Engineering the Campylobacter jejuni N-glycan to create an effective chicken vaccine

Scientific Reports

Volumn 6, Issue 1, 2016, Pages

  Nothaft, Harald ^a,b   Davis, Brandi ^c   Lock, Yee Ying ^c   Perez Munoz, Maria Elisa ^a   Vinogradov, Evgeny ^d   Walter, Jens ^a   Coros, Colin ^c   Szymanski, Christine M ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c Delta Genomics   (Canada)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE;

ANIMAL; BIRD DISEASE; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; CHICKEN; ESCHERICHIA COLI; GENETICS; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; VETERINARY;

ANIMALS; BACTERIAL VACCINES; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CHICKENS; ESCHERICHIA COLI; POULTRY DISEASES;

EID: 85007592512     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26511     Document Type: Article

References (79)

1. Friedman, C. J., Neiman, J., Wegener, H. C. & Tauxe, R. V. In Campylobacter (eds Nachamkim, I. & Blaser, M. J.) 121–38 (ASM Press, 2000).
2. Allos, B. M. Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis 32, 1201–6 (2001).
3. Mølbak, K. & Havelaar, A. In Campylobacter (eds Nachamkin, I., Szymanski, C. M. & Blaser, M. J.) 151–62 (ASM Press, 2008).
4. Yuki, N. & Odaka, M. Ganglioside mimicry as a cause of Guillain-Barre syndrome. Curr Opin Neurol 18, 557–61 (2005).
5. Annamalai, T. et al. Evaluation of nanoparticle-encapsulated outer membrane proteins for the control of Campylobacter jejuni colonization in chickens. Poult Sci 92, 2201–11 (2013).
6. Burr, D. H. et al. Prevention of disease in ferrets fed an inactivated whole cell Campylobacter jejuni vaccine. Vaccine 23, 4315–21 (2005).
7. Huang, J. L. et al. Intranasal immunization with chitosan/pCAGGS-flaA nanoparticles inhibits Campylobacter jejuni in a White Leghorn model. J Biomed Biotechnol 2010, doi: 10.1155/2010/589476 (2010).
8. Guerry, P. Nonlipopolysaccharide surface antigens of Campylobacter species. J Infect Dis 176 Suppl 2, S122–4 (1997).
9. Zhang, Q., Meitzler, J. C., Huang, S. & Morishita, T. Sequence polymorphism, predicted secondary structures and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect Immun 68, 5679–89 (2000).
10. Pei, Z. & Blaser, M. J. PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J Biol Chem 268, 18717–25 (1993).
11. Lin, J., Michel, L. O. & Zhang, Q. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother 46, 2124–31 (2002).
12. Zeng, X., Xu, F. & Lin, J. Molecular, antigenic and functional characteristics of ferric enterobactin receptor CfrA in Campylobacter jejuni. Infect Immun 77, 5437–48 (2009).
13. Logan, S. M. & Trust, T. J. Outer membrane characteristics of Campylobacter jejuni. Infect Immun 38, 898–906 (1982).
14. Blaser, M. J., Hopkins, J. A., Berka, R. M., Vasil, M. L. & Wang, W. L. Identification and characterization of Campylobacter jejuni outer membrane proteins. Infect Immun 42, 276–84 (1983).
15. Hu, Y., Huang, J. & Jiao, X. A. Screening of genes expressed in vivo during interaction between chicken and Campylobacter jejuni. J Microbiol Biotechnol 24, 217–24 (2013).
16. Nielsen, L. N. et al. Identification of immunogenic and virulence-associated Campylobacter jejuni proteins. Clin Vaccine Immunol 19, 113–9 (2012).
17. Hoppe, S., Bier, F. F. & von Nickisch-Rosenegk, M. Microarray-based method for screening of immunogenic proteins from bacteria. J Nanobiotechnology 10, 12 (2012).
18. Hu, Y. et al. Use of in vivo-induced antigen technology to identify in vivo expressed genes of Campylobacter jejuni during human infection. J Microbiol Biotechnol 24, 363–70 (2013).
19. Oakland, M., Jeon, B., Sahin, O., Shen, Z. & Zhang, Q. Functional characterization of a lipoprotein-encoding operon in Campylobacter jejuni. PLos One 6, e20084 (2011).
20. Khoury, C. A. & Meinersmann, R. J. A genetic hybrid of the Campylobacter jejuni flaA gene with LT-B of Escherichia coli and assessment of the efficacy of the hybrid protein as an oral chicken vaccine. Avian Dis 39, 812–20 (1995).
21. Zeng, X., Xu, F. & Lin, J. Development and Evaluation of CmeC Subunit Vaccine against Campylobacter jejuni. J Vaccines Vaccin 1, doi: 10.4172/2157-7560.1000112 (2010).
22. Layton, S. L. et al. Evaluation of Salmonella-vectored Campylobacter peptide epitopes for reduction of Campylobacter jejuni in broiler chickens. Clin Vaccine Immunol 18, 449–54 (2011).
23. Theoret, J. R. et al. The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination. Clin Vaccine Immunol 19, 1426–31 (2012).
24. Hacker, J., Blum-Oehler, G., Muhldorfer, I. & Tschape, H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23, 1089–97 (1997).
25. Huang, S., Sahin, O. & Zhang, Q. Infection-induced antibodies against the major outer membrane protein of Campylobacter jejuni mainly recognize conformational epitopes. FEMS Microbiol Lett 272, 137–43 (2007).
26. Pavlovskis, O. R. et al. Significance of flagella in colonization resistance of rabbits immunized with Campylobacter spp. Infect Immun 59, 2259–64 (1991).
27. Nuijten, P. J., van der Zeijst, B. A. & Newell, D. G. Localization of immunogenic regions on the flagellin proteins of Campylobacter jejuni 81116. Infect Immun 59, 1100–5 (1991).
28. Laniewski, P. et al. Evaluation of the immunogenicity of Campylobacter jejuni CjaA protein delivered by Salmonella enterica sv. Typhimurium strain with regulated delayed attenuation in chickens. World J Microbiol Biotechnol 30, 281–92 (2013).
29. Clark, J. D. et al. Eimeria species parasites as novel vaccine delivery vectors: anti-Campylobacter jejuni protective immunity induced by Eimeria tenella-delivered CjaA. Vaccine 30, 2683–8 (2012).
30. Wyszynska, A., Raczko, A., Lis, M. & Jagusztyn-Krynicka, E. K. Oral immunization of chickens with avirulent Salmonella vaccine strain carrying C. jejuni 72Dz/92 cjaA gene elicits specific humoral immune response associated with protection against challenge with wild-type Campylobacter. Vaccine 22, 1379–89 (2004).
31. Buckley, A. M. et al. Evaluation of live-attenuated Salmonella vaccines expressing Campylobacter antigens for control of C. jejuni in poultry. Vaccine 28, 1094–105 (2010).
32. Al-Adwani, S. R., Crespo, R. & Shah, D. H. Production and evaluation of chicken egg-yolk-derived antibodies against Campylobacter jejuni colonization-associated proteins. Foodborne Pathog Dis 10, 624–31 (2013).
33. Paul, N. C., Al-Adwani, S., Crespo, R. & Shah, D. H. Evaluation of passive immunotherapeutic efficacy of hyperimmunized egg yolk powder against intestinal colonization of Campylobacter jejuni in chickens. Poult Sci 93, 2779–87 (2014).
34. Jones, C. Vaccines based on the cell surface carbohydrates of pathogenic bacteria. An Acad Bras Cienc 77, 293–324 (2005).
35. Nothaft, H. et al. Diversity in the protein N-glycosylation pathways among Campylobacter species. Mol Cell Proteomics 11, 1203–19 (2012).
36. Szymanski, C. M. et al. Detection of conserved N-linked glycans and phase-variable lipooligosaccharides and capsules from campylobacter cells by mass spectrometry and high resolution magic angle spinning NMR spectroscopy. J Biol Chem 278, 24509–20 (2003).
37. Guerry, P. et al. Campylobacter polysaccharide capsules: virulence and vaccines. Front Cell Infect Microbiol 2, 7 (2012).
38. Bertolo, L. et al. The design of a capsule polysaccharide conjugate vaccine against Campylobacter jejuni serotype HS15. Carbohydr Res 366, 45–9 (2013).
39. Monteiro, M. A. et al. Capsule polysaccharide conjugate vaccine against diarrheal disease caused by Campylobacter jejuni. Infect Immun 77, 1128–36 (2009).
40. Wacker, M. et al. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298, 1790–3 (2002).
41. Young, N. M. et al. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem 277, 42530–9 (2002).
42. Alemka, A., Nothaft, H., Zheng, J. & Szymanski, C. M. N-Glycosylation of Campylobacter jejuni Surface Proteins Promotes Bacterial Fitness. Infect Immun 81, 1674–82 (2013).
43. Nothaft, H. & Szymanski, C. M. Protein glycosylation in bacteria: sweeter than ever. Nat Rev Microbiol 8, 765–78 (2010).
44. Nothaft, H. & Szymanski, C. M. Bacterial protein N-glycosylation: new perspectives and applications. J Biol Chem 288, 6912–20 (2013).
45. Kowarik, M. et al. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J 25, 1957–66 (2006).
46. Liu, D. & Reeves, P. R. Escherichia coli K12 regains its O antigen. Microbiology 140, 49–57 (1994).
47. Muller-Loennies, S., Lindner, B. & Brade, H. Structural analysis of oligosaccharides from lipopolysaccharide (LPS) of Escherichia coli K12 strain W3100 reveals a link between inner and outer core LPS biosynthesis. J Biol Chem 278, 34090–101 (2003).
48. Reid, C. W. et al. Affinity-capture tandem mass spectrometric characterization of polyprenyl-linked oligosaccharides: tool to study protein N-glycosylation pathways. Anal Chem 80, 5468–75 (2008).
49. Lin, J. Novel approaches for Campylobacter control in poultry. Foodborne Pathog Dis 6, 755–65 (2009).
50. de Zoete, M. R., van Putten, J. P. & Wagenaar, J. A. Vaccination of chickens against Campylobacter. Vaccine 25, 5548–57 (2007).
51. Szymanski, C. M., Goon, S., Allan, B. & Guerry, P. In Campylobacter: Molecular and Cellular Biology (eds Ketley, J. M. & Konkel, M. E.) 259–73 (Horizon Bioscience, 2005).
52. Szymanski, C. M., Burr, D. H. & Guerry, P. Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70, 2242–4 (2002).
53. Scott, N. E. et al. Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, HCD and ETD-MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol Cell Proteomics 10, MCP201–201–MCP201–218 (2011).
54. Avci, F. Y., Li, X., Tsuji, M. & Kasper, D. L. A mechanism for glycoconjugate vaccine activation of the adaptive immune system and its implications for vaccine design. Nat Med 17, 1602–9 (2011).
55. Bahrndorff, S., Gill, C., Lowenberger, C., Skovgard, H. & Hald, B. The effects of temperature and innate immunity on transmission of Campylobacter jejuni (Campylobacterales: Campylobacteraceae) between life stages of Musca domestica (Diptera: Muscidae). J Med Entomol 51, 670–7 (2014).
56. Sommer, H. M., Heuer, O. E., Sorensen, A. I. & Madsen, M. Analysis of factors important for the occurrence of Campylobacter in Danish broiler flocks. Prev Vet Med 111, 100–11 (2013).
57. Skovgard, H., Kristensen, K. & Hald, B. Retention of Campylobacter (Campylobacterales: Campylobacteraceae) in the house fly (Diptera: Muscidae). J Med Entomol 48, 1202–9 (2011).
58. Stern, N. J., Bailey, J. S., Blankenship, L. C., Cox, N. A. & McHan, F. Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Dis 32, 330–4 (1988).
59. Chen, L., Geys, H., Cawthraw, S., Havelaar, A. & Teunis, P. Dose response for infectivity of several strains of Campylobacter jejuni in chickens. Risk Anal 26, 1613–21 (2006).
60. Feldman, M. F. et al. Engineering N-linked protein glycosylation with diverse O-antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci USA 102, 3016–21 (2005).
61. Linton, D. et al. Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol Microbiol 55, 1695–703 (2005).
62. Alaimo, C. et al. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J 25, 967–76 (2006).
63. Heinrichs, D. E., Monteiro, M. A., Perry, M. B. & Whitfield, C. The assembly system for the lipopolysaccharide R2 core-type of Escherichia coli is a hybrid of those found in Escherichia coli K-12 and Salmonella enterica. Structure and function of the R2 WaaK and WaaL homologs. J Biol Chem 273, 8849–59 (1998).
64. Nothaft, H., Liu, X., Li, J. & Szymanski, C. M. Campylobacter jejuni free oligosaccharides: function and fate. Virulence 1, 546–50 (2010).
65. Nothaft, H., Liu, X., McNally, D. J., Li, J. & Szymanski, C. M. Study of free oligosaccharides derived from the bacterial N-glycosylation pathway. Proc Natl Acad Sci USA 106, 15019–24 (2009).
66. Nothaft, H., Liu, X., McNally, D. J. & Szymanski, C. M. N-linked protein glycosylation in a bacterial system. Methods Mol Biol 600, 227–43 (2010).
67. Linton, D. et al. Phase variation of a beta-1, 3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 37, 501–14 (2000).
68. Guerry, P. et al. Phase variation of Campylobacter jejuni 81–176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect Immun 70, 787–93 (2002).
69. Hendrixson, D. R. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol Microbiol 61, 1646–59 (2006).
70. Parkhill, J. et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–8 (2000).
71. Moxon, R., Bayliss, C. & Hood, D. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40, 307–33 (2006).
72. Aminian, M., Sivam, S., Lee, C. W., Halperin, S. A. & Lee, S. F. Expression and purification of a trivalent pertussis toxin-diphtheria toxin-tetanus toxin fusion protein in Escherichia coli. Protein Expr Purif 51, 170–8 (2007).
73. Masuko, T. et al. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem 339, 69–72 (2005).
74. Dwivedi, R., Nothaft, H., Reiz, B., Whittal, R. M. & Szymanski, C. M. Generation of free oligosaccharides from bacterial protein N-linked glycosylation systems. Biopolymers 99, 772–83 (2013).
75. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006 0008 (2006).
76. Islam, K., Khalil, I., Ahsan, C. R., Yasmin, M. & Nessa, J. Analysis of immune responses against H pylori in rabbits. World J Gastroenterol 13, 600–6 (2007).
77. Wetter, M. et al. Engineering, conjugation and immunogenicity assessment of Escherichia coli O121 O antigen for its potential use as a typhoid vaccine component. Glycoconj J 30, 511–22 (2013).
78. Rice, B. E., Lamichhane, C., Joseph, S. W. & Rollins, D. M. Development of a rapid and specific colony-lift immunoassay for detection and enumeration of Campylobacter jejuni, C. coli and C. lari. Clin Diagn Lab Immunol 3, 669–77 (1996).
79. Krumbeck, J. A. et al. In vivo selection to identify bacterial strains with enhanced ecological performance in synbiotic applications. Appl Environ Microbiol 81, 2455–65 (2015).