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Title: Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis

Abstract

Haemophilus parasuis is a Gram-negative bacterium that colonizes the upper respiratory tract of swine and is capable of causing a systemic infection, resulting in high morbidity and mortality. H. parasuis isolates display a wide range of virulence and virulence factors are largely unknown. Commercial bacterins are often used to vaccinate swine against H. parasuis, though strain variability and lack of cross-reactivity can make this an ineffective means of protection. Outer membrane vesicles (OMV) are spherical structures naturally released from the membrane of bacteria and OMV are often enriched in toxins, signaling molecules and other bacterial components. Examination of OMV structures has led to identification of virulence factors in a number of bacteria and they have been successfully used as subunit vaccines. We have isolated OMV from both virulent and avirulent strains of H. parasuis, have examined their protein content and assessed their ability to induce an immune response in the host. Lastly, vaccination with purified OMV derived from the virulent H. parasuis Nagasaki strain provided protection against challenge with a lethal dose of the bacteria.

Authors:
 [1];  [1];  [1];  [1];  [2]
  1. National Animal Disease Center, Agricultural Research Service, USDA, Ames, IA (United States)
  2. Univ. Paris Descartes, Paris (France)
Publication Date:
Research Org.:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States); Oak Ridge Associated Universities (ORAU), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1252954
Grant/Contract Number:  
AC05-06OR23100
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 3; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; swine; outer membrane proteins; vaccines; vesicles; virulence factors; proteases; vaccination and immunization; serum proteins

Citation Formats

McCaig, William D., Loving, Crystal L., Hughes, Holly R., Brockmeier, Susan L., and Charbit, Alain. Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0149132.
McCaig, William D., Loving, Crystal L., Hughes, Holly R., Brockmeier, Susan L., & Charbit, Alain. Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis. United States. https://doi.org/10.1371/journal.pone.0149132
McCaig, William D., Loving, Crystal L., Hughes, Holly R., Brockmeier, Susan L., and Charbit, Alain. Tue . "Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis". United States. https://doi.org/10.1371/journal.pone.0149132. https://www.osti.gov/servlets/purl/1252954.
@article{osti_1252954,
title = {Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis},
author = {McCaig, William D. and Loving, Crystal L. and Hughes, Holly R. and Brockmeier, Susan L. and Charbit, Alain},
abstractNote = {Haemophilus parasuis is a Gram-negative bacterium that colonizes the upper respiratory tract of swine and is capable of causing a systemic infection, resulting in high morbidity and mortality. H. parasuis isolates display a wide range of virulence and virulence factors are largely unknown. Commercial bacterins are often used to vaccinate swine against H. parasuis, though strain variability and lack of cross-reactivity can make this an ineffective means of protection. Outer membrane vesicles (OMV) are spherical structures naturally released from the membrane of bacteria and OMV are often enriched in toxins, signaling molecules and other bacterial components. Examination of OMV structures has led to identification of virulence factors in a number of bacteria and they have been successfully used as subunit vaccines. We have isolated OMV from both virulent and avirulent strains of H. parasuis, have examined their protein content and assessed their ability to induce an immune response in the host. Lastly, vaccination with purified OMV derived from the virulent H. parasuis Nagasaki strain provided protection against challenge with a lethal dose of the bacteria.},
doi = {10.1371/journal.pone.0149132},
journal = {PLoS ONE},
number = 3,
volume = 11,
place = {United States},
year = {Tue Mar 01 00:00:00 EST 2016},
month = {Tue Mar 01 00:00:00 EST 2016}
}

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Cited by: 38 works
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Works referenced in this record:

Update on the diagnosis of Haemophilus parasuis infection in pigs and novel genotyping methods
journal, November 2007


Haemophilus parasuis exhibits IgA protease activity but lacks homologs of the IgA protease genes of Haemophilus influenzae
journal, December 2011

  • Mullins, Michael A.; Register, Karen B.; Bayles, Darrell O.
  • Veterinary Microbiology, Vol. 153, Issue 3-4
  • DOI: 10.1016/j.vetmic.2011.06.004

Immune modulation by bacterial outer membrane vesicles
journal, May 2015

  • Kaparakis-Liaskos, Maria; Ferrero, Richard L.
  • Nature Reviews Immunology, Vol. 15, Issue 6
  • DOI: 10.1038/nri3837

Characterization and Comparative Analysis of the Genes Encoding Haemophilus parasuis Outer Membrane Proteins P2 and P5
journal, July 2009

  • Mullins, M. A.; Register, K. B.; Bayles, D. O.
  • Journal of Bacteriology, Vol. 191, Issue 19
  • DOI: 10.1128/jb.00469-09

Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts.
journal, January 1992


A comprehensive proteome map of the Haemophilus parasuis serovar 5
journal, May 2009


Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components
journal, August 2014

  • Pirbadian, S.; Barchinger, S. E.; Leung, K. M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
  • DOI: 10.1073/pnas.1410551111

Intranasal Immunization with Nontypeable Haemophilus influenzae Outer Membrane Vesicles Induces Cross-Protective Immunity in Mice
journal, August 2012


Pathogenicity and Immunity Studies of Haemophilus Parasuis Serotypes
journal, June 1993


Involvement of lipooligosaccharide heptose residues of Haemophilus parasuis SC096 strain in serum resistance, adhesion and invasion
journal, February 2013


Virulence and Draft Genome Sequence Overview of Multiple Strains of the Swine Pathogen Haemophilus parasuis
journal, August 2014


Enterohemorrhagic Escherichia coli Hemolysin Employs Outer Membrane Vesicles to Target Mitochondria and Cause Endothelial and Epithelial Apoptosis
journal, December 2013


Protection of vaccinated pigs against experimental infections with homologous and heterologous Hoemophilus parasuis
journal, October 2002


Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response
journal, April 2012


Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria
journal, July 2014


Outer membrane vesicles alter inflammation and coagulation mediators
journal, November 2014

  • Soult, Michael C.; Dobrydneva, Yuliya; Wahab, Kamal H.
  • Journal of Surgical Research, Vol. 192, Issue 1
  • DOI: 10.1016/j.jss.2014.05.007

Proteomic analysis of Vibrio cholerae outer membrane vesicles
journal, March 2014

  • Altindis, E.; Fu, Y.; Mekalanos, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
  • DOI: 10.1073/pnas.1403683111

Intercellular Nanotubes Mediate Bacterial Communication
journal, February 2011


Comparative proteome analysis of the extracellular proteins of two Haemophilus parasuis strains Nagasaki and SW114
journal, April 2014

  • Wei, Xingliang; Cao, Sanjie; Zhang, Luhua
  • Biochemical and Biophysical Research Communications, Vol. 446, Issue 4
  • DOI: 10.1016/j.bbrc.2014.03.049

Modification of the bicinchoninic acid protein assay to eliminate lipid interference in determining lipoprotein protein content
journal, August 1992


CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation
journal, June 2014


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Characterization of the key antigenic components of pertussis vaccine based on outer membrane vesicles
journal, October 2014


Protein selection and export via outer membrane vesicles
journal, August 2014

  • Bonnington, K. E.; Kuehn, M. J.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 8
  • DOI: 10.1016/j.bbamcr.2013.12.011

Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006

  • Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0606379103

Identification and characterization of novel immunogenic outer membrane proteins of Haemophilus parasuis serovar 5
journal, August 2009


Outer Membrane Vesicles Mediate Transport of Biologically Active Vibrio cholerae Cytolysin (VCC) from V. cholerae Strains
journal, September 2014


Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response
journal, August 2006


Gene Transfer Potential of Outer Membrane Vesicles of Acinetobacter baylyi and Effects of Stress on Vesiculation
journal, March 2014

  • Fulsundar, Shweta; Harms, Klaus; Flaten, Gøril E.
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/aem.04248-13

A basis for vaccine development: Comparative characterization of Haemophilus influenzae outer membrane vesicles
journal, May 2015

  • Roier, Sandro; Blume, Thomas; Klug, Lisa
  • International Journal of Medical Microbiology, Vol. 305, Issue 3
  • DOI: 10.1016/j.ijmm.2014.12.005

Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response
journal, August 2006


Protein selection and export via outer membrane vesicles
journal, August 2014

  • Bonnington, K. E.; Kuehn, M. J.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 8
  • DOI: 10.1016/j.bbamcr.2013.12.011

Trimeric Autotransporters of Haemophilus parasuis: Generation of an Extensive Passenger Domain Repertoire Specific for Pathogenic Strains
journal, November 2008

  • Pina, S.; Olvera, A.; Barcelo, A.
  • Journal of Bacteriology, Vol. 191, Issue 2
  • DOI: 10.1128/jb.00703-08

VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages
journal, January 2012

  • Costa-Hurtado, Mar; Ballester, Maria; Galofré-Milà, Nuria
  • Veterinary Research, Vol. 43, Issue 1
  • DOI: 10.1186/1297-9716-43-57

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli
journal, October 2007


Innate Cytokine Responses in Porcine Macrophage Populations: Evidence for Differential Recognition of Double-Stranded RNA
journal, December 2006


Identification of secreted proteins as novel antigenic vaccine candidates of Haemophilus parasuis serovar 5
journal, March 2015


Effect of Different Vaccine Formulations on the Development of Glässer's Disease Induced in Pigs by Experimental Haemophilus parasuis Infection
journal, February 2009

  • Martín de la Fuente, A. J.; Gutiérrez Martín, C. B.; Pérez Martínez, C.
  • Journal of Comparative Pathology, Vol. 140, Issue 2-3
  • DOI: 10.1016/j.jcpa.2008.10.007

Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles
journal, March 2010

  • Ellis, T. N.; Kuehn, M. J.
  • Microbiology and Molecular Biology Reviews, Vol. 74, Issue 1
  • DOI: 10.1128/mmbr.00031-09

Protection of Piglets by a Haemophilus parasuis Ghost Vaccine against Homologous Challenge
journal, March 2013

  • Hu, Mingming; Zhang, Yanhe; Xie, Fang
  • Clinical and Vaccine Immunology, Vol. 20, Issue 6
  • DOI: 10.1128/cvi.00676-12

Differences in phagocytosis susceptibility in Haemophilus parasuis strains
journal, February 2009

  • Olvera, Alexandre; Ballester, Maria; Nofrarias, Miquel
  • Veterinary Research, Vol. 40, Issue 3
  • DOI: 10.1051/vetres/2009007

Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles
journal, October 2010


Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria
journal, July 2014


Global proteomic profiling of native outer membrane vesicles derived fromEscherichia coli
journal, September 2007


Haemophilus parasuis exhibits IgA protease activity but lacks homologs of the IgA protease genes of Haemophilus influenzae
journal, December 2011

  • Mullins, Michael A.; Register, Karen B.; Bayles, Darrell O.
  • Veterinary Microbiology, Vol. 153, Issue 3-4
  • DOI: 10.1016/j.vetmic.2011.06.004

Immune modulation by bacterial outer membrane vesicles
journal, May 2015

  • Kaparakis-Liaskos, Maria; Ferrero, Richard L.
  • Nature Reviews Immunology, Vol. 15, Issue 6
  • DOI: 10.1038/nri3837

Protection of vaccinated pigs against experimental infections with homologous and heterologous Hoemophilus parasuis
journal, October 2002


CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation
journal, June 2014


Proteomic analysis of Vibrio cholerae outer membrane vesicles
journal, March 2014

  • Altindis, E.; Fu, Y.; Mekalanos, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
  • DOI: 10.1073/pnas.1403683111

Outer Membrane Vesicles Mediate Transport of Biologically Active Vibrio cholerae Cytolysin (VCC) from V. cholerae Strains
journal, September 2014


Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles
journal, October 2010


Differences in phagocytosis susceptibility in Haemophilus parasuis strains
journal, February 2009

  • Olvera, Alexandre; Ballester, Maria; Nofrarias, Miquel
  • Veterinary Research, Vol. 40, Issue 3
  • DOI: 10.1051/vetres/2009007

Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components
journal, August 2014

  • Pirbadian, S.; Barchinger, S. E.; Leung, K. M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
  • DOI: 10.1073/pnas.1410551111

Update on the diagnosis of Haemophilus parasuis infection in pigs and novel genotyping methods
journal, November 2007


Intranasal Immunization with Nontypeable Haemophilus influenzae Outer Membrane Vesicles Induces Cross-Protective Immunity in Mice
journal, August 2012


A comprehensive proteome map of the Haemophilus parasuis serovar 5
journal, May 2009


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response
journal, April 2012


Long-Distance Delivery of Bacterial Virulence Factors by Pseudomonas aeruginosa Outer Membrane Vesicles
journal, April 2009


Purification and renaturation of membrane neuraminidase from Haemophilus parasuis
journal, May 2003


Elicitation of Epithelial Cell-Derived Immune Effectors by Outer Membrane Vesicles of Nontypeable Haemophilus influenzae
journal, August 2011

  • Sharpe, Samantha W.; Kuehn, Meta J.; Mason, Kevin M.
  • Infection and Immunity, Vol. 79, Issue 11
  • DOI: 10.1128/iai.05332-11

Diversion of the host humoral response: a novel virulence mechanism of Haemophilus influenzae mediated via outer membrane vesicles
journal, June 2014

  • Deknuydt, Florence; Nordström, Therése; Riesbeck, Kristian
  • Journal of Leukocyte Biology, Vol. 95, Issue 6
  • DOI: 10.1189/jlb.1013527

Virulence and Draft Genome Sequence Overview of Multiple Strains of the Swine Pathogen Haemophilus parasuis
journal, August 2014


Effect of Different Vaccine Formulations on the Development of Glässer's Disease Induced in Pigs by Experimental Haemophilus parasuis Infection
journal, February 2009

  • Martín de la Fuente, A. J.; Gutiérrez Martín, C. B.; Pérez Martínez, C.
  • Journal of Comparative Pathology, Vol. 140, Issue 2-3
  • DOI: 10.1016/j.jcpa.2008.10.007

Involvement of lipooligosaccharide heptose residues of Haemophilus parasuis SC096 strain in serum resistance, adhesion and invasion
journal, February 2013


Haemophilus parasuis: new trends on diagnosis, epidemiology and control
journal, March 2004


Comparative proteome analysis of the extracellular proteins of two Haemophilus parasuis strains Nagasaki and SW114
journal, April 2014

  • Wei, Xingliang; Cao, Sanjie; Zhang, Luhua
  • Biochemical and Biophysical Research Communications, Vol. 446, Issue 4
  • DOI: 10.1016/j.bbrc.2014.03.049

Coinfection of pigs with porcine respiratory coronavirus and Bordetella bronchiseptica
journal, April 2008


Helicobacter pylori Outer Membrane Vesicles Modulate Proliferation and Interleukin-8 Production by Gastric Epithelial Cells
journal, September 2003


New Type of Outer Membrane Vesicle Produced by the Gram-Negative Bacterium Shewanella vesiculosa M7 T : Implications for DNA Content
journal, January 2013

  • Pérez-Cruz, Carla; Carrión, Ornella; Delgado, Lidia
  • Applied and Environmental Microbiology, Vol. 79, Issue 6
  • DOI: 10.1128/AEM.03657-12

Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006

  • Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0606379103

A Cross-Protection Experiment in Pigs Vaccinated with Haemophilus parasuis Serovars 2 and 5 Bacterins, and Evaluation of a Bivalent Vaccine under Laboratory and Field Conditions.
journal, January 2001

  • Takahashi, Kinya; Nagai, Shinya; Yagihashi, Takeshi
  • Journal of Veterinary Medical Science, Vol. 63, Issue 5
  • DOI: 10.1292/jvms.63.487

Cytokine expression in colostrum-deprived pigs immunized and challenged with Haemophilus parasuis
journal, August 2009

  • Fuente, A. J. Martín de la; Ferri, E. F. Rodríguez; Tejerina, F.
  • Research in Veterinary Science, Vol. 87, Issue 1
  • DOI: 10.1016/j.rvsc.2008.12.012

Haemophilus parasuis: new trends on diagnosis, epidemiology and control
journal, March 2004


Identification of secreted proteins as novel antigenic vaccine candidates of Haemophilus parasuis serovar 5
journal, March 2015


Enterohemorrhagic Escherichia coli Hemolysin Employs Outer Membrane Vesicles to Target Mitochondria and Cause Endothelial and Epithelial Apoptosis
journal, December 2013


Innate Cytokine Responses in Porcine Macrophage Populations: Evidence for Differential Recognition of Double-Stranded RNA
journal, December 2006


Diversion of the host humoral response: a novel virulence mechanism of Haemophilus influenzae mediated via outer membrane vesicles
journal, June 2014

  • Deknuydt, Florence; Nordström, Therése; Riesbeck, Kristian
  • Journal of Leukocyte Biology, Vol. 95, Issue 6
  • DOI: 10.1189/jlb.1013527

A basis for vaccine development: Comparative characterization of Haemophilus influenzae outer membrane vesicles
journal, May 2015

  • Roier, Sandro; Blume, Thomas; Klug, Lisa
  • International Journal of Medical Microbiology, Vol. 305, Issue 3
  • DOI: 10.1016/j.ijmm.2014.12.005

Intercellular Nanotubes Mediate Bacterial Communication
journal, February 2011


VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages
journal, January 2012

  • Costa-Hurtado, Mar; Ballester, Maria; Galofré-Milà, Nuria
  • Veterinary Research, Vol. 43, Issue 1
  • DOI: 10.1186/1297-9716-43-57

Virulence, Transmission, and Heterologous Protection of Four Isolates of Haemophilus parasuis
journal, July 2013

  • Brockmeier, Susan L.; Loving, Crystal L.; Mullins, Michael A.
  • Clinical and Vaccine Immunology, Vol. 20, Issue 9
  • DOI: 10.1128/cvi.00168-13

Production of Outer Membrane Vesicles and Outer Membrane Tubes by Francisella novicida
journal, December 2012

  • McCaig, W. D.; Koller, A.; Thanassi, D. G.
  • Journal of Bacteriology, Vol. 195, Issue 6
  • DOI: 10.1128/jb.02007-12

Works referencing / citing this record:

Bacterial outer membrane vesicles, a potential vaccine candidate in interactions with host cells based
journal, December 2018


The Therapeutic Benefit of Bacterial Membrane Vesicles
journal, June 2017

  • Bitto, Natalie; Kaparakis-Liaskos, Maria
  • International Journal of Molecular Sciences, Vol. 18, Issue 6
  • DOI: 10.3390/ijms18061287

High-throughput proteomics and the fight against pathogens
journal, January 2016

  • Horvatić, Anita; Kuleš, Josipa; Guillemin, Nicolas
  • Molecular BioSystems, Vol. 12, Issue 8
  • DOI: 10.1039/c6mb00223d

Extracellular Membrane Vesicles from Lactobacilli Dampen IFN-γ Responses in a Monocyte-Dependent Manner
journal, November 2019


Extracellular Membrane Vesicles from Lactobacilli Dampen IFN-γ Responses in a Monocyte-Dependent Manner
journal, November 2019


Outer Membrane Vesicles from Neisseria Meningitidis (Proteossome) Used for Nanostructured Zika Virus Vaccine Production
journal, May 2018


Environmentally controlled bacterial vesicle-mediated export: Environmentally controlled bacterial vesicle-mediated export
journal, October 2016

  • Orench-Rivera, Nichole; Kuehn, Meta J.
  • Cellular Microbiology, Vol. 18, Issue 11
  • DOI: 10.1111/cmi.12676

Limited Interactions between Streptococcus Suis and Haemophilus Parasuis in In Vitro Co-Infection Studies
journal, January 2018

  • Mathieu-Denoncourt, Annabelle; Letendre, Corinne; Auger, Jean-Philippe
  • Pathogens, Vol. 7, Issue 1
  • DOI: 10.3390/pathogens7010007

Limited Interactions between Streptococcus Suis and Haemophilus Parasuis in In Vitro Co-Infection Studies
journal, January 2018

  • Mathieu-Denoncourt, Annabelle; Letendre, Corinne; Auger, Jean-Philippe
  • Pathogens, Vol. 7, Issue 1
  • DOI: 10.3390/pathogens7010007

A novel nicotinamide adenine dinucleotide control strategy for increasing the cell density of Haemophilus parasuis
journal, March 2019

  • Cheng, Likun; Li, Feng; Li, Shuguang
  • Biotechnology Progress, Vol. 35, Issue 3
  • DOI: 10.1002/btpr.2794

Outer Membrane Vesicles from Neisseria Meningitidis (Proteossome) Used for Nanostructured Zika Virus Vaccine Production
journal, May 2018


Development of Serotype-Specific PCR Assays for Typing of Haemophilus parasuis Isolates Circulating in Southern China
journal, September 2017

  • Jia, Aiqing; Zhou, Ruyue; Fan, Huiying
  • Journal of Clinical Microbiology, Vol. 55, Issue 11
  • DOI: 10.1128/jcm.00688-17

The Therapeutic Benefit of Bacterial Membrane Vesicles
journal, June 2017

  • Bitto, Natalie; Kaparakis-Liaskos, Maria
  • International Journal of Molecular Sciences, Vol. 18, Issue 6
  • DOI: 10.3390/ijms18061287