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Annual Review of Microbiology

Volume 76, 2022

Emerging Concepts in Cholera Vaccine Design

Abstract

Cholera is a severe diarrheal disease caused by the bacterium and constitutes a significant public health threat in many areas of the world. infection elicits potent and long-lasting immunity, and efforts to develop cholera vaccines have been ongoing for more than a century. Currently available inactivated two-dose oral cholera vaccines are increasingly deployed to both prevent and actively curb cholera outbreaks, and they are key components of the global effort to eradicate cholera. However, these killed whole-cell vaccines have several limitations, and a variety of new oral and nonoral cholera vaccine platforms have recently been developed. Here, we review emerging concepts in cholera vaccine design and implementation that have been driven by insights from human and animal studies. As a prototypical vaccine-preventable disease, cholera continues to be an excellent target for the development and application of cutting-edge technologies and platforms that may transform vaccinology.

Keyword(s): cholera, vaccines, vaccinology, Vibrio cholerae
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2022-09-08
2024-04-28
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Literature Cited

  1. 1.
    Adekunle O, Dretler A, Kauffman RC, Cho A, Rouphael N, Wrammert J. 2021. Longitudinal analysis of human humoral responses after vaccination with a live attenuated V. cholerae vaccine. PLOS Negl. Trop. Dis. 15:9e0009743
     [Google Scholar]
  2. 2.
    Akter A, Kelly M, Charles RC, Harris JB, Calderwood SB et al. 2021. Parenteral vaccination with a cholera conjugate vaccine boosts vibriocidal and anti-OSP responses in mice previously immunized with an oral cholera vaccine. Am. J. Trop. Med. Hyg. 104:62024–30
     [Google Scholar]
  3. 3.
    Alam MM, Bufano MK, Xu P, Kalsy A, Yu Y et al. 2014. Evaluation in mice of a conjugate vaccine for cholera made from Vibrio cholerae O1 (Ogawa) O-specific polysaccharide. PLOS Negl. Trop. Dis. 8:2e2683
     [Google Scholar]
  4. 4.
    Alavi S, Mitchell JD, Cho JY, Liu R, Macbeth JC, Hsiao A. 2020. Interpersonal gut microbiome variation drives susceptibility and resistance to cholera infection. Cell 181:71533–46.e13
     [Google Scholar]
  5. 5.
    Albert MJ, Alam K, Ansaruzzaman M, Qadri F, Sack RB. 1994. Lack of cross-protection against diarrhea due to Vibrio cholerae O139 (Bengal strain) after oral immunization of rabbits with V. cholerae O1 vaccine strain CVD103-HgR. J. Infect. Dis. 169:1230–31
     [Google Scholar]
  6. 6.
    Albert MJ, Alam K, Rahman AS, Huda S, Sack RB. 1994. Lack of cross-protection against diarrhea due to Vibrio cholerae O1 after oral immunization of rabbits with V. cholerae O139 Bengal. J. Infect. Dis. 169:3709–10
     [Google Scholar]
  7. 7.
    Ali M, Emch M, Park JK, Yunus M, Clemens J. 2011. Natural cholera infection-derived immunity in an endemic setting. J. Infect. Dis. 204:6912–18
     [Google Scholar]
  8. 8.
    Ali M, Emch M, von Seidlein L, Yunus M, Sack DA et al. 2005. Herd immunity conferred by killed oral cholera vaccines in Bangladesh: a reanalysis. Lancet 366:947944–49
     [Google Scholar]
  9. 9.
    Ali M, Kim P, Zaman K, Clemens J. 2019. Herd protection of unvaccinated adults by oral cholera vaccines in rural Bangladesh. Int. Health 11:3229–34
     [Google Scholar]
  10. 10.
    Ali M, Nelson AR, Lopez AL, Sack DA. 2015. Updated global burden of cholera in endemic countries. PLOS Negl. Trop. Dis. 9:6e0003832
     [Google Scholar]
  11. 11.
    Ali M, Qadri F, Kim DR, Islam MT, Im J et al. 2021. Effectiveness of a killed whole-cell oral cholera vaccine in Bangladesh: further follow-up of a cluster-randomised trial. Lancet Infect. Dis. 21:101407–14
     [Google Scholar]
  12. 12.
    Ali M, Sur D, You YA, Kanungo S, Sah B et al. 2013. Herd protection by a bivalent killed whole-cell oral cholera vaccine in the slums of Kolkata, India. Clin. Infect. Dis. 56:81123–31
     [Google Scholar]
  13. 13.
    Altindis E, Fu Y, Mekalanos JJ. 2014. Proteomic analysis of Vibrio cholerae outer membrane vesicles. PNAS 111:15E1548–56
     [Google Scholar]
  14. 14.
    Amani A, Tatang CA, Bayiha CN, Woung M, Ngo Bama S et al. 2021. A reactive vaccination campaign with single dose oral cholera vaccine (OCV) during a cholera outbreak in Cameroon. Vaccine 39:81290–96
     [Google Scholar]
  15. 15.
    Anh DD, Lopez AL, Thiem VD, Grahek SL, Duong TN et al. 2011. Use of oral cholera vaccines in an outbreak in Vietnam: a case control study. PLOS Negl. Trop. Dis. 5:1e1006
     [Google Scholar]
  16. 16.
    Asaduzzaman M, Ryan ET, John M, Hang L, Khan AI et al. 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. 72:84448–54
     [Google Scholar]
  17. 17.
    Auger E, Deslandes V, Ramjeet M, Contreras I, Nash JHE et al. 2009. Host-pathogen interactions of Actinobacillus pleuropneumoniae with porcine lung and tracheal epithelial cells. Infect. Immun. 77:41426–41
     [Google Scholar]
  18. 18.
    Aumatell CM, Torrell JR, Zuckerman JN. 2011. Review of oral cholera vaccines: efficacy in young children. Infect. Drug Resist. 4:1155–60
     [Google Scholar]
  19. 19.
    Azman AS, Lauer SA, Bhuiyan TR, Luquero FJ, Leung DT et al. 2020. Vibrio cholerae O1 transmission in Bangladesh: insights from a nationally representative serosurvey. Lancet Microbe 1:8e336–43
     [Google Scholar]
  20. 20.
    Azman AS, Lessler J, Luquero FJ, Bhuiyan TR, Khan AI et al. 2019. Estimating cholera incidence with cross-sectional serology. Sci. Transl. Med. 11:480eaau6242
     [Google Scholar]
  21. 21.
    Bckström M, Holmgren J, Schödel F, Lebens M. 1995. Characterization of an internal permissive site in the cholera toxin B-subunit and insertion of epitopes from human immunodeficiency virus-1, hepatitis B virus and enterotoxigenic Escherichia coli. Gene 165:2163–71
     [Google Scholar]
  22. 22.
    Benítez JA, García L, Silva A, García H, Fando R et al. 1999. Preliminary assessment of the safety and immunogenicity of a new CTXΦ-negative, hemagglutinin/protease-defective El Tor strain as a cholera vaccine candidate. Infect. Immun. 67:2539–45
     [Google Scholar]
  23. 23.
    Bhattacharya SK, Sur D, Ali M, Kanungo S, You YA et al. 2013. 5 year efficacy of a bivalent killed whole-cell oral cholera vaccine in Kolkata, India: a cluster-randomised, double-blind, placebo-controlled trial. Lancet Infect. Dis. 13:121050–56
     [Google Scholar]
  24. 24.
    Binagwaho A, Nyatanyi T, Nutt CT, Wagner CM. 2012. Disease outbreaks: support for a cholera vaccine stockpile. Nature 487:740539
     [Google Scholar]
  25. 25.
    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. 78:104402–20
     [Google Scholar]
  26. 26.
    Bornside GH. 1981. Jaime Ferran and preventive inoculation against cholera. Bull. Hist. Med. 55:4516–32
     [Google Scholar]
  27. 27.
    Boutonnier A, Villeneuve S, Nato F, Dassy B, Fournier JM. 2001. Preparation, immunogenicity, and protective efficacy, in a murine model, of a conjugate vaccine composed of the polysaccharide moiety of the lipopolysaccharide of Vibrio cholerae O139 bound to tetanus toxoid. Infect. Immun. 69:53488–93
     [Google Scholar]
  28. 28.
    Butterton JR, Beattie DT, Gardel CL, Carroll PA, Hyman T et al. 1995. Heterologous antigen expression in Vibrio cholerae vector strains. Infect. Immun. 63:72689–96
     [Google Scholar]
  29. 29.
    Butterton JR, Ryan ET, Acheson DW, Calderwood SB. 1997. Coexpression of the B subunit of Shiga toxin 1 and EaeA from enterohemorrhagic Escherichia coli in Vibrio cholerae vaccine strains. Infect. Immun. 65:62127–35
     [Google Scholar]
  30. 30.
    Caro F, Place NM, Mekalanos JJ. 2019. Analysis of lipoprotein transport depletion in Vibrio cholerae using CRISPRi. PNAS 116:3417013–22 Erratum. 2019. PNAS 116 (38):19210
    [Google Scholar]
  31. 31.
    Chac D, Bhuiyan TR, Saha A, Alam MM, Salma U et al. 2021. Gut microbiota and development of Vibrio cholerae-specific long-term memory B cells in adults after whole-cell killed oral cholera vaccine. Infect. Immun. 89:9e0021721
     [Google Scholar]
  32. 32.
    Charles RC, Kelly M, Tam JM, Akter A, Hossain M et al. 2020. Humans surviving cholera develop antibodies against Vibrio cholerae O-specific polysaccharide that inhibit pathogen motility. mBio 11:6e02847–20
     [Google Scholar]
  33. 33.
    Chen WH, Cohen MB, Kirkpatrick BD, Brady RC, Galloway D et al. 2016. Single-dose live oral cholera vaccine CVD 103-HgR protects against human experimental infection with Vibrio cholerae O1 El Tor. Clin. Infect. Dis. 62:111329–35
     [Google Scholar]
  34. 34.
    Cho JY, Liu R, Macbeth JC, Hsiao A. 2021. The interface of Vibrio cholerae and the gut microbiome. Gut Microbes 13:11937015
     [Google Scholar]
  35. 35.
    Chowdhury MI, Sheikh A, Qadri F. 2009. Development of Peru-15 (CholeraGarde®), a live-attenuated oral cholera vaccine: 1991–2009. Expert Rev. Vaccines 8:121643–52
     [Google Scholar]
  36. 36.
    Chua BY, Wong CY, Mifsud EJ, Edenborough KM, Sekiya T et al. 2015. Inactivated influenza vaccine that provides rapid, innate-immune-system-mediated protection and subsequent long-term adaptive immunity. mBio 6:6e01024–15
     [Google Scholar]
  37. 37.
    Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. 2017. Cholera. Lancet 390:101011539–49
     [Google Scholar]
  38. 38.
    Clemens JD, Sack DA, Harris JR, Chakraborty J, Khan MR et al. 1986. Field trial of oral cholera vaccines in Bangladesh. Lancet 328:8499124–27
     [Google Scholar]
  39. 39.
    Clemens JD, Sack DA, Harris JR, Van Loon F, Chakraborty J et al. 1990. Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335:8684270–73
     [Google Scholar]
  40. 40.
    Cohen MB, Giannella RA, Bean J, Taylor DN, Parker S et al. 2002. Randomized, controlled human challenge study of the safety, immunogenicity, and protective efficacy of a single dose of Peru-15, a live attenuated oral cholera vaccine. Infect. Immun. 70:41965–70
     [Google Scholar]
  41. 41.
    Crisan CV, Hammer BK. 2020. The Vibrio cholerae type VI secretion system: toxins, regulators and consequences. Environ. Microbiol. 22:104112–22
     [Google Scholar]
  42. 42.
    Dalia AB, McDonough EK, Camilli A. 2014. Multiplex genome editing by natural transformation. PNAS 111:248937–42
     [Google Scholar]
  43. 43.
    Dalia AB, Seed KD, Calderwood SB, Camilli A. 2015. A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. PNAS 112:3310485–90
     [Google Scholar]
  44. 44.
    Di Luccia B, Ahern PP, Griffin NW, Cheng J, Guruge JL et al. 2020. Combined prebiotic and microbial intervention improves oral cholera vaccination responses in a mouse model of childhood undernutrition. Cell Host Microbe 27:6899–908.e5
     [Google Scholar]
  45. 45.
    Di Tommaso A, De Magistris MT, Bugnoli M, Marsili I, Rappuoli R, Abrignani S. 1994. Formaldehyde treatment of proteins can constrain presentation to T cells by limiting antigen processing. Infect. Immun. 62:51830–34
     [Google Scholar]
  46. 46.
    Domman D, Quilici M-L, Dorman MJ, Njamkepo E, Mutreja A et al. 2017. Integrated view of Vibrio cholerae in the Americas. Science 358:6364789–93
     [Google Scholar]
  47. 47.
    Duan F, March JC. 2010. Engineered bacterial communication prevents Vibrio cholerae virulence in an infant mouse model. PNAS 107:2511260–64
     [Google Scholar]
  48. 48.
    Fakoya B, Sit B, Waldor MK. 2020. Transient intestinal colonization by a live-attenuated oral cholera vaccine induces protective immune responses in streptomycin-treated mice. J. Bacteriol. 202:24e00232–20
     [Google Scholar]
  49. 49.
    Ferreras E, Chizema-Kawesha E, Blake A, Chewe O, Mwaba J et al. 2018. Single-dose cholera vaccine in response to an outbreak in Zambia. N. Engl. J. Med. 378:6577–79
     [Google Scholar]
  50. 50.
    Fiege JK, Block KE, Pierson MJ, Nanda H, Shepherd FK et al. 2021. Mice with diverse microbial exposure histories as a model for preclinical vaccine testing. Cell Host Microbe 29:121815–27.e6
     [Google Scholar]
  51. 51.
    Fu Y, Waldor MK, Mekalanos JJ. 2013. Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe 14:6652–63
     [Google Scholar]
  52. 52.
    Furuyama W, Reynolds P, Haddock E, Meade-White K, Quynh Le M et al. 2020. A single dose of a vesicular stomatitis virus-based influenza vaccine confers rapid protection against H5 viruses from different clades. npj Vaccines 5:14
     [Google Scholar]
  53. 53.
    García HM, Thompson R, Valera R, Fando R, Fumane J et al. 2011. A single dose of live-attenuated 638 Vibrio cholerae oral vaccine is safe and immunogenic in adult volunteers in Mozambique. Vaccimonitor 20:31–8
     [Google Scholar]
  54. 54.
    García L, Jidy MD, García H, Rodríguez BL, Fernández R et al. 2005. The vaccine candidate Vibrio cholerae 638 is protective against cholera in healthy volunteers. Infect. Immun. 73:53018–24
     [Google Scholar]
  55. 55.
    Glob. Task Force Cholera Control 2017. Ending cholera—a global roadmap to 2030 Rep., Glob. Task Force Cholera Control. https://www.gtfcc.org/wp-content/uploads/2019/10/gtfcc-ending-cholera-a-global-roadmap-to-2030.pdf
  56. 56.
    Graves PM, Deeks JJ, Demicheli V, Jefferson T 2010. Vaccines for preventing cholera: killed whole cell or other subunit vaccines (injected). Cochrane Database Syst. Rev. 2010 8CD000974
     [Google Scholar]
  57. 57.
    Gu H, Zeng X, Peng L, Xiang C, Zhou Y et al. 2021. Vaccination induces rapid protection against bacterial pneumonia via training alveolar macrophage in mice. eLife 10:0e69951
     [Google Scholar]
  58. 58.
    Gupta RK, Szu SC, Finkelstein RA, Robbins JB. 1992. Synthesis, characterization, and some immunological properties of conjugates composed of the detoxified lipopolysaccharide of Vibrio cholerae O1 serotype Inaba bound to cholera toxin. Infect. Immun. 60:83201–8
     [Google Scholar]
  59. 59.
    Gupta RK, Taylor DN, Bryla DA, Robbins JB, Szu SC. 1998. Phase 1 evaluation of Vibrio cholerae O1, serotype Inaba, polysaccharide-cholera toxin conjugates in adult volunteers. Infect. Immun. 66:73095–99
     [Google Scholar]
  60. 60.
    Hauke CA, Taylor RK. 2017. Production of putative enhanced oral cholera vaccine strains that express toxin-coregulated pilus. PLOS ONE 12:4e0175170
     [Google Scholar]
  61. 61.
    Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, RK Taylor, Levine MM. 1988. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168:41487–92
     [Google Scholar]
  62. 62.
    Ho BT, Fu Y, Dong TG, Mekalanos JJ. 2017. Vibrio cholerae type 6 secretion system effector trafficking in target bacterial cells. PNAS 114:359427–32
     [Google Scholar]
  63. 63.
    Holmgren J. 2021. Modern history of cholera vaccines and the pivotal role of icddr,b. J. Infect. Dis. 224:Suppl. 7S742–48
     [Google Scholar]
  64. 64.
    Hsiao A, Ahmed AMS, Subramanian S, Griffin NW, Drewry LL et al. 2014. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature 515:7527423–26
     [Google Scholar]
  65. 65.
    Hubbard TP, Billings G, Dörr T, Sit B, Warr AR et al. 2018. A live vaccine rapidly protects against cholera in an infant rabbit model. Sci. Transl. Med. 10:445eaap8423
     [Google Scholar]
  66. 66.
    Iyer AS, Harris JB. 2021. Correlates of protection for cholera. J. Infect. Dis. 224:12 Suppl 2 S732–37
     [Google Scholar]
  67. 67.
    Jeon S, Kelly M, Yun J, Lee B, Park M et al. 2021. Scalable production and immunogenicity of a cholera conjugate vaccine. Vaccine 39:476936–46
     [Google Scholar]
  68. 68.
    Kaisar MH, Bhuiyan MS, Akter A, Saleem D, Iyer AS et al. 2021. Vibrio cholerae sialidase-specific immune responses are associated with protection against cholera. mSphere 6:2e01232–20
     [Google Scholar]
  69. 69.
    Kamp HD, Patimalla-Dipali B, Lazinski DW, Wallace-Gadsden F, Camilli A. 2013. Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLOS Pathog 9:12e1003800
     [Google Scholar]
  70. 70.
    Kanungo S, Desai SN, Nandy RK, Bhattacharya MK, Kim DR et al. 2015. Flexibility of oral cholera vaccine dosing—a randomized controlled trial measuring immune responses following alternative vaccination schedules in a cholera hyper-endemic zone. PLOS Negl. Trop. Dis. 9:3e0003574
     [Google Scholar]
  71. 71.
    Kanungo S, Sen B, Ramamurthy T, Sur D, Manna B et al. 2014. Safety and immunogenicity of a live oral recombinant cholera vaccine VA1.4: a randomized, placebo controlled trial in healthy adults in a cholera endemic area in Kolkata, India. PLOS ONE 9:7e99381
     [Google Scholar]
  72. 72.
    Kaper JB, Lockman H, Baldini MM, Levine MM. 1984. Recombinant nontoxinogenic Vibrio cholerae strains as attenuated cholera vaccine candidates. Nature 308:5960655–58
     [Google Scholar]
  73. 73.
    Kaper JB, Michalski J, Ketley JM, Levine MM. 1994. Potential for reacquisition of cholera enterotoxin genes by attenuated Vibrio cholerae vaccine strain CVD 103-HgR. Infect. Immun. 62:41480–83
     [Google Scholar]
  74. 74.
    Karlsson SL, Ax E, Nygren E, Källgård S, Blomquist M et al. 2014. Development of stable Vibrio cholerae O1 Hikojima type vaccine strains co-expressing the Inaba and Ogawa lipopolysaccharide antigens. PLOS ONE 9:11e108521
     [Google Scholar]
  75. 75.
    Kauffman RC, Bhuiyan TR, Nakajima R, Mayo-Smith LM, Rashu R et al. 2016. Single-cell analysis of the plasmablast response to Vibrio cholerae demonstrates expansion of cross-reactive memory B cells. mBio 7:6e02021–16
     [Google Scholar]
  76. 76.
    Khatib AM, Ali M, von Seidlein L, Kim DR, Hashim R et al. 2012. Effectiveness of an oral cholera vaccine in Zanzibar: findings from a mass vaccination campaign and observational cohort study. Lancet Infect. Dis. 12:11837–44
     [Google Scholar]
  77. 77.
    Kim EJ, Lee CH, Nair GB, Kim DW. 2015. Whole-genome sequence comparisons reveal the evolution of Vibrio cholerae O1. Trends Microbiol 23:8479–89
     [Google Scholar]
  78. 78.
    Kirn TJ, Taylor RK. 2005. TcpF is a soluble colonization factor and protective antigen secreted by E1 Tor and classical O1 and O139 Vibrio cholerae serogroups. Infect. Immun. 73:84461–70
     [Google Scholar]
  79. 79.
    Krebs SJ, Taylor RK. 2011. Protection and attachment of Vibrio cholerae mediated by the toxin-coregulated pilus in the infant mouse model. J. Bacteriol. 193:195260–70
     [Google Scholar]
  80. 80.
    Lavelle EC, Ward RW. 2022. Mucosal vaccines—fortifying the frontiers. Nat. Rev. Immunol. 22:236–50
     [Google Scholar]
  81. 81.
    Lebens M, Terrinoni M, Karlsson SL, Larena M, Gustafsson-Hedberg T et al. 2016. Construction and preclinical evaluation of mmCT, a novel mutant cholera toxin adjuvant that can be efficiently produced in genetically manipulated Vibrio cholerae. Vaccine 34:182121–28
     [Google Scholar]
  82. 82.
    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. 81:72379–93
     [Google Scholar]
  83. 83.
    Leitner DR, Lichtenegger S, Temel P, Zingl FG, Ratzberger D et al. 2015. A combined vaccine approach against Vibrio cholerae and ETEC based on outer membrane vesicles. Front. Microbiol. 6:823
     [Google Scholar]
  84. 84.
    Leslie JL, Jenior ML, Vendrov KC, Standke AK, Barron MR et al. 2021. Protection from lethal Clostridioides difficile infection via intraspecies competition for cogerminant. mBio 12:2e00522–21
     [Google Scholar]
  85. 85.
    Leung DT, Chowdhury F, Calderwood SB, Qadri F, Ryan ET. 2012. Immune responses to cholera in children. Expert Rev. Anti. Infect. Ther. 10:4435–44
     [Google Scholar]
  86. 86.
    Leung T, Matrajt L. 2021. Protection afforded by previous Vibrio cholerae infection against subsequent disease and infection: a review. PLOS Negl. Trop. Dis. 15:5e0009383
     [Google Scholar]
  87. 87.
    Levine MM, Chen WH, Kaper JB, Lock M, Danzig L, Gurwith M. 2017. PaxVax CVD 103-HgR single-dose live oral cholera vaccine. Expert Rev. Vaccines 16:3197–213
     [Google Scholar]
  88. 88.
    Levine MM, Nalin DR, Craig JP, Hoover D, Bergquist EJ et al. 1979. Immunity of cholera in man: relative role of antibacterial versus antitoxic immunity. Trans. R. Soc. Trop. Med. Hyg. 73:13–9
     [Google Scholar]
  89. 89.
    Liao J, Gibson JA, Pickering BS, Watnick PI 2018. Sublingual adjuvant delivery by a live attenuated Vibrio cholerae-based antigen presentation platform. mSphere 3:3e00245–18
     [Google Scholar]
  90. 90.
    Liao J, Smith DR, Brynjarsdóttir J, Watnick PI. 2018. a self-assembling whole-cell vaccine antigen presentation platform. J. Bacteriol. 200:15e00752–17
     [Google Scholar]
  91. 91.
    Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, Zhu J. 2008. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. PNAS 105:289769–74
     [Google Scholar]
  92. 92.
    Lopez AL, Deen J, Azman AS, Luquero FJ, Kanungo S et al. 2018. Immunogenicity and protection from a single dose of internationally available killed oral cholera vaccine: a systematic review and metaanalysis. Clin. Infect. Dis. 66:121960–71
     [Google Scholar]
  93. 93.
    Lopez AL, Gonzales MLA, Aldaba JG, Nair GB. 2014. Killed oral cholera vaccines: history, development and implementation challenges. Ther. Adv. Vaccines 2:5123–36
     [Google Scholar]
  94. 94.
    Luquero FJ, Grout L, Ciglenecki I, Sakoba K, Traore B et al. 2014. Use of Vibrio cholerae vaccine in an outbreak in Guinea. N. Engl. J. Med. 370:222111–20
     [Google Scholar]
  95. 95.
    Lynn DJ, Benson SC, Lynn MA, Pulendran B. 2021. Modulation of immune responses to vaccination by the microbiota: implications and potential mechanisms. Nat. Rev. Immunol. 22:33–46
     [Google Scholar]
  96. 96.
    Mahalanabis D, Ramamurthy T, Nair GB, Ghosh A, Shaikh S et al. 2009. Randomized placebo controlled human volunteer trial of a live oral cholera vaccine VA1.3 for safety and immune response. Vaccine 27:354850–56
     [Google Scholar]
  97. 97.
    Manning PA, Heuzenroeder MW, Yeadon J, Leavesley DI, Reeves PR, Rowley D. 1986. Molecular cloning and expression in Escherichia coli K-12 of the O antigens of the Inaba and Ogawa serotypes of the Vibrio cholerae O1 lipopolysaccharides and their potential for vaccine development. Infect. Immun. 53:2272–77
     [Google Scholar]
  98. 98.
    Mekalanos JJ, Swartz DJ, Pearson GDN, Harford N, Groyne F, De Wilde M. 1983. Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306:5943551–57
     [Google Scholar]
  99. 99.
    Micoli F, MacLennan CA. 2020. Outer membrane vesicle vaccines. Semin. Immunol. 50:0101433
     [Google Scholar]
  100. 100.
    Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH et al. 2011. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477:7365462–65
     [Google Scholar]
  101. 101.
    Nandy RK, MJ Albert, Ghose AC. 1996. Serum antibacterial and antitoxin responses in clinical cholera caused by Vibrio cholerae O139 Bengal and evaluation of their importance in protection. Vaccine 14:121137–42
     [Google Scholar]
  102. 102.
    Nochi T, Yuki Y, Katakai Y, Shibata H, Tokuhara D et al. 2009. A rice-based oral cholera vaccine induces macaque-specific systemic neutralizing antibodies but does not influence pre-existing intestinal immunity. J. Immunol. 183:106538–44
     [Google Scholar]
  103. 103.
    Papenfort K, Bassler BL. 2016. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14:9576–88
     [Google Scholar]
  104. 104.
    Pezzoli L. 2020. Global oral cholera vaccine use, 2013–2018. Vaccine 38:Suppl. 1A132–40
     [Google Scholar]
  105. 105.
    Pollard AJ, Bijker EM. 2021. A guide to vaccinology: from basic principles to new developments. Nat. Rev. Immunol. 21:283–100
     [Google Scholar]
  106. 106.
    Price GA, Holmes RK. 2012. Evaluation of TcpF-A2-CTB chimera and evidence of additive protective efficacy of immunizing with TcpF and CTB in the suckling mouse model of cholera. PLOS ONE 7:8e42434
     [Google Scholar]
  107. 107.
    Price GA, McFann K, Holmes RK. 2013. Immunization with cholera toxin B subunit induces high-level protection in the suckling mouse model of cholera. PLOS ONE 8:2e57269
     [Google Scholar]
  108. 108.
    Pritchard JR, Chao MC, Abel S, Davis BM, Baranowski C et al. 2014. ARTIST: high-resolution genome-wide assessment of fitness using transposon-insertion sequencing. PLOS Genet 10:11e1004782
     [Google Scholar]
  109. 109.
    Qadri F, Ali M, Chowdhury F, Khan AI, Saha A et al. 2015. Feasibility and effectiveness of oral cholera vaccine in an urban endemic setting in Bangladesh: a cluster randomised open-label trial. Lancet 386:100011362–71
     [Google Scholar]
  110. 110.
    Qadri F, Chowdhury MI, Faruque SM, Salam MA, Ahmed T et al. 2005. Randomized, controlled study of the safety and immunogenicity of Peru-15, a live attenuated oral vaccine candidate for cholera, in adult volunteers in Bangladesh. J. Infect. Dis. 192:4573–79
     [Google Scholar]
  111. 111.
    Qadri F, Chowdhury MI, Faruque SM, Salam MA, Ahmed T et al. 2007. Peru-15, a live attenuated oral cholera vaccine, is safe and immunogenic in Bangladeshi toddlers and infants. Vaccine 25:2231–38
     [Google Scholar]
  112. 112.
    Qadri F, Wierzba TF, Ali M, Chowdhury F, Khan AI et al. 2016. Efficacy of a single-dose, inactivated oral cholera vaccine in Bangladesh. N. Engl. J. Med. 374:181723–32
     [Google Scholar]
  113. 113.
    Ramanathan R, Stibitz S, Pratt D, Roberts J. 2019. Use of controlled human infection models (CHIMs) to support vaccine development: US regulatory considerations. Vaccine 37:314256–61
     [Google Scholar]
  114. 114.
    Ratanasuwan W, Kim YH, Sah BK, Suwanagool S, Kim DR et al. 2015. Peru-15 (Choleragarde®), a live attenuated oral cholera vaccine, is safe and immunogenic in human immunodeficiency virus (HIV)-seropositive adults in Thailand. Vaccine 33:384820–26
     [Google Scholar]
  115. 115.
    Reyburn R, Deen JL, Grais RF, Bhattacharya SK, Sur D et al. 2011. The case for reactive mass oral cholera vaccinations. PLOS Negl. Trop. Dis. 5:1e952
     [Google Scholar]
  116. 116.
    Richie EE, Punjabi NH, Sidharta YY, Peetosutan KK, Sukandar MM et al. 2000. Efficacy trial of single-dose live oral cholera vaccine CVD 103-HgR in North Jakarta, Indonesia, a cholera-endemic area. Vaccine 18:222399–410
     [Google Scholar]
  117. 117.
    Ritter AS, Chowdhury F, Franke MF, Becker RL, Bhuiyan TR et al. 2019. Vibriocidal titer and protection from cholera in children. Open Forum Infect. Dis. 6:44–8
     [Google Scholar]
  118. 118.
    Rollenhagen JE, Kalsy A, Cerda F, John M, Harris JB et al. 2006. Transcutaneous immunization with toxin-coregulated pilin A induces protective immunity against Vibrio cholerae O1 El Tor challenge in mice. Infect. Immun. 74:105834–39
     [Google Scholar]
  119. 119.
    Rollenhagen JE, Kalsy A, Saksena R, Sheikh A, Alam MM et al. 2009. Transcutaneous immunization with a synthetic hexasaccharide-protein conjugate induces anti-Vibrio cholerae lipopolysaccharide responses in mice. Vaccine 27:364917–22
     [Google Scholar]
  120. 120.
    Ryan ET, Calderwood SB, Qadri F. 2006. Live attenuated oral cholera vaccines. Expert Rev. Vaccines 5:4483–94
     [Google Scholar]
  121. 121.
    Ryan ET, Leung DT, Jensen O, Weil AA, Bhuiyan TR et al. 2021. Systemic, mucosal, and memory immune responses following cholera. Trop. Med. Infect. Dis. 6:4192
     [Google Scholar]
  122. 122.
    Sack DA, Sack RB, Shimko J, Gomes G, O'Sullivan D et al. 1997. Evaluation of Peru-15, a new live oral vaccine for cholera, in volunteers. J. Infect. Dis. 176:1201–5
     [Google Scholar]
  123. 123.
    Saha A, Khan A, Salma U, Jahan N, Bhuiyan TR et al. 2016. The oral cholera vaccine Shanchol™ when stored at elevated temperatures maintains the safety and immunogenicity profile in Bangladeshi participants. Vaccine 34:131551–58
     [Google Scholar]
  124. 124.
    Saha D, LaRocque RC, Khan AI, Harris JB, Begum YA et al. 2004. Incomplete correlation of serum vibriocidal antibody titer with protection from Vibrio cholerae infection in urban Bangladesh. J. Infect. Dis. 189:122318–22
     [Google Scholar]
  125. 125.
    Sanchez J, Holmgren J. 2011. Cholera toxin—a foe & a friend. Indian J. Med. Res. 133:2153–63
     [Google Scholar]
  126. 126.
    Sayeed MA, Bufano MK, Xu P, Eckhoff G, Charles RC et al. 2015. A cholera conjugate vaccine containing O-specific polysaccharide (OSP) of V. cholerae O1 Inaba and recombinant fragment of tetanus toxin heavy chain (OSP:rTTHc) induces serum, memory and lamina proprial responses against OSP and is protective in mice. PLOS Negl. Trop. Dis. 9:7e0003881
     [Google Scholar]
  127. 127.
    Schild S, Nelson EJ, Camilli A. 2008. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect. Immun. 76:104554–63
     [Google Scholar]
  128. 128.
    Schrank GD, Verwey WF. 1976. Distribution of cholera organisms in experimental Vibrio cholerae infections: proposed mechanisms of pathogenesis and antibacterial immunity. Infect. Immun. 13:1195–203
     [Google Scholar]
  129. 129.
    Shaikh H, Lynch J, Kim J, Excler J-L. 2020. Current and future cholera vaccines. Vaccine 38:Suppl. 1A118–26
     [Google Scholar]
  130. 130.
    Sharma T, Joshi N, Kumar Mandyal A, Nordqvist SL, Lebens M et al. 2020. Development of Hillchol®, a low-cost inactivated single strain Hikojima oral cholera vaccine. Vaccine 38:507998–8009
     [Google Scholar]
  131. 131.
    Silva AJ, Eko FO, Benitez JA. 2008. Exploiting cholera vaccines as a versatile antigen delivery platform. Biotechnol. Lett. 30:4571–79
     [Google Scholar]
  132. 132.
    Sit B, Fakoya B, Zhang T, Billings G, Waldor MK. 2021. Dissecting serotype-specific contributions to live oral cholera vaccine efficacy. PNAS 118:7e2018032118
     [Google Scholar]
  133. 133.
    Sit B, Zhang T, Fakoya B, Akter A, Biswas R et al. 2019. Oral immunization with a probiotic cholera vaccine induces broad protective immunity against Vibrio cholerae colonization and disease in mice. PLOS Negl. Trop. Dis. 13:5e0007417
     [Google Scholar]
  134. 134.
    Sow SO, Tapia MD, Chen WH, Haidara FC, Kotloff KL et al. 2017. A randomized, placebo-controlled, double-blind Phase 2 trial comparing the reactogenicity and immunogenicity of a single standard dose to those of a high dose of CVD 103-HgR live attenuated oral cholera vaccine, with Shanchol inactivated oral vaccine as an open-label immunologic comparator. Clin. Vaccine Immunol. 24:12e00265–17
     [Google Scholar]
  135. 135.
    Suharyono, Simanjuntak C, Witham N, Punjabi N, Heppner DG et al. 1992. Safety and immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR in 5–9-year-old Indonesian children. Lancet 340:8821689–94
     [Google Scholar]
  136. 136.
    Sur D, Lopez AL, Kanungo S, Paisley A, Manna B et al. 2009. Efficacy and safety of a modified killed-whole-cell oral cholera vaccine in India: an interim analysis of a cluster-randomised, double-blind, placebo-controlled trial. Lancet 374:97021694–702
     [Google Scholar]
  137. 137.
    Tarique AA, Kalsy A, Arifuzzaman M, Rollins SM, Charles RC et al. 2012. Transcutaneous immunization with a Vibrio cholerae O1 Ogawa synthetic hexasaccharide conjugate following oral whole-cell cholera vaccination boosts vibriocidal responses and induces protective immunity in mice. Clin. Vaccine Immunol. 19:4594–602
     [Google Scholar]
  138. 138.
    Tokuhara D, Yuki Y, Nochi T, Kodama T, Mejima M et al. 2010. Secretory IgA-mediated protection against V. cholerae and heat-labile enterotoxin-producing enterotoxigenic Escherichia coli by rice-based vaccine. PNAS 107:198794–99
     [Google Scholar]
  139. 139.
    Trach DD, Clemens JD, Ke NT, Thuy HT, Son ND et al. 1997. Field trial of a locally produced, killed, oral cholera vaccine in Vietnam. Lancet 349:9047231–35
     [Google Scholar]
  140. 140.
    Valera R, García HM, Díaz Jidy M, Mirabal M, Armesto MI et al. 2009. Randomized, double-blind, placebo-controlled trial to evaluate the safety and immunogenicity of live oral cholera vaccine 638 in Cuban adults. Vaccine 27:476564–69
     [Google Scholar]
  141. 141.
    Valle E, Ledon T, Cedre B, Campos J, Valmaseda T et al. 2000. Construction and characterization of a nonproliferative El Tor cholera vaccine candidate derived from strain 638. Infect. Immun. 68:116411–18
     [Google Scholar]
  142. 142.
    Van Loon FPL, Clemens JD, Chakraborty J, Rao MR, Kay BA et al. 1996. Field trial of inactivated oral cholera vaccines in Bangladesh: results from 5 years of follow-up. Vaccine 14:2162–66
     [Google Scholar]
  143. 143.
    Waldor MK, Hotez PJ, Clemens JD. 2010. A national cholera vaccine stockpile—a new humanitarian and diplomatic resource. N. Engl. J. Med. 363:242279–82
     [Google Scholar]
  144. 144.
    Waldor MK, Mekalanos JJ. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:52701910–14
     [Google Scholar]
  145. 145.
    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. 85:1e00626–16
     [Google Scholar]
  146. 146.
    Weil AA, Becker RL, Harris JB. 2019. Vibrio cholerae at the intersection of immunity and the microbiome. mSphere 4:6e00597–19
     [Google Scholar]
  147. 147.
    Weil AA, Ellis CN, Debela MD, Bhuiyan TR, Rashu R et al. 2019. Posttranslational regulation of IL-23 production distinguishes the innate immune responses to live toxigenic versus heat-inactivated Vibrio cholerae. mSphere 4:4e00206–19
     [Google Scholar]
  148. 148.
    Weill F, Domman D, Njamkepo E, Tarr C, Rauzier J et al. 2017. Genomic history of the seventh pandemic of cholera in Africa. Science 358:6364785–89
     [Google Scholar]
  149. 149.
    Yuki Y, Nojima M, Hosono O, Tanaka H, Kimura Y et al. 2021. Oral MucoRice-CTB vaccine for safety and microbiota-dependent immunogenicity in humans: a phase 1 randomised trial. Lancet Microbe 2:9e429–40
     [Google Scholar]
  150. 150.
    Zhao W, Caro F, Robins W, Mekalanos JJ. 2018. Antagonism toward the intestinal microbiota and its effect on Vibrio cholerae virulence. Science 359:6372210–13
     [Google Scholar]
  151. 151.
    Zhu J, Mekalanos JJ. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell. 5:4647–56
     [Google Scholar]
  152. 152.
    Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. PNAS 99:53129–34
     [Google Scholar]
/content/journals/10.1146/annurev-micro-041320-033201
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Emerging Concepts in Cholera Vaccine Design
Annual Review of Microbiology 76, 681 (2022); https://doi.org/10.1146/annurev-micro-041320-033201
/content/journals/10.1146/annurev-micro-041320-033201
/content/journals/10.1146/annurev-micro-041320-033201
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