Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility
ABSTRACT The mechanism of protection against cholera afforded by previous illness or vaccination is currently unknown. We have recently shown that antibodies targeting O-specific polysaccharide (OSP) of Vibrio cholerae correlate highly with protection against cholera. V. cholerae is highly motile an...
Guardado en:
| Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
American Society for Microbiology
2020
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/d099d08206104bbf8c76536df01b508a |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:d099d08206104bbf8c76536df01b508a |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:d099d08206104bbf8c76536df01b508a2021-11-15T15:55:43ZHumans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility10.1128/mBio.02847-202150-7511https://doaj.org/article/d099d08206104bbf8c76536df01b508a2020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02847-20https://doaj.org/toc/2150-7511ABSTRACT The mechanism of protection against cholera afforded by previous illness or vaccination is currently unknown. We have recently shown that antibodies targeting O-specific polysaccharide (OSP) of Vibrio cholerae correlate highly with protection against cholera. V. cholerae is highly motile and possesses a flagellum sheathed in OSP, and motility of V. cholerae correlates with virulence. Using high-speed video microscopy and building upon previous animal-related work, we demonstrate that sera, polyclonal antibody fractions, and OSP-specific monoclonal antibodies recovered from humans surviving cholera block V. cholerae motility at both subagglutinating and agglutinating concentrations. This antimotility effect is reversed by preadsorbing sera and polyclonal antibody fractions with purified OSP and is associated with OSP-specific but not flagellin-specific monoclonal antibodies. Fab fragments of OSP-specific polyclonal antibodies do not inhibit motility, suggesting a requirement for antibody-mediated cross-linking in motility inhibition. We show that OSP-specific antibodies do not directly affect V. cholerae viability, but that OSP-specific monoclonal antibody highly protects against death in the murine cholera model. We used in vivo competitive index studies to demonstrate that OSP-specific antibodies impede colonization and survival of V. cholerae in intestinal tissues and that this impact is motility dependent. Our findings suggest that the impedance of motility by antibodies targeting V. cholerae OSP contributes to protection against cholera. IMPORTANCE Cholera is a severe dehydrating illness of humans caused by Vibrio cholerae. V. cholerae is a highly motile bacterium that has a single flagellum covered in lipopolysaccharide (LPS) displaying O-specific polysaccharide (OSP), and V. cholerae motility correlates with its ability to cause disease. The mechanisms of protection against cholera are not well understood; however, since V. cholerae is a noninvasive intestinal pathogen, it is likely that antibodies that bind the pathogen or its products in the intestinal lumen contribute to protection from infection. Here, we demonstrate that OSP-specific antibodies isolated from humans surviving cholera in Bangladesh inhibit V. cholerae motility and are associated with protection against challenge in a motility-dependent manner.Richelle C. CharlesMeagan KellyJenny M. TamAklima AkterMotaher HossainKamrul IslamRajib BiswasMohammad KamruzzamanFahima ChowdhuryAshraful I. KhanDaniel T. LeungAna WeilRegina C. LaRocqueTaufiqur Rahman BhuiyanAtiqur RahmanLeslie M. Mayo-SmithRachel L. BeckerJatin M. VyasChristina S. FahertyKourtney P. NickersonSamantha GiffenAlaina S. RitterMatthew K. WaldorPeng XuPavol KováčStephen B. CalderwoodRobert C. KauffmanJens WrammertFirdausi QadriJason B. HarrisEdward T. RyanAmerican Society for MicrobiologyarticleVibrio choleraecholerahumanmotilitypathogenesisMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Vibrio cholerae cholera human motility pathogenesis Microbiology QR1-502 |
| spellingShingle |
Vibrio cholerae cholera human motility pathogenesis Microbiology QR1-502 Richelle C. Charles Meagan Kelly Jenny M. Tam Aklima Akter Motaher Hossain Kamrul Islam Rajib Biswas Mohammad Kamruzzaman Fahima Chowdhury Ashraful I. Khan Daniel T. Leung Ana Weil Regina C. LaRocque Taufiqur Rahman Bhuiyan Atiqur Rahman Leslie M. Mayo-Smith Rachel L. Becker Jatin M. Vyas Christina S. Faherty Kourtney P. Nickerson Samantha Giffen Alaina S. Ritter Matthew K. Waldor Peng Xu Pavol Kováč Stephen B. Calderwood Robert C. Kauffman Jens Wrammert Firdausi Qadri Jason B. Harris Edward T. Ryan Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| description |
ABSTRACT The mechanism of protection against cholera afforded by previous illness or vaccination is currently unknown. We have recently shown that antibodies targeting O-specific polysaccharide (OSP) of Vibrio cholerae correlate highly with protection against cholera. V. cholerae is highly motile and possesses a flagellum sheathed in OSP, and motility of V. cholerae correlates with virulence. Using high-speed video microscopy and building upon previous animal-related work, we demonstrate that sera, polyclonal antibody fractions, and OSP-specific monoclonal antibodies recovered from humans surviving cholera block V. cholerae motility at both subagglutinating and agglutinating concentrations. This antimotility effect is reversed by preadsorbing sera and polyclonal antibody fractions with purified OSP and is associated with OSP-specific but not flagellin-specific monoclonal antibodies. Fab fragments of OSP-specific polyclonal antibodies do not inhibit motility, suggesting a requirement for antibody-mediated cross-linking in motility inhibition. We show that OSP-specific antibodies do not directly affect V. cholerae viability, but that OSP-specific monoclonal antibody highly protects against death in the murine cholera model. We used in vivo competitive index studies to demonstrate that OSP-specific antibodies impede colonization and survival of V. cholerae in intestinal tissues and that this impact is motility dependent. Our findings suggest that the impedance of motility by antibodies targeting V. cholerae OSP contributes to protection against cholera. IMPORTANCE Cholera is a severe dehydrating illness of humans caused by Vibrio cholerae. V. cholerae is a highly motile bacterium that has a single flagellum covered in lipopolysaccharide (LPS) displaying O-specific polysaccharide (OSP), and V. cholerae motility correlates with its ability to cause disease. The mechanisms of protection against cholera are not well understood; however, since V. cholerae is a noninvasive intestinal pathogen, it is likely that antibodies that bind the pathogen or its products in the intestinal lumen contribute to protection from infection. Here, we demonstrate that OSP-specific antibodies isolated from humans surviving cholera in Bangladesh inhibit V. cholerae motility and are associated with protection against challenge in a motility-dependent manner. |
| format |
article |
| author |
Richelle C. Charles Meagan Kelly Jenny M. Tam Aklima Akter Motaher Hossain Kamrul Islam Rajib Biswas Mohammad Kamruzzaman Fahima Chowdhury Ashraful I. Khan Daniel T. Leung Ana Weil Regina C. LaRocque Taufiqur Rahman Bhuiyan Atiqur Rahman Leslie M. Mayo-Smith Rachel L. Becker Jatin M. Vyas Christina S. Faherty Kourtney P. Nickerson Samantha Giffen Alaina S. Ritter Matthew K. Waldor Peng Xu Pavol Kováč Stephen B. Calderwood Robert C. Kauffman Jens Wrammert Firdausi Qadri Jason B. Harris Edward T. Ryan |
| author_facet |
Richelle C. Charles Meagan Kelly Jenny M. Tam Aklima Akter Motaher Hossain Kamrul Islam Rajib Biswas Mohammad Kamruzzaman Fahima Chowdhury Ashraful I. Khan Daniel T. Leung Ana Weil Regina C. LaRocque Taufiqur Rahman Bhuiyan Atiqur Rahman Leslie M. Mayo-Smith Rachel L. Becker Jatin M. Vyas Christina S. Faherty Kourtney P. Nickerson Samantha Giffen Alaina S. Ritter Matthew K. Waldor Peng Xu Pavol Kováč Stephen B. Calderwood Robert C. Kauffman Jens Wrammert Firdausi Qadri Jason B. Harris Edward T. Ryan |
| author_sort |
Richelle C. Charles |
| title |
Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| title_short |
Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| title_full |
Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| title_fullStr |
Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| title_full_unstemmed |
Humans Surviving Cholera Develop Antibodies against <named-content content-type="genus-species">Vibrio cholerae</named-content> O-Specific Polysaccharide That Inhibit Pathogen Motility |
| title_sort |
humans surviving cholera develop antibodies against <named-content content-type="genus-species">vibrio cholerae</named-content> o-specific polysaccharide that inhibit pathogen motility |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/d099d08206104bbf8c76536df01b508a |
| work_keys_str_mv |
AT richelleccharles humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT meagankelly humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT jennymtam humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT aklimaakter humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT motaherhossain humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT kamrulislam humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT rajibbiswas humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT mohammadkamruzzaman humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT fahimachowdhury humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT ashrafulikhan humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT danieltleung humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT anaweil humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT reginaclarocque humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT taufiqurrahmanbhuiyan humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT atiqurrahman humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT lesliemmayosmith humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT rachellbecker humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT jatinmvyas humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT christinasfaherty humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT kourtneypnickerson humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT samanthagiffen humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT alainasritter humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT matthewkwaldor humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT pengxu humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT pavolkovac humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT stephenbcalderwood humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT robertckauffman humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT jenswrammert humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT firdausiqadri humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT jasonbharris humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility AT edwardtryan humanssurvivingcholeradevelopantibodiesagainstnamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentospecificpolysaccharidethatinhibitpathogenmotility |
| _version_ |
1718427178674159616 |