Meningococcal outer membrane vesicle composition-dependent activation of the innate immune response

Infection and Immunity

Volumn 84, Issue 10, 2016, Pages 3024-3033

  Zariri, Afshin ^a,b   Beskers, Joep ^c   van de Waterbeemd, Bas ^a,d   Hamstra, Hendrik Jan ^c   Bindels, Tim H E ^a   van Riet, Elly ^a   van Putten, Jos P M ^b   van der Ley, Peter ^a  

^a Institute for Translational Vaccinology   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^d Janssen Research and Development   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; COMPLEMENT FACTOR H; DETERGENT; EDETIC ACID; FACTOR H BINDING PROTEIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; LIPID A DERIVATIVE; LIPOPROTEIN; PORB PROTEIN; PROGRAMMED DEATH 1 LIGAND 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; CYTOKINE; LIPID A; OUTER MEMBRANE PROTEIN; TOLL LIKE RECEPTOR;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEACYLATION; DENDRITIC CELL; DNA MODIFICATION; GENE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; INNATE IMMUNITY; LPXL1 GENE; MEMBRANE VESICLE; MUTATION; NEISSERIA MENINGITIDIS; NONHUMAN; OUTER MEMBRANE; PAGL GENE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; CHEMISTRY; DRUG EFFECTS; IMMUNOLOGY; MENINGOCOCCOSIS; METABOLISM; MONOCYTE; PHYSIOLOGY;

BACTERIAL OUTER MEMBRANE PROTEINS; CYTOKINES; DENDRITIC CELLS; DETERGENTS; EDETIC ACID; HUMANS; IMMUNITY, INNATE; LIPID A; MENINGOCOCCAL INFECTIONS; MONOCYTES; NEISSERIA MENINGITIDIS; TOLL-LIKE RECEPTORS;

EID: 84994229450     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00635-16     Document Type: Article

References (36)

1. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. 2006. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188:5385-5392. http://dx.doi.org/10.1128/JB.00498-06.
2. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63:545-558. http://dx.doi.org/10.1111/j.1365-2958.2006.05522.x.
3. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163-184. http://dx.doi.org/10.1146/annurev.micro.091208.073413.
4. Bjune G, Hoiby EA, Gronnesby JK, Arnesen O, Fredriksen JH, Halstensen A, Holten E, Lindbak AK, Nokleby H, Rosenqvist E, Solberg LK, Closs O, Froholm LO, Lystrad A, Bakketeig LS, Hareide B, Halstensen A, Holten E. 1991. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 338:1093-1096. http://dx.doi.org/10.1016/0140-6736(91)91961-S.
5. Sierra GV, Campa HC, Varcacel NM, Garcia IL, Izquierdo PL, Sotolongo PF, Casanueva GV, Rico CO, Rodriguez CR, Terry MH. 1991 Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann 14:195-207. (Discussion, 14:208-110.)
6. Thornton V, Lennon D, Rasanathan K, O'Hallahan J, Oster P, Stewart J, Tilman S, Aaberge I, Feiring B, Nokleby H, Rosenqvist E, White K, Reid S, Mulholland K, Wakefield MJ, Martin D. 2006. Safety and immunogenicity of New Zealand strain meningococcal serogroup BOMV vaccine in healthy adults: beginning of epidemic control. Vaccine 24: 1395-1400. http://dx.doi.org/10.1016/j.vaccine.2005.09.043.
7. Leitner DR, Feichter S, Schild-Prufert K, Rechberger GN, Reidl J, Schild S. 2013. Lipopolysaccharide modifications of a cholera vaccine candidate based on outer membrane vesicles reduce endotoxicity and reveal the major protective antigen. Infect Immun 81:2379-2393. http://dx.doi.org/10.1128/IAI.01382-12.
8. Rossi O, Pesce I, Giannelli C, Aprea S, Caboni M, Citiulo F, Valentini S, Ferlenghi I, MacLennan CA, D'Oro U, Saul A, Gerke C. 2014. Modulation of endotoxicity of Shigella generalized modules for membrane antigens (GMMA) by genetic lipid A modifications: relative activation of TLR4 and TLR2 pathways in different mutants. J Biol Chem 289: 24922-24935. http://dx.doi.org/10.1074/jbc. M114.566570.
9. van de Waterbeemd B, Mommen GP, Pennings JL, Eppink MH, Wijffels RH, van der Pol LA, de Jong AP. 2013. Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines. J Proteome Res 12:1898-1908. http://dx.doi.org/10.1021/pr301208g.
10. Koeberling O, Seubert A, GranoffDM. 2008. Bactericidal antibody responses elicited by a meningococcal outer membrane vesicle vaccine with overexpressed factor H-binding protein and genetically attenuated endotoxin. J Infect Dis 198:262-270. http://dx.doi.org/10.1086/589308.
11. van de Waterbeemd B, Zomer G, Kaaijk P, Ruiterkamp N, Wijffels RH, van den Dobbelsteen GP, van der Pol LA. 2013. Improved production process for native outer membrane vesicle vaccine against Neisseria meningitidis. PLoS One 8:e65157. http://dx.doi.org/10.1371/journal.pone.0065157.
12. van de Waterbeemd B, Streefland M, van der Ley P, Zomer B, van Dijken H, Martens D, Wijffels R, van der Pol L. 2010. Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine 28:4810-4816. http://dx.doi.org/10.1016/j.vaccine.2010.04.082.
13. 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. http://dx.doi.org/10.1128/IAI.69.10.5981-5990.2001.
14. Geurtsen J, Steeghs L, Hamstra HJ, Ten Hove J, de Haan A, Kuipers B, Tommassen J, van der Ley P. 2006. Expression of the lipopolysaccharidemodifying enzymes PagP and PagL modulates the endotoxic activity of Bordetella pertussis. Infect Immun 74:5574-5585. http://dx.doi.org/10.1128/IAI.00834-06.
15. Geurtsen J, Steeghs L, Hove JT, van der Ley P, Tommassen J. 2005. Dissemination of lipidAdeacylases (pagL) among gram-negative bacteria: identification of active-site histidine and serine residues. J Biol Chem 280: 8248-8259. http://dx.doi.org/10.1074/jbc. M414235200.
16. Pupo E, Hamstra HJ, Meiring H, van der Ley P. 2014. Lipopolysaccharide engineering in Neisseria meningitidis: structural analysis of different pentaacyl lipid A mutants and comparison of their modified agonist properties. J Biol Chem 289:8668-8680. http://dx.doi.org/10.1074/jbc. M114.554345.
17. Holten E. 1979. Serotypes of Neisseria meningitidis isolated from patients in Norway during the first six months of 1978. J Clin Microbiol 9:186-188.
18. van der Ley P, van der Biezen J, Poolman JT. 1995. Construction of Neisseria meningitidis strains carrying multiple chromosomal copies of the porA gene for use in the production of a multivalent outer membrane vesicle vaccine. Vaccine 13:401-407. http://dx.doi.org/10.1016/0264-410X(95)98264-B.
19. Tommassen J, Vermeij P, Struyve M, Benz R, Poolman JT. 1990. Isolation of Neisseria meningitidis mutants deficient in class 1 (porA) and class 3 (porB) outer membrane proteins. Infect Immun 58:1355-1359.
20. Claassen I, Meylis J, van der Ley P, Peeters C, Brons H, Robert J, Borsboom D, van der Ark A, van Straaten I, Roholl P, Kuipers B, Poolman J. 1996. Production, characterization and control of a Neisseria meningitidis hexavalent class 1 outer membrane protein containing vesicle vaccine. Vaccine 14:1001-1008. http://dx.doi.org/10.1016/0264-410X(96)00020-5.
21. Zollinger WD, Mandrell RE, Griffiss JM, Altieri P, Berman S. 1979. Complex of meningococcal group B polysaccharide and type 2 outer membrane protein immunogenic in man. J Clin Invest 63:836-848. http://dx.doi.org/10.1172/JCI109383.
22. Dixon GL, Newton PJ, Chain BM, Katz D, Andersen SR, Wong S, van der Ley P, Klein N, Callard RE. 2001. Dendritic cell activation and cytokine production induced by group B Neisseria meningitidis: interleukin-12 production depends on lipopolysaccharide expression in intact bacteria. Infect Immun 69:4351-4357. http://dx.doi.org/10.1128/IAI.69.7.4351-4357.2001.
23. Sallusto F, Lanzavecchia A. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179:1109-1118. http://.dx.doi.org/10.1084/jem.179.4.1109.
24. Masignani V, Comanducci M, Giuliani MM, Bambini S, Adu-Bobie J, Arico B, Brunelli B, Pieri A, Santini L, Savino S, Serruto D, Litt D, Kroll S, Welsch JA, GranoffDM, Rappuoli R, Pizza M. 2003. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med 197:789-799. http://dx.doi.org/10.1084/jem.20021911.
25. Welsch JA, Rossi R, Comanducci M, GranoffDM. 2004. Protective activity of monoclonal antibodies to genome-derived neisserial antigen 1870, a Neisseria meningitidis candidate vaccine. J Immunol 172:5606-5615 http://dx.doi.org/10.4049/jimmunol.172.9.5606.
26. Massari P, Visintin A, Gunawardana J, Halmen KA, King CA, Golenbock DT, Wetzler LM. 2006. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J Immunol 176:2373-2380. http://dx.doi.org/10.4049/jimmunol.176.4.2373.
27. Singleton TE, Massari P, Wetzler LM. 2005. Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J Immunol 174: 3545-3550. http://dx.doi.org/10.4049/jimmunol.174.6.3545.
28. Perrett KP, McVernon J, Richmond PC, Marshall H, Nissen M, August A, Percell S, Toneatto D, Nolan T. 2015. Immune responses to a recombinant, four-component, meningococcal serogroup B vaccine (4CMenB) in adolescents: a phase III, randomized, multicentre, lot-to-lot consistency study. Vaccine http://dx.doi.org/10.1016/j.vaccine.2015.06.103.
29. Keiser PB, Biggs-Cicatelli S, Moran EE, Schmiel DH, Pinto VB, Burden RE, Miller LB, Moon JE, Bowden RA, Cummings JF, Zollinger WD. 2011. A phase 1 study of a meningococcal native outer membrane vesicle vaccine made from a group B strain with deleted lpxL1 and synX, over-expressed factor H binding protein, two PorAs and stabilized OpcA expression. Vaccine 29:1413-1420. http://dx.doi.org/10.1016/j.vaccine.2010.12.039.
30. van der Ley P, van den Dobbelsteen G. 2011. Next-generation outer membrane vesicle vaccines against Neisseria meningitidis based on nontoxic LPS mutants. HumVaccin 7:886-890. http://dx.doi.org/10.4161/hv.7.8.16086.
31. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO. 2009. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458:1191-1195. http://dx.doi.org/10.1038/nature07830.
32. Ohto U, Fukase K, Miyake K, Shimizu T. 2012. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc Natl Acad Sci U S A 109:7421-7426. http://dx.doi.org/10.1073/pnas.1201193109.
33. Steeghs L, van Vliet SJ, Uronen-Hansson H, van Mourik A, Engering A, Sanchez-Hernandez M, Klein N, Callard R, van Putten JP, van der Ley P, van Kooyk Y, van de Winkel JG. 2006. Neisseria meningitidis expressing lgtB lipopolysaccharide targets DC-SIGN and modulates dendritic cell function. Cell Microbiol 8:316-325. http://dx.doi.org/10.1111/j.1462-5822.2005.00623.x.
34. Jones HE, Copland A, Hamstra HJ, Cohen J, Brown J, Klein N, van der Ley P, Dixon G. 2014. LOS oligosaccharide modification enhances dendritic cell responses to meningococcal native outer membrane vesicles expressing a non-toxic lipid A. Cell Microbiol 16:519-534. http://dx.doi.org/10.1111/cmi.12231.
35. Biagini M, Garibaldi M, Aprea S, Pezzicoli A, Doro F, Becherelli M, Taddei AR, Tani C, Tavarini S, Mora M, Teti G, D'Oro U, Nuti S, Soriani M, Margarit I, Rappuoli R, Grandi G, Norais N. 2015. The human pathogen Streptococcus pyogenes releases lipoproteins as lipoprotein-rich membrane vesicles. Mol Cell Proteomics 14:2138-2149. http://dx.doi.org/10.1074/mcp. M114.045880.
36. Frosch M, Schultz E, Glenn-Calvo E, Meyer TF. 1990. Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination. Mol Microbiol 4:1215-1218. http://dx.doi.org/10.1111/j.1365-2958.1990.tb00697.x.