Browse > Article
http://dx.doi.org/10.4014/jmb.1705.05028

Outer Membrane Vesicles Derived from Salmonella Enteritidis Protect against the Virulent Wild-Type Strain Infection in a Mouse Model  

Liu, Qiong (Department of Medical Microbiology, School of Medicine, Nanchang University)
Yi, Jie (Institute of Preventive Veterinary Medicine, Sichuan Agricultural University)
Liang, Kang (Institute of Preventive Veterinary Medicine, Sichuan Agricultural University)
Zhang, Xiangmin (Department of Pharmaceutical Sciences, Eugene Applebaum College of Pharmacy/Health Sciences, Wayne State University)
Liu, Qing (College of Animal Science and Technology, Southwest University)
Publication Information
Journal of Microbiology and Biotechnology / v.27, no.8, 2017 , pp. 1519-1528 More about this Journal
Abstract
Foodborne contamination and salmonellosis caused by Salmonella Enteritidis (S. Enteritidis) are a significant threat to human health and poultry enterprises. Outer membrane vesicles (OMVs), which are naturally secreted by gram-negative bacteria, could be a good vaccine option because they have many biologically active substances, including lipopolysaccharides (LPS), outer membrane proteins (OMPs), and phospholipids, as well as periplasmic components. In the present study, we purified OMVs derived from S. Enteritidis and analyzed their characteristics through silver staining and sodium dodecyl sulfate polyacrylamide gel electrophoresis. In total, 108 proteins were identified in S. Enteritidis OMVs through liquid chromatography tandem mass spectrometry analysis, and OMPs, periplasmic proteins, and extracellular proteins (49.9% of total proteins) were found to be enriched in the OMVs compared with bacterial cells. Furthermore, native OMVs used in immunizations by either the intranasal route or the intraperitoneal route could elicit significant humoral and mucosal immune responses and provide strong protective efficiency against a lethal dose (~100-fold $LD_{50}$) of the wild-type S. Enteritidis infection. These results indicated that S. Enteritidis OMVs might be an ideal vaccine strategy for preventing S. Enteritidis diseases.
Keywords
Outer membrane vesicles; Salmonella Enteritidis; protection;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Guard-Petter J. 2001. The chicken, the egg and Salmonella enteritidis. Environ. Microbiol. 3: 421-430.   DOI
2 Chai S J, W hite P L, Lathrop S L, S olghan SM, Medu s C, McGlinchey BM, et al. 2012. Salmonella enterica serotype Enteritidis: increasing incidence of domestically acquired infections. Clin. Infect. Dis. 54: S488-S497.   DOI
3 Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, et al. 2010. Food-borne diseases-the challenges of 20 years ago still persist while new ones continue to emerge. Int. J. Food Microbiol. 139: S3-S15.   DOI
4 Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50: 882-889.   DOI
5 Van Immerseel F, De Buck J, Pasmans F, Bohez L, Boyen F, Haesebrouck F, et al. 2004. Intermittent long-term shedding and induction of carrier birds after infection of chickens early posthatch with a low or high dose of Salmonella Enteritidis. Poult. Sci. 83: 1911-1916.   DOI
6 Seo KH, Holt PS, Gast RK, Hofacre CL. 2000. Combined effect of antibiotic and competitive exclusion treatment on Salmonella Enteritidis fecal shedding in molted laying hens. J. Food Protect. 63: 545-548.   DOI
7 Molbak K, Gerner-Smidt P, Wegener HC. 2002. Increasing quinolone resistance in Salmonella enterica serotype Enteritidis. Emerg. Infect. Dis. 8: 514-515.   DOI
8 Threlfall EJ. 2002. Antimicrobial drug resistance in Salmonella: problems and perspectives in food-and waterborne infections. FEMS Microbiol. Rev. 26: 141-148.   DOI
9 Mastroeni P, Chabalgoity J, Dunstan S, Maskell D, Dougan G. 2001. Salmonella: immune responses and vaccines. Vet. J. 161: 132-164.   DOI
10 Toyota-Hanatani Y, Kyoumoto Y, Baba E, Ekawa T, Ohta H, Tani H, et al. 2009. Importance of subunit vaccine antigen of major Fli C antigenic site of Salmonella Enteritidis II: a challenge trial. Vaccine 27: 1680-1684.   DOI
11 Hormaeche CE, Mastroeni P, Harrison JA, de Hormaeche RD, Svenson S, Stocker BA. 1996. Protection against oral challenge three months after i.v. immunization of BALBc mice with live Aro Salmonella typhimurium and Salmonella enteritidis vaccines is serotype (species)-dependent and only partially determined by the main LPS O antigen. Vaccine 14: 251-259.   DOI
12 Kulkarni HM, Jagannadham MV. 2014. Biogenesis and multifaceted roles of outer membrane vesicles from gramnegative bacteria. Microbiology 160: 2109-2121.   DOI
13 Beveridge TJ. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181: 4725-4733.
14 Okamura M, Lillehoj HS, Raybourne RB, Babu U, Heckert R. 2003. Antigen-specific lymphocyte proliferation and interleukin production in chickens immunized with killed Salmonella enteritidis vaccine or experimental subunit vaccines. Avian Dis. 47: 1331-1338.   DOI
15 Bonnington KE, Kuehn MJ. 2014. Protein selection and export via outer membrane vesicles. Biochim. Biophys. Acta 1843: 1612-1619.   DOI
16 Deatherage BL, Cookson BT. 2012. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 80: 1948-1957.   DOI
17 Ellis TN, Kuehn MJ. 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74: 81-94.   DOI
18 De Cort W, Geeraerts S, Balan V, Elroy M, Haesebrouck F, Ducatelle R, et al. 2013. A Salmonella Enteritidis hilAssrAfliG deletion mutant is a safe live vaccine strain that confers protection against colonization by Salmonella Enteritidis in broilers. Vaccine 31: 5104-5110.   DOI
19 Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. 2012. Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379: 2489-2499.   DOI
20 Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262-265.   DOI
21 Wang S, Duan H, Zhang W, Li JW. 2007. Analysis of bacterial foodborne disease outbreaks in China between 1994 and 2005. FEMS Immunol. Med. Microbiol. 51: 8-13.   DOI
22 Taylor M, Leslie M, Ritson M, Stone J, Cox W, Hoang L, et al. 2012. Investigation of the concurrent emergence of Salmonella Enteritidis in humans and poultry in British Columbia, Canada, 2008-2010. Zoonoses Public Health 59: 584-592.   DOI
23 Jawad AA, Al-Charrakh AH. 2016. Outer membrane protein C (ompC) gene as the target for diagnosis of Salmonella species isolated from human and animal sources. Avicenna J. Med. Biotechnol. 8: 42-45.
24 Cho Y, Park S, Barate AK, Truong QL, Han JH, Jung C-H, et al. 2015. Proteomic analysis of outer membrane proteins in Salmonella enterica Enteritidis. J. Microbiol. Biotechnol. 25: 288-295.   DOI
25 Bjerre A, Brusletto B, Mollnes TE, Fritzsonn E, Rosenqvist E, Wedege E, et al. 2002. Complement activation induced by purified Neisseria meningitidis lipopolysaccharide (LPS), outer membrane vesicles, whole bacteria, and an LPS-free mutant. J. Infect. Dis. 185: 220-228.   DOI
26 Elhenawy W, Debelyy MO, Feldman MF. 2014. Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio 5: e00909-00914.
27 Koeberling O, Seubert A, Granoff DM. 2008. Bactericidal antibody responses elicited by a meningococcal outer membrane vesicle vaccine with overexpressed factor Hbinding protein and genetically attenuated endotoxin. J. Infect. Dis. 198: 262-270.   DOI
28 Kong Q, Yang J, Liu Q, Alamuri P, Roland KL, Curtiss R. 2011. Effect of deletion of genes involved in lipopolysaccharide core and O-antigen synthesis on virulence and immunogenicity of Salmonella enterica serovar Typhimurium. Infect. Immun. 79: 4227-4239.   DOI
29 Bomberger JM, MacEachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA. 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5: e1000382.   DOI
30 Yonezawa H, Osaki T, Woo T, Kurata S, Zaman C, Hojo F, et al. 2011. Analysis of outer membrane vesicle protein involved in biofilm formation of Helicobacter pylori. Anaerobe 17: 388-390.   DOI
31 Collins BS. 2011. Gram-negative outer membrane vesicles in vaccine development. Discov. Med. 12: 7-15.
32 McConnell MJ, Rumbo C, Bou G, Pachon J. 2011. Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine 29: 5705-5710.   DOI
33 Petersen H, Nieves W, Russell-Lodrigue K, Roy CJ, Morici LA. 2014. Evaluation of a Burkholderia pseudomallei outer membrane vesicle vaccine in nonhuman primates. Procedia Vaccinol. 8: 38-42.   DOI
34 Acevedo R, Fernandez S, Zayas C, Acosta A, Sarmiento ME, Ferro VA, et al. 2014. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol. 5: 121.
35 Liu Q, Liu Q, Zhao X, Liu T, Yi J, Liang K, et al. 2016. Immunogenicity and cross-protective efficacy induced by outer membrane proteins from Salmonella Typhimurium mutants with truncated LPS in mice. Int. J. Mol. Sci. 17: 416.   DOI
36 Liu Q, Liu Q, Jie Y, Kang L, Bo H, Zhang X, et al. 2016. Outer membrane vesicles from flagellin-deficient Salmonella enterica serovar Typhimurium induce cross-reactive immunity and provide cross-protection against heterologous Salmonella challenge. Sci. Rep. 6: 34776.   DOI
37 MacLennan CA, Martin LB, Micoli F. 2014. Vaccines against invasive Salmonella disease: current status and future directions. Hum. Vaccin. Immunother. 10: 1478-1493.   DOI
38 Durand D, Ochoa TJ, Bellomo SM, Contreras CA, Bustamante VH, Ruiz J, Cleary TG. 2013. Detection of secretory immunoglobulin A in human colostrum as mucosal immune response against proteins of the type three secretion system of Salmonella, Shigella and Enteropathogenic Escherichia coli. Pediatr. Infect. Dis. J. 32: 1122-1126.   DOI
39 Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19: 2645-2655.   DOI
40 Collins F. 1969. Effect of specific immune mouse serum on the growth of Salmonella enteritidis in nonvaccinated mice challenged by various routes. J. Bacteriol. 97: 667-675.
41 Kuipers K, Daleke-Schermerhorn MH, Jong WSP, Hagen-Jongman CMT, Opzeeland FV, Simonetti E, et al. 2015. Salmonella outer membrane vesicles displaying high densities of pneumococcal antigen at the surface offer protection against colonization. Vaccine 33: 2022-2029.   DOI
42 Ernst RK, Guina T, Miller SI. 2001. Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microb. Infect. 3: 1327-1334.   DOI
43 McGhee JR, Mestecky J, Dertzbaugh MT, Eldridge JH, Hirasawa M, Kiyono H. 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10: 75-88.   DOI
44 de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, et al. 2008. Comprehensive mass-spectrometrybased proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254.   DOI
45 Kraehenbuhl J-P, Neutra MR. 1992. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 72: 853-879.   DOI
46 Quakyi EK, Frasch CE, Buller N, Tsai CM. 1999. Immunization with meningococcal outer-membrane protein vesicles containing lipooligosaccharide protects mice against lethal experimental group B Neisseria meningitidis infection and septic shock. J. Infect. Dis. 180: 747-754.   DOI
47 Desmidt M, Ducatelle R, Haesebrouck F. 1997. Pathogenesis of Salmonella Enteritidis phage type four after experimental infection of young chickens. Vet. Microbiol. 56: 99-109.   DOI
48 Hitchcock P, Brown T. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silverstained polyacrylamide gels. J. Bacteriol. 154: 269-277.
49 Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.   DOI
50 Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, et al. 2009. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4: 698-705.   DOI
51 Lee EY, Choi DS, Kim KP, Gho YS. 2008. Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 27: 535-555.   DOI
52 Choi DS, Kim DK, Choi SJ, Lee J, Choi JP, Rho S, et al. 2011. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 11: 3424-3429.   DOI
53 Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ, et al. 2007. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7: 3143-3153.   DOI
54 Lee J, Kim OY, Gho YS. 2016. Proteomic profiling of gramnegative bacterial outer membrane vesicles: current perspectives. Proteomics Clin. Appl. 10: 897-909.   DOI
55 Wurpel DJ, Moriel DG, Totsika M, Easton DM, Schembri MA. 2015. Comparative analysis of the uropathogenic Escherichia coli surface proteome by tandem mass-spectrometry of artificially induced outer membrane vesicles. J. Proteomics 115: 93-106.   DOI
56 Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29.   DOI