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Review Article

Outer membrane proteins and vesicles as promising vaccine candidates against Vibrio spp. infections

, &
Received 19 Oct 2022, Accepted 02 May 2023, Published online: 05 Jun 2023

References

  • Alaniz RC, Deatherage BL, Lara JC, Cookson BT. 2007. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol. 179(11):7692–7701.
  • Asaduzzaman M, Ryan ET, John M, Hang L, Khan AI, Faruque ASG, Taylor RK, Calderwood SB, Qadri F. 2004. The major subunit of the toxin-coregulated pilus TcpA induces mucosal and systemic immunoglobulin A immune responses in patients with cholera caused by Vibrio cholerae O1 and O139. Infect Immun. 72(8):4448–4454.
  • Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK, Qadri F, Martinez-Urtaza J. 2018. Vibrio spp. infections. Nat Rev Dis Primers. 4(1):8.
  • Baker-Austin C, Stockley L, Rangdale R, Martinez?Urtaza J. 2010. Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ Microbiol Rep. 2(1):7–18.
  • Berczi I, Bertok L, Bereznai T. 1966. Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can J Microbiol. 12(5):1070–1071.
  • Bielig H, Rompikuntal PK, Dongre M, Zurek B, Lindmark B, Ramstedt M, Wai SN, Kufer TA. 2011. NOD-like receptor activation by outer membrane vesicles from Vibrio cholerae non-O1 non-O139 strains is modulated by the quorum-sensing regulator HapR. Infect Immun. 79(4):1418–1427.
  • Bishop AL, Schild S, Patimalla B, Klein B, Camilli A. 2010. Mucosal immunization with Vibrio cholerae outer membrane vesicles provides maternal protection mediated by antilipopolysaccharide antibodies that inhibit bacterial motility. Infect Immun. 78(10):4402–4420.
  • Bishop AL, Tarique AA, Patimalla B, Calderwood SB, Qadri F, Camilli A. 2012. Immunization of mice with Vibrio cholerae outer-membrane vesicles protects against hyperinfectious challenge and blocks transmission. J Infect Dis. 205(3):412–421.
  • Bitar A, Aung KM, Wai SN, Hammarström ML. 2019. Vibrio cholerae derived outer membrane vesicles modulate the inflammatory response of human intestinal epithelial cells by inducing microRNA-146a. Sci Rep. 9(1):1–11.
  • Bittel M, Reichert P, Sarfati I, Dressel A, Leikam S, Uderhardt S, Stolzer I, Phu TA, Ng M, Vu NK, et al. 2021. Visualizing transfer of microbial biomolecules by outer membrane vesicles in microbe?host?communication in vivo. J Extracell Vesicles. 10(12):e12159.
  • Botos I, Majdalani N, Mayclin SJ, McCarthy JG, Lundquist K, Wojtowicz D, Barnard TJ, Gumbart JC, Buchanan SK. 2016. Structural and functional characterization of the LPS transporter LptDE from Gram-negative pathogens. Structure. 24(6):965–976.
  • Cai SH, Yao SY, Lu YS, Wu ZH, Jian JC, Wang B. 2010. Immune response in Lutjanus erythropterus induced by the major outer membrane protein (OmpU) of Vibrio alginolyticus. Dis Aquat Organ. 90(1):63–68.
  • [CDC] Centers for Disease Control 2017. Vibrio species causing Vibriosis CDC
  • Chakrabarti D, Chatterjee AN. 1984. Studies on heterogeneous lipopolysaccharide fractions of Vibrio cholerae 569B. J Gen Microbiol. 130(8):2023–2026.
  • Chakrabarti SR, Chaudhuri K, Sen K, Das J. 1996. Porins of Vibrio cholerae: purification and characterization of OmpU. J Bacteriol. 178(2):524–530.
  • Chatterjee D, Chaudhuri K. 2013. Vibrio cholerae 0395 outer membrane vesicles modulate intestinal epithelial cells in a NODI protein-dependent manner and induce dendritic cell-mediated Th2/Th17 cell responses. J Biol Chem. 288(6):4299–4309.
  • Clemens J, Shin S, Sur D, Nair GB, Holmgren J. 2011. New-generation vaccines against cholera. Nat Rev Gastroenterol Hepatol. 8(12):701–710.
  • Cowan SW, Garavito RM, Jansonius JN, Jenkins JA, Karlsson R, König N, Pai EF, Pauptit RA, Rizkallah PJ, Rosenbusch JP, et al. 1995. The structure of OmpF porin in a tetragonal crystal form. Structure. 3(10):1041–1050.
  • Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M, Lloyd SJ, Shin DS, Getzoff ED, Yeager M, et al. 2003. Type IV pilin structure and assembly: x -ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell. 11(5):1139–1150.
  • Domínguez-Medina CC, Pérez-Toledo M, Schager AE, Marshall JL, Cook CN, Bobat S, Hwang H, Chun BJ, Logan E, Bryant JA, et al. 2020. Outer membrane protein size and LPS O-antigen define protective antibody targeting to the Salmonella surface. Nat Commun. 11(1):851.
  • Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG, Stansfeld PJ, He C, Zhang Y, Wang W, Dong C. 2014. Structural basis for outer membrane lipopolysaccharide insertion. Nature. 511(7507):52–56.
  • Duret G, Delcour AH. 2006. Deoxycholic acid blocks Vibrio cholerae OmpT but not OmpU porin. J Biol Chem. 281(29):19899–19905.
  • Elluri S, Enow C, Vdovikova S, Rompikuntal PK, Dongre M, Carlsson S, Pal A, Uhlin BE, Wai SN. 2014. Outer membrane vesicles mediate transport of biologically active Vibrio cholerae cytolysin (VCC) from V. cholerae strains. PLoS One. 9(9):e106731.
  • Franklin MW, Slusky JS. 2018. Tight turns of outer membrane proteins: an analysis of sequence, structure, and hydrogen bonding. J Mol Biol. 430(18 Pt B):3251–3265.
  • Fu X, Zhang J, Li T, Zhang M, Li J, Kan B. 2017. The outer membrane protein OmpW enhanced V. cholerae growth in hypersaline conditions by transporting carnitine. Front Microbiol. 8:2703.
  • Fujihara M, Muroi M, Tanamoto KI, Suzuki T, Azuma H, Ikeda H. 2003. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol Ther. 100(2):171–194.
  • Furuyama N, Sircili MP. 2021. Outer membrane vesicles (OMVs) produced by Gram-negative bacteria: structure, functions, biogenesis, and vaccine application. Biomed Res Int. 2021:1–16.
  • Gnopo YM, Watkins HC, Stevenson TC, DeLisa MP, Putnam D. 2017. Designer outer membrane vesicles as immunomodulatory systems–Reprogramming bacteria for vaccine delivery. Adv Drug Deliv Rev. 114:132–142.
  • Goo SY, Lee H-J, Kim WH, Han K-L, Park D-K, Lee H-J, Kim SM, Kim K-S, Lee K-H, Park S-J. 2006. Identification of OmpU of Vibrio vulnificus as a fibronectin-binding protein and its role in bacterial pathogenesis. Infect Immun. 74(10):5586–5594.
  • Gulati A, Kumar R, Mukhopadhaya A. 2019. Differential recognition of Vibrio parahaemolyticus OmpU by Toll-like receptors in monocytes and macrophages for the induction of pro-inflammatory responses. Infect Immun. 87(5):e00809-18.
  • Hall RH, Losonsky G, Silveira AP, Taylor RK, Mekalanos JJ, Witham ND, Levine MM. 1991. Immunogenicity of Vibrio cholerae O1 toxin-coregulated pili in experimental and clinical cholera. Infect Immun. 59(7):2508–2512.
  • Hang L, John M, Asaduzzaman M, Bridges EA, Vanderspurt C, Kirn TJ, Taylor RK, Hillman JD, Progulske-Fox A, Handfield M, et al. 2003. Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc Natl Acad Sci U S A. 100(14):8508–8513.
  • Hong H, Patel DR, Tamm LK, van den Berg B. 2006. The outer membrane protein OmpW forms an eight-stranded-barrel with a hydrophobic channel. J Biol Chem. 281(11):7568–7577.
  • Hubbard TP, Chao MC, Abel S, Blondel CJ, Abel Zur Wiesch P, Zhou X, Davis BM, Waldor MK. 2016. Genetic analysis of Vibrio parahaemolyticus intestinal colonization. Proc Natl Acad Sci U S A. 113(22):6283–6288.
  • Iliev DB, Liarte CQ, MacKenzie S, Goetz FW. 2005. Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular pattern (PAMP) bearing agents. Mol Immunol. 42(10):1215–1223.
  • Jalajakumari MB, Manning PA. 1990. Nucleotide sequence of the gene, ompW, encoding a 22kDa immunogenic outer membrane protein of Vibrio cholerae. Nucleic Acids Res. 18(8):2180.
  • Jones MK, Oliver JD. 2009. Vibrio vulnificus: disease and pathogenesis. Infect Immun. 77(5):1723–1733.
  • Jonson G, Holmgren J, Svennerholm AM. 1991. Epitope differences in toxin-coregulated pili produced by classical and El Tor Vibrio cholerae O1. Microb Pathog. 11(3):179–188.
  • Kaur D, Gandhi S, Mukhopadhaya A. 2021. Salmonella typhimurium adhesin OmpV activates host immunity to confer protection against systemic and gastrointestinal infection in mice. Infect Immun. 89(8):e0012121.
  • Kawai T, Takeuchi O, Fujita T, Inoue J, Mühlradt PF, Sato S, Hoshino K, Akira S. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol. 167(10):5887–5894.
  • Khan J, Sharma PK, Mukhopadhaya A. 2015. Vibrio cholerae porin OmpU mediates M1-polarization of macrophages/monocytes via TLR1/TLR2 activation. Immunobiology. 220(11):1199–1209.
  • Kim SW, Lee JS, Park SB, Lee AR, Jung JW, Chun JH, Lazarte JMS, Kim J, Seo J-S, Kim J-H, et al. 2020. The importance of porins and? -lactamase in outer membrane vesicles on the hydrolysis of? -lactam antibiotics. IJMS. 21(8):2822.
  • Kim YR, Kim BU, Kim SY, Kim CM, Na HS, Koh JT, Choy HE, Rhee JH, Lee SE. 2010. Outer membrane vesicles of Vibrio vulnificus deliver cytolysin-hemolysin VvhA into epithelial cells to induce cytotoxicity. Biochem Biophys Res Commun. 399(4):607–612.
  • Koebnik R, Locher KP, Van Gelder P. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol. 37(2):239–253.
  • Lange S, Magnadóttir B. 2003. Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum. Comp Biochem Physiol B Biochem Mol Biol. 136(1):99–106.
  • Lee J, Yoon YJ, Kim JH, Dinh NTH, Go G, Tae S, Park K-S, Park HT, Lee C, Roh T-Y, et al. 2018. Outer membrane vesicles derived from Escherichia coli regulate neutrophil migration by induction of endothelial IL-8. Front Microbiol. 9:2268.
  • Leitner DR, Feichter S, Schild-Prüfert K, Rechberger GN, Reidl J, Schild S. 2013. Lipopolysaccharide modifications of a cholera vaccine candidate based on outer membrane vesicles reduce endotoxicity and reveal the major protective antigen. Infect Immun. 81(7):2379–2393.
  • Li H, Zhang W, Dong C. 2018. Crystal structure of the outer membrane protein OmpU from Vibrio cholerae at 2.2 Å resolution. Acta Crystallogr D Struct Biol. 74(Pt 1):21–29.
  • Li N, Yang Z, Bai J, Fu X, Liu L, Shi C, Wu S. 2010. A shared antigen among Vibrio species: outer membrane protein-OmpK as a versatile Vibriosis vaccine candidate in Orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol. 28(5-6):952–956.
  • Longini IM, Jr, Nizam A, Ali M, Yunus M, Shenvi N, Clemens JD. 2007. Controlling endemic cholera with oral vaccines. PLoS Med. 4(11):e336.
  • Lv T, Dai F, Zhuang Q, Zhao X, Shao Y, Guo M, Lv Z, Li C, Zhang W. 2020. Outer membrane protein OmpU is related to iron balance in Vibrio alginolyticus. Microbiol Res. 230:126350.
  • Maiti B, Dubey S, Munang’Andu HM, Karunasagar I, Karunasagar I, Evensen Ø. 2020. Application of outer membrane protein-based vaccines against major bacterial fish pathogens in India. Front Immunol. 11:1362.
  • Mao Z, He C, Qiu Y, Chen J. 2011. Expression of Vibrio harveyi ompK in the yeast Pichia pastoris: the first step in developing an oral vaccine against Vibriosis? Aquaculture. 318(3-4):268–272.
  • Mathur J, Waldor MK. 2004. The Vibrio cholerae ToxR-regulated porin OmpU confers resistance to antimicrobial peptides. Infect Immun. 72(6):3577–3583.
  • Molaee N, Mosayebi G, Amozande-Nobaveh A, Soleyman MR, Abtahi H. 2017. Evolution of the Immune response against recombinant proteins (TcpA, TcpB, and FlaA) as a candidate subunit cholera vaccine. Journal of Immunology Research. 2017:1–8.
  • Mondal A, Tapader R, Chatterjee NS, Ghosh A, Sinha R, Koley H, Saha DR, Chakrabarti MK, Wai SN, Pal A. 2016. Cytotoxic and inflammatory responses induced by outer membrane vesicle-associated biologically active proteases from Vibrio cholerae. Infect Immun. 84(5):1478–1490.
  • Nandi B, Nandy RK, Sarkar A, Ghose AC. 2005. Structural features, properties and regulation of the outer-membrane protein W (OmpW) of Vibrio cholerae. Microbiology (Reading). 151(Pt 9):2975–2986.
  • Netea MG, van Deuren M, Kullberg BJ, Cavaillon JM, Van der Meer JW. 2002. Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol. 23(3):135–139.
  • Nezafat N, Karimi Z, Eslami M, Mohkam M, Zandian S, Ghasemi Y. 2016. Designing an efficient multi-epitope peptide vaccine against Vibrio cholerae via combined immunoinformatics and protein interaction based approaches. Comput Biol Chem. 62:82–95.
  • Nguyen HT, Nguyen TTT, Chen YC, Vu?Khac H, Wang PC, Chen SC. 2018. Enhanced immune responses and effectiveness of refined outer membrane protein vaccines against Vibrio harveyi in orange?spotted grouper (Epinephelus coioides). J Fish Dis. 41(9):1349–1358.
  • Nikaido H, Vaara M. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 49(1):1–32.
  • Ningqiu L, Junjie B, Shuqin W, Xiaozhe F, Haihua L, Xing Y, Cunbin S. 2008. An outer membrane protein, OmpK, is an effective vaccine candidate for Vibrio harveyi in Orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol. 25(6):829–833.
  • Okuda S, Sherman DJ, Silhavy TJ, Ruiz N, Kahne D. 2016. Lipopolysaccharide transport and assembly at the outer membrane: the PEZ model. Nat Rev Microbiol. 14(6):337–345.
  • Ou G, Rompikuntal PK, Bitar A, Lindmark B, Vaitkevicius K, Wai SN, Hammarström ML. 2009. Vibrio cholerae cytolysin causes an inflammatory response in human intestinal epithelial cells that is modulated by the PrtV protease. PLoS One. 4(11):e7806.
  • Pathania M, Acosta-Gutierrez S, Bhamidimarri SP, Baslé A, Winterhalter M, Ceccarelli M, van den Berg B. 2018. Unusual constriction zones in the major porins OmpU and OmpT from Vibrio cholerae. Structure. 26(5):708–721.e4.
  • Paul S, Chaudhuri K, Chatterjee AN, Das J. 1992. Presence of exposed phospholipids in the outer membrane of Vibrio cholerae. J Gen Microbiol. 138(4):755–761.
  • Payne SM, Mey AR, Wyckoff EE. 2016. Vibrio iron transport: evolutionary adaptation to life in multiple environments. Microbiol Mol Biol Rev. 80(1):69–90.
  • Pilsl H, Smajs D, Braun V. 1999. Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J Bacteriol. 181(11):3578–3581.
  • Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 282(5396):2085–2088.
  • Pore D, Chakrabarti MK. 2013. Outer membrane protein A (OmpA) from Shigella flexneri 2a: a promising subunit vaccine candidate. Vaccine. 31(36):3644–3650.
  • Provenzano D, Klose KE. 2000. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci U S A. 97(18):10220–10224.
  • Qasim M, Wrage M, Nüse B, Mattner J. 2022. Shigella outer membrane vesicles as promising targets for vaccination. IJMS. 23(2):994.
  • Qian R, Chu W, Mao Z, Zhang C, Wei Y, Yu L. 2007. Expression, characterization and immunogenicity of a major outer membrane protein from vibrio alginolyticus. Acta Biochim Biophys Sin (Shanghai). 39(3):194–200.
  • Qiao S, Luo Q, Zhao Y, Zhang XC, Huang Y. 2014. Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature. 511(7507):108–111.
  • Rappuoli R, Bottomley MJ, D’Oro U, Finco O, De Gregorio E. 2016. Reverse vaccinology 2.0: human immunology instructs vaccine antigen design. J Exp Med. 213(4):469–481.
  • Rasti ES, Brown AC. 2019. Cholera toxin encapsulated within several Vibrio cholerae O1 serotype Inaba outer membrane vesicles lacks a functional B-subunit. Toxins. 11(4):207.
  • Rawling EG, Brinkman FS, Hancock RE. 1998. Roles of the carboxy-terminal half of Pseudomonas aeruginosa major outer membrane protein OprF in cell shape, growth in low-osmolarity medium, and peptidoglycan association. J Bacteriol. 180(14):3556–3562.
  • Rollenhagen JE, Kalsy A, Cerda F, John M, Harris JB, Larocque RC, Qadri F, Calderwood SB, Taylor RK, Ryan ET. 2006. Transcutaneous immunization with toxin-coregulated pilin A induces protective immunity against Vibrio cholerae O1 El Tor challenge in mice. Infect Immun. 74(10):5834–5839.
  • Roy N, Barman S, Ghosh A, Pal A, Chakraborty K, Das SS, Saha DR, Yamasaki S, Koley H. 2010. Immunogenicity and protective efficacy of Vibrio cholerae outer membrane vesicles in rabbit model. FEMS Immunol Med Microbiol. 60(1):18–27.
  • Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ. 2008. Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A. 105(14):5537–5542.
  • Sakharwade SC, Mukhopadhaya A. 2015. Vibrio cholerae porin OmpU induces LPS tolerance by attenuating TLR-mediated signaling. Mol Immunol. 68(2 Pt A):312–324.
  • Sakharwade SC, Sharma PK, Mukhopadhaya A. 2013. Vibrio cholerae porin OmpU induces pro-inflammatory responses, but down-regulates LPS-mediated effects in RAW 264.7, THP-1 and human PBMCs. PLoS One. 8(9):e76583.
  • Sarkar M, Chaudhuri K. 2004. Association of adherence and motility in interleukin 8 induction in human intestinal epithelial cells by Vibrio cholerae. Microbes Infect. 6(7):676–685.
  • Schild S, Nelson EJ, Camilli A. 2008. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect Immun. 76(10):4554–4563.
  • Schwechheimer C, Kuehn MJ. 2015. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 13(10):605–619.
  • Sengupta TK, Chaudhuri KEYA, Majumdar SABITA, Lohia ANURADHA, Chatterjee AN, Das J. 1992. Interaction of Vibrio cholerae cells with beta-lactam antibiotics: emergence of resistant cells at a high frequency. Antimicrob Agents Chemother. 36(4):788–795.
  • Seppola M, Larsen AN, Steiro K, Robertsen B, Jensen I. 2008. zCharacterization and expression analysis of the interleukin genes, IL-1?, IL-8 and IL-10, in Atlantic cod (Gadus morhua L.)Mol Immunol. 45(4):887–897.
  • Selvaraj V, Sampath K, Sekar V. 2004. Extraction and characterization of lipopolysaccharide from Aeromonas hydrophila and its effects on survival and hematology of the carp, Cyprinus carpio. AFS. 17(2):163–173.
  • Shearer J, Jefferies D, Khalid S. 2019. Outer membrane proteins OmpA, FhuA, OmpF, EstA, BtuB, and OmpX have unique lipopolysaccharide fingerprints. J Chem Theory Comput. 15(4):2608–2619.
  • Silvaraj S, Yasin ISM, Karim MMA, Saad MZ. 2020. Elucidating the efficacy of vaccination against Vibriosis in lates calcarifer using two recombinant protein vaccines containing the outer membrane protein k (R-ompk) of vibrio alginolyticus and the dna chaperone j (r-dnaj) of vibrio harveyi. Vaccines. 8(4):660.
  • Sinclair D, Abba K, Zaman K, Qadri F, Graves PM, Cochrane Infectious Diseases Group 2011. Oral vaccines for preventing cholera. Cochr Database Syst Rev. 2011(3):CD008603.
  • Sinha R, Howlader DR, Ta A, Mitra S, Das S, Koley H. 2017. Retinoic acid pre-treatment down regulates V. cholerae outer membrane vesicles induced acute inflammation and enhances mucosal immunity. Vaccine. 35(28):3534–3547.
  • Sinha R, Koley H, Nag D, Mitra S, Mukhopadhyay AK, Chattopadhyay B. 2015. Pentavalent outer membrane vesicles of Vibrio cholerae induce adaptive immune response and protective efficacy in both adult and passive suckling mice models. Microbes Infect. 17(3):215–227.
  • Souod N, Kargar M, Hoseini MH, Jafarinia M. 2021. Fusion-expressed CtxB-TcpA-C-CPE improves both systemic and mucosal humoral and T-cell responses against cholera in mice. Microb Pathog. 157:104978.
  • Sperandio V, Giron JA, Silveira WD, Kaper JB. 1995. The OmpU outer membrane protein, a potential adherence factor of Vibrio cholerae. Infect Immun. 63(11):4433–4438.
  • Sun D, Lafferty MJ, Peek JA, Taylor RK. 1997. Domains within the Vibrio cholerae toxin coregulated pilin subunit that mediate bacterial colonization. Gene. 192(1):79–85.
  • Taheri F, Nazarian S, Ahmadi TS, Gargari SLM. 2020. Protective effects of egg yolk immunoglobulins (IgYs) developed against recombinant immunogens CtxB, OmpW and TcpA on infant mice infected with Vibrio cholerae. Int Immunopharmacol. 89(Pt B):107054.
  • Tang X, Wang H, Liu F, Sheng X, Xing J, Zhan W. 2019. Recombinant outer membrane protein T (OmpT) of Vibrio ichthyoenteri, a potential vaccine candidate for flounder (Paralichthys olivaceus. Microb Pathog. 126:185–192.
  • Taylor RK, Kirn TJ, Meeks MD, Wade TK, Wade WF. 2004. A Vibrio cholerae classical TcpA amino acid sequence induces protective antibody that binds an area hypothesized to be important for toxin-coregulated pilus structure. Infect Immun. 72(10):6050–6060.
  • Vaitkevicius K, Rompikuntal PK, Lindmark B, Vaitkevicius R, Song T, Wai SN. 2008. The metalloprotease PrtV from Vibrio cholerae: purification and properties. Febs J. 275(12):3167–3177.
  • Vakili A, Gargari SLM, Nazarian S, Amani J. 2018. Designing and Expression of Recombinant Chimeric Protein Containing CtxB and OmpW from Vibrio Cholerae and Evaluation of Its lmmunogenicity. Iran J Immunol. 15(3):207–220.
  • Wang Q, Chen J, Liu R, Jia J. 2011. Identification and evaluation of an outer membrane protein OmpU from a pathogenic Vibrio harveyi isolate as vaccine candidate in turbot (Scophthalmus maximus). Lett Appl Microbiol. 53(1):22–29.
  • Wang W, Chanda W, Zhong M. 2015. The relationship between biofilm and outer membrane vesicles: a novel therapy overview. FEMS Microbiol Lett. 362(15):fnv117.
  • Wang Z, Lazinski DW, Camilli A. 2017. Immunity provided by an outer membrane vesicle cholera vaccine is due to O-antigen-specific antibodies inhibiting bacterial motility. Infect Immun. 85(1):e00626-16.
  • Weiss BL, Wu Y, Schwank JJ, Tolwinski NS, Aksoy S. 2008. An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proc Natl Acad Sci U S A. 105(39):15088–15093.
  • World Health Organization 2016. Weekly epidemiological record. Weekly Epidemiological Record. 21:421–428.
  • Xiao M, Lai Y, Sun J, Chen G, Yan A. 2016. Transcriptional regulation of the outer membrane porin gene ompW reveals its physiological role during the transition from the aerobic to the anaerobic lifestyle of Escherichia coli. Front Microbiol. 7:799.
  • Xu H, Xing J, Tang X, Sheng X, Zhan W. 2019. Intramuscular administration of a DNA vaccine encoding OmpK antigen induces humoral and cellular immune responses in flounder (Paralichthys olivaceus) and improves protection against Vibrio anguillarum. Fish Shellfish Immunol. 86:618–626.
  • Yang JS, Jeon JH, Jang MS, Kang S-S, Ahn KB, Song M, Yun C-H, Han SH. 2018. Vibrio cholerae OmpU induces IL-8 expression in human intestinal epithelial cells. Mol Immunol. 93:47–54.
  • Zha Z, Li C, Li W, Ye Z, Pan J. 2016. LptD is a promising vaccine antigen and potential immunotherapeutic target for protection against Vibrio species infection. Sci Rep. 6(1):1–13.
  • Zhang C, Yu L, Qian R. 2008. Cloning and expression of Vibrio harveyi OmpK* and GAPDH* genes and their potential application as vaccines in large yellow croakers Pseudosciaena crocea. J Aquat Anim Health. 20(1):1–11.
  • Zhang J, Kong X, Zhou C, Li L, Nie G, Li X. 2014. Toll-like receptor recognition of bacteria in fish: ligand specificity and signal pathways. Fish Shellfish Immunol. 41(2):380–388.
  • Zhu Z, Dong C, Weng S, He J. 2019. Identification of outer membrane protein TolC as the major adhesin and potential vaccine candidate for Vibrio harveyi in hybrid grouper, Epinephelus fuscoguttatus (♀) × E. lanceolatus (♂). Fish Shellfish Immunol. 86:143–151.
  • Zuckerman JN, Rombo L, Fisch A. 2007. The true burden and risk of cholera: implications for prevention and control. Lancet Infect Dis. 7(8):521–530.

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