Intranasal delivery of Salmonella OMVs decorated with Chlamydia trachomatis antigens induces specific local and systemic immune responses

References

• Newman L, Rowley J, Hoorn SV, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M. 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;10:1–12. doi:10.1371/journal.pone.0143304.
   Web of Science ®Google Scholar
• Schautteet K, De Clercq E, Vanrompay D. Chlamydia trachomatis vaccine research through the years. Infect Dis Obstet Gynecol. 2011;2011:1–9. doi:10.1155/2011/963513.
   Google Scholar
• Christensen S, McMahon RM, Martin JL, Huston WM. Life inside and out: making and breaking protein disulfide bonds in Chlamydia. Crit Rev Microbiol. 2019;45:33–50. doi:10.1080/1040841X.2018.1538933.
   PubMed Web of Science ®Google Scholar
• Panzetta ME, Valdivia RH, Saka HA. Chlamydia persistence: a survival strategy to evade antimicrobial effects in-vitro and in-vivo. Front Microbiol. 2018;9:1–11. doi:10.3389/fmicb.2018.03101.
   PubMed Web of Science ®Google Scholar
• Borges ÁH, Follmann F, Dietrich J. Chlamydia trachomatis vaccine development–a view on the current challenges and how to move forward. Expert Rev Vaccines. 2022;21(11):1555–1567. doi:10.1080/14760584.2022.2117694.
   PubMed Web of Science ®Google Scholar
• Murray SM, McKay PF. Chlamydia trachomatis: cell biology, immunology and vaccination. Vaccine. 2021;39(22):2965–2975. doi:10.1016/j.vaccine.2021.03.043.
   PubMed Web of Science ®Google Scholar
• Wong WF, Chambers JP, Gupta R, Arulanandam BP. Chlamydia and its many ways of escaping the host immune system. J Pathog. 2019;2019:1–9. doi:10.1155/2019/8604958.
   Web of Science ®Google Scholar
• Azegami T, Yuki Y, Kiyono H. Challenges in mucosal vaccines for the control of infectious diseases. Int Immunol. 2014;26(9):517–528. doi:10.1093/intimm/dxu063.
   PubMed Web of Science ®Google Scholar
• Brandtzaeg P. Induction of secretory immunity and memory at mucosal surfaces. Vaccine. 2007;25(30):5467–5484. doi:10.1016/j.vaccine.2006.12.001.
   PubMed Web of Science ®Google Scholar
• Raeven RHM, Rockx-Brouwer D, Kanojia G, van der Maas L, Bindels THE, ten Have R, van Riet E, Metz B, Kersten GFA. Intranasal immunization with outer membrane vesicle pertussis vaccine confers broad protection through mucosal IgA and Th17 responses. Sci Rep. 2020;10(1):1–11. doi:10.1038/s41598-020-63998-2.
   PubMed Web of Science ®Google Scholar
• van der Ley PA, Zariri A, van Riet E, Oosterhoff D, Kruiswijk CP. An intranasal OMV-based vaccine induces high mucosal and systemic protecting immunity against a SARS-CoV-2 infection. Front Immunol. 2021 Aug 25;12:457644. doi:10.3389/fimmu.2021.781280.
   Web of Science ®Google Scholar
• Jiang L, Driedonks TAP, Jong WSP, Dhakal S, Bart van den Berg van Saparoea H, Sitaras I, Zhou R, Caputo C, Littlefield K, Lowman M, et al. A bacterial extracellular vesicle‐based intranasal vaccine against SARS‐CoV‐2 protects against disease and elicits neutralizing antibodies to wild‐type and Delta variants. J Extracell Vesicles. 2022;11(3):11. doi:10.1002/jev2.12192.
   Web of Science ®Google Scholar
• Sartorio MG, Pardue EJ, Feldman MF, Haurat MF. Bacterial outer membrane vesicles: from discovery to applications. Annu Rev Microbiol. 2021;75(1):609–630. doi:10.1146/annurev-micro-052821-031444.
   PubMedGoogle Scholar
• Long Q, Zheng P, Zheng X, Li W, Hua L, Yang Z, Huang W, Ma Y. Engineered bacterial membrane vesicles are promising carriers for vaccine design and tumor immunotherapy. Adv Drug Deliv Rev. 2022;186:114321. doi:10.1016/j.addr.2022.114321.
   PubMed Web of Science ®Google Scholar
• Daleke-Schermerhorn MH, Felix T, Soprova Z, ten Hagen-Jongman CM, Vikström D, Majlessi L, Beskers J, Follmann F, de Punder K, van der Wel NN, et al. Decoration of outer membrane vesicles with multiple antigens by using an autotransporter approach. Appl Environ Microbiol. 2014;80(18):5854–5865. doi:10.1128/AEM.01941-14.
   PubMed Web of Science ®Google Scholar
• Kuipers K, Jong WSP, van der Gaast-de Jongh CE, Houben D, van Opzeeland F, Simonetti E, van Selm S, de Groot R, Koenders MI, Azarian T, et al. Th17-mediated cross protection against pneumococcal carriage by vaccination with a variable antigen. Infect Immun. 2017;85(10):1–13. doi:10.1128/IAI.00281-17.
   Web of Science ®Google Scholar
• Schetters STT, Jong WSP, Horrevorts SK, Kruijssen LJW, Engels S, Stolk D, Daleke-Schermerhorn MH, Garcia-Vallejo J, Houben D, Unger WWJ, et al. Outer membrane vesicles engineered to express membrane-bound antigen program dendritic cells for cross-presentation to CD8+ T cells. Acta Biomater. 2019;91:248–257. doi:10.1016/j.actbio.2019.04.033.
   PubMed Web of Science ®Google Scholar
• Kuipers K, Daleke-Schermerhorn MH, Jong WSP, ten Hagen-Jongman CM, van Opzeeland F, Simonetti E, Luirink J, de Jonge MI. Salmonella outer membrane vesicles displaying high densities of pneumococcal antigen at the surface offer protection against colonization. Vaccine. 2015;33:2022–2029. doi:10.1016/j.vaccine.2015.03.010.
   PubMed Web of Science ®Google Scholar
• Hays MP, Houben D, Yang Y, Luirink J, Hardwidge PR. Immunization with Skp delivered on outer membrane vesicles protects mice against enterotoxigenic Escherichia coli challenge. Front Cell Infect Microbiol. 2018;8:1–5. doi:10.3389/fcimb.2018.00132.
   PubMed Web of Science ®Google Scholar
• Phan TH, Kuijl C, Huyn D, Jong WSP, Luirink J, Van Ulsen P. Overproducing the BAM complex improves secretion of difficult-to-secrete recombinant autotransporter chimeras. Microb Cell Fact. 2021;20(1):1–17. doi:10.1186/s12934-021-01668-2.
   PubMed Web of Science ®Google Scholar
• van den Berg van Saparoea HB, Houben D, de Jonge MI, Jong WSP, Luirink J. Display of recombinant proteins on bacterial outer membrane vesicles by using protein ligation. Appl Environ Microbiol. 2018;84:1–17. doi:10.1128/AEM.02567-17.
   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(6):978–989. doi:10.1093/infdis/jiv137.
   PubMed Web of Science ®Google Scholar
• Tagawa Y, Ishikawa H, Yuasa N. Purification and partial characterization of the major outer membrane protein of Haemophilus somnus. Infect Immun. 1993;61(1):91–96. doi:10.1128/iai.61.1.91-96.1993.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Marañón MJ, Bush RM, Peterson EM, Schirmer T, de la Maza LM. Prediction of the membrane-spanning β-strands of the major outer membrane protein of Chlamydia. Protein Sci. 2009;11:1854–1861. doi:10.1110/ps.3650102.
   Google Scholar
• Abraham S, Juel HB, Bang P, Cheeseman HM, Dohn RB, Cole T, Kristiansen MP, Korsholm KS, Lewis D, Olsen AW, et al. Safety and immunogenicity of the chlamydia vaccine candidate CTH522 adjuvanted with CAF01 liposomes or aluminium hydroxide: a first-in-human, randomised, double-blind, placebo-controlled, phase 1 trial. Lancet Infect Dis. 2019;19(10):1091–1100. doi:10.1016/S1473-3099(19)30279-8.
   PubMed Web of Science ®Google Scholar
• Backert S, Bernegger S, Skórko-Glonek J, Wessler S. Extracellular HtrA serine proteases: an emerging new strategy in bacterial pathogenesis. Cell Microbiol. 2018;20(6):1–9. doi:10.1111/cmi.12845.
   Web of Science ®Google Scholar
• Skorko-Glonek J, Zurawa-Janicka D, Koper T, Jarzab M, Figaj D, Glaza P, Lipinska B. HtrA protease family as therapeutic targets. Curr Pharm Des. 2012;19(6):977–1009. doi:10.2174/1381612811319060003.
   Web of Science ®Google Scholar
• Skorko-Glonek J, Figaj D, Zarzecka U, Przepiora T, Renke J, Lipinska B. The extracellular bacterial HtrA proteins as potential therapeutic targets and vaccine candidates. Curr Med Chem. 2017;24(20). doi:10.2174/0929867323666161223145825.
   PubMed Web of Science ®Google Scholar
• Wu X, Lei L, Gong S, Chen D, Flores R, Zhong G. The chlamydial periplasmic stress response serine protease cHtrA is secreted into host cell cytosol. BMC Microbiol. 2011;11(1):11. doi:10.1186/1471-2180-11-87.
   PubMedGoogle Scholar
• Huston WM, Theodoropoulos C, Mathews SA, Timms P. Chlamydia trachomatis responds to heat shock, penicillin induced persistence, and IFN-gamma persistence by altering levels of the extracytoplasmic stress response protease HtrA. BMC Microbiol. 2008;8(1):1–16. doi:10.1186/1471-2180-8-190.
   PubMedGoogle Scholar
• Rantsi T, Land JA, Joki-Korpela P, Ouburg S, Hokynar K, Paavonen J, Tiitinen A, Puolakkainen M. Predictive values of serum chlamydia trachomatis troa and htra igg antibodies as markers of persistent infection in the detection of pelvic adhesions and tubal occlusion. Microorganisms. 2019;7(10):1–10. doi:10.3390/microorganisms7100391.
   Web of Science ®Google Scholar
• Huston WM, Swedberg JE, Harris JM, Walsh TP, Mathews SA, Timms P. The temperature activated HtrA protease from pathogen Chlamydia trachomatis acts as both a chaperone and protease at 37 °C. FEBS Lett. 2007;581(18):3382–3386. doi:10.1016/j.febslet.2007.06.039.
   PubMed Web of Science ®Google Scholar
• Mamat U, Woodard RW, Wilke K, Souvignier C, Mead D, Steinmetz E, Terry K, Kovacich C, Zegers A, Knox C. Endotoxin-free protein production—ClearColiTM technology. Nat Methods. 2013;10:916–916. doi:10.1038/nmeth.f.367.
   Google Scholar
• Keeble AH, Banerjee A, Ferla MP, Reddington SC, Anuar INAK, Howarth M. Evolving accelerated amidation by SpyTag/SpyCatcher to analyze membrane dynamics. Angew Chem - Int Ed. 2017;56:16521–16525. doi:10.1002/anie.201707623.
   PubMed Web of Science ®Google Scholar
• van Beek LF, Surmann K, van den Berg van Saparoea HB, Houben D, Jong WSP, Hentschker C, Ederveen THA, Mitsi E, Ferreira DM, van Opzeeland F, et al. Exploring metal availability in the natural niche of streptococcus pneumoniae to discover potential vaccine antigens. Virulence. 2020;11:1310–1328. doi:10.1080/21505594.2020.1825908.
   PubMedGoogle Scholar
• Van Beek LF, Langereis JD, Van Saparoea HBVDB, Gillard J, Jong WSP, Van Opzeeland FJ, Mesman R, Van Niftrik L, Joosten I, Diavatopoulos DA, et al. Intranasal vaccination with protein bodies elicit strong protection against Streptococcus pneumoniae colonization Intranasal vaccination with protein bodies elicit strong protection against Streptococcus pneumoniae colonization. Vaccine. 2021;39:6920–6929. doi:10.1016/j.vaccine.2021.10.006.
   PubMed Web of Science ®Google Scholar
• Huynh DT, Jong WSP, Koningstein GM, Van Ulsen P, Luirink J. Overexpression of the bam complex improves the production of Chlamydia trachomatis MOMP in the E. coli outer membrane. Int J Mol Sci. 2022;23(13):1–16. doi:10.3390/ijms23137393.
   Web of Science ®Google Scholar
• Zarzecka U, Modrak-Wójcik A, Figaj D, Apanowicz M, Lesner A, Bzowska A, Lipinska B, Zawilak-Pawlik A, Backert S, Skorko-Glonek J. Properties of the HtrA protease from bacterium Helicobacter pylori whose activity is indispensable for growth under stress conditions. Front Microbiol. 2019;10:1–16. doi:10.3389/fmicb.2019.00961.
   PubMed Web of Science ®Google Scholar
• Albrecht N, Tegtmeyer N, Sticht H, Skórko-Glonek J, Backert S. Amino-terminal processing of Helicobacter pylori serine protease HtrA: role in oligomerization and activity regulation. Front Microbiol. 2018;9:1–16. doi:10.3389/fmicb.2018.00642.
   PubMed Web of Science ®Google Scholar
• Badamchi-Zadeh A, McKay PF, Korber BT, Barinaga G, Walters AA, Nunes A, Gomes JP, Follmann F, Tregoning JS, Shattock RJ. A multi-component prime-boost vaccination regimen with a consensus MOMP antigen enhances Chlamydia trachomatis clearance. Front Immunol. 2016;7. doi:10.3389/fimmu.2016.00162.
   PubMed Web of Science ®Google Scholar
• Olivares-Zavaleta N, Whitmire WM, Kari L, Sturdevant GL, Caldwell HD. CD8 + T cells define an unexpected role in live-attenuated vaccine protective immunity against Chlamydia trachomatis infection in Macaques. J Immunol. 2014;192(10):4648–4654. doi:10.4049/jimmunol.1400120.
   PubMed Web of Science ®Google Scholar
• Platteel ACM, Marit de Groot A, Keller C, Andersen P, Ovaa H, Kloetzel PM, Mishto M, Sijts AJAM. Strategies to enhance immunogenicity of cDNA vaccine encoded antigens by modulation of antigen processing. Vaccine. 2016;34(42):5132–5140. doi:10.1016/j.vaccine.2016.08.039.
   PubMed Web of Science ®Google Scholar
• Harrer A, Boehm M, Backert S, Tegtmeyer N. Overexpression of serine protease HtrA enhances disruption of adherens junctions, paracellular transmigration and type IV secretion of CagA by Helicobacter pylori. Gut Pathog. 2017;9(1):1–12. doi:10.1186/s13099-017-0189-6.
   PubMedGoogle Scholar
• Wern JE, Sorensen MR, Olsen AW, Andersen P, Follmann F. 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;8:1–11. doi:10.3389/fimmu.2017.00569.
   PubMed Web of Science ®Google Scholar
• Dieu N, Tran N, Olsen AW, Follmann F. Th1/Th17 T cell tissue-resident immunity increases protection, but is not required in a vaccine strategy against genital infection with Chlamydia trachomatis. Front Immunol. 2021;12:1–12. doi:10.3389/fimmu.2021.790463.
   Web of Science ®Google Scholar
• Coleman MA, Lorenzen E, Contreras V, Olsen AW, Andersen P, Desjardins D, Rosenkrands I, Juel HB, Delache B, Langlois S, et al. Chlamydia trachomatis vaccination regimes induce antibody and T cell responses and accelerate clearance of infection in a non-human primate model. Front Immunol. 2022;13:1–13. doi:10.3389/fimmu.2022.1057375.
   Web of Science ®Google Scholar
• Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res. 2008;36:509–512. doi:10.1093/nar/gkn202.
   PubMed Web of Science ®Google Scholar
• Du G, Qin M, Sun X. Recent progress in application of nanovaccines for enhancing mucosal immune responses. Acta Pharm Sin B. 2022;13(6):2334–2345. doi:10.1016/j.apsb.2022.08.010.
   PubMed Web of Science ®Google Scholar
• Knisely JM, Buyon LE, Mandt R, Farkas R, Balasingam S, Bok K, Buchholz UJ, Souza MPD, Gordon JL, King DFL, et al. Mucosal vaccines for SARS-CoV-2: scienti fi c gaps and opportunities — workshop report. NPJ Vaccines. 2022;8(1):1–7. doi:10.1038/s41541-023-00654-6.
   Web of Science ®Google Scholar
• Huynh DT, Jong WSP, Oudejans MAH, van den Berg van Saparoea HB, Luirink J, Van Ulsen P. Heterologous display of Chlamydia trachomatis PmpD passenger at the surface of Salmonella OMVs. Membranes. 2023;13(4):1–18. doi:10.3390/membranes13040366.
   Web of Science ®Google Scholar
• Ma H, Cummins DD, Edelstein NB, Gomez J, Khan A, Llewellyn MD, Picudella T, Willsey SR, Nangia S. Modeling diversity in structures of bacterial outer membrane lipids. J Chem Theory Comput. 2017;13(2):811–824. doi:10.1021/acs.jctc.6b00856.
   PubMed Web of Science ®Google Scholar
• Bartolini E, Ianni E, Frigimelica E, Petracca R, Galli G, Scorza FB, Norais N, Laera D, Giusti F, Pierleoni A, et al. Recombinant outer membrane vesicles carrying Chlamydia muridarum HtrA induce antibodies that neutralize chlamydial infection in vitro. J Extracell Vesicles. 2013;2. doi:10.3402/jev.v2i0.20181.
   PubMedGoogle Scholar
• Irene C, Fantappiè L, Caproni E, Zerbini F, Anesi A, Tomasi M, Zanella I, Stupia S, Prete S, Valensin S, et al. Bacterial outer membrane vesicles engineered with lipidated antigens as a platform for Staphylococcus aureus vaccine. Proc Natl Acad Sci USA. 2019;116(43):21780–21788. doi:10.1073/pnas.1905112116.
   PubMed Web of Science ®Google Scholar
• Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol. 2006;6(2):148–158. doi:10.1038/nri1777.
   PubMed Web of Science ®Google Scholar
• Lorenzen E, Follmann F, Bøje S, Erneholm K, Olsen AW, Agerholm JS, Jungersen G, Andersen P. Intramuscular priming and intranasal boosting induce strong genital immunity through secretory IgA in minipigs infected with Chlamydia trachomatis. Front Immunol. 2015;6:1–12. doi:10.3389/fimmu.2015.00628.
   PubMed Web of Science ®Google Scholar
• Garcia-Del Rio L, Diaz-Rodriguez P, Pedersen GK, Christensen D, Landin M. Sublingual boosting with a novel mucoadhesive thermogelling hydrogel following parenteral CAF01 priming as a strategy against Chlamydia trachomatis. Adv Healthc Mater. 2022;2102508:1–9. doi:10.1002/adhm.202102508.
   Google Scholar
• Kuczkowska K, Myrbråten I, Øverland L, Eijsink VGH, Follmann F, Mathiesen G, Dietrich J, Dean D. Lactobacillus plantarum producing a Chlamydia trachomatis antigen induces a specific IgA response after mucosal booster immunization. PLoS One. 2017;12(5):1–16. doi:10.1371/journal.pone.0176401.
   Web of Science ®Google Scholar
• Brandtzaeg P, Farstad IN, Haraldsen G. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol Today. 1999;20(6):267–277. doi:10.1016/S0167-5699(99)01468-1.
   PubMedGoogle Scholar
• Rose F, Wern JE, Gavins F, Andersen P, Follmann F, Foged C. A strong adjuvant based on glycol-chitosan-coated lipid-polymer hybrid nanoparticles potentiates mucosal immune responses against the recombinant Chlamydia trachomatis fusion antigen CTH522. J Controlled Release. 2018;271:88–97. doi:10.1016/j.jconrel.2017.12.003.
   PubMed Web of Science ®Google Scholar
• Mestecky J, Moldoveanu Z, Russell MW. Immunologic uniqueness of the genital tract: challenge for vaccine development. Am J Reprod Immunol. 2005;53(5):208–214. doi:10.1111/j.1600-0897.2005.00267.x.
   PubMed Web of Science ®Google Scholar
• 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. 1983;39(3):1491–1494. doi:10.1128/iai.39.3.1491-1494.1983.
   PubMed Web of Science ®Google Scholar
• Nguyen NDNT, Olsen AW, Lorenzen E, Andersen P, Hvid M, Follmann F, Dietrich J. Parenteral vaccination protects against transcervical infection with Chlamydia trachomatis and generate tissue-resident T cells post-challenge. NPJ Vaccines [Internet]. 2020;5(1):1–12. doi:10.1038/s41541-020-0157-x.
   PubMed Web of Science ®Google Scholar
• Liang S, Bulir D, Kaushic C, Mahony J. Considerations for the rational design of a Chlamydia vaccine. Hum Vaccin Immunother [Internet]. 2017;13:831–835. doi:10.1080/21645515.2016.1252886.
   PubMed Web of Science ®Google Scholar
• Brunham RC. Problems with understanding Chlamydia trachomatis immunology. J Infect Dis. 2022;225:2043–2049. doi:10.1093/infdis/jiab610.
   PubMed Web of Science ®Google Scholar
• Lorenzen E, Contreras V, Olsen AW, Andersen P, Desjardins D, Rosenkrands I, Juel HB, Delache B, Langlois S, Delaugerre C, et al. Multi-component prime-boost Chlamydia trachomatis vaccination regimes induce antibody and T cell responses and accelerate clearance of infection in a non-human primate model. Front Immunol. 2022;13. doi:10.3389/fimmu.2022.1057375.
   PubMed Web of Science ®Google Scholar
• Wang P, Sidney J, Dow C, Mothé B, Sette A, Peters B, Stormo G. A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput Biol. 2008;4(4):4. doi:10.1371/journal.pcbi.1000048.
   Web of Science ®Google Scholar
• Tindle RW, Croft S, Herd K, Malcolm K, Geczy AF, Stewart T, Fernando GJP, Hospital A. A vaccine conjugate of ‘ISCAR’ immunocarrier and peptide epitopes of the E7 cervical cancer-associated protein of human papillomavirus type 16 elicits specific Th1- and Th2-type responses in immunized mice in the absence of oil-based adjuvants. Clin Exp Immunol. 1995;101:265–271. doi:10.1111/j.1365-2249.1995.tb08349.x.
   PubMed Web of Science ®Google Scholar
• Sturdevant GL, Caldwell HD. Innate immunity is sufficient for the clearance of Chlamydia trachomatis from the female mouse genital tract. Pathog Dis. 2014;72(1):70–73. doi:10.1111/2049-632X.12164.
   PubMed Web of Science ®Google Scholar
• Rajeeve K, Sivadasan R. Transcervical mouse infections with Chlamydia trachomatis and determination of bacterial burden. Bio Protoc. 2020;10:10. doi:10.21769/BioProtoc.3506.
   Web of Science ®Google Scholar
• van den Berg van Saparoea HB, Houben D, Kuijl C, Luirink J, Jong WSP. Combining protein ligation systems to expand the functionality of semi-synthetic outer membrane vesicle nanoparticles. Front Microbiol. 2020;11:1–10. doi:10.3389/fmicb.2020.00890.
   PubMed Web of Science ®Google Scholar