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Review

Future of human Chlamydia vaccine: potential of self-adjuvanting biodegradable nanoparticles as safe vaccine delivery vehicles

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Pages 217-227 | Received 17 Nov 2017, Accepted 29 Jan 2018, Published online: 06 Feb 2018

References

  • Stephens RS, Tam MR, Kuo CC, et al. Monoclonal antibodies to Chlamydia trachomatis: antibody specificities and antigen characterization. J Immunol. 1982;128(3):1083–1089.
  • Stephens RS, Wagar EA, Schoolnik GK. High-resolution mapping of serovar-specific and common antigenic determinants of the major outer membrane protein of Chlamydia trachomatis. J Exp Med. 1988;167:817–831.
  • Bandea CI, Kubota K, Brown TM, et al. Typing of Chlamydia trachomatis strains from urine samples by amplification and sequencing the major outer membrane protein gene (omp1). Sex Transm Infect. 2001;77(6):419–422.
  • Bush RM, Everett KD. Molecular evolution of the Chlamydiaceae. Int J Syst Evol Microbiol. 2001;51(Pt 1):203–220.
  • Schachter J, Stephens RS, Timms P, et al. Radical changes to chlamydial taxonomy are not necessary just yet. Int J Syst Evol Microbiol. 2001;51(Pt 1):251–253.
  • Schachter J. Infection and disease epidemiology. In: Stephens RS, editor. Chlamydia: intracellular biology, pathogenesis, and immunity. Washington, DC: ASM; 1999. p. 139–169.
  • Taylor H. Trachoma: a blinding scourge from the Bronze age to the twenty-first century. Victoria, Australia: Haddington Press Pty Ltd; 2008.
  • WHO. Global prevalence and incidence of selected curable sexually transmitted infections: overview and estimates. Geneva: World Health Organization; 2001.
  • CDC. Sexually transmitted diseases, treatment guidelines, 2010. MMWR. 2010;59(RR–12).
  • (CDC) CfDCaP. Sexually transmitted disease surveillance 2013. Atlanta, GA USA: U.S. Department of Health and Human Services; 2014. (Ed.^(Eds).
  • Newman L, Rowley J, Vander Hoorn S, 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(12):e0143304.
  • Westrom L, Joesoef R, Reynolds G, et al. Pelvic inflammatory inflammatory disease and infertility: a cohort study of 1,844 women with laparoscopically verified disease and 657 control women with normal laparoscopy results. Sex Transm Dis. 1992;19:185–192.
  • Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. N Engl J Med. 2015;372(21):2039–2048.
  • De La Maza LM, Zhong G, Brunham RC. Update on Chlamydia trachomatis Vaccinology. Clin Vaccine Immunol. 2017;24(4):e00543–00516.
  • Kumar S, Hammerschlag M. Acute respiratory infection due to Chlamydia pneumoniae: current status of diagnostic methods. Clin Infect Dis. 2007;44:568–576.
  • Kuo CC, Jackson LA, Campbell LA, et al. Chlamydia pneumoniae (TWAR). Clin Microbiol Rev. 1995;8(4):451–461.
  • Mahdi OS, Byrne GI, Kalayoglu M. Emerging strategies in the diagnosis, prevention and treatment of chlamydial infections. Expert Opin Ther Pat. 2001;11(8):1253–1265.
  • Gaillat J. Clinical manifestations of Chlamydia pneumoniae infections. Revue De Med Interne. 1996;17:987–999.
  • Everett KD. Chlamydia and Chlamydiales: more than meets the eye. Vet Microbiol. 2000;75(2):109–126.
  • Saikku P, Wang SP, Kleemola M, et al. An epidemic of mild pneumonia due to an unusual strain of Chlamydia psittaci. J Infect Dis. 1985;151:832–839.
  • (WHO) WHO. Report of the 2nd global scientific meeting on trachoma. (Ed.^(Eds) Geneva Switzerland: WHO; 2003.
  • Schachter J. NAATs to diagnose Chlamydia trachomatis genital infection: a promise still unfulfilled. Expert Rev Mol Diagn. 2001;1(2):137–144.
  • Thein J, Zhao P, Liu H, et al. Does clinical diagnosis indicate chlamydial infection in areas with a low prevalence of trachoma? Ophthalmic Epidemiol. 2002;9(4):263–269.
  • Johnson RE, Newhall WJ, Papp JR, et al. Screening tests to detect Chlamydia trachomatis and Neisseria gonorrhoeae infections–2002. MMWR Recomm Rep. 2002;51(RR–15):1–38. quiz CE31-34.
  • Rees E. The treatment of pelvic inflammatory disease. Am J Obstet Gynecol. 1980;138:1042–1047.
  • Paavonen J, Wolner-Hanssen P. Chlamydia trachomatis: a major threat to reproduction. J Hum Reprod. 1989;4:111–124.
  • Stamm WE, Guinan ME, Johnson C, et al. Effect of treatment regimens for Neisseria gonorrhoeae on simultaneous infection with chlamydia trachomatis. N Engl J Med. 1984;310:545–549.
  • CDC. Sexually transmitted disease surveillance, 2000. Atlanta, GA: US Department of Health and Human Services, CDC; 2001. (Ed.^(Eds).
  • Nieuwenhuis RF, Ossewaarde JM, Gotz HM, et al. Resurgence of Lymphogranuloma venereum in western Europe: an outbreak of Chlamydia trachomatis serovar L2 proctitis in The Netherlands among men who have sex with men. Clin Infect Dis (CID). 2004;39:996–1003.
  • West S. Global elimination of blinding trachoma by 2020: where are we? Ophthalmic Epidemiol. 2009;16(4):205.
  • Brunham RC, Rekart ML. The arrested immunity hypothesis and the epidemiology of Chlamydia control. Sex Transm Dis. 2008;35(1):53–54.
  • Holm SO, Jha HC, Bhatta RC, et al. Comparison of two azithromycin distribution strategies for controlling trachoma in Nepal. Bull World Health Organ. 2001;79(3):194–200.
  • Diamant J, Benis R, Schachter J, et al. Pooling of Chlamydia laboratory tests to determine the prevalence of ocular Chlamydia trachomatis infection. Ophthalmic Epidemiol. 2001;8(2–3):109–117.
  • Bain DL, Lietman T, Rasmussen S, et al. Chlamydial genovar distribution after community wide antibiotic treatment. J Infect Dis. 2001;184(12):1581–1588.
  • Dawson CR, Schachter J. Should trachoma be treated with antibiotics? Lancet. 2002;359(9302):184–185.
  • Bragina EY, Gomberg MA, Dmitriev GA. Electron microscopic evidence of persistent chlamydial infection following treatment. J Eur Acad Dermatol Venereol. 2001;15(5):405–409.
  • Byrne GI. Chlamydial treatment failures: a persistent problem? J Eur Acad Dermatol Venereol. 2001;15(5):381.
  • Dreses-Werringloer U, Padubrin I, Jurgens-Saathoff B, et al. Persistence of Chlamydia trachomatis is induced by ciprofloxacin and Ofloxacin in vitro. Antimicrob Agents Chemother. 2000;44(12):3288–3297.
  • Miyashita N, Fukano H, Hara H, et al. Recurrent pneumonia due to persistent Chlamydia pneumoniae infection. Intern Med. 2002;41(1):30–33.
  • Rees E, Tait IA, Hobson D, et al. Persistence of Chlamydial infection after treatment for neonatal conjunctivitis. Arch Dis Child. 1981;56:193–198.
  • Babalola OE, Bage SD. The persistence of Chlamydial inclusions in clinically quiescent trachoma. West Afr J Med. 1992;11(1):55–61.
  • Thejls H, Gnarpe J, Lundkvist O, et al. Diagnosis and prevalence of persistent Chlamydia infection in infertile women: tissue culture, direct antigen detection, and serology. Fertil Steril. 1991;55(2):304–310.
  • Dean D, Suchland RJ, Stamm WE. Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J Infect Dis. 2000;182:909–916.
  • Smith A, Munoz B, Hsieh YH, et al. OmpA genotypic evidence for persistent ocular Chlamydia trachomatis infection in Tanzania village women. Ophthalmic Epidemiol. 2001;8(2–3):127–135.
  • Ward H, Ronn M, Ward H, et al. Contribution of sexually transmitted infections to the sexual transmission of HIV. Curr Opin HIV AIDS. 2010;5:305–310.
  • Wilkinson D, Rutherford G. Population-based interventions for reducing sexually transmitted infections, including HIV infection. Cochrane Databse Syst Rev. 2001;(2):CD001220.
  • Kilmarx PH, Mock PA, Levine WC. Effect of Chlamydia trachomatis coinfection on HIV shedding in genital tract secretion. Sex Transm Dis. 2001;28(6):347–348.
  • Mcclelland RS, Wang CC, Mandaliya K, et al. Treatment of cervicitis is associated with decreased cervical shedding of HIV-1. Aids. 2001;15(1):105–110.
  • Simonetti AC, Melo JH, De Souza PR, et al. de Lima Filho JL. Immunological’s host profile for HPV and chlamydia trachomatis, a cervical cancer cofactor. Microbes Infect. 2009;11(4):435–442.
  • Cohen CR, Brunham RC. Pathogenesis of Chlamydia induced pelvic inflammatory disease. Sex Transm Infect. 1999;75(1):21–24.
  • Ssemanda EN, Munoz B, Harding-Esch EM, et al. Mass treatment with azithromycin for trachoma control: participation clusters in households. PLoS Negl Trop Dis. 2010;4(10): pii: e838.
  • 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(1):119–127.
  • Yu H, Karunakaran KP, Jiang X, et al. Subunit vaccines for the prevention of mucosal infection with Chlamydia trachomatis. Expert Rev Vaccines. 2016;15(8):977–988.
  • Igietseme JU, Eko FO, Black CM. Chlamydia vaccines: recent developments and the role of adjuvants in future formulations. Expert Rev Vaccines. 2011;10(11):1585–1596.
  • Liang S, Bulir D, Kaushic C, et al. Considerations for the rational design of a Chlamydia vaccine. Hum Vaccin Immunother. 2017;13(4):831–835.
  • Grayston JT, Woolridge RL, Wang SP, et al. Field studies of protection from infection by experimental trachoma virus vaccine in preschool-aged children on Taiwan. Proc Soc Exp Biol Med. 1963;112:589–595.
  • Woolridge RL, Grayston JT, Chang IH, et al. Long-term follow-up of the initial (1959–1960) trachoma vaccine field trial on Taiwan. Am J Ophthalmol. 1967;63:1650–1655.
  • Wang SP, Grayston JT, Alexander ER. Trachoma vaccine studies in monkeys. Am J Ophthalmol. 1967;63:1615–1620.
  • Clements C, Dhir SP, Grayston JT, et al. Long term follow-up study of a trachoma vaccine trial in villages of Northern India. Am J Ophthalmol. 1979;87(3):350–353.
  • Grayston JT, Wang SP, Yang YF, et al. The effect of trachoma virus vaccine on the course of experimental trachoma infection in blind human volunteers. J Exp Med. 1962;115:1009–1022.
  • Bietti GB, Guerra P, Vozza R, et al. Results of large-scale vaccination against trachoma in East Africa (Ethiopia) 1960-1965. Am J Ophthalmol. 1966;61(5 Pt 2):1010–1029.
  • Sowa S, Sowa J, Collier LH, et al. Trachoma vaccine field trials in The Gambia. J Hyg (Lond). 1969;67(4):699–717.
  • Schachter J. Overview of Chlamydia trachomatis infection and the requirements for a vaccine. Rev Infect Dis. 1985;7:713–716.
  • Schachter J, Dawson CR. The epidemiology of trachoma predicts more blindness in the future. Sex Transm Dis. 1990;Suppl. 69:55–62.
  • Rodolaki A, Salinas J, Papp J. Recent advances on ovine chlamydial abortion. Vet Res. 1998;29(3–4):275–288.
  • Brunham RC, Rey-Ladino J. Immunology of chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol. 2005;5(2):149–161.
  • Rockey D, Wang J, Lei L, et al. Chlamydia vaccine candidates and tools for chlamydial antigen discovery. Expert Rev Vaccines. 2008;8(10):1365–1377.
  • Longbottom D, Livingstone M. Vaccination against Chlmaydial infections of man and animals. Vet J. 2006;171(2):263–275.
  • Chalmers WS, Simpson J, Lee SJ, et al. Use of a live Chlamydial vaccine to prevent ovine enzootic abortion. Vet Rec. 1997;141(3):63–67.
  • Hafner LM, McNeilly C. Vaccines for Chlamydia infections of the female genital tract. Future Microbiol. 2008;3(1):67–77.
  • Stephens RS. Chlamydial genomics and vaccine antigen discovery. J Infect Dis. 2000;181(Suppl 3):S521–S523.
  • Stephens RS, Lammel CJ. Chlamydia outer membrane protein discovery using genomics. Curr Opin Microbiol. 2001;4(1):16–20.
  • Kawa DE, Stephens RS. Antigenic topology of chlamydial PorB protein and identification of targets for immune neutralization of infectivity. J Immunol. 2002;168(10):5184–5191.
  • 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. 2000;181:S544–S551.
  • Donati M, Sambri V, Comanducci M, et al. DNA immunzation with pgp3 gene of Chlamydia trachomatis inhibits the spread of chlamydial infection from the lower to the upper genital tract in C3H/HeN mice. Vaccine. 2003;21(11–12):1089–1093.
  • Sharma J, Bosnic AM, Piper JM, et al. Human antibody responses to a Chlamydia-secreted protease factor. Infect Immun. 2004;72(12):7164–7171.
  • Belland RJ, Scidmore MA, Crane DD, et al. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Pnas. 2001;98(24):13984–13989.
  • Slepenkin A, De La Maza LM, Peterson EM. Interaction between components of the type III secretion system of Chlamydiaceae. J Bacteriol. 2005;187(2):473–479.
  • Meoni E, Faenzi E, Frigimelica E, et al. CT043, a protective antigen that induces a CD4+ Th1 response during Chlamydia trachomatis infection in mice and humans. Infect Immun. 2009;77(9):4168–4176.
  • Follmann F, Olsen AW, Jensen KT, et al. Antigenic profiling of a Chlamydia trachomatis gene-expression library. J Infect Dis. 2008;197(6):897–905.
  • Cochrane M, Armitage C, O’Meara C, et al. Towards a Chlamydia trachomatis vaccine: how close are we? Future Microbiol. 2010;5(12):1833–1856.
  • De La Maza LM, Peterson EM. Vaccines for Chlamydia trachomatis infections. Curr Opin Investig Drugs. 2002;3(7):980–986.
  • Hafner L, Beagley K, Timms P. Chlamydia trachomatis infection: host immune responses and potential vaccines. Mucosal Immunol. 2008;1(2):116–130.
  • Igietseme JU, He Q, Eko FO, et al. Development of vaccines to prevent chlamydial STDs. Mucosal Immunol Update. 2005;13(4):12–17.
  • Morrison RP, Caldwell HD. Immunity to murine chlamydial genital infection. Infect Immun. 2002;70(6):2741–2751.
  • Loomis WP, Starnbach MN. T cell responses to Chlamydia trachomatis. Curr Opin Microbiol. 2002;5(1):87–91.
  • Igietseme JU, Black CM, Caldwell HD. Chlamydia vaccine: strategies and status. BioDrugs. 2002;16(1):19–35.
  • Stary G, Olive A, Radovic-Moreno AF, et al. VACCINES. A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science. 2015;348(6241):aaa8205.
  • Johnson R, Brunham R. Tissue-resident T cells as the central paradigm of Chlamydia immunity. Infect Immun. 2016;84(4):868–873.
  • Igietseme J, Eko F, He Q, et al. Delivery of Chlamydia vaccines. Expert Opin Drug Deliv. 2005;2(3):549–562.
  • Kamphorst AO, Araki K, Ahmed R. Beyond adjuvants: immunomodulation strategies to enhance T cell immunity. Vaccine. 2015;33(Suppl 2):B21–28.
  • Cheng C, Pal S, Tifrea D, et al. de la Maza LM. A vaccine formulated with a combination of TLR-2 and TLR-9 adjuvants and the recombinant major outer membrane protein elicits a robust immune response and significant protection against a Chlamydia muridarum challenge. Microbes Infect. 2014;16(3):244–252.
  • Akagi T, Baba M, Akashi M. Biodegradable nanoparticles as vaccine adjuvants and delivery systems: Regulation of immune responses by nanoparticle-based vaccine. In: Kunugi S, Yamaoka T, editors. Polymers in nanomedicine. Advances in polymer science, vol 247. Berlin, Heidelberg: Springer; 2011. p. 31–64.
  • Gutjahr A, Phelip C, Coolen AL, et al. Biodegradable polymeric nanoparticles-based vaccine adjuvants for lymph nodes targeting. Vaccines (Basel). 2016;4:4.
  • Rank RG. Models of immunity. In: Stephens RS, editor. Chlamydia: intracellular biology, pathogenesis and immunity. Washington, DC: ASM Press; 1999. p. 239–295.
  • Champion CI, Kickhoefer VA, Liu G, et al. A vault nanoparticle vaccine induces protective mucosal immunity. PLoS One. 2009;4(4):e5409.
  • Igietseme JU, Eko FO, He Q, et al. Developing effective delivery systems for Chlamydia vaccines. Curr Opin Mol Ther. 2004;6(2):182–194.
  • Dc M, Hu V, Rl B, et al. Towards a safe and effective Chlamydial vaccine: lessons from the eye. Vaccine. 2014;32(14):1572–1578.
  • Timms P, Hafner L. Development of a vaccine for Chlamydia trachomatis: challenges and current progress. Vaccine: Dev Ther. 2015;5:45–58.
  • Poston TB, Gottlieb SL, Darville T. Status of vaccine research and development of vaccines for Chlamydia trachomatis infection. Vaccine. 2017; pii:S0264-410X. DOI:10.1016/j.vaccine.2017.01.023.
  • Poston TB, Darville T. Chlamydia trachomatis: protective adaptive responses and prospects for a vaccine. Curr Top Microbiol Immunol. 2016 [Epub ahead of print].
  • Peres C, Matos AI, Conniot J, et al. Poly(lactic acid)-based particulate systems are promising tools for immune modulation. Acta Biomater. 2017;48:41–57.
  • Bennet D, Kim S. Polymer nanoparticles for smart drug delivery. In: Ali Demir, editor. Application of nanotechnology in drug delivery. London: InTech; 2014.
  • Zhao L, Seth A, Wibowo N, et al. Nanoparticle vaccines. Vaccine. 2014;32(3):327–337.
  • Gregory AE, Titball R, Williamson D. Vaccine delivery using nanoparticles. Front Cell Infect Microbiol. 2013;3:13.
  • Kamaly N, Xiao Z, Pm V, et al. Targeted polymeric therapeutic nanoparticles: design, development and clinical translation. Chem Soc Rev. 2012;41(7):2971–3010.
  • Danhier F, Ansorena E, Silva JM, et al. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012;161(2):505–522.
  • Makadia HK, Siegel SJ. Poly Lactic-co-Glycolic Acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers (Basel). 2011;3(3):1377–1397.
  • Fairley SJ, Singh SR, Yilma AN, et al. Chlamydia trachomatis recombinant MOMP encapsulated in PLGA nanoparticles triggers primarily T helper 1 cellular and antibody immune responses in mice: a desirable candidate nano vaccine. Int J Nanomed. 2013;8:2085–2099.
  • Jiang J, Liu G, Kickhoefer VA, et al. A protective vaccine against Chlamydia genital infection using vault nanoparticles without an added adjuvant. Vaccines (Basel). 2017;5:1.
  • Dixit S, Singh SR, Yilma AN, et al. Poly(lactic acid)-poly(ethylene glycol) nanoparticles provide sustained delivery of a Chlamydia trachomatis recombinant MOMP peptide and potentiate systemic adaptive immune responses in mice. Nanomedicine. 2014;10(6):1311–1321.
  • D’Avila Carvalho EC. Synthesis and characterization of poly(D,L-Lactide-co-Glycolide) copolymer. J Biomater Nanobiotechnol. 2012;03(02):208–225.
  • Xiao RZ, Zeng ZW, Zhou GL, et al. Recent advances in PEG-PLA block copolymer nanoparticles. Int J Nanomed. 2010;5:1057–1065.
  • Taha MA, Singh SR, Dennis VA. Biodegradable PLGA85/15 nanoparticles as a delivery vehicle for Chlamydia trachomatis recombinant MOMP-187 peptide. Nanotechnology. 2012;23(32):325101.
  • Indu Bala SH, Ravi Kumar MNV. PLGA nanoparticles in drug delivery: the state of the art. Crit Rev Ther Drug Carrier Syst. 2004;21(5):387–422.
  • Lutsiak ME, Kwon GS, Samuel J. Biodegradable nanoparticle delivery of a Th2-biased peptide for induction of Th1 immune responses. J Pharm Pharmacol. 2006;58(6):739–747.
  • Eko FO, He Q, Brown T, et al. A novel recombinant multisubunit vaccine against chlamydia. J Immunol. 2004;173(5):3375–3382.
  • Dai C, Wang B, Zhao H. Microencapsulation peptide and protein drugs delivery system. Colloids Surf B Biointerfaces. 2005;41(2–3):117–120.
  • Jiang P, Cai Y, Chen J, et al. Evaluation of tandem Chlamydia trachomatis MOMP multi-epitopes vaccine in BALB/c mice model. Vaccine. 2017;35(23):3096–3103.
  • O’Meara CP, Armitage CW, Harvie MC, et al. Immunization with a MOMP-based vaccine protects mice against a pulmonary chlamydia challenge and identifies a disconnection between infection and pathology. PLoS One. 2013;8(4):e61962.
  • Singh SR, Hulett K, Pillai SR, et al. Mucosal immunization with recombinant MOMP genetically linked with modified cholera toxin confers protection against Chlamydia trachomatis infection. Vaccine. 2006;24(8):1213–1224.
  • Fu C, Sun X, Liu D, et al. Biodegradable tri-block copolymer poly(lactic acid)-poly(ethylene glycol)-poly(l-lysine)(PLA-PEG-PLL) as a non-viral vector to enhance gene transfection. Int J Mol Sci. 2011;12(2):1371–1388.
  • Xu Q, Ensign LM, Boylan NJ, et al. Impact of surface polyethylene glycol (PEG) density on biodegradable nanoparticle transport in mucus ex vivo and distribution in vivo. ACS Nano. 2015;9(9):9217–9227.
  • Zou W, Liu C, Chen Z, et al. Characterization of cationic PLA-PEG nanoparticles for delivery of plasmid DNA. Nanoscale Res Lett. 2009;4(9):982–992.
  • Grossen P, Witzigmann D, Sieber S, et al. PEG-PCL-based nanomedicines: a biodegradable drug delivery system and its application. J Control Release. 2017;260:46–60.
  • Radovic-Moreno AF, Lu TK, Puscasu VA, et al. Surface charge-switching polymeric nanoparticles for bacterial cell wall-targeted delivery of antibiotics. ACS Nano. 2012;6(5):4279–4287.
  • Boje S, Olsen AW, Erneholm K, et al. A multi-subunit Chlamydia vaccine inducing neutralizing antibodies and strong IFN-gamma(+) CMI responses protects against a genital infection in minipigs. Immunol Cell Biol. 2016;94(2):185–195.
  • Lebel ME, Daudelin JF, Chartrand K, et al. Nanoparticle adjuvant sensing by TLR7 enhances CD8+ T cell-mediated protection from Listeria monocytogenes infection. J Immunol. 2014;192(3):1071–1078.
  • Cheng C, Jain P, Bettahi I, et al. de la Maza LM. A TLR2 agonist is a more effective adjuvant for a Chlamydia major outer membrane protein vaccine than ligands to other TLR and NOD receptors. Vaccine. 2011;29(38):6641–6649.
  • Swaminathan G, Thoryk EA, Cox KS, et al. A novel lipid nanoparticle adjuvant significantly enhances B cell and T cell responses to sub-unit vaccine antigens. Vaccine. 2016;34(1):110–119.
  • Wilson KL, Xiang SD, Plebanski M. Montanide, Poly I:C and nanoparticle based vaccines promote differential suppressor and effector cell expansion: a study of induction of CD8 T cells to a minimal Plasmodium berghei epitope. Front Microbiol. 2015;6:29.
  • Jang SI, Lillehoj HS, Lee SH, et al. Montanide IMS 1313 N VG PR nanoparticle adjuvant enhances antigen-specific immune responses to profilin following mucosal vaccination against Eimeria acervulina. Vet Parasitol. 2011;182(2–4):163–170.
  • Waghmare A, Deopurkar RL, Salvi N, et al. Comparison of Montanide adjuvants, IMS 3012 (Nanoparticle), ISA 206 and ISA 35 (Emulsion based) along with incomplete Freund’s adjuvant for hyperimmunization of equines used for production of polyvalent snake antivenom. Vaccine. 2009;27(7):1067–1072.
  • Kachura MA, Hickle C, Kell SA, et al. A CpG-Ficoll nanoparticle adjuvant for anthrax protective antigen enhances immunogenicity and provides single-immunization protection against inhaled anthrax in monkeys. J Immunol. 2016;196(1):284–297.
  • Miura N, Shaheen SM, Akita H, et al. A KALA-modified lipid nanoparticle containing CpG-free plasmid DNA as a potential DNA vaccine carrier for antigen presentation and as an immune-stimulative adjuvant. Nucleic Acids Res. 2015;43(3):1317–1331.
  • Wern JE, Sorensen MR, Olsen AW, et al. Simultaneous subcutaneous and intranasal administration of a CAF01-adjuvanted chlamydia vaccine elicits elevated IgA and protective Th1/Th17 responses in the genital tract. Front Immunol. 2017;8:569.
  • Ralli-Jain P, Tifrea D, Cheng C, et al. de la Maza LM. Enhancement of the protective efficacy of a Chlamydia trachomatis recombinant vaccine by combining systemic and mucosal routes for immunization. Vaccine. 2010;28(48):7659–7666.
  • Brown TH, David J, Acosta-Ramirez E, et al. Comparison of immune responses and protective efficacy of intranasal prime-boost immunization regimens using adenovirus-based and CpG/HH2 adjuvanted-subunit vaccines against genital Chlamydia muridarum infection. Vaccine. 2012;30(2):350–360.
  • Semete B, Booysen L, Lemmer Y, et al. In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomedicine. 2010;6(5):662–671.
  • Childs TS, Webley WC. In vitro assessment of chlamydial antigen display, delivery and processing by halobacterial gas vesicles. In: 2011 ASM general meeting; 2011; Session 197; Abstract #2215.
  • Bode C, Zhao G, Steinhagen F, et al. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines. 2011;10(4):499–511.
  • Cambridge CD, Singh SR, Waffo AB, et al. Formulation, characterization, and expression of a recombinant MOMP Chlamydia trachomatis DNA vaccine encapsulated in chitosan nanoparticles. Int J Nanomed. 2013;8:1759–1771.
  • Schijns VE, Lavelle EC. Trends in vaccine adjuvants. Expert Rev Vaccines. 2011;10(4):539–550.

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