Evaluating the role of conserved amino acids in bacterial O-oligosaccharyltransferases by in vivo, in vitro and limited proteolysis assays

Glycobiology

Volumn 24, Issue 1, 2014, Pages 39-50

  Musumeci, Matias A ^a   Faridmoayer, Amirreza ^a   Watanabe, Yasuharu ^a   Feldman, Mario F ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

bacteria; limited proteolysis; O linked glycosylation; O oligosaccharyltransferases

Indexed keywords

ALANINE; AMINO ACID DERIVATIVE; BACTERIAL ENZYME; DIOLEOYLPHOSPHATIDYLGLYCEROL; GLYCAN; HISTIDINE; LIGASE; LIPID; LIPID A; MEMBRANE PROTEIN; MUTANT PROTEIN; O ANTIGEN; O OLIGOSACCHARYLTRANSFERASE; OLIGOSACCHARIDE; PILIN; UNCLASSIFIED DRUG; WAAL LIGASE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME MECHANISM; ESCHERICHIA COLI; EVALUATION; IN VITRO STUDY; IN VIVO STUDY; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; SEQUENCE HOMOLOGY; WILD TYPE;

BACTERIA; LIMITED PROTEOLYSIS; O-LINKED GLYCOSYLATION; O-OLIGOSACCHARYLTRANSFERASES;

BACTERIAL PROTEINS; GLYCOSYLATION; GRAM-NEGATIVE BACTERIA; HEXOSYLTRANSFERASES; LIPOPOLYSACCHARIDES; MEMBRANE PROTEINS; SEQUENCE ANALYSIS, PROTEIN;

EID: 84890395031     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt087     Document Type: Article

References (45)

1. Abeyrathne PD, Lam JS. 2007. WaaL of Pseudomonas aeruginosa utilizes ATP in in vitro ligation of O antigen onto lipid A-core. Mol Microbiol. 65:1345-1359.
2. Alaimo C, Catrein I, Morf L, Marolda CL, Callewaert N, Valvano MA, Feldman MF, Aebi M. 2006. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. Embo J. 25:967-976.
3. Anonsen JH, Egge-Jacobsen W, Aas FE, Borud B, Koomey M, Vik A. 2012. Novel protein substrates of the phospho-form modification system in Neisseria gonorrhoeae and their connection to O-linked protein glycosylation. Infect Immun. 80:22-30.
4. Asakura H, Churin Y, Bauer B, Boettcher JP, Bartfeld S, Hashii N, Kawasaki N, Mollenkopf HJ, Jungblut PR, Brinkmann V, et al. 2010. Helicobacter pylori HP0518 affects flagellin glycosylation to alter bacterial motility. Mol Microbiol. 78:1130-1144.
5. Borud B, Aas FE, Vik A, Winther-Larsen HC, Egge-Jacobsen W, Koomey M. 2010. Genetic, structural, and antigenic analyses of glycan diversity in the O-linked protein glycosylation systems of human Neisseria species. J Bacteriol. 192:2816-2829.
6. Castric P. 1995. pilO, a gene required for glycosylation of Pseudomonas aeruginosa pilin. Microbiology. 141(Pt 5):1247-1254.
7. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, Imhaus AF, Martin P, Trellet M, Clary G, et al. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science. 331:778-782.
8. Dykxhoorn DM, St Pierre R, Linn T. 1996. A set of compatible tac promoter expression vectors. Gene. 177:133-136.
9. Faridmoayer A, Fentabil MA, Haurat MF, Yi W, Woodward R, Wang PG, Feldman MF. 2008. Extreme substrate promiscuity of the Neisseria oligosaccharyl transferase involved in protein O-glycosylation. J Biol Chem. 283:34596-34604.
10. Faridmoayer A, Fentabil MA, Mills DC, Klassen JS, Feldman MF. 2007. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J Bacteriol. 189:8088-8098.
11. Feldman MF, Wacker M, Hernandez M, Hitchen PG, Marolda CL, Kowarik M, Morris HR, Dell A, Valvano MA, Aebi M. 2005. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci USA. 102:3016-3021.
12. Fisher CL, Pei GK. 1997. Modification of a PCR-based site-directed mutagenesis method. Biotechniques. 23:570-571, 574.
13. Fletcher CM, Coyne MJ, Villa OF, Chatzidaki-Livanis M, Comstock LE. 2009. A general O-glycosylation system important to the physiology of a major human intestinal symbiont. Cell. 137:321-331.
14. Fontana A, de Laureto PP, Spolaore B, Frare E, Picotti P, Zambonin M. 2004. Probing protein structure by limited proteolysis. Acta Biochim Pol. 51:299-321.
15. Forest KT, Dunham SA, Koomey M, Tainer JA. 1999. Crystallographic structure reveals phosphorylated pilin from Neisseria: Phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol. 31:743-752.
16. Gebhart C, Ielmini MV, Reiz B, Price NL, Aas FE, Koomey M, Feldman MF. 2012. Characterization of exogenous bacterial oligosaccharyltransferases in Escherichia coli reveals the potential for O-linked protein glycosylation in Vibrio cholerae and Burkholderia thailandensis. Glycobiology. 7:962-974.
17. Hart GW, Greis KD, Dong LY, Blomberg MA, Chou TY, Jiang MS, Roquemore EP, Snow DM, Kreppel LK, Cole RN, et al. 1995. O-linked N-acetylglucosamine: The "yin-yang" of Ser/Thr phosphorylation? Nuclear and cytoplasmic glycosylation. Adv Exp Med Biol. 376:115-123.
18. Hegge FT, Hitchen PG, Aas FE, Kristiansen H, Lovold C, Egge-Jacobsen W, Panico M, Leong WY, Bull V, Virji M, et al. 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci USA. 101:10798-10803.
19. Iwashkiw JA, Seper A, Weber BS, Scott NE, Vinogradov E, Stratilo C, Reiz B, Cordwell SJ, Whittal R, Schild S, et al. 2012. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog. 8:e1002758.
20. Iwashkiw JA, Vozza NF, Kinsella RL, Feldman MF. 2013. Pour some sugar on it: The expanding world of bacterial protein O-linked glycosylation. Mol Microbiol. 1:14-28.
21. Jaffee MB, Imperiali B. 2011. Exploiting topological constraints to reveal buried sequence motifs in the membrane-bound N-linked oligosaccharyl transferases. Biochemistry. 50:7557-7567.
22. Kall L, Krogh A, Sonnhammer EL. 2004. A combined transmembrane topology and signal peptide prediction method. J Mol Biol. 338:1027-1036.
23. Ku SC, Schulz BL, Power PM, Jennings MP. 2009. The pilin O-glycosylation pathway of pathogenic Neisseria is a general system that glycosylates AniA, an outer membrane nitrite reductase. Biochem Biophys Res Commun. 378:84-89.
24. Lefebre MD, Valvano MA. 2002. Construction and evaluation of plasmid vectors opti ized for constitutive and regulated gene expression in Burkholderia cepacia complex isolates. Appl EnvironMicrobiol. 68:5956-5964.
25. Marceau M, Forest K, Beretti JL, Tainer J, Nassif X. 1998. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol. 27:705-715.
26. Marolda CL, Feldman MF, Valvano MA. 1999. Genetic organization of the O7-specific lipopolysaccharide biosynthesis cluster of Escherichia coli VW187 (O7:K1). Microbiology. 145(Pt 9):2485-2495.
27. Morand PC, Tattevin P, Eugene E, Beretti JL, Nassif X. 2001. The adhesive property of the type IV pilus-associated component PilC1 of pathogenic Neisseria is supported by the conformational structure of the N-terminal part of the molecule. Mol Microbiol. 40:846-856.
28. Musumeci MA, Hug I, Scott N, Ielmini MV, Foster LJ, Wang PG, Feldman MF. 2013. In vitro activity of Neisseria meningitidis PglL O- oligosaccharyltransferase with diverse synthetic lipid donors and a UDP-activated sugar. J Biol Chem. 288:10578-10587.
29. Musumeci MA, Ielmini MV, Feldman MF. 2013. In vitro glycosylation assay for bacterial oligosaccharyltransferases. Methods Mol Biol. 1022:161-171.
30. Perez JM, McGarry MA, Marolda CL, Valvano MA. 2008. Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol Microbiol. 70:1424-1440.
31. Power PM, Seib KL, Jennings MP. 2006. Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem Biophys Res Commun. 347:904-908.
32. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM. 2009. Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc Natl Acad Sci USA. 106:1760-1765.
33. Schild S, Lamprecht AK, Reidl J. 2005. Molecular and functional characterization of O antigen transfer in Vibrio cholerae. J Biol Chem. 280:25936-25947.
34. Schulz BL, Jen FE, Power PM, Jones CE, Fox KL, Ku SC, Blanchfield JT, Jennings MP. 2013. Identification of bacterial protein O- oligosaccharyltransferases and their glycoprotein substrates. PLoS One. 8:e62768.
35. Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Boucherie H, Mann M. 1996. Linking genome and proteome by mass spectrometry: Large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA. 93:14440-14445.
36. Stimson E, Virji M, Barker S, Panico M, Blench I, Saunders J, Payne G, Moxon ER, Dell A, Morris HR. 1996. Discovery of a novel protein modification: Alpha-glycerophosphate is a substituent of meningococcal pilin. Biochem J. 316(Pt 1):29-33.
37. Stimson E, Virji M, Makepeace K, Dell A, Morris HR, Payne G, Saunders JR, Jennings MP, Barker S, Panico M, et al. 1995. Meningococcal pilin: A glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol. 17:1201-1214.
38. Twine SM, Reid CW, Aubry A, McMullin DR, Fulton KM, Austin J, Logan SM. 2009. Motility and flagellar glycosylation in Clostridium difficile. J Bacteriol. 191:7050-7062.
39. Vik A, Aas FE, Anonsen JH, Bilsborough S, Schneider A, Egge-Jacobsen W, Koomey M. 2009. Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae. Proc Natl Acad Sci USA. 106:4447-4452.
40. Voisin S, Kus JV, Houliston S, St-Michael F, Watson D, Cvitkovitch DG, Kelly J, Brisson JR, Burrows LL. 2007. Glycosylation of Pseudomonas aeruginosa strain Pa5196 type IV pilins with mycobacterium-like alpha-1,5-linked d-Araf oligosaccharides. J Bacteriol. 189:151-159.
41. Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM, North SJ, Panico M, Morris HR, Dell A, Wren BW, et al. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science. 298:1790-1793.
42. Wang N, Mackenzie L, De Souza AG, Zhong H, Goss G, Li L. 2007. Proteome profile of cytosolic component of zebrafish liver generated by LC-ESI MS/ MS combined with trypsin digestion and microwave-assisted acid hydrolysis. J Proteome Res. 6:263-272.
43. Warren MJ, Jennings MP. 2003. Identification and characterization of pptA: -Rfaut Gene Involved In The Phase-variable Expression Of Phosphorylcholine On Pili Of Neisseria Meningitidis Gene Involved In The Phase-variable Expression Of Phosphorylcholine On Pili Of Neisseria Meningitidis. Infect Immun. 71:6892-6898.
44. Weiser JN, Goldberg JB, Pan N, Wilson L, Virji M. 1998. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect Immun. 66:4263-4267.
45. Young NM, Brisson JR, Kelly J, Watson DC, Tessier L, Lanthier PH, Jarrell HC, Cadotte N, St Michael F, Aberg E, et al. 2002. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem. 277:42530-42539.