaccine 19(28-29), 4061-4071 (2001). (Pubitemid 32566332)
153. Jones GE, Jones KA, Machell J, Brebner J, Anderson E, How S. Efficacy trials with tissue-culture grown, inactivated vaccines against chlamydial abortion in sheep. Vaccine 13(8), 715-723 (1995).
154. Igietseme JU, Murdin A. Induction of protective immunity against Chlamydia trachomatis genital infection by a vaccine based on major outer membrane protein-lipophilic immune response-stimulating complexes. Infect. Immun. 68(12), 6798-6806 (2000).
155. Dong-Ji Z, Yang X, Shen C, Lu H, Murdin A, Brunham RC. Priming with Chlamydia trachomatis major outer membrane protein (MOMP) DNA followed by MOMP ISCOM boosting enhances protection and is associated with increased immunoglobulin A and Th1 cellular immune responses. Infect. Immun. 68(6), 3074-3078 (2000).
156. Pal S, Peterson EM, Rappuoli R, Ratti G, de la Maza LM. Immunization with the Chlamydh trachomatis major outer membrane protein, using adjuvants developed for human vaccines, can induce partial protection in a mouse model against a genital challenge. Vaccine 24(6), 766-775 (2006). (Pubitemid 43190083)
157. He Q, Martinez-Sobrido L, Eko FO et al. Live-attenuated influenza viruses as delivery vectors for Chlamydia vaccines. Immunology 122(1), 28-37 (2007). • Exploration of the utility of a library-based recombinant approach to create live virus vectors of candidate chlamydial vaccines. (Pubitemid 47222592)
158. Murdin AD, Su H, Klein MH, Caldwell HD. Poliovirus hybrids expressing neutralization epitopes from variable domains I and IV of the major outer membrane protein of Chlamydia trachomatis elicit broadly cross-reactive C. trachomatis-neutralizing antibodies. Infect. Immun. 63(3), 1116-1121 (1995).
159. Hansen J, Jensen KT, Follmann F, Agger EM, Theisen M, Andersen P. Liposome delivery of Chlamydia muridarum major outer membrane protein primes a Th1 response that protects against genital chlamydial infection in a mouse model. J. Infect. Dis. 198(5), 758-767 (2008). • Important demonstration that a combination of novel delivery mechanisms or adjuvants with known chlamydial immunogens may be critical for the development of a protective and useful antichlamydial vaccine for humans.
160. Champion CI, Kickhoefer VA, Liu G et al. A vault nanoparticle vaccine induces protective mucosal immunity. PLoS ONE 4(4), e5409 (2009). •• Exciting manuscript describing the use of a highly unusual recombinant vaccine for delivery of known chlamydial antigens, leading to protection from infection.
161. Gondek DC, Roan NR, Starnbach MN. T cell responses in the absence of IFN-γ exacerbate uterine infection with Chlamydia trachomatis. J. Immunol. 183(2), 1313-1319 (2009).