Articles Service
Share this article on :
Metrics
Review
Food Microbiology and Biotechnology (FMB) | Food Biotechnology
Bacterial Outer Membrane Vesicles as a Delivery System for Virulence Regulation
Department of Molecular Science and Technology, Department of Applied Chemistry and Biological Engineering, Ajou University, Suwon 16499, Republic of Korea
Received: April 29, 2016; Accepted: May 23, 2016
J. Microbiol. Biotechnol. 2016; 26(8): 1343-1347
Published August 28, 2016 https://doi.org/10.4014/jmb.1604.04080
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Outer membrane vesicles (OMVs) are spherical nanostructures that are ubiquitously shed
from gram-negative bacteria both in vitro and in vivo. Recent findings revealed that OMVs,
which contain diverse components derived from the parent bacterium, play an important role
in communication with neighboring bacteria and the environment. Furthermore, nanoscale
proteoliposomes decorated with pathogen-associated molecules attract considerable attention
as a non-replicative carrier for vaccines and drug materials. This review introduces recent
advances in OMV biogenesis and discusses the roles of OMVs in the context of bacterial
communication and virulence regulation. It also describes the remarkable accomplishments in
OMV engineering for diverse therapeutic applications.
Keywords
Outer membrane vesicle, Virulence, Pathogen, Biogenesis
References
- Alaniz RC, Deatherage BL, Lara JC, Cookson BT. 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. J. Immunol. 179: 7692-7701.
- Bai J, Kim SI, Ryu S, Yoon H. 2014. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect. Immun. 82: 4001-4010.
- Collins BS. 2011. Gram-negative outer membrane vesicles in vaccine development. Discov. Med. 12: 7-15.
- Duperthuy M, Sjostrom AE, Sabharwal D, Damghani F, Uhlin BE, Wai SN. 2013. Role of the Vibrio cholerae matrix protein Bap1 in cross-resistance to antimicrobial peptides. PLoS Pathog. 9: e1003620.
- Evans AG, Davey HM, Cookson A, Currinn H, Cooke-Fox G, Stanczyk PJ, Whitworth DE. 2012. Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology 158: 2742-2752.
- Fulsundar S, Harms K, Flaten GE, Johnsen PJ, Chopade BA, Nielsen KM. 2014. Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl. Environ. Microbiol. 80: 3469-3483.
- Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, et al. 2008. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect. Immun. 76: 1825-1836.
- Imayoshi R, Cho T, Kaminishi H. 2011. NO production in RAW264 cells stimulated with Porphyromonas gingivalis extracellular vesicles. Oral Dis. 17: 83-89.
- Jose J, Meyer TF. 2007. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol. Mol. Biol. Rev. 71: 600-619.
- Kesty NC, Kuehn MJ. 2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279: 2069-2076.
- Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23: 4538-4549.
- Kim JY, Doody AM, Chen DJ, Cremona GH, Shuler ML, Putnam D, DeLisa MP. 2008. Engineered bacterial outer membrane vesicles with enhanced functionality. J. Mol. Biol. 380: 51-66.
- Mashburn-Warren LM, Whiteley M. 2006. Special delivery:vesicle trafficking in prokaryotes. Mol. Microbiol. 61: 839-846.
- Prados-Rosales R, Weinrick BC, Pique DG, Jacobs WR Jr, Casadevall A, Rodriguez GM. 2014. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J. Bacteriol. 196: 1250-1256.
- Rakoff-Nahoum S, Coyne MJ, Comstock LE. 2014. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24: 40-49.
- Schaar V, Nordstrom T, Morgelin M, Riesbeck K. 2011. Moraxella catarrhalis outer membrane vesicles carry betalactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin. Antimicrob. Agents Chemother. 55: 3845-3853.
- Schaar V, Uddback I, Nordstrom T, Riesbeck K. 2014. Group A streptococci are protected from amoxicillin-mediated killing by vesicles containing beta-lactamase derived from Haemophilus influenzae. J. Antimicrob. Chemother. 69: 117-120.
- Schertzer JW, Whiteley M. 2012. A bilayer-couple model of bacterial outer membrane vesicle biogenesis. MBio 3.
- Schroeder J, Aebischer T. 2009. Recombinant outer membrane vesicles to augment antigen-specific live vaccine responses. Vaccine 27: 6748-6754.
- Schwechheimer C, Kulp A, Kuehn MJ. 2014. Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol. 14: 324.
- Schwechheimer C, Rodriguez DL, Kuehn MJ. 2015. NlpImediated modulation of outer membrane vesicle production through peptidoglycan dynamics in Escherichia coli. Microbiologyopen 4: 375-389.
- Schwechheimer C, Sullivan CJ, Kuehn MJ. 2013. Envelope control of outer membrane vesicle production in gramnegative bacteria. Biochemistry 52: 3031-3040.
- Sharpe SW, Kuehn MJ, Mason KM. 2011. Elicitation of epithelial cell-derived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect. Immun. 79: 4361-4369.
- Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK. 2012. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12: 509-520.
- Soderblom T, Oxhamre C, Wai SN, Uhlen P, Aperia A, Uhlin BE, Richter-Dahlfors A. 2005. Effects of the Escherichia coli toxin cytolysin A on mucosal immunostimulation via epithelial Ca2+ signalling and Toll-like receptor 4. Cell Microbiol. 7: 779-788.
- Stentz R, Horn N, Cross K, Salt L, Brearley C, Livermore DM, Carding SR. 2015. Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against beta-lactam antibiotics. J. Antimicrob. Chemother. 70: 701-709.
- Tran AX, Karbarz MJ, Wang X, Raetz CR, McGrath SC, Cotter RJ, Trent MS. 2004. Periplasmic cleavage and modification of the 1-phosphate group of Helicobacter pylori lipid A. J. Biol. Chem. 279: 55780-55791.
- van der Ley P, Steeghs L, Hamstra HJ, ten Hove J, Zomer B, van Alphen L. 2001. Modification of lipid A biosynthesis in Neisseria meningitidis lpxL mutants: influence on lipopolysaccharide structure, toxicity, and adjuvant activity. Infect. Immun. 69: 5981-5990.
- Velimirov B, Hagemann S. 2011. Mobilizable bacterial DNA packaged into membrane vesicles induces serial transduction. Mob. Genet. Elements 1: 80-81.
- Vidakovics ML, Jendholm J, Morgelin M, Mansson A, Larsson C, Cardell LO, Riesbeck K. 2010. B cell activation by outer membrane vesicles - a novel virulence mechanism. PLoS Pathog. 6: e1000724.
- Winter J, Letley D, Rhead J, Atherton J, Robinson K. 2014. Helicobacter pylori membrane vesicles stimulate innate proand anti-inflammatory responses and induce apoptosis in Jurkat T cells. Infect. Immun. 82: 1372-1381.
- Yaron S, Kolling GL, Simon L, Matthews KR. 2000. Vesiclemediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl. Environ. Microbiol. 66: 4414-4420.
- Yoon H, Ansong C, Adkins JN, Heffron F. 2011. Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages. Infect. Immun. 79: 2182-2192.
- Zhao K, Deng X, He C, Yue B, Wu M. 2013. Pseudomonas aeruginosa outer membrane vesicles modulate host immune responses by targeting the Toll-like receptor 4 signaling pathway. Infect. Immun. 81: 4509-4518.
Related articles in JMB
-
Research article | 2016-01-28Comparative Genomic Analysis Reveals That the 20K and 38K Prophages in Listeria monocytogenes Serovar 4a Strains Lm850658 and M7 Contribute to Genetic Diversity but Not to Virulence
Chun Fang , Tong Cao , Ying Shan , Ye Xia , Yongping Xin , Changyong Cheng , Houhui Song , John Bowman , Xiaoliang Li , Xiangyang Zhou and Weihuan Fang -
Research article | 2014-11-28
Correlation between pr1 and pr2 Gene Content and Virulence in Metarhizium anisopliae Strains
Ninfa M. Rosas-García , Osvaldo Ávalos-de-León , Jesús M. Villegas-Mendoza , Maribel Mireles-Martínez , J. E. Barboza-Corona and J. C. Castañeda-Ramírez -
| 2009-10-28
Multi-Immunogenic Outer Membrane Vesicles Derived from an MsbBDeficient Salmonella enterica Serovar Typhimurium Mutant
Sang-Rae Lee , Sang-Hyun Kim , Kang-Jin Jeong , Keun-Su Kim , Young-Hyun Kim , Sung-Jin Kim , Ekyune Kim , Jung-Woo Kim and Kyu-Tae Chang
PDF
Standard view
Export citation
Share Article
Review
J. Microbiol. Biotechnol. 2016; 26(8): 1343-1347
Published online August 28, 2016 https://doi.org/10.4014/jmb.1604.04080
Copyright © The Korean Society for Microbiology and Biotechnology.
Bacterial Outer Membrane Vesicles as a Delivery System for Virulence Regulation
Hyunjin Yoon 1*
Department of Molecular Science and Technology, Department of Applied Chemistry and Biological Engineering, Ajou University, Suwon 16499, Republic of Korea
Received: April 29, 2016; Accepted: May 23, 2016
Abstract
Outer membrane vesicles (OMVs) are spherical nanostructures that are ubiquitously shed
from gram-negative bacteria both in vitro and in vivo. Recent findings revealed that OMVs,
which contain diverse components derived from the parent bacterium, play an important role
in communication with neighboring bacteria and the environment. Furthermore, nanoscale
proteoliposomes decorated with pathogen-associated molecules attract considerable attention
as a non-replicative carrier for vaccines and drug materials. This review introduces recent
advances in OMV biogenesis and discusses the roles of OMVs in the context of bacterial
communication and virulence regulation. It also describes the remarkable accomplishments in
OMV engineering for diverse therapeutic applications.
Keywords: Outer membrane vesicle, Virulence, Pathogen, Biogenesis
References
- Alaniz RC, Deatherage BL, Lara JC, Cookson BT. 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. J. Immunol. 179: 7692-7701.
- Bai J, Kim SI, Ryu S, Yoon H. 2014. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect. Immun. 82: 4001-4010.
- Collins BS. 2011. Gram-negative outer membrane vesicles in vaccine development. Discov. Med. 12: 7-15.
- Duperthuy M, Sjostrom AE, Sabharwal D, Damghani F, Uhlin BE, Wai SN. 2013. Role of the Vibrio cholerae matrix protein Bap1 in cross-resistance to antimicrobial peptides. PLoS Pathog. 9: e1003620.
- Evans AG, Davey HM, Cookson A, Currinn H, Cooke-Fox G, Stanczyk PJ, Whitworth DE. 2012. Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology 158: 2742-2752.
- Fulsundar S, Harms K, Flaten GE, Johnsen PJ, Chopade BA, Nielsen KM. 2014. Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl. Environ. Microbiol. 80: 3469-3483.
- Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, et al. 2008. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect. Immun. 76: 1825-1836.
- Imayoshi R, Cho T, Kaminishi H. 2011. NO production in RAW264 cells stimulated with Porphyromonas gingivalis extracellular vesicles. Oral Dis. 17: 83-89.
- Jose J, Meyer TF. 2007. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol. Mol. Biol. Rev. 71: 600-619.
- Kesty NC, Kuehn MJ. 2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279: 2069-2076.
- Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23: 4538-4549.
- Kim JY, Doody AM, Chen DJ, Cremona GH, Shuler ML, Putnam D, DeLisa MP. 2008. Engineered bacterial outer membrane vesicles with enhanced functionality. J. Mol. Biol. 380: 51-66.
- Mashburn-Warren LM, Whiteley M. 2006. Special delivery:vesicle trafficking in prokaryotes. Mol. Microbiol. 61: 839-846.
- Prados-Rosales R, Weinrick BC, Pique DG, Jacobs WR Jr, Casadevall A, Rodriguez GM. 2014. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J. Bacteriol. 196: 1250-1256.
- Rakoff-Nahoum S, Coyne MJ, Comstock LE. 2014. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24: 40-49.
- Schaar V, Nordstrom T, Morgelin M, Riesbeck K. 2011. Moraxella catarrhalis outer membrane vesicles carry betalactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin. Antimicrob. Agents Chemother. 55: 3845-3853.
- Schaar V, Uddback I, Nordstrom T, Riesbeck K. 2014. Group A streptococci are protected from amoxicillin-mediated killing by vesicles containing beta-lactamase derived from Haemophilus influenzae. J. Antimicrob. Chemother. 69: 117-120.
- Schertzer JW, Whiteley M. 2012. A bilayer-couple model of bacterial outer membrane vesicle biogenesis. MBio 3.
- Schroeder J, Aebischer T. 2009. Recombinant outer membrane vesicles to augment antigen-specific live vaccine responses. Vaccine 27: 6748-6754.
- Schwechheimer C, Kulp A, Kuehn MJ. 2014. Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol. 14: 324.
- Schwechheimer C, Rodriguez DL, Kuehn MJ. 2015. NlpImediated modulation of outer membrane vesicle production through peptidoglycan dynamics in Escherichia coli. Microbiologyopen 4: 375-389.
- Schwechheimer C, Sullivan CJ, Kuehn MJ. 2013. Envelope control of outer membrane vesicle production in gramnegative bacteria. Biochemistry 52: 3031-3040.
- Sharpe SW, Kuehn MJ, Mason KM. 2011. Elicitation of epithelial cell-derived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect. Immun. 79: 4361-4369.
- Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK. 2012. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12: 509-520.
- Soderblom T, Oxhamre C, Wai SN, Uhlen P, Aperia A, Uhlin BE, Richter-Dahlfors A. 2005. Effects of the Escherichia coli toxin cytolysin A on mucosal immunostimulation via epithelial Ca2+ signalling and Toll-like receptor 4. Cell Microbiol. 7: 779-788.
- Stentz R, Horn N, Cross K, Salt L, Brearley C, Livermore DM, Carding SR. 2015. Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against beta-lactam antibiotics. J. Antimicrob. Chemother. 70: 701-709.
- Tran AX, Karbarz MJ, Wang X, Raetz CR, McGrath SC, Cotter RJ, Trent MS. 2004. Periplasmic cleavage and modification of the 1-phosphate group of Helicobacter pylori lipid A. J. Biol. Chem. 279: 55780-55791.
- van der Ley P, Steeghs L, Hamstra HJ, ten Hove J, Zomer B, van Alphen L. 2001. Modification of lipid A biosynthesis in Neisseria meningitidis lpxL mutants: influence on lipopolysaccharide structure, toxicity, and adjuvant activity. Infect. Immun. 69: 5981-5990.
- Velimirov B, Hagemann S. 2011. Mobilizable bacterial DNA packaged into membrane vesicles induces serial transduction. Mob. Genet. Elements 1: 80-81.
- Vidakovics ML, Jendholm J, Morgelin M, Mansson A, Larsson C, Cardell LO, Riesbeck K. 2010. B cell activation by outer membrane vesicles - a novel virulence mechanism. PLoS Pathog. 6: e1000724.
- Winter J, Letley D, Rhead J, Atherton J, Robinson K. 2014. Helicobacter pylori membrane vesicles stimulate innate proand anti-inflammatory responses and induce apoptosis in Jurkat T cells. Infect. Immun. 82: 1372-1381.
- Yaron S, Kolling GL, Simon L, Matthews KR. 2000. Vesiclemediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl. Environ. Microbiol. 66: 4414-4420.
- Yoon H, Ansong C, Adkins JN, Heffron F. 2011. Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages. Infect. Immun. 79: 2182-2192.
- Zhao K, Deng X, He C, Yue B, Wu M. 2013. Pseudomonas aeruginosa outer membrane vesicles modulate host immune responses by targeting the Toll-like receptor 4 signaling pathway. Infect. Immun. 81: 4509-4518.
