Hijacking bacterial glycosylation for the production of glycoconjugates, from vaccines to humanised glycoproteins

Journal of Pharmacy and Pharmacology

Volumn 67, Issue 3, 2015, Pages 338-350

  Cuccui, Jon ^a   Wren, Brendan ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

glycoconjugates; humanised glycoproteins; PglB; vaccines

Indexed keywords

B LYMPHOCYTE RECEPTOR; BACTERIAL POLYSACCHARIDE; BACTERIAL VACCINE; GLYCOCONJUGATE; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; HAEMOPHILUS INFLUENZAE VACCINE; IMMUNOGLOBULIN G ANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOSE; MENINGOCOCCUS VACCINE; MONOCLONAL ANTIBODY; OLIGOSACCHARYLTRANSFERASE; PGLB PROTEIN; PNEUMOCOCCUS VACCINE; SHIGELLA VACCINE; STAPHYLOCOCCUS VACCINE; TULAREMIA VACCINE; UNCLASSIFIED DRUG; DOLICHYL-DIPHOSPHOOLIGOSACCHARIDE - PROTEIN GLYCOTRANSFERASE; MEMBRANE PROTEIN; POLYSACCHARIDE; VACCINE;

ACTINOBACILLUS PLEUROPNEUMONIAE; ANTIBODY PRODUCTION; BIOTECHNOLOGICAL PROCEDURES; CAMPYLOBACTER JEJUNI; CONJUGATION; ESCHERICHIA COLI; FRANCISELLA TULARENSIS; HUMAN; MENINGOCOCCOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; PROTEIN GLYCOSYLATION; REVIEW; SACCHAROMYCES CEREVISIAE; SHIGELLA DYSENTERIAE; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; T LYMPHOCYTE ACTIVATION; VACCINE PRODUCTION; ANIMAL; BACTERIAL INFECTIONS; BIOSYNTHESIS; BIOTECHNOLOGY; CAMPYLOBACTER; METABOLISM; MICROBIOLOGY;

ANIMALS; BACTERIAL INFECTIONS; BIOTECHNOLOGY; CAMPYLOBACTER; GLYCOCONJUGATES; GLYCOPROTEINS; HEXOSYLTRANSFERASES; HUMANS; MEMBRANE PROTEINS; POLYSACCHARIDES; VACCINES;

EID: 84925670301     PISSN: 00223573     EISSN: 20427158     Source Type: Journal    
DOI: 10.1111/jphp.12321     Document Type: Review

References (64)

1. Coutinho A, Moller G,. B cell mitogenic properties of thymus-independent antigens. Nat New Biol 1973; 245: 12-14.
2. Timens W, et al. Immaturity of the human splenic marginal zone in infancy. Possible contribution to the deficient infant immune response. J Immunol 1989; 143: 3200-3206.
3. Shi Y, et al. Regulation of aged humoral immune defense against pneumococcal bacteria by IgM memory B cell. J Immunol 2005; 175: 3262-3267.
4. Avery OT, Goebel WF,. Chemo-immunological studies on conjugated carbohydrate-proteins: II. Immunological specificity of synthetic sugar-protein antigens. J Exp Med 1929; 50: 533-550.
5. Schneerson R, et al. Preparation, characterization, and immunogenicity of Haemophilus influenzae type b polysaccharide-protein conjugates. J Exp Med 1980; 152: 361-376.
6. Schneerson R, et al. Haemophilus influenzae type B polysaccharide-protein conjugates: model for a new generation of capsular polysaccharide vaccines. Prog Clin Biol Res 1980; 47: 77-94.
7. Kuberan B, Linhardt RJ,. Carbohydrate based vaccine. Curr Org Chem 2000; 4: 653-677.
8. Brady C, et al. A new paradigm for rapidly translating novel conjugate vaccines into the clinic. Bioprocess Tech 2012; 10: 50-55.
9. Watt JP, et al. Burden of disease caused by Haemophilus influenzae type b in children younger than 5 years: global estimates. Lancet 2009; 374: 903-911.
10. Ladhani SN,. Two decades of experience with the Haemophilus influenzae serotype b conjugate vaccine in the United Kingdom. Clin Ther 2012; 34: 385-399.
11. Bentley SD, et al. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2006; 2: e31.
12. Grijalva CG, et al. Decline in pneumonia admissions after routine childhood immunisation with pneumococcal conjugate vaccine in the USA: a time-series analysis. Lancet 2007; 369: 1179-1186.
13. Yazdankhah SP, Caugant DA,. Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 2004; 53 (Pt 9): 821-832.
14. Daugla DM, et al. Effect of a serogroup A meningococcal conjugate vaccine (PsA-TT) on serogroup A meningococcal meningitis and carriage in Chad: a community study [corrected]. Lancet 2014; 383: 40-47.
15. Avci FY, et al. A mechanism for glycoconjugate vaccine activation of the adaptive immune system and its implications for vaccine design. Nat Med 2011; 17: 1602-1609.
16. Sleytr UB, Thorne KJ,. Chemical characterization of the regularly arranged surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum. J Bacteriol 1976; 126: 377-383.
17. Scott NE, et al. Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol Cell Proteomics 2011; 10: M000031-MCP201.
18. Grass S, et al. The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol Microbiol 2003; 48: 737-751.
19. McCann JR, St Geme JW III,. The HMW1C-like glycosyltransferases-an enzyme family with a sweet tooth for simple sugars. PLoS Pathog 2014; 10: e1003977.
20. Faridmoayer A, et al. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J Bacteriol 2007; 189: 8088-8098.
21. Benz I, Schmidt MA,. Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol 2001; 40: 1403-1413.
22. Fry BN, et al. The lipopolysaccharide biosynthesis locus of Campylobacter jejuni 81116. Microbiology 1998; 144 (Pt 8): 2049-2061.
23. Szymanski CM, et al. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 1999; 32: 1022-1030.
24. Parkhill J, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000; 403: 665-668.
25. Young NM, et al. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem 2002; 277: 42530-42539.
26. Linton D, et al. Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol Microbiol 2005; 55: 1695-1703.
27. Feldman MF, et al. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci U S A 2005; 102: 3016-3021.
28. Wacker M, et al. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc Natl Acad Sci U S A 2006; 103: 7088-7093.
29. Petrescu AJ, et al. Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 2004; 14: 103-114.
30. Kowarik M, et al. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J 2006; 25: 1957-1966.
31. Kowarik M, et al. N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 2006; 314: 1148-1150.
32. Chen MM, et al. Polyisoprenol specificity in the Campylobacter jejuni N-linked glycosylation pathway. Biochemistry 2007; 46: 14342-14348.
33. Lizak C, et al. X-ray structure of a bacterial oligosaccharyltransferase. Nature 2011; 474: 350-355.
34. Ielmini MV, Feldman MF,. Desulfovibrio desulfuricans PglB homolog possesses oligosaccharyltransferase activity with relaxed glycan specificity and distinct protein acceptor sequence requirements. Glycobiology 2011; 21: 734-742.
35. Ihssen J, et al. Production of glycoprotein vaccines in Escherichia coli. Microb Cell Fact 2010; 9: 61.
36. Cuccui J, et al. Exploitation of bacterial N-linked glycosylation to develop a novel recombinant glycoconjugate vaccine against Francisella tularensis. Open Biol 2013; 3: 130002.
37. Wacker M, et al. Prevention of Staphylococcus aureus infections by glycoprotein vaccines synthesized in Escherichia coli. J Infect Dis 2014; 209: 1551-1561.
38. Fisher AC, et al. Production of secretory and extracellular N-linked glycoproteins in Escherichia coli. Appl Environ Microbiol 2011; 77: 871-881.
39. Byrd W, et al. Protective efficacy of conjugate vaccines against experimental challenge with porcine Actinobacillus pleuropneumoniae. Vet Immunol Immunopathol 1992; 34: 307-324.
40. Byrd W, Kadis S,. Preparation, characterization, and immunogenicity of conjugate vaccines directed against Actinobacillus pleuropneumoniae virulence determinants. Infect Immun 1992; 60: 3042-3051.
41. Iwashkiw JA, et al. Exploiting the Campylobacter jejuni protein glycosylation system for glycoengineering vaccines and diagnostic tools directed against brucellosis. Microb Cell Fact 2012; 11: 13.
42. Zielinska DF, et al. Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol Cell 2012; 46: 542-548.
43. Chu CS, et al. Profile of native N-linked glycan structures from human serum using high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. Proteomics 2009; 9: 1939-1951.
44. Varki A, Lowe JB,. Biological roles of glycans. In:, Varki A, et al., eds. Essentials of Glycobiology, 2nd edn. Huntington, NY: Cold Spring Harbor, 2009: 1-14.
45. Varki A, et al. Glycans in development and systemic physiology. In:, Varki A, et al., eds. Essentials of Glycobiology, 2nd edn. Huntington, NY: Cold Spring Harbor, 2009: 1-6.
46. Bertozzi CR, et al. Glycans in biotechnology and the pharmaceutical industry. In:, Varki A, et al., eds. Essentials of Glycobiology, 2nd edn. Huntington, NY: Cold Spring Harbor, 2009: 1-14.
47. Aggarwal RS,. What's fueling the biotech engine-2012 to 2013. Nat Biotechnol 2014; 32: 32-39.
48. Ghaderi D, et al. Production platforms for biotherapeutic glycoproteins. Occurrence, impact, and challenges of non-human sialylation. Biotechnol Genet Eng Rev 2012; 28: 147-175.
49. Jenkins N, et al. Getting the glycosylation right: implications for the biotechnology industry. Nat Biotechnol 1996; 14: 975-981.
50. Nystedt J, et al. Human CMP-N-acetylneuraminic acid hydroxylase is a novel stem cell marker linked to stem cell-specific mechanisms. Stem Cells 2010; 28: 258-267.
51. Flesher AR, et al. Fluorophore-labeled carbohydrate analysis of immunoglobulin fusion proteins: correlation of oligosaccharide content with in vivo clearance profile. Biotechnol Bioeng 1995; 46: 399-407.
52. Son Y-D, et al. Enhanced sialylation of recombinant human erythropoietin in Chinese hamster ovary cells by combinatorial engineering of selected genes. Glycobiology 2011; 21: 1019-1028.
53. Valderrama-Rincon JD, et al. An engineered eukaryotic protein glycosylation pathway in Escherichia coli. Nat Chem Biol 2012; 8: 434-436.
54. Meuris L, et al. GlycoDelete engineering of mammalian cells simplifies N-glycosylation of recombinant proteins. Nat Biotechnol 2014; 32: 485-489.
55. Naegeli A, et al. Molecular analysis of an alternative N-glycosylation machinery by functional transfer from Actinobacillus pleuropneumoniae to Escherichia coli. J Biol Chem 2014; 289: 2170-2179.
56. Lomino JV, et al. A two-step enzymatic glycosylation of polypeptides with complex N-glycans. Bioorg Med Chem 2013; 21: 2262-2270.
57. Hug I, et al. Exploiting bacterial glycosylation machineries for the synthesis of a Lewis antigen-containing glycoprotein. J Biol Chem 2011; 286: 37887-37894.
58. Schwarz F, et al. A combined method for producing homogenous glycoproteins with eukaryotic N-glycosylation. Nat Chem Biol 2010; 6: 264-266.
59. Faridmoayer A, et al. Extreme substrate promiscuity of the Neisseria oligosaccharyl transferase involved in protein O-glycosylation. J Biol Chem 2008; 283: 34596-34604.
60. Descroix K, et al. Inhibition of galactosyltransferases by a novel class of donor analogues. J Med Chem 2012; 55: 2015-2024.
61. Iwashkiw JA, et al. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog 2012; 8: e1002758.
62. Guerry P, et al. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol Microbiol 2006; 60: 299-311.
63. Karlyshev AV, et al. The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 2004; 150 (Pt 6): 1957-1964.
64. Lithgow KV, et al. A general protein O-glycosylation system within the Burkholderia cepacia complex is involved in motility and virulence. Mol Microbiol 2014; 92: 116-137.