2,459
Views
52
CrossRef citations to date
0
Altmetric
Review

Chlamydial polymorphic membrane proteins: regulation, function and potential vaccine candidates

, , &
Pages 11-22 | Received 17 Jul 2015, Accepted 17 Oct 2015, Published online: 31 Dec 2015

References

  • Everett KD. Chlamydia and Chlamydiales: more than meets the eye. Vet Microbiol 2000; 75:109–26; PMID:10889402; http://dx.doi.org/10.1016/S0378-1135(00)00213-3
  • Sachse K, Laroucau K, Riege K, Wehner S, Dilcher M, Creasy HH, Weidmann M, Myers G, Vorimore F, Vicari N, et al. Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacea sp. nov. Syst Appl Microbiol 2014; 37:79–88; PMID:24461712; http://dx.doi.org/10.1016/j.syapm.2013.12.004
  • Wheelhouse N, Longbottom D. Endemic and emerging chlamydial infections of animals and their zoonotic implications. Transbound Emerg Dis 2012; 59:283–91; PMID:22099945; http://dx.doi.org/10.1111/j.1865-1682.2011.01274.x
  • Baud D, Goy G, Jaton K, Osterheld MC, Blumer S, Borel N, Vial Y, Hohlfeld P, Pospischil A, Greub G. Role of Chlamydia trachomatis in miscarriage. Emerg Infect Dis 2011; 17:1630–5; PMID:21888787; http://dx.doi.org/10.3201/eid1709.100865
  • Baud D, Goy G, Vasilevsky S, Osterheld MC, Roth-Kleiner M, Croxatto A, Greub G. Roles of bovine Waddlia chondrophila and Chlamydia trachomatis in human preterm birth. New Microbes New Infect 2015; 3:41–5; PMID:25755892; http://dx.doi.org/10.1016/j.nmni.2014.11.004
  • Baud D, Greub G. Intracellular bacteria and adverse pregnancy outcomes. Clin Microbiol Infect 2011; 17:1312–22; PMID:21884294; http://dx.doi.org/10.1111/j.1469-0691.2011.03604.x
  • Baud D, Regan L, Greub G. Emerging role of Chlamydia and Chlamydia-like organisms in adverse pregnancy outcomes. Curr Opin Infect Dis 2008; 21:70–6; PMID:18192789; http://dx.doi.org/10.1097/QCO.0b013e3282f3e6a5
  • Hornung S, Thuong BC, Gyger J, Kebbi-Beghdadi C, Vasilevsky S, Greub G, Baud D. Role of Chlamydia trachomatis and emerging Chlamydia-related bacteria in ectopic pregnancy in Vietnam. Epidemiol Infect 2015; (12):2635–8; http://dx.doi.org/10.1017/S0950268814003616
  • Karaer A, Mert I, Cavkaytar S, Batioglu S. Serological investigation of the role of selected sexually transmitted infections in the aetiology of ectopic pregnancy. Eur J Contracept Reprod Health Care 2013; 18:68–74; PMID:23256948; http://dx.doi.org/10.3109/13625187.2012.744818
  • Kavanagh K, Wallace LA, Robertson C, Wilson P, Scoular A. Estimation of the risk of tubal factor infertility associated with genital chlamydial infection in women: a statistical modelling study. Int J Epidemiol 2013; 42:493–503; PMID:23505256; http://dx.doi.org/10.1093/ije/dyt011
  • Vasilevsky S, Greub G, Nardelli-Haefliger D, Baud D. Genital Chlamydia trachomatis: understanding the roles of innate and adaptive immunity in vaccine research. Clin Microbiol Rev 2014; 27:346–70; PMID:24696438; http://dx.doi.org/10.1128/CMR.00105-13
  • World Health Organization. Global incidence and prevalence of selected curable sexually transmitted infections. 2008
  • Burton MJ, Mabey DC. The global burden of trachoma: a review. PLoS Negl Trop Dis 2009; 3:e460; PMID:19859534; http://dx.doi.org/10.1371/journal.pntd.0000460
  • Hu VH, Holland MJ, Burton MJ. Trachoma: protective and pathogenic ocular immune responses to Chlamydia trachomatis. PLoS Negl Trop Dis 2013; 7:e2020; PMID:23457650; http://dx.doi.org/10.1371/journal.pntd.0002020
  • Wyrick PB. Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis 2010; 201 Suppl 2:S88–95; PMID:20470046; http://dx.doi.org/10.1086/652394
  • Fadel S, Eley A. Chlamydia trachomatis OmcB protein is a surface-exposed glycosaminoglycan-dependent adhesin. J Med Microbiol 2007; 56:15–22; PMID:17172511; http://dx.doi.org/10.1099/jmm.0.46801-0
  • Tan C, Hsia RC, Shou H, Carrasco JA, Rank RG, Bavoil PM. Variable expression of surface-exposed polymorphic membrane proteins in in vitro-grown Chlamydia trachomatis. Cell Microbiol 2010; 12:174–87; PMID:19811502; http://dx.doi.org/10.1111/j.1462-5822.2009.01389.x
  • Longbottom D, Russell M, Dunbar SM, Jones GE, Herring AJ. Molecular cloning and characterization of the genes coding for the highly immunogenic cluster of 90-kgdalton envelope proteins from the Chlamydia psittaci subtype that causes abortion in sheep. Infect Immun 1998; 66:1317–24; PMID:9529048
  • Longbottom D, Russell M, Jones GE, Lainson FA, Herring AJ. Identification of a multigene family coding for the 90 kDa proteins of the ovine abortion subtype of Chlamydia psittaci. FEMS Microbiol Lett 1996; 142:277–81; PMID:8810511; http://dx.doi.org/10.1111/j.1574-6968.1996.tb08443.x
  • Azuma Y, Hirakawa H, Yamashita A, Cai Y, Rahman MA, Suzuki H, Mitaku S, Toh H, Goto S, Murakami T, et al. Genome sequence of the cat pathogen, Chlamydophila felis. DNA Res 2006; 13:15–23; PMID:16766509; http://dx.doi.org/10.1093/dnares/dsi027
  • Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K, et al. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 2000; 28:1397–406; PMID:10684935; http://dx.doi.org/10.1093/nar/28.6.1397
  • Read TD, Myers GS, Brunham RC, Nelson WC, Paulsen IT, Heidelberg J, Holtzapple E, Khouri H, Federova NB, Carty HA, et al. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res 2003; 31:2134–47; PMID:12682364; http://dx.doi.org/10.1093/nar/gkg321
  • Thomson NR, Yeats C, Bell K, Holden MT, Bentley SD, Livingstone M, Cerdeño-Tárraga AM, Harris B, Doggett J, Ormond D, et al. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res 2005; 15:629–40; PMID:15837807; http://dx.doi.org/10.1101/gr.3684805
  • Voigt A, Schofl G, Saluz HP. The Chlamydia psittaci genome: a comparative analysis of intracellular pathogens. PLoS One 2012; 7:e35097; PMID:22506068; http://dx.doi.org/10.1371/journal.pone.0035097
  • Bachmann NL, Fraser TA, Bertelli C, Jelocnik M, Gillett A, Funnell O, Flanagan C, Myers GS, Timms P, Polkinghorne A. Comparative genomics of koala, cattle and sheep strains of Chlamydia pecorum. BMC Genomics 2014; 15:667; PMID:25106440; http://dx.doi.org/10.1186/1471-2164-15-667
  • Kalman S, Mitchell W, Marathe R, Lammel C, Fan J, Hyman RW, Olinger L, Grimwood J, Davis RW, Stephens RS. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat Genet 1999; 21:385–9; PMID:10192388; http://dx.doi.org/10.1038/7716
  • Voigt A, Schofl G, Heidrich A, Sachse K, Saluz HP. Full-length de novo sequence of the Chlamydophila psittaci type strain, 6BC. J Bacteriol 2011; 193:2662–3; PMID:21441521; http://dx.doi.org/10.1128/JB.00236-11
  • Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, et al. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 1998; 282:754–9; PMID:9784136; http://dx.doi.org/10.1126/science.282.5389.754
  • Carlson JH, Porcella SF, McClarty G, Caldwell HD. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect Immun 2005; 73:6407–18; PMID:16177312; http://dx.doi.org/10.1128/IAI.73.10.6407-6418.2005
  • Kebbi-Beghdadi C, Domröse A, Becker E, Cisse OH, Hegemann JH, Greub G. OmpA family proteins and Pmp-like autotransporter: new adhesins of Waddlia chondrophila. Pathog Dis 2015; 73(6):ftv035; In Press; http://dx.doi.org/10.1093/femspd/ftv035
  • 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 2007; 2:e568; PMID:17593967; http://dx.doi.org/10.1371/journal.pone.0000568
  • Vandahl BB, Pedersen AS, Gevaert K, Holm A, Vandekerckhove J, Christiansen G, Birkelund S. The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. BMC Microbiol 2002; 2:36; PMID:12453305; http://dx.doi.org/10.1186/1471-2180-2-36
  • 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 2004; 51:319–34; PMID:14756775; http://dx.doi.org/10.1046/j.1365-2958.2003.03838.x
  • Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004; 68:692–744; PMID:15590781; http://dx.doi.org/10.1128/MMBR.68.4.692-744.2004
  • Dautin N, Barnard TJ, Anderson DE, Bernstein HD. Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J 2007; 26:1942–52; PMID:17347646; http://dx.doi.org/10.1038/sj.emboj.7601638
  • Dautin N, Bernstein HD. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 2007; 61:89–112; PMID:17506669; http://dx.doi.org/10.1146/annurev.micro.61.080706.093233
  • Henderson IR, Lam AC. Polymorphic proteins of Chlamydia spp. - autotransporters beyond the Proteobacteria. Trends Microbiol 2001; 9:573–8; PMID:11728862; http://dx.doi.org/10.1016/S0966-842X(01)02234-X
  • Henderson IR, Nataro JP. Virulence functions of autotransporter proteins. Infect Immun 2001; 69:1231–43; PMID:11179284; http://dx.doi.org/10.1128/IAI.69.3.1231-1243.2001
  • Leyton DL, Rossiter AE, Henderson IR. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 2012; 10:213–25; PMID:22337167; http://dx.doi.org/10.1038/nrmicro2733
  • Tseng TT, Tyler BM, Setubal JC. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 2009; 9 Suppl 1:S2; PMID:19278550; http://dx.doi.org/10.1186/1471-2180-9-S1-S2
  • Rockey DD, Lenart J, Stephens RS. Genome sequencing and our understanding of chlamydiae. Infect Immun 2000; 68:5473–9; PMID:10992442; http://dx.doi.org/10.1128/IAI.68.10.5473-5479.2000
  • Grimwood J, Stephens RS. Computational analysis of the polymorphic membrane protein superfamily of Chlamydia trachomatis and Chlamydia pneumoniae. Microb Comp Genomics 1999; 4:187–201; PMID:10587946; http://dx.doi.org/10.1089/omi.1.1999.4.187
  • Grimwood J, Olinger L, Stephens RS. Expression of Chlamydia pneumoniae polymorphic membrane protein family genes. Infect Immun 2001; 69:2383–9; PMID:11254597; http://dx.doi.org/10.1128/IAI.69.4.2383-2389.2001
  • Vandahl BB, Birkelund S, Demol H, Hoorelbeke B, Christiansen G, Vandekerckhove J, Gevaert K. Proteome analysis of the Chlamydia pneumoniae elementary body. Electrophoresis 2001; 22:1204–23; PMID:11358148; http://dx.doi.org/10.1002/1522-2683()22:6%3c1204::AID-ELPS1204%3e3.0.CO;2-M
  • Christiansen G, Pedersen AS, Hjerno K, Vandahl B, Birkelund S. Potential relevance of Chlamydia pneumoniae surface proteins to an effective vaccine. J Infect Dis 2000; 181 Suppl 3:S528–37; PMID:10839754; http://dx.doi.org/10.1086/315633
  • Goodall JC, Yeo G, Huang M, Raggiaschi R, Gaston JS. Identification of Chlamydia trachomatis antigens recognized by human CD4+ T lymphocytes by screening an expression library. Eur J Immunol 2001; 31:1513–22; PMID:11465108; http://dx.doi.org/10.1002/1521-4141(200105)31:5%3c1513::AID-IMMU1513%3e3.0.CO;2-U
  • Crane DD, Carlson JH, Fischer ER, Bavoil P, Hsia RC, Tan C, Kuo CC, Caldwell HD. Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc Natl Acad Sci U S A 2006; 103:1894–9; PMID:16446444; http://dx.doi.org/10.1073/pnas.0508983103
  • Tan C, Hsia RC, Shou H, Haggerty CL, Ness RB, Gaydos CA, Dean D, Scurlock AM, Wilson DP, Bavoil PM. Chlamydia trachomatis-infected patients display variable antibody profiles against the nine-member polymorphic membrane protein family. Infect Immun 2009; 77:3218–26; PMID:19487469; http://dx.doi.org/10.1128/IAI.01566-08
  • Gomes JP, Nunes A, Bruno WJ, Borrego MJ, Florindo C, Dean D. Polymorphisms in the nine polymorphic membrane proteins of Chlamydia trachomatis across all serovars: evidence for serovar Da recombination and correlation with tissue tropism. J Bacteriol 2006; 188:275–86; PMID:16352844; http://dx.doi.org/10.1128/JB.188.1.275-286.2006
  • Mygind P, Christiansen G, Persson K, Birkelund S. Detection of Chlamydia trachomatis-specific antibodies in human sera by recombinant major outer-membrane protein polyantigens. J Med Microbiol 2000; 49:457–65; PMID:10798559; http://dx.doi.org/10.1099/0022-1317-49-5-457
  • Shaw AC, Gevaert K, Demol H, Hoorelbeke B, Vandekerckhove J, Larsen MR, Roepstorff P, Holm A, Christiansen G, Birkelund S. Comparative proteome analysis of Chlamydia trachomatis serovar A, D and L2. Proteomics 2002; 2:164–86; PMID:11840563; http://dx.doi.org/10.1002/1615-9861(200202)2:2%3c164::AID-PROT164%3e3.0.CO;2-U
  • Tanzer RJ, Hatch TP. Characterization of outer membrane proteins in Chlamydia trachomatis LGV serovar L2. J Bacteriol 2001; 183:2686–90; PMID:11274132; http://dx.doi.org/10.1128/JB.183.8.2686-2690.2001
  • Skipp P, Robinson J, O'Connor CD, Clarke IN. Shotgun proteomic analysis of Chlamydia trachomatis. Proteomics 2005; 5:1558–73; PMID:15838905; http://dx.doi.org/10.1002/pmic.200401044
  • Carrasco JA, Tan C, Rank RG, Hsia RC, Bavoil PM. Altered developmental expression of polymorphic membrane proteins in penicillin-stressed Chlamydia trachomatis. Cell Microbiol 2011; 13:1014–25; PMID:21504531; http://dx.doi.org/10.1111/j.1462-5822.2011.01598.x
  • Nunes A, Gomes JP, Mead S, Florindo C, Correia H, Borrego MJ, Dean D. Comparative expression profiling of the Chlamydia trachomatis pmp gene family for clinical and reference strains. PLoS One 2007; 2:e878; PMID:17849007; http://dx.doi.org/10.1371/journal.pone.0000878
  • Barbour AG, Amano K, Hackstadt T, Perry L, Caldwell HD. Chlamydia trachomatis has penicillin-binding proteins but not detectable muramic acid. J Bacteriol 1982; 151:420–8; PMID:7085567
  • Lee CK, Bowie WR, Alexander ER. In vitro assays of the efficacy of antimicrobial agents in controlling Chlamydia trachomatis propagation. Antimicrob Agents Chemother 1978; 13:441–5; PMID:162541; http://dx.doi.org/10.1128/AAC.13.3.441
  • Swanson KA, Taylor LD, Frank SD, Sturdevant GL, Fischer ER, Carlson JH, Whitmire WM, Caldwell HD. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect Immun 2009; 77:508–16; PMID:19001072; http://dx.doi.org/10.1128/IAI.01173-08
  • Becker E, Hegemann JH. All subtypes of the Pmp adhesin family are implicated in chlamydial virulence and show species-specific function. Microbiologyopen 2014; 3:544–56; PMID:24985494; http://dx.doi.org/10.1002/mbo3.186
  • Molleken K, Schmidt E, Hegemann JH. Members of the Pmp protein family of Chlamydia pneumoniae mediate adhesion to human cells via short repetitive peptide motifs. Mol Microbiol 2010; 78:1004–17; PMID:21062373; http://dx.doi.org/10.1111/j.1365-2958.2010.07386.x
  • Finco O, Bonci A, Agnusdei M, Scarselli M, Petracca R, Norais N, Ferrari G, Garaguso I, Donati M, Sambri V, et al. Identification of new potential vaccine candidates against Chlamydia pneumoniae by multiple screenings. Vaccine 2005; 23:1178–88; PMID:15629361; http://dx.doi.org/10.1016/j.vaccine.2004.07.045
  • Girard V, Mourez M. Adhesion mediated by autotransporters of Gram-negative bacteria: structural and functional features. Res Microbiol 2006; 157:407–16; PMID:16725315; http://dx.doi.org/10.1016/j.resmic.2006.02.001
  • Molleken K, Becker E, Hegemann JH. The Chlamydia pneumoniae invasin protein Pmp21 recruits the EGF receptor for host cell entry. PLoS Pathog 2013; 9:e1003325; PMID:23633955; http://dx.doi.org/10.1371/journal.ppat.1003325
  • Su H, Watkins NG, Zhang YX, Caldwell HD. Chlamydia trachomatis-host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect Immun 1990; 58:1017–25; PMID:2318528
  • Kari L, Southern TR, Downey CJ, Watkins HS, Randall LB, Taylor LD, Sturdevant GL, Whitmire WM, Caldwell HD. Chlamydia trachomatis polymorphic membrane protein D is a virulence factor involved in early host-cell interactions. Infect Immun 2014; 82:2756–62; PMID:24733093; http://dx.doi.org/10.1128/IAI.01686-14
  • Taylor BD, Darville T, Tan C, Bavoil PM, Ness RB, Haggerty CL. The role of Chlamydia trachomatis polymorphic membrane proteins in inflammation and sequelae among women with pelvic inflammatory disease. Infect Dis Obstet Gynecol 2011; 2011:989762; PMID:22028586; http://dx.doi.org/10.1155/2011/989762
  • Gomes JP, Hsia RC, Mead S, Borrego MJ, Dean D. Immunoreactivity and differential developmental expression of known and putative Chlamydia trachomatis membrane proteins for biologically variant serovars representing distinct disease groups. Microbes Infect 2005; 7:410–20; PMID:15784185; http://dx.doi.org/10.1016/j.micinf.2004.11.014
  • Niessner A, Kaun C, Zorn G, Speidl W, Turel Z, Christiansen G, Pedersen AS, Birkelund S, Simon S, Georgopoulos A, et al. Polymorphic membrane protein (PMP) 20 and PMP 21 of Chlamydia pneumoniae induce proinflammatory mediators in human endothelial cells in vitro by activation of the nuclear factor-kappaB pathway. J Infect Dis 2003; 188:108–13; PMID:12825178; http://dx.doi.org/10.1086/375827
  • Grayston JT, Woolridge RL, Wang SP, Yen CH, Yang CY, Cheng KH, Chang IH. Field studies of protection from infection by experimental trachoma virus vaccine in preschool-aged children on Taiwan. Proc Soc Exp Biol Med 1963; 112:589–95; PMID:13950005; http://dx.doi.org/10.3181/00379727-112-28112
  • Sowa S, Sowa J, Collier LH, Blyth WA. Trachoma vaccine field trials in The Gambia. J Hyg 1969; 67:699–717; PMID:5261212; http://dx.doi.org/10.1017/S0022172400042157
  • Detmer A, Glenting J. Live bacterial vaccines - a review and identification of potential hazards. Microb Cell Fact 2006; 5:23; PMID:16796731; http://dx.doi.org/10.1186/1475-2859-5-23
  • Brunham RC, Rey-Ladino J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol 2005; 5:149–61; PMID:15688042; http://dx.doi.org/10.1038/nri1551
  • Kari L, Whitmire WM, Crane DD, Reveneau N, Carlson JH, Goheen MM, Peterson EM, Pal S, de la Maza LM, Caldwell HD. Chlamydia trachomatis native major outer membrane protein induces partial protection in nonhuman primates: implication for a trachoma transmission-blocking vaccine. J Immunol 2009; 182:8063–70; PMID:19494332; http://dx.doi.org/10.4049/jimmunol.0804375
  • Pal S, Peterson EM, Rappuoli R, Ratti G, de la Maza LM. Immunization with the Chlamydia trachomatis major outer membrane protein, using adjuvants developed for human vaccines, can induce partial protection in a mouse model against a genital challenge. Vaccine 2006; 24:766–75; PMID:16199110; http://dx.doi.org/10.1016/j.vaccine.2005.08.074
  • Singh SR, Hulett K, Pillai SR, Dennis VA, Oh MK, Scissum-Gunn K. Mucosal immunization with recombinant MOMP genetically linked with modified cholera toxin confers protection against Chlamydia trachomatis infection. Vaccine 2006; 24:1213–24; PMID:16194585; http://dx.doi.org/10.1016/j.vaccine.2005.08.097
  • Grotenbreg GM, Roan NR, Guillen E, Meijers R, Wang JH, Bell GW, Starnbach MN, Ploegh HL. Discovery of CD8+ T cell epitopes in Chlamydia trachomatis infection through use of caged class I MHC tetramers. Proc Natl Acad Sci U S A 2008; 105:3831–6; PMID:18245382; http://dx.doi.org/10.1073/pnas.0711504105
  • Baehr W, Zhang YX, Joseph T, Su H, Nano FE, Everett KD, Caldwell HD. Mapping antigenic domains expressed by Chlamydia trachomatis major outer membrane protein genes. Proc Natl Acad Sci U S A 1988; 85:4000–4; PMID:2453883; http://dx.doi.org/10.1073/pnas.85.11.4000
  • Finco O, Frigimelica E, Buricchi F, Petracca R, Galli G, Faenzi E, Meoni E, Bonci A, Agnusdei M, Nardelli F, et al. Approach to discover T- and B-cell antigens of intracellular pathogens applied to the design of Chlamydia trachomatis vaccines. Proc Natl Acad Sci U S A 2011; 108:9969–74; PMID:21628568; http://dx.doi.org/10.1073/pnas.1101756108
  • Ortiz L, Demick KP, Petersen JW, Polka M, Rudersdorf RA, Van der Pol B, Jones R, Angevine M, DeMars R. Chlamydia trachomatis major outer membrane protein (MOMP) epitopes that activate HLA class II-restricted T cells from infected humans. J Immunol 1996; 157:4554–67; PMID:8906834
  • Eko FO, He Q, Brown T, McMillan L, Ifere GO, Ananaba GA, Lyn D, Lubitz W, Kellar KL, Black CM, et al. A novel recombinant multisubunit vaccine against Chlamydia. J Immunol 2004; 173:3375–82; PMID:15322201; http://dx.doi.org/10.4049/jimmunol.173.5.3375
  • Starnbach MN, Loomis WP, Ovendale P, Regan D, Hess B, Alderson MR, Fling SP. An inclusion membrane protein from Chlamydia trachomatis enters the MHC class I pathway and stimulates a CD8+ T cell response. J Immunol 2003; 171:4742–9; PMID:14568950; http://dx.doi.org/10.4049/jimmunol.171.9.4742
  • Chaganty BK, Murthy AK, Evani SJ, Li W, Guentzel MN, Chambers JP, Zhong G, Arulanandam BP. Heat denatured enzymatically inactive recombinant chlamydial protease-like activity factor induces robust protective immunity against genital chlamydial challenge. Vaccine 2010; 28:2323–9; PMID:20056182; http://dx.doi.org/10.1016/j.vaccine.2009.12.064
  • Li W, Murthy AK, Guentzel MN, Seshu J, Forsthuber TG, Zhong G, Arulanandam BP. Antigen-specific CD4+ T cells produce sufficient IFN-gamma to mediate robust protective immunity against genital Chlamydia muridarum infection. J Immunol 2008; 180:3375–82; PMID:18292563; http://dx.doi.org/10.4049/jimmunol.180.5.3375
  • Fling SP, Sutherland RA, Steele LN, Hess B, D'Orazio SE, Maisonneuve J, Lampe MF, Probst P, Starnbach MN. CD8+ T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis. Proc Natl Acad Sci U S A 2001; 98:1160–5; PMID:11158611; http://dx.doi.org/10.1073/pnas.98.3.1160
  • Coler RN, Bhatia A, Maisonneuve JF, Probst P, Barth B, Ovendale P, Fang H, Alderson M, Lobet Y, Cohen J, et al. Identification and characterization of novel recombinant vaccine antigens for immunization against genital Chlamydia trachomatis. FEMS Immunol Med Microbiol 2009; 55:258–70; PMID:19281568; http://dx.doi.org/10.1111/j.1574-695X.2008.00527.x
  • Karunakaran KP, Rey-Ladino J, Stoynov N, Berg K, Shen C, Jiang X, Gabel BR, Yu H, Foster LJ, Brunham RC. Immunoproteomic discovery of novel T cell antigens from the obligate intracellular pathogen Chlamydia. J Immunol 2008; 180:2459–65; PMID:18250455; http://dx.doi.org/10.4049/jimmunol.180.4.2459
  • Mygind T, Vandahl B, Pedersen AS, Christiansen G, Hollsberg P, Birkelund S. Identification of an in vivo CD4+ T cell-mediated response to polymorphic membrane proteins of Chlamydia pneumoniae during experimental infection. FEMS Immunol Med Microbiol 2004; 40:129–37; PMID:14987731; http://dx.doi.org/10.1016/S0928-8244(03)00300-6
  • Yu H, Jiang X, Shen C, Karunakaran KP, Brunham RC. Novel Chlamydia muridarum T cell antigens induce protective immunity against lung and genital tract infection in murine models. J Immunol 2009; 182:1602–8; PMID:19155509; http://dx.doi.org/10.4049/jimmunol.182.3.1602
  • Yu H, Jiang X, Shen C, Karunakaran KP, Jiang J, Rosin NL, Brunham RC. 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 α and IFN-gamma/interleukin-17 double-positive CD4+ T cells. Infect Immun 2010; 78:2272–82; PMID:20231405; http://dx.doi.org/10.1128/IAI.01374-09
  • Yu H, Karunakaran KP, Jiang X, Brunham RC. Evaluation of a multisubunit recombinant polymorphic membrane protein and major outer membrane protein T cell vaccine against Chlamydia muridarum genital infection in three strains of mice. Vaccine 2014; 32:4672–80; PMID:24992718; http://dx.doi.org/10.1016/j.vaccine.2014.06.002
  • Yu H, Karunakaran KP, Jiang X, Shen C, Andersen P, Brunham RC. Chlamydia muridarum T cell antigens and adjuvants that induce protective immunity in mice. Infect Immun 2012; 80:1510–8; PMID:22290151; http://dx.doi.org/10.1128/IAI.06338-11
  • Johnson RM, Yu H, Kerr MS, Slaven JE, Karunakaran KP, Brunham RC. PmpG303-311, a protective vaccine epitope that elicits persistent cellular immune responses in Chlamydia muridarum-immune mice. Infect Immun 2012; 80:2204–11; PMID:22431650; http://dx.doi.org/10.1128/IAI.06339-11
  • Karunakaran KP, Yu H, Jiang X, Chan Q, Moon KM, Foster LJ, Brunham RC. Outer membrane proteins preferentially load MHC class II peptides: Implications for as a Chlamydia trachomatis T cell vaccine. Vaccine 2015; 33(18):2159–66; PMID:25738816
  • Li LX, McSorley SJ. B cells enhance antigen-specific CD4 T cell priming and prevent bacteria dissemination following Chlamydia muridarum genital tract infection. PLoS Pathog 2013; 9:e1003707; PMID:24204262; http://dx.doi.org/10.1371/journal.ppat.1003707
  • Zhu Y, Jiang J, Said-Sadier N, Boxx G, Champion C, Tetlow A, Kickhoefer VA, Rome LH, Ojcius DM, Kelly KA. Activation of the NLRP3 inflammasome by vault nanoparticles expressing a chlamydial epitope. Vaccine 2015; 33:298–306; PMID:25448112; http://dx.doi.org/10.1016/j.vaccine.2014.11.028
  • Pan Q, Pais R, Ohandjo A, He C, He Q, Omosun Y, Igietseme JU, Eko FO. Comparative evaluation of the protective efficacy of two formulations of a recombinant Chlamydia abortus subunit candidate vaccine in a mouse model. Vaccine 2015; 33(15):1865–72
  • Zhou J, Qiu C, Cao XA, Lin G. Construction and immunogenicity of recombinant adenovirus expressing the major outer membrane protein (MOMP) of Chlamydophila psittaci in chicks. Vaccine 2007; 25:6367–72; PMID:17640776; http://dx.doi.org/10.1016/j.vaccine.2007.06.031
  • Liu S, Sun W, Chu J, Huang X, Wu Z, Yan M, Zhang Q, Zhao P, Igietseme JU, Black CM, et al. Construction of Recombinant HVT Expressing PmpD, and Immunological Evaluation against Chlamydia psittaci and Marek's Disease Virus. PLoS One 2015; 10:e0124992; PMID:25893439; http://dx.doi.org/10.1371/journal.pone.0124992
  • Stary G, Olive A, Radovic-Moreno AF, Gondek D, Alvarez D, Basto PA, Perro M, Vrbanac VD, Tager AM, Shi J, et al. VACCINES. A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science 2015; 348:aaa8205; PMID:26089520; http://dx.doi.org/10.1126/science.aaa8205
  • Kiselev AO, Skinner MC, Lampe MF. Analysis of pmpD expression and PmpD post-translational processing during the life cycle of Chlamydia trachomatis serovars A, D, and L2. PLoS One 2009; 4:e5191; PMID:19367336; http://dx.doi.org/10.1371/journal.pone.0005191
  • Gomes JP, Bruno WJ, Borrego MJ, Dean D. Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer. J Bacteriol 2004; 186:4295–306; PMID:15205432; http://dx.doi.org/10.1128/JB.186.13.4295-4306.2004
  • Mygind PH, Christiansen G, Roepstorff P, Birkelund S. Membrane proteins PmpG and PmpH are major constituents of Chlamydia trachomatis L2 outer membrane complex. FEMS Microbiol Lett 2000; 186:163–9; PMID:10802165; http://dx.doi.org/10.1111/j.1574-6968.2000.tb09098.x
  • Wheelhouse NM, Sait M, Aitchison K, Livingstone M, Wright F, McLean K, Inglis NF, Smith DG, Longbottom D. Processing of Chlamydia abortus polymorphic membrane protein 18D during the chlamydial developmental cycle. PLoS One 2012; 7:e49190; PMID:23145118; http://dx.doi.org/10.1371/journal.pone.0049190
  • Wheelhouse N, Sait M, Wilson K, Aitchison K, McLean K, Smith DG, Longbottom D. Expression patterns of five polymorphic membrane proteins during the Chlamydia abortus developmental cycle. Vet Microbiol 2012; 160:525–9; PMID:22776512; http://dx.doi.org/10.1016/j.vetmic.2012.06.017
  • Stemke-Hale K, Kaltenboeck B, DeGraves FJ, Sykes KF, Huang J, Bu CH, Johnston SA. Screening the whole genome of a pathogen in vivo for individual protective antigens. Vaccine 2005; 23:3016–25; PMID:15811648; http://dx.doi.org/10.1016/j.vaccine.2004.12.013

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.