Protection of outbred mice against a vaginal challenge by a Chlamydia trachomatis serovar E recombinant major outer membrane protein vaccine is dependent on phosphate substitution in the adjuvant

References

• Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One. 2015;10:e0143304. doi:10.1371/journal.pone.0143304.
   PubMed Web of Science ®Google Scholar
• CDC. Sexually transmitted disease surveillance 2017. prevention DoS, ed. Atlanta, GA: Department of Health and Human Services; 2018. p. 1–168
   Google Scholar
• Miller WC, Ford CA, Morris M, Handcock MS, Schmitz JL, Hobbs MM, Cohen MS, Harris KM, Udry JR. Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA. 2004;291:2229–36. doi:10.1001/jama.291.18.2229.
   PubMed Web of Science ®Google Scholar
• Ness RB, Smith KJ, Chang CC, Schisterman EF, Bass DC. Prediction of pelvic inflammatory disease among young, single, sexually active women. Sex Transm Dis. 2006;33:137–42. doi:10.1097/01.olq.0000187205.67390.d1.
   PubMed Web of Science ®Google Scholar
• Stamm W. Chlamydia trachomatis infections of the adult. In: Holmes KK, WE Stamm PS, Piot P, Wasserheit JW, Corey L, Cohen MS, Watts DH, editors. Sex transm dis. New York, NY: McGrawHill Book Co.; 2008. p. 575–93.
   Google Scholar
• Arth C, Von Schmidt B, Grossman M, Schachter J. Chlamydial pneumonitis. J Pediatr. 1978;93:447–49. doi:10.1016/S0022-3476(78)81155-X.
   PubMed Web of Science ®Google Scholar
• Darville T. Chlamydia trachomatis infections in neonates and young children. Semin Pediatr Infect Dis. 2005;16:235–44. doi:10.1053/j.spid.2005.06.004.
   PubMedGoogle Scholar
• Stutman HR, Rettig PJ, Reyes S. Chlamydia trachomatis as a cause of pneumonitis and pleural effusion. J Pediatr. 1984;104:588–91. doi:10.1016/S0022-3476(84)80554-5.
   PubMed Web of Science ®Google Scholar
• Schachter J, Dawson CR. Human chlamydial infections. Littleton (Mass): PSG Pub. Co.; 1978.
   Google Scholar
• Wang SP, Grayston JT. A potency test for trachoma vaccine utilizing the mouse toxicity prevention test. Am J Ophthalmol. 1967;63:Suppl:1443–54. doi:10.1016/0002-9394(67)94130-X.
   Web of Science ®Google Scholar
• Taylor HR. Trachoma: a blinding scourge from the Bronze Age to the twenty-first century. Victoria (Australia): Haddington Press Pry Ltd; 2008.
   Google Scholar
• Brunham RC, Rey-Ladino J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol. 2005;5:149–61. doi:10.1038/nri1551.
   PubMed Web of Science ®Google Scholar
• Morrison RP, Caldwell HD. Immunity to murine chlamydial genital infection. Infect Immun. 2002;70:2741–51. doi:10.1128/IAI.70.6.2741-2751.2002.
   PubMed Web of Science ®Google Scholar
• 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. 2003;171:6187–97. doi:10.4049/jimmunol.171.11.6187.
   PubMed Web of Science ®Google Scholar
• Karimi O, Ouburg S, de Vries HJ, Pena AS, Pleijster J, Land JA, Morre SA. TLR2 haplotypes in the susceptibility to and severity of Chlamydia trachomatis infections in Dutch women. Drugs Today (Barc). 2009;45(Suppl):B:67–74.
   Google Scholar
• European Centre for Disease Prevention and Control. Guidance on chlamydia control in Europe - 2015. Stockholm, Sweden: ECDC; 2016.
   Google Scholar
• Westrom L, Joesoef R, Reynolds G, Hagdu A, Thompson SE. Pelvic inflammatory disease and fertility. A cohort study of 1,844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex Transm Dis. 1992;19:185–92. doi:10.1097/00007435-199207000-00001.
   PubMed Web of Science ®Google Scholar
• Brunham RC, Pourbohloul B, Mak S, White R, Rekart ML. The unexpected impact of a Chlamydia trachomatis infection control program on susceptibility to reinfection. J Infect Dis. 2005;192:1836–44. doi:10.1086/jid.2005.192.issue-10.
   PubMed Web of Science ®Google Scholar
• Gotz H, Lindback J, Ripa T, Arneborn M, Ramsted K, Ekdahl K. Is the increase in notifications of Chlamydia trachomatis infections in Sweden the result of changes in prevalence, sampling frequency or diagnostic methods? Scand J Infect Dis. 2002;34:28–34. doi:10.1080/00365540110077001.
   PubMed Web of Science ®Google Scholar
• de la Maza MA, de la Maza LM. A new computer model for estimating the impact of vaccination protocols and its application to the study of Chlamydia trachomatis genital infections. Vaccine. 1995;13:119–27. doi:10.1016/0264-410X(95)80022-6.
   PubMed Web of Science ®Google Scholar
• Farris CM, Morrison RP. Vaccination against chlamydia genital infection utilizing the murine C. muridarum model. Infect Immun. 2011;79:986–96. doi:10.1128/IAI.00881-10.
   PubMed Web of Science ®Google Scholar
• Rockey DD, Wang J, Lei L, Zhong G. Chlamydia vaccine candidates and tools for chlamydial antigen discovery. Expert Rev Vaccines. 2009;8:1365–77. doi:10.1586/erv.09.98.
   PubMed Web of Science ®Google Scholar
• de la Maza LM, Zhong G, Brunham RC. Update on Chlamydia trachomatis vaccinology. Clin Vaccine Immunol. 2017;24:e00543–16.
   PubMed Web of Science ®Google Scholar
• Zhong G, Brunham RC, de la Maza LM, Darville T, Deal C. National Institute of Allergy and Infectious Diseases workshop report: “Chlamydia vaccines: the way forward”. Vaccine. 2017;37:7346–54.
   PubMed Web of Science ®Google Scholar
• Phillips S, Quigley BL, Timms P. Seventy years of chlamydia vaccine research - limitations of the past and directions for the future. Front Microbiol. 2019;10:70. doi:10.3389/fmicb.2019.00070.
   PubMed Web of Science ®Google Scholar
• 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. 2005;73:8153–60. doi:10.1128/IAI.73.12.8153-8160.2005.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1128/CMR.00105-13.
   PubMed Web of Science ®Google Scholar
• Watkinson A, Soliakov A, Ganesan A, Hirst K, Lebutt C, Fleetwood K, Fusco PC, Fuerst TR, Lakey JH. Increasing the potency of an alhydrogel-formulated anthrax vaccine by minimizing antigen-adjuvant interactions. Clin Vaccine Immunol. 2013;20:1659–68. doi:10.1128/CVI.00320-13.
   PubMedGoogle Scholar
• Hansen B, Belfast M, Soung G, Song L, Egan PM, Capen R, HogenEsch H, Mancinelli R, Hem SL. Effect of the strength of adsorption of hepatitis B surface antigen to aluminum hydroxide adjuvant on the immune response. Vaccine. 2009;27:888–92. doi:10.1016/j.vaccine.2008.11.078.
   PubMed Web of Science ®Google Scholar
• Iyer S, HogenEsch H, Hem SL. Effect of the degree of phosphate substitution in aluminum hydroxide adjuvant on the adsorption of phosphorylated proteins. Pharm Dev Technol. 2003;8:81–86. doi:10.1081/PDT-120017526.
   PubMed Web of Science ®Google Scholar
• Ljutic B, Ochs M, Messham B, Ming M, Dookie A, Harper K, Ausar SF. Formulation, stability and immunogenicity of a trivalent pneumococcal protein vaccine formulated with aluminum salt adjuvants. Vaccine. 2012;30:2981–88. doi:10.1016/j.vaccine.2012.02.038.
   PubMed Web of Science ®Google Scholar
• Visan L, Sanchez V, Kania M, de Montfort A, de la Maza LM, Ausar SF. Phosphate substitution in an AlOOH - TLR4 adjuvant system (SPA08) modulates the immunogenicity of Serovar E MOMP from Chlamydia trachomatis. Hum Vaccin Immunother. 2016;12:2341–50. doi:10.1080/21645515.2016.1168958.
   PubMed Web of Science ®Google Scholar
• Pal S, Peterson EM, de la Maza LM. Induction of protective immunity against a Chlamydia trachomatis genital infection in three genetically distinct strains of mice. Immunology. 2003;110:368–75. doi:10.1046/j.1365-2567.2003.01748.x.
   PubMed Web of Science ®Google Scholar
• Polkinghorne A, Hanger J, Timms P. Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas. Vet Microbiol. 2013;165:214–23. doi:10.1016/j.vetmic.2013.02.026.
   PubMed Web of Science ®Google Scholar
• Kollipara A, Polkinghorne A, Wan C, Kanyoka P, Hanger J, Loader J, Callaghan J, Bell A, Ellis W, Fitzgibbon S, et al. Genetic diversity of Chlamydia pecorum strains in wild koala locations across Australia and the implications for a recombinant C. pecorum major outer membrane protein based vaccine. Vet Microbiol. 2013;167:513–22. doi:10.1016/j.vetmic.2013.08.009.
   PubMed Web of Science ®Google Scholar
• Kollipara A, Wan C, Rawlinson G, Brumm J, Nilsson K, Polkinghorne A, Beagley K, Timms P. Antigenic specificity of a monovalent versus polyvalent MOMP based Chlamydia pecorum vaccine in koalas (Phascolarctos cinereus). Vaccine. 2013;31:1217–23. doi:10.1016/j.vaccine.2012.12.057.
   PubMed Web of Science ®Google Scholar
• Kollipara A, George C, Hanger J, Loader J, Polkinghorne A, Beagley K, Timms P. Vaccination of healthy and diseased koalas (Phascolarctos cinereus) with a Chlamydia pecorum multi-subunit vaccine: evaluation of immunity and pathology. Vaccine. 2012;30:1875–85. doi:10.1016/j.vaccine.2011.12.125.
   PubMed Web of Science ®Google Scholar
• Nyari S, Booth R, Quigley BL, Waugh CA, Timms P. Therapeutic effect of a Chlamydia pecorum recombinant major outer membrane protein vaccine on ocular disease in koalas (Phascolarctos cinereus). PLoS One. 2019;14:e0210245. doi:10.1371/journal.pone.0210245.
   PubMed Web of Science ®Google Scholar
• Marangoni A, Foschi C, Nardini P, D’Antuono A, Banzola N, Di Francesco A, Ostanello F, Russo I, Donati M, Cevenini R, et al. Chlamydia trachomatis serovar distribution and other sexually transmitted coinfections in subjects attending an STD outpatients clinic in Italy. New Microbiol. 2012;35:215–19.
   PubMed Web of Science ®Google Scholar
• Morre SA, Rozendaal L, van Valkengoed IG, Boeke AJ, van Voorst Vader PC, Schirm J, de Blok S, van Den Hoek JA, van Doornum GJ, Meijer CJ, et al. Urogenital Chlamydia trachomatis serovars in men and women with a symptomatic or asymptomatic infection: an association with clinical manifestations? J Clin Microbiol. 2000;38:2292–96.
   PubMed Web of Science ®Google Scholar
• van Duynhoven YT, Ossewaarde JM, Derksen-Nawrocki RP, van der Meijden WI. van de Laar MJ. Chlamydia trachomatis genotypes: correlation with clinical manifestations of infection and patients’ characteristics. Clin Infect Dis. 1998;26:314–22. doi:10.1086/516291.
   PubMed Web of Science ®Google Scholar
• Verweij SP, Lanjouw E, Bax CJ, Quint KD, Oostvogel PM, Dorr PJ, Pleijster J, de Vries HJ, Peters RP, Ouburg S, et al. Serovar D and E of serogroup B induce highest serological responses in urogenital Chlamydia trachomatis infections. BMC Infect Dis. 2014;14:3. doi:10.1186/1471-2334-14-3.
   PubMed Web of Science ®Google Scholar
• Caldwell HD, Kromhout J, Schachter J. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun. 1981;31:1161–76. doi:10.1128/IAI.31.3.1161-1176.1981.
   PubMed Web of Science ®Google Scholar
• Pal S, Fielder TJ, Peterson EM, de la Maza LM. Protection against infertility in a BALB/c mouse salpingitis model by intranasal immunization with the mouse pneumonitis biovar of Chlamydia trachomatis. Infect Immun. 1994;62:3354–62. doi:10.1128/IAI.62.8.3354-3362.1994.
   PubMed Web of Science ®Google Scholar
• Cheng C, Bettahi I, Cruz-Fisher MI, Pal S, Jain P, Jia Z, Holmgren J, Harandi AM, de la Maza LM. Induction of protective immunity by vaccination against Chlamydia trachomatis using the major outer membrane protein adjuvanted with CpG oligodeoxynucleotide coupled to the nontoxic B subunit of cholera toxin. Vaccine. 2009;27:6239–46. doi:10.1016/j.vaccine.2009.07.108.
   PubMed Web of Science ®Google Scholar
• de la Maza LM, Pal S, Khamesipour A, Peterson EM. Intravaginal inoculation of mice with the Chlamydia trachomatis mouse pneumonitis biovar results in infertility. Infect Immun. 1994;62:2094–97. doi:10.1128/IAI.62.5.2094-2097.1994.
   PubMed Web of Science ®Google Scholar
• Pal S, Peterson EM, de la Maza LM. Susceptibility of mice to vaginal infection with Chlamydia trachomatis mouse pneumonitis is dependent on the age of the animal. Infect Immun. 2001;69:5203–06. doi:10.1128/IAI.69.8.5203-5206.2001.
   PubMed Web of Science ®Google Scholar
• Buwitt-Beckmann U, Heine H, Wiesmuller K-H, Jung G, Brock R, Akira S, Ulmer A. Toll-like receptor 6-independent signaling by diacylated lipopeptides. Eur J Immunol. 2005;35:282–89. doi:10.1002/eji.200424955.
   PubMed Web of Science ®Google Scholar
• Swenson CE, Schachter J. Infertility as a consequence of chlamydial infection of the upper genital tract in female mice. Sex Transm Dis. 1984;11:64–67. doi:10.1097/00007435-198404000-00002.
   PubMed Web of Science ®Google Scholar
• 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. 1988;56:885–91. doi:10.1128/IAI.56.4.885-891.1988.
   PubMed Web of Science ®Google Scholar
• de la Maza LM, Peterson EM, Goebel JM, Fennie CW, Czarniecki CW. Interferon-induced inhibition of Chlamydia trachomatis: dissociation from antiviral and antiproliferative effects. Infect Immun. 1985;47:719–22. doi:10.1128/IAI.47.3.719-722.1985.
   PubMed Web of Science ®Google Scholar
• Festing MF, Altman DG. Guidelines for the design and statistical analysis of experiments using laboratory animals. Ilar J. 2002;43:244–58. doi:10.1093/ilar.43.4.244.
   PubMedGoogle Scholar
• HogenEsch H, O’Hagan DT, Fox CB. Optimizing the utilization of aluminum adjuvants in vaccines: you might just get what you want. NPJ Vaccines. 2018;3:51. doi:10.1038/s41541-018-0089-x.
   PubMed Web of Science ®Google Scholar
• Al-Zeer MA, Al-Younes HM, Lauster D, Abu Lubad M, Meyer TF. Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins. Autophagy. 2013;9:50–62. doi:10.4161/auto.22482.
   PubMed Web of Science ®Google Scholar
• Batteiger BE, Xu F, Johnson RE, Rekart ML. Protective immunity to Chlamydia trachomatis genital infection: evidence from human studies. J Infect Dis. 2010;201(Suppl 2):S178–89. doi:10.1086/652400.
   PubMed Web of Science ®Google Scholar
• Rank RG, Whittum-Hudson JA. Protective immunity to chlamydial genital infection: evidence from animal studies. J Infect Dis. 2010;201(Suppl 2):S168–77. doi:10.1086/652399.
   PubMedGoogle Scholar
• Zhong GM, Peterson EM, Czarniecki CW, Schreiber RD, de la Maza LM. Role of endogenous gamma interferon in host defense against Chlamydia trachomatis infections. Infect Immun. 1989;57:152–57. doi:10.1128/IAI.57.1.152-157.1989.
   PubMed Web of Science ®Google Scholar
• Olsen AW, Lorenzen EK, Rosenkrands I, Follmann F, Andersen P. Protective effect of vaccine promoted neutralizing antibodies against the intracellular pathogen Chlamydia trachomatis. Front Immunol. 2017;8:1652. doi:10.3389/fimmu.2017.01652.
   PubMed Web of Science ®Google Scholar
• Peterson EM, Cheng X, Motin VL, de la Maza LM. Effect of immunoglobulin G isotype on the infectivity of Chlamydia trachomatis in a mouse model of intravaginal infection. Infect Immun. 1997;65:2693–99. doi:10.1128/IAI.65.7.2693-2699.1997.
   PubMed Web of Science ®Google Scholar
• Poston TB, Darville T. Chlamydia trachomatis: protective adaptive responses and prospects for a vaccine. Curr Top Microbiol Immunol. 2018;412:217–37. doi:10.1007/82_2016_6.
   PubMed Web of Science ®Google Scholar
• Peterson EM, Cheng X, Pal S, de la Maza LM. Effects of antibody isotype and host cell type on in vitro neutralization of Chlamydia trachomatis. Infect Immun. 1993;61:498–503. doi:10.1128/IAI.61.2.498-503.1993.
   PubMed Web of Science ®Google Scholar
• 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. 1997;15:575–82. doi:10.1016/S0264-410X(97)00206-5.
   PubMed Web of Science ®Google Scholar
• Pal S, Bravo J, Peterson EM, de la Maza LM. 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. 2008;76:5581–87. doi:10.1128/IAI.00574-08.
   PubMed Web of Science ®Google Scholar
• Farris CM, Morrison SG, Morrison RP. CD4+ T cells and antibody are required for optimal major outer membrane protein vaccine-induced immunity to Chlamydia muridarum genital infection. Infect Immun. 2010;78:4374–83. doi:10.1128/IAI.00622-10.
   PubMed Web of Science ®Google Scholar
• Olsen AW, Follmann F, Erneholm K, Rosenkrands I, Andersen P. Protection against Chlamydia trachomatis infection and upper genital tract pathological changes by vaccine-promoted neutralizing antibodies directed to the VD4 of the major outer membrane protein. J Infect Dis. 2015;212:978–89. doi:10.1093/infdis/jiv137.
   PubMed Web of Science ®Google Scholar
• Gottlieb SL, Johnston C. Future prospects for new vaccines against sexually transmitted infections. Curr Opin Infect Dis. 2017;30:77–86. doi:10.1097/QCO.0000000000000343.
   PubMed Web of Science ®Google Scholar
• Carmichael JR, Pal S, Tifrea D, de la Maza LM. Induction of protection against vaginal shedding and infertility by a recombinant Chlamydia vaccine. Vaccine. 2011;29:5276–83. doi:10.1016/j.vaccine.2011.05.013.
   PubMed Web of Science ®Google Scholar
• Kari L, Whitmire WM, Crane DD, Reveneau N, Carlson JH, Goheen MM, Peterson EM, Pal S, Luis M, et al. 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. doi:10.4049/jimmunol.0804375.
   PubMed Web of Science ®Google Scholar
• Tifrea DF, Pal S, Popot JL, Cocco MJ, de la Maza LM. Increased immunoaccessibility of MOMP epitopes in a vaccine formulated with amphipols may account for the very robust protection elicited against a vaginal challenge with Chlamydia muridarum. J Immunol. 2014;192:5201–13. doi:10.4049/jimmunol.1303392.
   PubMed Web of Science ®Google Scholar
• Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci. 1992;89:12180–84. doi:10.1073/pnas.89.24.12180.
   PubMed Web of Science ®Google Scholar
• Lowy DR, Schiller JT. Prophylactic human papillomavirus vaccines. J Clin Invest. 2006;116:1167–73. doi:10.1172/JCI28607.
   PubMed Web of Science ®Google Scholar
• Qiu S, Zhang J, Tian Y, Yang Y, Huang H, Yang D, Lu M, Xu Y. Reduced antigenicity of naturally occurring hepatitis B surface antigen variants with substitutions at the amino acid residue 126. Intervirology. 2008;51:400–06. doi:10.1159/000205265.
   PubMed Web of Science ®Google Scholar
• Ionescu-Matiu I, Kennedy RC, Sparrow JT, Culwell AR, Sanchez Y, Melnick JL, Dreesman GR. Epitopes associated with a synthetic hepatitis B surface antigen peptide. J Immunol. 1983;130:1947–52.
   PubMed Web of Science ®Google Scholar
• Nicolle C, Cuenod A, Baizot L. Etude experimentale du trachome. Arch Instit Pasteur de Tunis. 1913;4:157–82.
   Google Scholar
• Brunham RC, Rappuoli R. Chlamydia trachomatis control requires a vaccine. Vaccine. 2013;31:1892–97. doi:10.1016/j.vaccine.2013.01.024.
   PubMed Web of Science ®Google Scholar
• Fulginiti VA, Eller JJ, Downie AW, Kempe CH. Altered reactivity to measles virus. A typical measles in children previously immunized with inactivated measles virus vaccines. JAMA. 1967;202:1075–80. doi:10.1001/jama.1967.03130250057008.
   PubMed Web of Science ®Google Scholar
• van Drunen Littel-van den Hurk S, Watkiss E. Pathogenesis of respiratory syncytial virus. Current Opinion in Virology. 2012;2:300–05. doi:10.1016/j.coviro.2012.01.008.
   PubMed Web of Science ®Google Scholar
• Levine MM. New generation vaccines. New York, NY: Informa Healthcare USA, Inc.; 2010.
   Google Scholar
• Plotkin SA, Orenstein WA, Offit PA. Plotkin’s vaccines. Philadelphia (PA): Elsevier; 2018.
   Google Scholar
• Olsen AW, Theisen M, Christensen D, Follmann F, Andersen P. Protection against Chlamydia promoted by a subunit vaccine (CTH1) compared with a primary intranasal infection in a mouse genital challenge model. PLoS One. 2010;5:e10768. doi:10.1371/journal.pone.0010768.
   PubMed Web of Science ®Google Scholar
• Tuffrey M, Taylor-Robinson D. Progesterone as a key factor in the development of a mouse model for genital-tract infection with Chlamydia trachomatis. FEMS Microbiol Lett. 1981;12:111–15. doi:10.1111/j.1574-6968.1981.tb07622.x.
   Web of Science ®Google Scholar
• Tuffrey M, Falder P, Gale J, Taylor-Robinson D. Salpingitis in mice induced by human strains of Chlamydia trachomatis. Br J Exp Pathol. 1986;67:605–16.
   PubMedGoogle Scholar
• Darville T, Andrews CW Jr., Laffoon KK, Shymasani W, Kishen LR, Rank RG. Mouse strain-dependent variation in the course and outcome of chlamydial genital tract infection is associated with differences in host response. Infect Immun. 1997;65:3065–73. doi:10.1128/IAI.65.8.3065-3073.1997.
   PubMed Web of Science ®Google Scholar