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Title: Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens

Abstract

Burkholderia pseudomallei (Bp) and Burkholderia mallei (Bm), the etiologic agents of melioidosis and glanders, respectively, cause severe disease in both humans and animals. Studies have highlighted the importance of Bp and Bm lipopolysaccharides (LPS) as vaccine candidates. Here we describe the synthesis of seven oligosaccharides as the minimal structures featuring all of the reported acetylation/methylation patterns associated with Bp and Bm LPS O-antigens (OAgs). Our approach is based on the conversion of an L-rhamnose into a 6-deoxy-L-talose residue at a late stage of the synthetic sequence. Using biochemical and biophysical methods, we demonstrate the binding of several Bp and Bm LPS-specific monoclonal antibodies with terminal OAg residues. Mice immunized with terminal disaccharide–CRM197 constructs produced high-titer antibody responses that crossreacted with Bm-like OAgs. Collectively, these studies serve as foundation for the development of novel therapeutics, diagnostics, and vaccine candidates to combat diseases caused by Bp and Bm.

Authors:
 [1];  [2];  [3];  [4];  [1];  [1];  [5];  [6];  [7];  [7];  [6];  [6];  [8];  [4];  [4];  [9]
  1. Université de Poitiers (France)
  2. Université de Poitiers (France); Wroclaw Univ. of Environmental and Life Sciences (Poland)
  3. Univ. of Nevada School of Medicine, Reno, NV (United States); Prince of Songkla Univ., Songkhla (Thailand)
  4. Univ. of South Alabama, Mobile, AL (United States)
  5. Univ. Paris-Saclay, Versailles (France)
  6. Università di Napoli Federico II, Complesso Universitario Monte S. Angelo, Naples (Italy)
  7. Mahidol Univ., Bangkok (Thailand)
  8. Univ. of Nevada School of Medicine, Reno, NV (United States)
  9. Université de Poitiers (France); Univ. of Quebec, Laval QC (Canada)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1535102
Grant/Contract Number:  
FG02-93ER20097
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Tamigney Kenfack, Marielle, Mazur, Marcelina, Nualnoi, Teerapat, Shaffer, Teresa L., Ngassimou, Abba, Blériot, Yves, Marrot, Jérôme, Marchetti, Roberta, Sintiprungrat, Kitisak, Chantratita, Narisara, Silipo, Alba, Molinaro, Antonio, AuCoin, David P., Burtnick, Mary N., Brett, Paul J., and Gauthier, Charles. Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens. United States: N. p., 2017. Web. doi:10.1038/s41467-017-00173-8.
Tamigney Kenfack, Marielle, Mazur, Marcelina, Nualnoi, Teerapat, Shaffer, Teresa L., Ngassimou, Abba, Blériot, Yves, Marrot, Jérôme, Marchetti, Roberta, Sintiprungrat, Kitisak, Chantratita, Narisara, Silipo, Alba, Molinaro, Antonio, AuCoin, David P., Burtnick, Mary N., Brett, Paul J., & Gauthier, Charles. Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens. United States. doi:10.1038/s41467-017-00173-8.
Tamigney Kenfack, Marielle, Mazur, Marcelina, Nualnoi, Teerapat, Shaffer, Teresa L., Ngassimou, Abba, Blériot, Yves, Marrot, Jérôme, Marchetti, Roberta, Sintiprungrat, Kitisak, Chantratita, Narisara, Silipo, Alba, Molinaro, Antonio, AuCoin, David P., Burtnick, Mary N., Brett, Paul J., and Gauthier, Charles. Mon . "Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens". United States. doi:10.1038/s41467-017-00173-8. https://www.osti.gov/servlets/purl/1535102.
@article{osti_1535102,
title = {Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens},
author = {Tamigney Kenfack, Marielle and Mazur, Marcelina and Nualnoi, Teerapat and Shaffer, Teresa L. and Ngassimou, Abba and Blériot, Yves and Marrot, Jérôme and Marchetti, Roberta and Sintiprungrat, Kitisak and Chantratita, Narisara and Silipo, Alba and Molinaro, Antonio and AuCoin, David P. and Burtnick, Mary N. and Brett, Paul J. and Gauthier, Charles},
abstractNote = {Burkholderia pseudomallei (Bp) and Burkholderia mallei (Bm), the etiologic agents of melioidosis and glanders, respectively, cause severe disease in both humans and animals. Studies have highlighted the importance of Bp and Bm lipopolysaccharides (LPS) as vaccine candidates. Here we describe the synthesis of seven oligosaccharides as the minimal structures featuring all of the reported acetylation/methylation patterns associated with Bp and Bm LPS O-antigens (OAgs). Our approach is based on the conversion of an L-rhamnose into a 6-deoxy-L-talose residue at a late stage of the synthetic sequence. Using biochemical and biophysical methods, we demonstrate the binding of several Bp and Bm LPS-specific monoclonal antibodies with terminal OAg residues. Mice immunized with terminal disaccharide–CRM197 constructs produced high-titer antibody responses that crossreacted with Bm-like OAgs. Collectively, these studies serve as foundation for the development of novel therapeutics, diagnostics, and vaccine candidates to combat diseases caused by Bp and Bm.},
doi = {10.1038/s41467-017-00173-8},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {7}
}

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    Works referencing / citing this record:

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    journal, September 1980

    • Schmidt, Richard R.; Michel, Josef
    • Angewandte Chemie International Edition in English, Vol. 19, Issue 9
    • DOI: 10.1002/anie.198007311

    Synthesis of All Eight Stereoisomeric 6-Deoxy- L -hexopyranosyl Donors - Trends in Using Stereoselective Reductions or Mitsunobu Epimerizations : Synthesis of 6-Deoxy-
    journal, October 2014

    • Frihed, Tobias Gylling; Pedersen, Christian Marcus; Bols, Mikael
    • European Journal of Organic Chemistry, Vol. 2014, Issue 35
    • DOI: 10.1002/ejoc.201403074

    Temperature dependence of ligand–protein complex formation as reflected by saturation transfer difference NMR experiments
    journal, January 2007

    • Groves, Patrick; Kövér, Katalin E.; André, Sabine
    • Magnetic Resonance in Chemistry, Vol. 45, Issue 9
    • DOI: 10.1002/mrc.2041

    Detailed structural analysis of the O-polysaccharide expressed by Burkholderia thailandensis E264
    journal, December 2012


    Revised structures for the predominant O-polysaccharides expressed by Burkholderia pseudomallei and Burkholderia mallei
    journal, November 2013


    Progress toward development of vaccines against melioidosis: A review
    journal, August 2010


    A gold nanoparticle-linked glycoconjugate vaccine against Burkholderia mallei
    journal, February 2015

    • Gregory, Anthony E.; Judy, Barbara M.; Qazi, Omar
    • Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 11, Issue 2
    • DOI: 10.1016/j.nano.2014.08.005

    Lipopolysaccharide from Burkholderia thailandensis E264 provides protection in a murine model of melioidosis
    journal, November 2010


    Protection of non-human primates against glanders with a gold nanoparticle glycoconjugate vaccine
    journal, January 2015


    Halide ion catalyzed glycosidation reactions. Syntheses of .alpha.-linked disaccharides
    journal, July 1975

    • Lemieux, R. U.; Hendriks, K. B.; Stick, R. V.
    • Journal of the American Chemical Society, Vol. 97, Issue 14
    • DOI: 10.1021/ja00847a032

    Regioselective Activation of Glycosyl Acceptors by a Diarylborinic Acid-Derived Catalyst
    journal, September 2011

    • Gouliaras, Christina; Lee, Doris; Chan, Lina
    • Journal of the American Chemical Society, Vol. 133, Issue 35
    • DOI: 10.1021/ja2062715

    Multivalent display of minimal Clostridium difficile glycan epitopes mimics antigenic properties of larger glycans
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    • Broecker, Felix; Hanske, Jonas; Martin, Christopher E.
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    • Limmathurotsakul, Direk; Golding, Nick; Dance, David A. B.
    • Nature Microbiology, Vol. 1, Issue 1
    • DOI: 10.1038/nmicrobiol.2015.8

    Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei
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    • Wiersinga, W. Joost; van der Poll, Tom; White, Nicholas J.
    • Nature Reviews Microbiology, Vol. 4, Issue 4
    • DOI: 10.1038/nrmicro1385

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    journal, February 2015

    • Currie, Bart
    • Seminars in Respiratory and Critical Care Medicine, Vol. 36, Issue 01
    • DOI: 10.1055/s-0034-1398389

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    • DOI: 10.1073/pnas.0401351101

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    • Charuchaimontri, Chadarat; Suputtamongkol, Yupin; Nilakul, Churairat
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    • DOI: 10.1086/520441

    Passive protection against Burkholderia pseudomallei infection in mice by monoclonal antibodies against capsular polysaccharide, lipopolysaccharide or proteins
    journal, December 2002


    Evaluation of lipopolysaccharide and capsular polysaccharide as subunit vaccines against experimental melioidosis
    journal, December 2004


    Biological activities of lipopolysaccharide of Burkholderia (Pseudomonas) pseudomallei
    journal, March 1996


    The wbiA locus is required for the 2- O -acetylation of lipopolysaccharides expressed by Burkholderia pseudomallei and Burkholderia thailandensis
    journal, January 2003


    Glanders in Animals: A Review on Epidemiology, Clinical Presentation, Diagnosis and Countermeasures: Glanders in Solipeds
    journal, May 2012


    Passive Protection of Diabetic Rats with Antisera Specific for the Polysaccharide Portion of the Lipopolysaccharide Isolated from Pseudomonas pseudomallei
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    • Bryan, Larry E.; Wong, Sallene; Woods, Don E.
    • Canadian Journal of Infectious Diseases, Vol. 5, Issue 4
    • DOI: 10.1155/1994/856850

    Activation of Toll-like receptors by Burkholderia pseudomallei
    journal, January 2008

    • West, T. Eoin; Ernst, Robert K.; Jansson-Hutson, Malinka J.
    • BMC Immunology, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2172-9-46

    Melioidosis Vaccines: A Systematic Review and Appraisal of the Potential to Exploit Biodefense Vaccines for Public Health Purposes
    journal, January 2012

    • Peacock, Sharon J.; Limmathurotsakul, Direk; Lubell, Yoel
    • PLoS Neglected Tropical Diseases, Vol. 6, Issue 1
    • DOI: 10.1371/journal.pntd.0001488

    Polysaccharide Specific Monoclonal Antibodies Provide Passive Protection against Intranasal Challenge with Burkholderia pseudomallei
    journal, April 2012


    Survey of Innate Immune Responses to Burkholderia pseudomallei in Human Blood Identifies a Central Role for Lipopolysaccharide
    journal, November 2013


    Recombinant Salmonella Expressing Burkholderia mallei LPS O Antigen Provides Protection in a Murine Model of Melioidosis and Glanders
    journal, July 2015


    Strategies toward vaccines against Burkholderia mallei and Burkholderia pseudomallei
    journal, November 2008


    Present and future therapeutic strategies for melioidosis and glanders
    journal, March 2010

    • Estes, D. Mark; Dow, Steven W.; Schweizer, Herbert P.
    • Expert Review of Anti-infective Therapy, Vol. 8, Issue 3
    • DOI: 10.1586/eri.10.4


    journal, April 2015


    Development of Burkholderia mallei and pseudomallei vaccines
    journal, January 2013

    • Silva, Ediane B.; Dow, Steven W.
    • Frontiers in Cellular and Infection Microbiology, Vol. 3
    • DOI: 10.3389/fcimb.2013.00010

    Development of Vaccines Against Burkholderia Pseudomallei
    journal, January 2011


    Production of a recombinant vaccine candidate against Burkholderia pseudomallei exploiting the bacterial N-glycosylation machinery
    journal, July 2014

    • Garcia-Quintanilla, Fatima; Iwashkiw, Jeremy A.; Price, Nancy L.
    • Frontiers in Microbiology, Vol. 5
    • DOI: 10.3389/fmicb.2014.00381

    Synthesis of Disaccharides Containing 6-Deoxy-a-L-talose as Potential Heparan Sulfate Mimetics
    journal, August 2012