Immunization with Outer Membrane Vesicles Displaying Designer Glycotopes Yields Class-Switched, Glycan-Specific Antibodies

Cell Chemical Biology

Volumn 23, Issue 6, 2016, Pages 655-665

  Valentine, Jenny L ^a   Chen, Linxiao ^a   Perregaux, Emily C ^c   Weyant, Kevin B ^a   Rosenthal, Joseph A ^a   Heiss, Christian ^d   Azadi, Parastoo ^d   Fisher, Adam C ^b   Putnam, David ^a,c   Moe, Gregory R ^e   Merritt, Judith H ^b   DeLisa, Matthew P ^a,c  

^a Cornell University   (United States)

^b Glycobia Inc   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTIGEN; GLYCAN DERIVATIVE; GLYCAN SPECIFIC ANTIBODY; GLYCOTOPE DERIVATIVE; POLYSIALIC ACID; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; EPITOPE; OUTER MEMBRANE PROTEIN; POLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL OUTER MEMBRANE; BIOSYNTHESIS; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOSTIMULATION; MEMBRANE VESICLE; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; ANIMAL; ANTIGEN ANTIBODY REACTION; BAGG ALBINO MOUSE; CHEMISTRY; GENE REARRANGEMENT; IMMUNOLOGY;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGEN-ANTIBODY REACTIONS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; EPITOPES; FEMALE; IMMUNIZATION; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MICE, INBRED BALB C; NEISSERIA MENINGITIDIS, SEROGROUP B; POLYSACCHARIDES;

EID: 84976352030     PISSN: 24519456     EISSN: 24519448     Source Type: Journal    
DOI: 10.1016/j.chembiol.2016.05.014     Document Type: Article

References (55)

1. S. Adluri, F. Helling, S. Ogata, S. Zhang, S.H. Itzkowitz, K.O. Lloyd, and P.O. Livingston Immunogenicity of synthetic TF-KLH (keyhole limpet hemocyanin) and sTn-KLH conjugates in colorectal carcinoma patients Cancer Immunol. Immunother. 41 1995 185 192
2. R.C. Alaniz, B.L. Deatherage, J.C. Lara, and B.T. Cookson 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 2007 7692 7701
3. K.R. Anumula, and P.B. Taylor A comprehensive procedure for preparation of partially methylated alditol acetates from glycoprotein carbohydrates Anal. Biochem. 203 1992 101 108
4. M.A. Apicella, J.M. Griffis, and H. Schneider Isolation and characterization of lipopolysaccharides, lipooligosaccharides, and lipid A V.L. Clarke, P.M. Bavoil, Bacterial Pathogenesis 1997 Academic Press San Diego, CA 123 133
5. R.D. Astronomo, and D.R. Burton Carbohydrate vaccines: developing sweet solutions to sticky situations? Nat. Rev. Drug Discov. 9 2010 308 324
6. F.Y. Avci, and D.L. Kasper How bacterial carbohydrates influence the adaptive immune system Annu. Rev. Immunol. 28 2010 107 130
7. J.L. Baker, L. Chen, J.A. Rosenthal, D. Putnam, and M.P. DeLisa Microbial biosynthesis of designer outer membrane vesicles Curr. Opin. Biotechnol. 29C 2014 76 84
8. A. Bernadac, M. Gavioli, J.C. Lazzaroni, S. Raina, and R. Lloubes Escherichia coli tol-pal mutants form outer membrane vesicles J. Bacteriol. 180 1998 4872 4878
9. S. Bernatchez, C.M. Szymanski, N. Ishiyama, J. Li, H.C. Jarrell, P.C. Lau, A.M. Berghuis, N.M. Young, and W.W. Wakarchuk A single bifunctional UDP-GlcNAc/Glc 4-epimerase supports the synthesis of three cell surface glycoconjugates in Campylobacter jejuni J. Biol. Chem. 280 2005 4792 4802
10. O. Blixt, J. Brown, M.J. Schur, W. Wakarchuk, and J.C. Paulson Efficient preparation of natural and synthetic galactosides with a recombinant beta-1,4-galactosyltransferase-/UDP-4'-gal epimerase fusion protein J. Org. Chem. 66 2001 2442 2448
11. D.A. Calarese, H.K. Lee, C.Y. Huang, M.D. Best, R.D. Astronomo, R.L. Stanfield, H. Katinger, D.R. Burton, C.H. Wong, and I.A. Wilson Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12 Proc. Natl. Acad. Sci. USA 102 2005 13372 13377
12. D.J. Chen, N. Osterrieder, S.M. Metzger, E. Buckles, A.M. Doody, M.P. DeLisa, and D. Putnam Delivery of foreign antigens by engineered outer membrane vesicle vaccines Proc. Natl. Acad. Sci. USA 107 2010 3099 3104
13. L.E. Comstock, and D.L. Kasper Bacterial glycans: key mediators of diverse host immune responses Cell 126 2006 847 850
14. J. Cuccui, and B. Wren Hijacking bacterial glycosylation for the production of glycoconjugates, from vaccines to humanised glycoproteins J. Pharm. Pharmacol. 67 2014 338 350
15. J. Cuccui, R.M. Thomas, M.G. Moule, R.V. D'Elia, T.R. Laws, D.C. Mills, D. Williamson, T.P. Atkins, J.L. Prior, and B.W. Wren Exploitation of bacterial N-linked glycosylation to develop a novel recombinant glycoconjugate vaccine against Francisella tularensis Open Biol. 3 2013 130002
16. D.A. Daines, L.F. Wright, D.O. Chaffin, C.E. Rubens, and R.P. Silver NeuD plays a role in the synthesis of sialic acid in Escherichia coli K1 FEMS Microbiol. Lett. 189 2000 281 284
17. T.N. Ellis, S.A. Leiman, and M.J. Kuehn Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components Infect Immun. 78 2010 3822 3831
18. M.F. Feldman, M. Wacker, M. Hernandez, P.G. Hitchen, C.L. Marolda, M. Kowarik, H.R. Morris, A. Dell, M.A. Valvano, and M. Aebi Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli Proc. Natl. Acad. Sci. USA 102 2005 3016 3021
19. C.E. Frasch Preparation of bacterial polysaccharide-protein conjugates: analytical and manufacturing challenges Vaccine 27 2009 6468 6470
20. K.J. Glover, E. Weerapana, and B. Imperiali In vitro assembly of the undecaprenylpyrophosphate-linked heptasaccharide for prokaryotic N-linked glycosylation Proc. Natl. Acad. Sci. USA 102 2005 14255 14259
21. A.R. Gorringe, and R. Pajon Bexsero: a multicomponent vaccine for prevention of meningococcal disease Hum. Vaccin. Immunother. 8 2012 174 183
22. D.M. Granoff, A. Bartoloni, S. Ricci, E. Gallo, D. Rosa, N. Ravenscroft, V. Guarnieri, R.C. Seid, A. Shan, W.R. Usinger, and et al. Bactericidal monoclonal antibodies that define unique meningococcal B polysaccharide epitopes that do not cross-react with human polysialic acid J. Immunol. 160 1998 5028 5036
23. B.B. Haab Using lectins in biomarker research: addressing the limitations of sensitivity and availability Proteomics Clin. Appl. 6 2012 346 350
24. J. Heimburg-Molinaro, M. Lum, G. Vijay, M. Jain, A. Almogren, and K. Rittenhouse-Olson Cancer vaccines and carbohydrate epitopes Vaccine 29 2011 8802 8826
25. J. Ihssen, M. Kowarik, S. Dilettoso, C. Tanner, M. Wacker, and L. Thony-Meyer Production of glycoprotein vaccines in Escherichia coli Microb. Cell Fact. 9 2010 61
26. J. Ihssen, J. Haas, M. Kowarik, L. Wiesli, M. Wacker, T. Schwede, and L. Thony-Meyer Increased efficiency of Campylobacter jejuni N-oligosaccharyltransferase PglB by structure-guided engineering Open Biol. 5 2015 140227
27. K. Ilg, E. Yavuz, C. Maffioli, B. Priem, and M. Aebi Glycomimicry: display of the GM3 sugar epitope on Escherichia coli and Salmonella enterica sv Typhimurium Glycobiology 20 2010 1289 1297
28. J.Y. Kim, A.M. Doody, D.J. Chen, G.H. Cremona, M.L. Shuler, D. Putnam, and M.P. DeLisa Engineered bacterial outer membrane vesicles with enhanced functionality J. Mol. Biol. 380 2008 51 66
29. L.M. Krug, G. Ragupathi, K.K. Ng, C. Hood, H.J. Jennings, Z. Guo, M.G. Kris, V. Miller, B. Pizzo, L. Tyson, and et al. Vaccination of small cell lung cancer patients with polysialic acid or N-propionylated polysialic acid conjugated to keyhole limpet hemocyanin Clin. Cancer Res. 10 2004 916 923
30. J.J. Lavinder, A.P. Horton, G. Georgiou, and G.C. Ippolito Next-generation sequencing and protein mass spectrometry for the comprehensive analysis of human cellular and serum antibody repertoires Curr. Opin. Chem. Biol. 24 2015 112 120
31. R. Lotan, E. Skutelsky, D. Danon, and N. Sharon The purification, composition, and specificity of the anti-T lectin from peanut (Arachis hypogaea) J. Biol. Chem. 250 1975 8518 8523
32. X.M. Luo, M.Y. Lei, R.A. Feidi, A.P. West Jr., A.B. Balazs, P.J. Bjorkman, L. Yang, and D. Baltimore Dimeric 2G12 as a potent protection against HIV-1 PLoS Pathog. 6 2010 e1001225
33. U. Mamat, T.C. Meredith, P. Aggarwal, A. Kuhl, P. Kirchhoff, B. Lindner, A. Hanuszkiewicz, J. Sun, O. Holst, and R.W. Woodard Single amino acid substitutions in either YhjD or MsbA confer viability to 3-deoxy-d-manno-oct-2-ulosonic acid-depleted Escherichia coli Mol. Microbiol. 67 2008 633 648
34. D. Martin, L. McCallum, A. Glennie, N. Ruijne, P. Blatchford, J. O'Hallahan, and P. Oster Validation of the serum bactericidal assay for measurement of functional antibodies against group B meningococci associated with vaccine trials Vaccine 23 2005 2218 2221
35. A.J. McBroom, A.P. Johnson, S. Vemulapalli, and M.J. Kuehn Outer membrane vesicle production by Escherichia coli is independent of membrane instability J. Bacteriol. 188 2006 5385 5392
36. G.R. Moe, S. Tan, and D.M. Granoff Differences in surface expression of NspA among Neisseria meningitidis group B strains Infect. Immun. 67 1999 5664 5675
37. G.R. Moe, T.S. Bhandari, and B.A. Flitter Vaccines containing de-N-acetyl sialic acid elicit antibodies protective against Neisseria meningitidis groups B and C J. Immunol. 182 2009 6610 6617
38. M. Muralinath, M.J. Kuehn, K.L. Roland, and R. Curtiss 3rd Immunization with Salmonella enterica serovar Typhimurium-derived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with Streptococcus pneumoniae Infect. Immun. 79 2011 887 894
39. M. Nonaka, M.N. Fukuda, C. Gao, Z. Li, H. Zhang, M.I. Greene, D.M. Peehl, T. Feizi, and M. Fukuda Determination of carbohydrate structure recognized by prostate-specific F77 monoclonal antibody through expression analysis of glycosyltransferase genes J. Biol. Chem. 289 2014 16478 16486
40. K. Ohtsubo, and J.D. Marth Glycosylation in cellular mechanisms of health and disease Cell 126 2006 855 867
41. K.S. Park, K.H. Choi, Y.S. Kim, B.S. Hong, O.Y. Kim, J.H. Kim, C.M. Yoon, G.Y. Koh, Y.K. Kim, and Y.S. Gho Outer membrane vesicles derived from Escherichia coli induce systemic inflammatory response syndrome PLoS One 5 2010 e11334
42. S.S. Pinho, and C.A. Reis Glycosylation in cancer: mechanisms and clinical implications Nat. Rev. Cancer 15 2015 540 555
43. B. Priem, M. Gilbert, W.W. Wakarchuk, A. Heyraud, and E. Samain A new fermentation process allows large-scale production of human milk oligosaccharides by metabolically engineered bacteria Glycobiology 12 2002 235 240
44. R. Raman, S. Raguram, G. Venkataraman, J.C. Paulson, and R. Sasisekharan Glycomics: an integrated systems approach to structure-function relationships of glycans Nat. Methods 2 2005 817 824
45. J.B. Robbins, R. Schneerson, G. Xie, L.A. Hanson, and M.A. Miller Capsular polysaccharide vaccine for Group B Neisseria meningitidis, Escherichia coli K1, and Pasteurella haemolytica A2 Proc. Natl. Acad. Sci. USA 108 2011 17871 17875
46. H. Sanders, and I.M. Feavers Adjuvant properties of meningococcal outer membrane vesicles and the use of adjuvants in Neisseria meningitidis protein vaccines Expert Rev. Vaccines 10 2011 323 334
47. V.S. Terra, D.C. Mills, L.E. Yates, S. Abouelhadid, J. Cuccui, and B.W. Wren Recent developments in bacterial protein glycan coupling technology and glycoconjugate vaccine design J. Med. Microbiol. 61 2012 919 926
48. J.D. Valderrama-Rincon, A.C. Fisher, J.H. Merritt, Y.Y. Fan, C.A. Reading, K. Chhiba, C. Heiss, P. Azadi, M. Aebi, and M.P. DeLisa An engineered eukaryotic protein glycosylation pathway in Escherichia coli Nat. Chem. Biol. 8 2012 434 436
49. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etzler Essentials of Glycobiology Second Edition 2009 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
50. E.R. Vimr, W. Aaronson, and R.P. Silver Genetic analysis of chromosomal mutations in the polysialic acid gene cluster of Escherichia coli K1 J. Bacteriol. 171 1989 1106 1117
51. L.X. Wang, and J.V. Lomino Emerging technologies for making glycan-defined glycoproteins ACS Chem. Biol. 7 2012 110 122
52. L.M. Willis, J. Stupak, M.R. Richards, T.L. Lowary, J. Li, and C. Whitfield Conserved glycolipid termini in capsular polysaccharides synthesized by ATP-binding cassette transporter-dependent pathways in Gram-negative pathogens Proc. Natl. Acad. Sci. USA 110 2013 7868 7873
53. E. Yavuz, C. Maffioli, K. Ilg, M. Aebi, and B. Priem Glycomimicry: display of fucosylation on the lipo-oligosaccharide of recombinant Escherichia coli K12 Glycoconj. J. 28 2011 39 47
54. W. Yi, J. Shao, L. Zhu, M. Li, M. Singh, Y. Lu, S. Lin, H. Li, K. Ryu, J. Shen, and et al. Escherichia coli O86 O-antigen biosynthetic gene cluster and stepwise enzymatic synthesis of human blood group B antigen tetrasaccharide J. Am. Chem. Soc. 127 2005 2040 2041
55. G. Zhang, H. Zhang, Q. Wang, P. Lal, A.M. Carroll, M. de la Llera-Moya, X. Xu, and M.I. Greene Suppression of human prostate tumor growth by a unique prostate-specific monoclonal antibody F77 targeting a glycolipid marker Proc. Natl. Acad. Sci. USA 107 2010 732 737