The actinobacillus pleuropneumoniae HMW1C-like glycosyltransferase mediates N-Linked glycosylation of the haemophilus influenzae HMW1 adhesin

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Choi, Kyoung Jae ^a   Grass, Susan ^b   Paek, Seonghee ^a   St Geme III, Joseph W ^b   Yeo, Hye Jeong ^a  

^a University of Houston   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ASPARAGINE; GALACTOSE; GLUCOSE; GLYCOSYLTRANSFERASE; HMW1 ADHESIN; PROTEIN HMW1C; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; HMW1 PROTEIN, BACTERIA;

ACTINOBACILLUS PLEUROPNEUMONIAE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM ADHERENCE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; GLUCOSE TRANSPORT; HAEMOPHILUS INFLUENZAE; HEXOSE TRANSPORT; NONHUMAN; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; STRUCTURE ACTIVITY RELATION; AMINO ACID SEQUENCE; BIOLOGY; CATALYSIS; CHEMISTRY; EPITHELIUM CELL; GLYCOSYLATION; HUMAN; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

ACTINOBACILLUS PLEUROPNEUMONIAE; EUKARYOTA; HAEMOPHILUS INFLUENZAE;

ACTINOBACILLUS PLEUROPNEUMONIAE; ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL ADHESION; CATALYSIS; COMPUTATIONAL BIOLOGY; EPITHELIAL CELLS; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HAEMOPHILUS INFLUENZAE; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 78651248164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015888     Document Type: Article

References (44)

1. Barenkamp SJ, Leininger E (1992) Cloning, expression, and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecularweight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect Immun 60: 1302-1313.
2. St Geme JW, 3rd, Falkow S, Barenkamp SJ (1993) High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci U S A 90: 2875-2879.
3. St Geme JW, 3rd, Kumar VV, Cutter D, Barenkamp SJ (1998) Prevalence and distribution of the hmw and hia genes and the HMW and Hia adhesins among genetically diverse strains of nontypeable Haemophilus influenzae. Infect Immun 66: 364-368.
4. St Geme JW, 3rd, Yeo HJ (2009) A prototype two-partner secretion pathway: the Haemophilus influenzae HMW1 and HMW2 adhesin systems. Trends Microbiol 17: 355-360.
5. Grass S, Buscher AZ, Swords WE, Apicella MA, Barenkamp SJ, et al. (2003) The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol Microbiol 48: 737-751.
6. Gross J, Grass S, Davis AE, Gilmore-Erdmann P, Townsend RR, et al. (2008) The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual Nlinked carbohydrate modification. J Biol Chem 283: 26010-26015.
7. Grass S, Lichti CF, Townsend RR, Gross J, St Geme JW, 3rd (2010) The Haemophilus influenzae HMW1C protein is a glycosyltransferase that transfers hexose residues to asparagine sites in the HMW1 adhesin. PLoS Pathog 6(5): e1000919.
8. Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
9. Vigerust DJ, Shepherd VL (2007) Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 15: 211-218.
10. Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA (2001) Glycosylation and the immune system. Science 291: 2370-2376.
11. Guerry P, Szymanski CM (2008) Campylobacter sugars sticking out. Trends Microbiol 16: 428-435.
12. Szymanski CM, Wren BW (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3: 225-237.
13. Schmidt MA, Riley LW, Benz I (2003) Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol 11: 554-561.
14. Zhou M, Wu H (2009) Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology 155: 317-327.
15. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328: 307-317.
16. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
17. Clarke AJ, Hurtado-Guerrero R, Pathak S, Schüttelkopf AW, Borodkin V, et al. (2008) Structural insights into mechanism and specificity of O-GlcNAc transferase. EMBO J 27: 2780-2788.
18. Martinez-Fleites C, Macauley MS, He Y, Shen DL, Vocadlo DJ, et al. (2008) Structure of an O-GlcNAc transferase homolog provides insight into intracellular glycosylation. Nat Struct Mol Biol 15: 764-765.
19. Sebunya TN, Saunders JR (1983) Haemophilus pleuropneumoniae infection in swine: a review. J Am Vet Med Assoc 182: 1331-1337.
20. Gosselin S, Alhussaini M, Streiff MB, Takabayashi K, Palcic MM (1994) A continuous spectrophotometric assay for glycosyltransferases. Anal Biochem 220: 92-97.
21. Kreppel LK, Blomberg MA, Hart GW (1997) Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J Biol Chem 272: 9308-9315.
22. Kreppel LK, Hart GW (1999) Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J Biol Chem 274: 32015-32022.
23. Iyer SP, Hart GW (2003) Roles of the tetratricopeptide repeat domain in OGlcNAc transferase targeting and protein substrate specificity. J Biol Chem 278: 24608-24616.
24. Wang Z, Gucek M, Hart GW (2008) Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc Natl Acad Sci U S A 105: 13793-13798.
25. Jinek M, Chen YW, Clausen H, Cohen SM, Conti E (2004) Structural insights into the Notch-modifying glycosyltransferase Fringe. Nat Struct Mol Biol 11: 1001-1007.
26. Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77: 521-555.
27. Moréra S, Imberty A, Aschke-Sonnenborn U, Rüger W, Freemont PS (1999) T4 phage beta-glucosyltransferase: substrate binding and proposed catalytic mechanism. J Mol Biol 292: 717-730.
28. Mulichak AM, Losey HC, Walsh CT, Garavito RM (2001) Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics. Structure 9: 547-557.
29. Grizot S, Salem M, Vongsouthi V, Durand L, Moreau F, et al. (2006) Structure of the Escherichia coli heptosyltransferase WaaC: binary complexes with ADP and ADP-2-deoxy-2-fluoro heptose. J Mol Biol 363: 383-394.
30. Brazier-Hicks M, Offen WA, Gershater MC, Revett TJ, Lim EK, et al. (2007) Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proc Natl Acad Sci U S A 104: 20238-20243.
31. Hu Y, Chen L, Ha S, Gross B, Falcone B, et al. (2003) Crystal structure of the MurG:UDP-GlcNAc complex reveals common structural principles of a superfamily of glycosyltransferases. Proc Natl Acad Sci U S A 100: 845-849.
32. Lubas WA, Hanover JA (2000) Functional expression of O-linked GlcNAc transferase. Domain structure and substrate specificity. J Biol Chem 275: 10983-10988.
33. Kuo C, Takahashi N, Swanson AF, Ozeki Y, Hakomori S (1996) An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J Clin Invest 98: 2813-2818.
34. Lindenthal C, Elsinghorst EA (1999) Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect Immun 67: 4084-4091.
35. Goon S, Kelly JF, Logan SM, Ewing CP, Guerry P (2003) Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene. Mol Microbiol 50: 659-671.
36. Herrmann JL, O'Gaora P, Gallagher A, Thole JE, Young DB (1996) Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J 15: 3547-3554.
37. Marceau M, Nassif X (1999) Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J Bacteriol 181: 656-661.
38. Romain F, Horn C, Pescher P, Namane A, Riviere M, et al. (1999) Deglycosylation of the 45/47-kilodalton antigen complex of Mycobacterium tuberculosis decreases its capacity to elicit in vivo or in vitro cellular immune responses. Infect Immun 67: 5567-5572.
39. Charbonneau ME, Girard V, Nikolakakis A, Campos M, Berthiaume F, et al. (2007) O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J Bacteriol 189: 8880-8889.
40. Barenkamp SJ, St Geme JW, 3rd (1994) Genes encoding high-molecular-weight adhesion proteins of nontypeable Haemophilus influenzae are part of gene clusters. Infect Immun 62: 3320-3328.
41. Kirkpatrick AS, Yokoyama T, Choi KJ, Yeo HJ (2009) Campylobacter jejuni Fatty Acid Synthase II: Structural and functional analysis of b-hydroxyacyl-ACP dehydratase (FabZ). Biochem Biophys Res Commun 380: 407-412.
42. Buscher AZ, Burmeister K, Barenkamp SJ, St Geme JW, 3rd (2004) Evolutionary and functional relationships among the nontypeable Haemophilus influenzae HMW family of adhesins. J Bacteriol 186: 4209-4217.
43. Buscher AZ, Grass S, Heuser J, Roth R, St Geme JW, 3rd (2006) Surface anchoring of a bacterial adhesin secreted by the two-partner secretion pathway. Mol Microbiol 61: 470-483.
44. Yokoyama T, Paek S, Ewing CP, Guerry P, Yeo HJ (2008) Structure of a sigma28-regulated nonflagellar virulence protein from Campylobacter jejuni. J Mol Biol 384: 364-376.