Outer membrane vesicles displaying engineered glycotopes elicit protective antibodies

Chen, Linxiao; Valentine, Jenny L.; Huang, Chung-Jr; Endicott, Christine E.; Moeller, Tyler D.; Rasmussen, Jed A.; Fletcher, Joshua R.; Boll, Joseph M.; Rosenthal, Joseph A.; Dobruchowska, Justyna; Wang, Zhirui; Heiss, Christian; Azadi, Parastoo; Putnam, David; Trent, M. Stephen; Jones, Bradley D.; DeLisa, Matthew P.

doi:10.1073/pnas.1518311113

Title: Outer membrane vesicles displaying engineered glycotopes elicit protective antibodies

Journal Article · 06 June 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1518311113 · OSTI ID:1256136

^[1]; Valentine, Jenny L. ^[1]; Huang, Chung-Jr ^[1]; Endicott, Christine E. ^[1]; Moeller, Tyler D. ^[1]; Rasmussen, Jed A. ^[2]; Fletcher, Joshua R. ^[3]; Boll, Joseph M. ^[4]; Rosenthal, Joseph A. ^[5]; Dobruchowska, Justyna ^[6]; Wang, Zhirui ^[6]; Heiss, Christian ^[6]; Azadi, Parastoo ^[6]; Putnam, David ^[7]; Trent, M. Stephen ^[4]; Jones, Bradley D. ^[8]; DeLisa, Matthew P. ^[7]

Cornell Univ., Ithaca, NY (United States). Robert Frederick Smith School of Chemical and Biomolecular Engineering
Univ. of Iowa, Iowa City, IA (United States). Dept. of Microbiology
Univ. of Iowa, Iowa City, IA (United States). Genetics Program
Univ. of Texas, Austin, TX (United States). Dept. of Molecular Biosciences; Univ. of Georgia College of Veterinary Medicine, Athens, GA (United States). Dept. of Infectious Diseases
Cornell Univ., Ithaca, NY (United States). Nancy E. and Peter C. Meinig School of Biomedical Engineering
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Cornell Univ., Ithaca, NY (United States). Robert Frederick Smith School of Chemical and Biomolecular Engineering. Nancy E. and Peter C. Meinig School of Biomedical Engineering
Univ. of Iowa, Iowa City, IA (United States). Dept. of Microbiology. Genetics Program

The O-antigen polysaccharide (O-PS) component of lipopolysaccharides on the surface of gram-negative bacteria is both a virulence factor and a B-cell antigen. Antibodies elicited by O-PS often confer protection against infection; therefore, O-PS glycoconjugate vaccines have proven useful against a number of different pathogenic bacteria. However, conventional methods for natural extraction or chemical synthesis of O-PS are technically demanding, inefficient, and expensive. In this paper, we describe an alternative methodology for producing glycoconjugate vaccines whereby recombinant O-PS biosynthesis is coordinated with vesiculation in laboratory strains of Escherichia coli to yield glycosylated outer membrane vesicles (glycOMVs) decorated with pathogen-mimetic glycotopes. Using this approach, glycOMVs corresponding to eight different pathogenic bacteria were generated. For example, expression of a 17-kb O-PS gene cluster from the highly virulent Francisella tularensis subsp. tularensis (type A) strain Schu S4 in hypervesiculating E. coli cells yielded glycOMVs that displayed F. tularensis O-PS. Immunization of BALB/c mice with glycOMVs elicited significant titers of O-PS–specific serum IgG antibodies as well as vaginal and bronchoalveolar IgA antibodies. Importantly, glycOMVs significantly prolonged survival upon subsequent challenge with F. tularensis Schu S4 and provided complete protection against challenge with two different F. tularensis subsp. holarctica (type B) live vaccine strains, thereby demonstrating the vaccine potential of glycOMVs. Finally, given the ease with which recombinant glycotopes can be expressed on OMVs, the strategy described here could be readily adapted for developing vaccines against many other bacterial pathogens.

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Research Organization:: Univ. of Georgia, Athens, GA (United States); Cornell Univ., Ithaca, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Inst. of Health (NIH) (United States); New York State Office of Science, Technology and Academic Research (NYSTAR) (United States); US Army Research Office (ARO); Midwest Regional Center of Excellence (MRCE) for Biodefense and Emerging Infectious Disease Research (United States)

Contributing Organization:: Univ. of Iowa, Iowa City, IA (United States); Univ. of Texas, Austin, TX (United States)

Grant/Contract Number:: FG02-93ER20097; DMR-1120296; CBET 1159581; CBET 1264701; GM088905-01; EB005669-01; AI044642; AI057160; GM008629; AI064184; AI076322; GM10349010; W911NF-12-1-0390

OSTI ID:: 1256136

Alternate ID(s):: OSTI ID: 1349046

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 26; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 90 works

Citation information provided by
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References (81)

Purified Lipopolysaccharide from Francisella tularensis Live Vaccine Strain (LVS) Induces Protective Immunity against LVS Infection That Requires B Cells and Gamma Interferon Dreisbach, V. C.; Cowley, S.; Elkins, K. L. Infection and Immunity, Vol. 68, Issue 4 https://doi.org/10.1128/IAI.68.4.1988-1996.2000	journal	April 2000
T Cell-Independent Antigens Type 2 Mond, James J.; Lees, Andrew; Snapper, Clifford M. Annual Review of Immunology, Vol. 13, Issue 1 https://doi.org/10.1146/annurev.iy.13.040195.003255	journal	April 1995
Exploitation of bacterial N -linked glycosylation to develop a novel recombinant glycoconjugate vaccine against Francisella tularensis Cuccui, Jon; Thomas, Rebecca M.; Moule, Madeleine G. Open Biology, Vol. 3, Issue 5 https://doi.org/10.1098/rsob.130002	journal	May 2013
Biosynthesis and Assembly of Capsular Polysaccharides in Escherichia coli Whitfield, Chris Annual Review of Biochemistry, Vol. 75, Issue 1, p. 39-68 https://doi.org/10.1146/annurev.biochem.75.103004.142545	journal	June 2006
Preparation of bacterial polysaccharide–protein conjugates: Analytical and manufacturing challenges Frasch, Carl E. Vaccine, Vol. 27, Issue 46 https://doi.org/10.1016/j.vaccine.2009.06.013	journal	October 2009
γδ T Cells Provide an Early Source of Interferon γ in Tumor Immunity Gao, Yunfei; Yang, Wancai; Pan, Meng The Journal of Experimental Medicine, Vol. 198, Issue 3 https://doi.org/10.1084/jem.20030584	journal	August 2003
Working toward the Future: Insights into Francisella tularensis Pathogenesis and Vaccine Development Pechous, R. D.; McCarthy, T. R.; Zahrt, T. C. Microbiology and Molecular Biology Reviews, Vol. 73, Issue 4 https://doi.org/10.1128/MMBR.00028-09	journal	November 2009
Discovery of new biosynthetic pathways: the lipid A story Raetz, Christian R. H.; Guan, Ziqiang; Ingram, Brian O. Journal of Lipid Research, Vol. 50, Issue Supplement https://doi.org/10.1194/jlr.R800060-JLR200	journal	October 2008
Recent developments in bacterial protein glycan coupling technology and glycoconjugate vaccine design Terra, V. S.; Mills, D. C.; Yates, L. E. Journal of Medical Microbiology, Vol. 61, Issue Pt_7 https://doi.org/10.1099/jmm.0.039438-0	journal	April 2012
Immunization with Salmonella enterica Serovar Typhimurium-Derived Outer Membrane Vesicles Delivering the Pneumococcal Protein PspA Confers Protection against Challenge with Streptococcus pneumoniae Muralinath, Maneesha; Kuehn, Meta J.; Roland, Kenneth L. Infection and Immunity, Vol. 79, Issue 2 https://doi.org/10.1128/IAI.00950-10	journal	November 2010
Lipopolysaccharide Endotoxins Raetz, Christian R. H.; Whitfield, Chris Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135414	journal	June 2002
Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis Fulop, Mark; Mastroeni, Pietro; Green, Michael Vaccine, Vol. 19, Issue 31 https://doi.org/10.1016/S0264-410X(01)00189-X	journal	August 2001
Bexsero: A multicomponent vaccine for prevention of meningococcal disease Gorringe, Andrew R.; Pajón, Rolando Human Vaccines & Immunotherapeutics, Vol. 8, Issue 2 https://doi.org/10.4161/hv.18500	journal	February 2012
Optimising the use of conjugate vaccines to prevent disease caused by Haemophilus influenzae type b, Neisseria meningitidis and Streptococcus pneumoniae Trotter, Caroline L.; McVernon, Jodie; Ramsay, Mary E. Vaccine, Vol. 26, Issue 35 https://doi.org/10.1016/j.vaccine.2008.05.073	journal	August 2008
Microbial biosynthesis of designer outer membrane vesicles Baker, Jenny L.; Chen, Linxiao; Rosenthal, Joseph A. Current Opinion in Biotechnology, Vol. 29 https://doi.org/10.1016/j.copbio.2014.02.018	journal	October 2014
Characterization of the O antigen gene cluster and structural analysis of the O antigen of Francisella tularensis subsp. tularensis Prior, J. L. Journal of Medical Microbiology, Vol. 52, Issue 10 https://doi.org/10.1099/jmm.0.05184-0	journal	October 2003
Antibody-mediated immunity induced by engineered Escherichia coli OMVs carrying heterologous antigens in their lumen Fantappiè, Laura; de Santis, Micaela; Chiarot, Emiliano Journal of Extracellular Vesicles, Vol. 3, Issue 1 https://doi.org/10.3402/jev.v3.24015	journal	January 2014
Carbohydrate vaccines: developing sweet solutions to sticky situations? Astronomo, Rena D.; Burton, Dennis R. Nature Reviews Drug Discovery, Vol. 9, Issue 4 https://doi.org/10.1038/nrd3012	journal	April 2010
Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli Balsalobre, Carlos; Silvan, Jose Manuel; Berglund, Stina Molecular Microbiology, Vol. 59, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04938.x	journal	January 2006
T-cell–B-cell cooperation Mitchison, N. A. Nature Reviews Immunology, Vol. 4, Issue 4 https://doi.org/10.1038/nri1334	journal	April 2004
Conjugate vaccines: Conjugate vaccines Goldblatt, D. Clinical & Experimental Immunology, Vol. 119, Issue 1 https://doi.org/10.1046/j.1365-2249.2000.01109.x	journal	January 2000
Adjuvant properties of meningococcal outer membrane vesicles and the use of adjuvants in Neisseria meningitidis protein vaccines Sanders, Holly; Feavers, Ian M. Expert Review of Vaccines, Vol. 10, Issue 3 https://doi.org/10.1586/erv.11.10	journal	March 2011
Delivery of foreign antigens by engineered outer membrane vesicle vaccines Chen, D. J.; Osterrieder, N.; Metzger, S. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 7 https://doi.org/10.1073/pnas.0805532107	journal	January 2010
Identification, Characterization and Immunogenicity of an O-Antigen Capsular Polysaccharide of Francisella tularensis Apicella, Michael A.; Post, Deborah M. B.; Fowler, Andrew C. PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011060	journal	July 2010
B Cell Mitogenic Properties of Thymus-independent Antigens Coutinho, Antonio; MÖLler, GÖRan Nature New Biology, Vol. 245, Issue 140 https://doi.org/10.1038/newbio245012a0	journal	September 1973
Tularaemia: bioterrorism defence renews interest in Francisella tularensis Oyston, Petra C. F.; Sjöstedt, Anders; Titball, Richard W. Nature Reviews Microbiology, Vol. 2, Issue 12 https://doi.org/10.1038/nrmicro1045	journal	December 2004
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 Alaniz, Robert C.; Deatherage, Brooke L.; Lara, Jimmie C. The Journal of Immunology, Vol. 179, Issue 11 https://doi.org/10.4049/jimmunol.179.11.7692	journal	November 2007
How Bacterial Carbohydrates Influence the Adaptive Immune System Avci, Fikri Y.; Kasper, Dennis L. Annual Review of Immunology, Vol. 28, Issue 1 https://doi.org/10.1146/annurev-immunol-030409-101159	journal	March 2010
Somatic antigens of Shigella: Structure of the O-specific polysaccharide chain of the Shigella dysenteriae type 7 lipopolysaccharide Knirel, Yuriy A.; Dashunin, Vladimir V.; Shashkov, Alexander S. Carbohydrate Research, Vol. 179 https://doi.org/10.1016/0008-6215(88)84109-0	journal	August 1988
A Novel Role for Plasmin-Mediated Degradation of Opsonizing Antibody in the Evasion of Host Immunity by Virulent, but Not Attenuated, Francisella tularensis Crane, Deborah D.; Warner, Shayna L.; Bosio, Catharine M. The Journal of Immunology, Vol. 183, Issue 7 https://doi.org/10.4049/jimmunol.0901655	journal	September 2009
Engineered Bacterial Outer Membrane Vesicles with Enhanced Functionality Kim, Jae-Young; Doody, Anne M.; Chen, David J. Journal of Molecular Biology, Vol. 380, Issue 1 https://doi.org/10.1016/j.jmb.2008.03.076	journal	June 2008
Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli Feldman, M. F.; Wacker, M.; Hernandez, M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 8 https://doi.org/10.1073/pnas.0500044102	journal	February 2005
Innate B cell helpers reveal novel types of antibody responses Vinuesa, Carola G.; Chang, Pheh-Ping Nature Immunology, Vol. 14, Issue 2 https://doi.org/10.1038/ni.2511	journal	January 2013
Pathogenicity and molecular genetics of O-specific side-chain lipopolysaccharides of Escherichia coli Valvano, Miguel A. Canadian Journal of Microbiology, Vol. 38, Issue 7 https://doi.org/10.1139/m92-117	journal	July 1992
Mechanistic Insight into the TH1-Biased Immune Response to Recombinant Subunit Vaccines Delivered by Probiotic Bacteria-Derived Outer Membrane Vesicles Rosenthal, Joseph A.; Huang, Chung-Jr.; Doody, Anne M. PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112802	journal	November 2014
Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems Wacker, M.; Feldman, M. F.; Callewaert, N. Proceedings of the National Academy of Sciences, Vol. 103, Issue 18 https://doi.org/10.1073/pnas.0509207103	journal	April 2006
Exploitation of bacterial N -linked glycosylation to develop a novel recombinant glycoconjugate vaccine against Francisella tularensis Cuccui, Jon; Thomas, Rebecca M.; Moule, Madeleine G. Open Biology, Vol. 3, Issue 5 https://doi.org/10.1098/rsob.130002	journal	May 2013
Conjugate vaccines Finn, A. Archives of Disease in Childhood, Vol. 90, Issue 7 https://doi.org/10.1136/adc.2005.072173	journal	July 2005
Conjugate vaccines Lockhart, Stephen Expert Review of Vaccines, Vol. 2, Issue 5 https://doi.org/10.1586/14760584.2.5.633	journal	October 2003
Incorporation of Heterologous Outer Membrane and Periplasmic Proteins into Escherichia coli Outer Membrane Vesicles Kesty, Nicole C.; Kuehn, Meta J. Journal of Biological Chemistry, Vol. 279, Issue 3 https://doi.org/10.1074/jbc.M307628200	journal	October 2003
Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles Kulp, Adam; Kuehn, Meta J. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073413	journal	October 2010
Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis Holst, Johan; Martin, Diana; Arnold, Richard Vaccine, Vol. 27 https://doi.org/10.1016/j.vaccine.2009.04.071	journal	June 2009
Elucidation of a novel Vibrio cholerae lipid A secondary hydroxy-acyltransferase and its role in innate immune recognition: Incorporation of hydroxy fatty acids into V. cholerae LPS by LpxN Hankins, Jessica V.; Madsen, James A.; Giles, David K. Molecular Microbiology, Vol. 81, Issue 5 https://doi.org/10.1111/j.1365-2958.2011.07765.x	journal	July 2011
Lipopolysaccharide Endotoxins Raetz, Christian R. H.; Whitfield, Chris Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135414	journal	June 2002
Expression cloning of Yersinia enterocolitica 0 : 3 rfb gene cluster in Escherichia coli K12 Al-Hendy, Ayman; Toivanen, Paavo; Skurnik, Mikael Microbial Pathogenesis, Vol. 10, Issue 1 https://doi.org/10.1016/0882-4010(91)90065-I	journal	January 1991
Role of lipopolysaccharide and a major outer membrane protein from Francisella tularensis in the induction of immunity against tularemia Fulop, Mark; Manchee, Richard; Titball, Richard Vaccine, Vol. 13, Issue 13 https://doi.org/10.1016/0264-410X(95)00062-6	journal	January 1995
Preparation of bacterial polysaccharide–protein conjugates: Analytical and manufacturing challenges Frasch, Carl E. Vaccine, Vol. 27, Issue 46 https://doi.org/10.1016/j.vaccine.2009.06.013	journal	October 2009
γδ T Cells Provide an Early Source of Interferon γ in Tumor Immunity Gao, Yunfei; Yang, Wancai; Pan, Meng The Journal of Experimental Medicine, Vol. 198, Issue 3 https://doi.org/10.1084/jem.20030584	journal	August 2003
Conjugate Vaccines Parthasarathy, A.; Yadav, Sangeeta A Ready Reckoner for Vaccinations https://doi.org/10.5005/jp/books/11116_10	book	January 2010
Vaccines based on the cell surface carbohydrates of pathogenic bacteria Jones, Christopher Anais da Academia Brasileira de Ciências, Vol. 77, Issue 2 https://doi.org/10.1590/S0001-37652005000200009	journal	June 2005
Naturally Produced Outer Membrane Vesicles from Pseudomonas aeruginosa Elicit a Potent Innate Immune Response via Combined Sensing of Both Lipopolysaccharide and Protein Components Ellis, T. N.; Leiman, S. A.; Kuehn, M. J. Infection and Immunity, Vol. 78, Issue 9 https://doi.org/10.1128/IAI.00433-10	journal	July 2010
Cognate Stimulatory B-Cell–T-Cell Interactions Are Critical for T-Cell Help Recruited by Glycoconjugate Vaccines Guttormsen, Hilde-Kari; Sharpe, Arlene H.; Chandraker, Anil K. Infection and Immunity, Vol. 67, Issue 12 https://doi.org/10.1128/IAI.67.12.6375-6384.1999	journal	December 1999
Escherichia coli tol-pal Mutants Form Outer Membrane Vesicles Bernadac, Alain; Gavioli, Marthe; Lazzaroni, Jean-Claude Journal of Bacteriology, Vol. 180, Issue 18 https://doi.org/10.1128/JB.180.18.4872-4878.1998	journal	September 1998
Immunology of bacterial polysaccharide antigens Weintraub, Andrej Carbohydrate Research, Vol. 338, Issue 23, p. 2539-2547 https://doi.org/10.1016/j.carres.2003.07.008	journal	November 2003
Recombinant outer membrane vesicles carrying Chlamydia muridarum HtrA induce antibodies that neutralize chlamydial infection in vitro Bartolini, Erika; Ianni, Elvira; Frigimelica, Elisabetta Journal of Extracellular Vesicles, Vol. 2, Issue 1 https://doi.org/10.3402/jev.v2i0.20181	journal	January 2013
Protective B-cell epitopes of Francisella tularensis O-polysaccharide in a mouse model of respiratory tularaemia: Protective epitopes of Francisella tularensis O-antigen Lu, Zhaohua; Madico, Guillermo; Roche, Marly I. Immunology, Vol. 136, Issue 3 https://doi.org/10.1111/j.1365-2567.2012.03589.x	journal	June 2012
Structure of the O-antigen of Francisella tularensis strain 15 Vinogradov, Eugeny V.; Shashkov, Alexander S.; Knirel, Yuriy A. Carbohydrate Research, Vol. 214, Issue 2 https://doi.org/10.1016/0008-6215(91)80036-M	journal	July 1991
Modulating the innate immune response by combinatorial engineering of endotoxin Needham, Brittany D.; Carroll, Sean M.; Giles, David K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 4 https://doi.org/10.1073/pnas.1218080110	journal	January 2013
Production of glycoprotein vaccines in Escherichia coli Ihssen, Julian; Kowarik, Michael; Dilettoso, Sandro Microbial Cell Factories, Vol. 9, Issue 1 https://doi.org/10.1186/1475-2859-9-61	journal	January 2010
Production of Secretory and Extracellular N-Linked Glycoproteins in Escherichia coli Fisher, Adam C.; Haitjema, Charles H.; Guarino, Cassandra Applied and Environmental Microbiology, Vol. 77, Issue 3 https://doi.org/10.1128/AEM.01901-10	journal	December 2010
Characterization of bacteria using its O-antigen with surface-enhanced Raman scattering Osorio-Román, I. O.; Aroca, R. F.; Astudillo, J. The Analyst, Vol. 135, Issue 8 https://doi.org/10.1039/c0an00061b	journal	January 2010
Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli Balsalobre, Carlos; Silvan, Jose Manuel; Berglund, Stina Molecular Microbiology, Vol. 59, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04938.x	journal	January 2006
Pathogenicity and molecular genetics of O-specific side-chain lipopolysaccharides of Escherichia coli Valvano, Miguel A. Canadian Journal of Microbiology, Vol. 38, Issue 7 https://doi.org/10.1139/m92-117	journal	July 1992
Immunologic Memory Induced by a Glycoconjugate Vaccine in a Murine Adoptive Lymphocyte Transfer Model Guttormsen, Hilde-Kari; Wetzler, Lee M.; Finberg, Robert W. Infection and Immunity, Vol. 66, Issue 5 https://doi.org/10.1128/IAI.66.5.2026-2032.1998	journal	May 1998
Antibody-mediated immunity induced by engineered Escherichia coli OMVs carrying heterologous antigens in their lumen Fantappiè, Laura; de Santis, Micaela; Chiarot, Emiliano Journal of Extracellular Vesicles, Vol. 3, Issue 1 https://doi.org/10.3402/jev.v3.24015	journal	January 2014
Tularaemia: bioterrorism defence renews interest in Francisella tularensis Oyston, Petra C. F.; Sjöstedt, Anders; Titball, Richard W. Nature Reviews Microbiology, Vol. 2, Issue 12 https://doi.org/10.1038/nrmicro1045	journal	December 2004
Elucidation of a novel Vibrio cholerae lipid A secondary hydroxy-acyltransferase and its role in innate immune recognition: Incorporation of hydroxy fatty acids into V. cholerae LPS by LpxN Hankins, Jessica V.; Madsen, James A.; Giles, David K. Molecular Microbiology, Vol. 81, Issue 5 https://doi.org/10.1111/j.1365-2958.2011.07765.x	journal	July 2011
Inactivated Francisella tularensis Live Vaccine Strain Protects against Respiratory Tularemia by Intranasal Vaccination in an Immunoglobulin A-Dependent Fashion Baron, S. D.; Singh, R.; Metzger, D. W. Infection and Immunity, Vol. 75, Issue 5 https://doi.org/10.1128/IAI.01606-06	journal	February 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 Alaniz, R. C.; Deatherage, B. L.; Lara, J. C. The Journal of Immunology, Vol. 180, Issue 5 https://doi.org/10.4049/jimmunol.180.5.3612-b	journal	February 2008
A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates Domon, Bruno; Costello, Catherine E. Glycoconjugate Journal, Vol. 5, Issue 4 https://doi.org/10.1007/BF01049915	journal	January 1988
Evaluation of the establishment of herd immunity in the population by means of serological surveys and vaccination coverage Plans-Rubió, Pedro Human Vaccines & Immunotherapeutics, Vol. 8, Issue 2 https://doi.org/10.4161/hv.18444	journal	February 2012
Putting endotoxin to work for us: Monophosphoryl lipid A as a safe and effective vaccine adjuvant Casella, C. R.; Mitchell, T. C. Cellular and Molecular Life Sciences, Vol. 65, Issue 20 https://doi.org/10.1007/s00018-008-8228-6	journal	August 2008
Engineered Bacterial Outer Membrane Vesicles with Enhanced Functionality Kim, Jae-Young; Doody, Anne M.; Chen, David J. Journal of Molecular Biology, Vol. 380, Issue 1 https://doi.org/10.1016/j.jmb.2008.03.076	journal	June 2008
Successful Protection against Tularemia in C57BL/6 Mice Is Correlated with Expansion of Francisella tularensis-Specific Effector T Cells Griffin, Amanda J.; Crane, Deborah D.; Wehrly, Tara D. Clinical and Vaccine Immunology, Vol. 22, Issue 1 https://doi.org/10.1128/CVI.00648-14	journal	November 2014
B Cell Mitogenic Properties of Thymus-independent Antigens Coutinho, Antonio; MÖLler, GÖRan Nature New Biology, Vol. 245, Issue 140 https://doi.org/10.1038/newbio245012a0	journal	September 1973
Somatic antigens of Shigella: Structure of the O-specific polysaccharide chain of the Shigella dysenteriae type 7 lipopolysaccharide Knirel, Yuriy A.; Dashunin, Vladimir V.; Shashkov, Alexander S. Carbohydrate Research, Vol. 179 https://doi.org/10.1016/0008-6215(88)84109-0	journal	August 1988
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 Alaniz, Robert C.; Deatherage, Brooke L.; Lara, Jimmie C. The Journal of Immunology, Vol. 179, Issue 11 https://doi.org/10.4049/jimmunol.179.11.7692	journal	November 2007
New vaccine platform? Flemming, Alexandra Nature Reviews Drug Discovery, Vol. 9, Issue 3 https://doi.org/10.1038/nrd3117	journal	March 2010
Francisella tularensis Schu S4 Lipopolysaccharide Core Sugar and O-Antigen Mutants Are Attenuated in a Mouse Model of Tularemia Rasmussen, Jed A.; Post, Deborah M. B.; Gibson, Bradford W. Infection and Immunity, Vol. 82, Issue 4 https://doi.org/10.1128/IAI.01640-13	journal	January 2014
Expression of Heterologous Antigens in Commensal Neisseria spp.: Preservation of Conformational Epitopes with Vaccine Potential O'Dwyer, C. A.; Reddin, K.; Martin, D. Infection and Immunity, Vol. 72, Issue 11 https://doi.org/10.1128/IAI.72.11.6511-6518.2004	journal	October 2004
Bexsero: A multicomponent vaccine for prevention of meningococcal disease Gorringe, Andrew R.; Pajón, Rolando Human Vaccines & Immunotherapeutics, Vol. 8, Issue 2 https://doi.org/10.4161/hv.18500	journal	February 2012

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Immunization with outer membrane vesicles displaying conserved surface polysaccharide antigen elicits broadly antimicrobial antibodies Stevenson, Taylor C.; Cywes-Bentley, Colette; Moeller, Tyler D. Proceedings of the National Academy of Sciences, Vol. 115, Issue 14 https://doi.org/10.1073/pnas.1718341115	journal	March 2018
Differential Cultivation of Francisella tularensis Induces Changes in the Immune Response to and Protective Efficacy of Whole Cell-Based Inactivated Vaccines Kumar, Sudeep; Sunagar, Raju; Pham, Giang Frontiers in Immunology, Vol. 7 https://doi.org/10.3389/fimmu.2016.00677	journal	January 2017
Natural and engineered bacterial outer membrane vesicles Qing, Guangchao; Gong, Ningqiang; Chen, Xiaohui Biophysics Reports, Vol. 5, Issue 4 https://doi.org/10.1007/s41048-019-00095-6	journal	August 2019
Pushing the envelope: LPS modifications and their consequences Simpson, Brent W.; Trent, M. Stephen Nature Reviews Microbiology, Vol. 17, Issue 7 https://doi.org/10.1038/s41579-019-0201-x	journal	May 2019
Environmentally controlled bacterial vesicle-mediated export: Environmentally controlled bacterial vesicle-mediated export Orench-Rivera, Nichole; Kuehn, Meta J. Cellular Microbiology, Vol. 18, Issue 11 https://doi.org/10.1111/cmi.12676	journal	October 2016
Protein Carriers for Glycoconjugate Vaccines: History, Selection Criteria, Characterization and New Trends Micoli, Francesca; Adamo, Roberto; Costantino, Paolo Molecules, Vol. 23, Issue 6 https://doi.org/10.3390/molecules23061451	journal	June 2018
Protein Carriers for Glycoconjugate Vaccines: History, Selection Criteria, Characterization and New Trends Micoli, Francesca; Adamo, Roberto; Costantino, Paolo Molecules, Vol. 23, Issue 6 https://doi.org/10.3390/molecules23061451	journal	June 2018
Recent advances in the production of recombinant glycoconjugate vaccines Kay, Emily; Cuccui, Jon; Wren, Brendan W. npj Vaccines, Vol. 4, Issue 1 https://doi.org/10.1038/s41541-019-0110-z	journal	May 2019
Single-pot glycoprotein biosynthesis using a cell-free transcription-translation system enriched with glycosylation machinery Jaroentomeechai, Thapakorn; Stark, Jessica C.; Natarajan, Aravind Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05110-x	journal	July 2018
Bacterial membrane vesicles: Biogenesis, immune regulation and pathogenesis: Bacterial membrane vesicles: Biogenesis, immune regulation and pathogenesis Pathirana, Rishi D.; Kaparakis-Liaskos, Maria Cellular Microbiology, Vol. 18, Issue 11 https://doi.org/10.1111/cmi.12658	journal	September 2016
Recent advances in the production of recombinant glycoconjugate vaccines Kay, Emily; Cuccui, Jon; Wren, Brendan W. npj Vaccines, Vol. 4, Issue 1 https://doi.org/10.1038/s41541-019-0110-z	journal	May 2019
Glycoconjugate vaccine using a genetically modified O antigen induces protective antibodies to Francisella tularensis Stefanetti, Giuseppe; Okan, Nihal; Fink, Avner Proceedings of the National Academy of Sciences, Vol. 116, Issue 14 https://doi.org/10.1073/pnas.1900144116	journal	March 2019
Single-pot glycoprotein biosynthesis using a cell-free transcription-translation system enriched with glycosylation machinery Jaroentomeechai, Thapakorn; Stark, Jessica C.; Natarajan, Aravind Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05110-x	journal	July 2018
Glycoengineering bioconjugate vaccines, therapeutics, and diagnostics in E. coli Harding, Christian M.; Feldman, Mario F. Glycobiology, Vol. 29, Issue 7 https://doi.org/10.1093/glycob/cwz031	journal	May 2019
Advances and Opportunities in Nanoparticle- and Nanomaterial-Based Vaccines against Bacterial Infections Lin, Leon Chien-Wei; Chattopadhyay, Saborni; Lin, Jung-Chen Advanced Healthcare Materials, Vol. 7, Issue 13 https://doi.org/10.1002/adhm.201701395	journal	March 2018
Intranasal administration of a two-dose adjuvanted multi-antigen TMV-subunit conjugate vaccine fully protects mice against Francisella tularensis LVS challenge McCormick, Alison A.; Shakeel, Aisha; Yi, Chris PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0194614	journal	April 2018
Fantastic voyage: the journey of intestinal microbiota-derived microvesicles through the body Stentz, Régis; Carvalho, Ana L.; Jones, Emily J. Biochemical Society Transactions, Vol. 46, Issue 5 https://doi.org/10.1042/bst20180114	journal	August 2018
Fantastic voyage: the journey of intestinal microbiota-derived microvesicles through the body Stentz, Régis; Carvalho, Ana L.; Jones, Emily J. Biochemical Society Transactions, Vol. 46, Issue 5 https://doi.org/10.1042/bst20180114	journal	August 2018
Intranasal administration of a two-dose adjuvanted multi-antigen TMV-subunit conjugate vaccine fully protects mice against Francisella tularensis LVS challenge McCormick, Alison A.; Shakeel, Aisha; Yi, Chris PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0194614	journal	April 2018
Glycoconjugate vaccines: current approaches towards faster vaccine design Micoli, Francesca; Del Bino, Linda; Alfini, Renzo Expert Review of Vaccines, Vol. 18, Issue 9 https://doi.org/10.1080/14760584.2019.1657012	journal	August 2019

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