N-glycosylation of campylobacter jejuni surface proteins promotes bacterial fitness

Infection and Immunity

Volumn 81, Issue 5, 2013, Pages 1674-1682

  Alemka, Abofu ^a,c   Nothaft, Harald ^a   Zheng, Jing ^b   Szymanski, Christine M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c Innovotech Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; METALLOPROTEINASE; SERINE PROTEINASE; TRYPSIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL VIABILITY; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; HEAT TREATMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN GLYCOSYLATION;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CECUM; CHICKENS; COLONY COUNT, MICROBIAL; GLYCOSYLATION; HEXOSYLTRANSFERASES; MEMBRANE PROTEINS; PEPTIDE HYDROLASES; POLYSACCHARIDES, BACTERIAL; POULTRY DISEASES;

EID: 84877799105     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01370-12     Document Type: Article

References (46)

1. Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ. 2008. Host-pathogen interactions in Campylobacter infections: the host perspective. Clin. Microbiol. Rev. 21:505-518.
2. Young KT, Davis LM, Dirita VJ. 2007. Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 5:665-679.
3. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. 2008. Mucins in the mucosal barrier to infection. Mucosal Immunol. 1:183-197.
4. Alemka A, Clyne M, Shanahan F, Tompkins T, Corcionivoschi N, Bourke B. 2010. Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect. Immun. 78:2812-2822.
5. Van Deun K, Pasmans F, Ducatelle R, Flahou B, Vissenberg K, Martel A, Van den Broeck W, Van Immerseel F, Haesebrouck F. 2008. Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut. Vet. Microbiol. 130:285-297.
6. Szymanski CM, Wren BW. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
7. Nothaft H, Szymanski CM. 2011. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8:765-778.
8. Schwarz F, Lizak C, Fan YY, Fleurkens S, Kowarik M, Aebi M. 2011. Relaxed acceptor site specificity of bacterial oligosaccharyltransferase in vivo. Glycobiology 21:45-54.
9. Szymanski CM, Yao R, Ewing CP, Trust TJ, Guerry P. 1999. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32:1022-1030.
10. Kelly J, Jarrell H, Millar L, Tessier L, Fiori LM, Lau PC, Allan B, Szymanski CM. 2006. Biosynthesis of the N-linked glycan in Campylobacter jejuni and addition onto protein through block transfer. J. Bacteriol. 188:2427-2434.
11. Scott NE, Parker BL, Connolly AM, Paulech J, Edwards AV, Crossett B, Falconer L, Kolarich D, Djordjevic SP, Hojrup P, Packer NH, Larsen MR, Cordwell SJ. 2011. 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 10:M000031-MCP000201.
12. Hendrixson DR, DiRita VJ. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52:471-484.
13. Szymanski CM, Burr DH, Guerry P. 2002. Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70:2242-2244.
14. van Sorge NM, Bleumink NM, van Vliet SJ, Saeland E, van der Pol WL, van Kooyk Y, van Putten JP. 2009. N-glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL. Cell. Microbiol. 11:1768-1781.
15. Palyada K, Threadgill D, Stintzi A. 2004. Iron acquisition and regulation in Campylobacter jejuni. J. Bacteriol. 186:4714-4729.
16. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, Jagels K, Karlyshev AV, Moule S, Pallen MJ, Penn CW, Quail MA, Rajandream MA, Rutherford KM, van Vliet AH, Whitehead S, Barrell BG. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
17. Scott NE, Nothaft H, Edwards AV, Labbate M, Djordjevic SP, Larsen MR, Szymanski CM, Cordwell SJ. 2012. Modification of the Campylobacter jejuni N-linked glycan by EptC protein-mediated addition of phosphoethanolamine. J. Biol. Chem. 287:29384-29396.
18. Waseh S, Hanifi-Moghaddam P, Coleman R, Masotti M, Ryan S, Foss M, MacKenzie R, Henry M, Szymanski CM, Tanha J. 2010. Orally administered P22 phage tailspike protein reduces salmonella colonization in chickens: prospects of a novel therapy against bacterial infections. PLoS One 5:e13904. doi:10.1371/journal.pone.0013904.
19. Korlath JA, Osterholm MT, Judy LA, Forfang JC, Robinson RA. 1985. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J. Infect. Dis. 152:592-596.
20. Nothaft H, Liu X, McNally DJ, Li J, Szymanski CM. 2009. Study of free oligosaccharides derived from the bacterial N-glycosylation pathway. Proc. Natl. Acad. Sci. U. S. A. 106:15019-15024.
21. Watson RO, Galan JE. 2008. Campylobacter jejuni survives within epithelial cells by avoiding delivery to lysosomes. PLoS Pathog. 4:e14. doi:10.1371/journal.ppat.0040014.
22. Lake-Bakaar G, McKavanagh S, Rubio CE, Epstein O, Summerfield JA. 1980. Measurement of trypsin in duodenal juice by radioimmunoassay. Gut 21:402-407.
23. Kahns AH, Buur A, Bundgaard H. 1993. Prodrugs of peptides. 18. Synthesis and evaluation of various esters of desmopressin (dDAVP). Pharm. Res. 10:68-74.
24. 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 diverseOantigen lipopolysaccharide structures in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102:3016-3021.
25. Schilling O, Huesgen PF, Barre O, Auf dem Keller U, Overall CM. 2011. Characterization of the prime and non-prime active site specificities of proteases by proteome-derived peptide libraries and tandem mass spectrometry. Nat. Protoc. 6:111-120.
26. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M. 2005. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell Proteomics 4:1265-1272.
27. Shinoda K, Tomita M, Ishihama Y. 2010. emPAI Calc-for the estimation of protein abundance from large-scale identification data by liquid chromatography-tandem mass spectrometry. Bioinformatics 26:576-577.
28. Alemka A, Whelan S, Gough R, Clyne M, Gallagher ME, Carrington SD, Bourke B. 2010. Purified chicken intestinal mucin attenuates Campylobacter jejuni pathogenicity in vitro. J. Med. Microbiol. 59:898-903.
29. Hogan SP, Seidu L, Blanchard C, Groschwitz K, Mishra A, Karow ML, Ahrens R, Artis D, Murphy AJ, Valenzuela DM, Yancopoulos GD, Rothenberg ME. 2006. Resistin-like molecule beta regulates innate colonic function: barrier integrity and inflammation susceptibility. J. Allergy Clin. Immunol. 118:257-268.
30. Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM, North SJ, Panico M, Morris HR, Dell A, Wren BW, Aebi M. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790-1793.
31. Jackson DN, Davis B, Tirado SM, Duggal M, van Frankenhuyzen JK, Deaville D, Wijesinghe MA, Tessaro M, Trevors JT. 2009. Survival mechanisms and culturability of Campylobacter jejuni under stress conditions. Antonie Van Leeuwenhoek 96:377-394.
32. Pryjma M, Apel D, Huynh S, Parker CT, Gaynor EC. 2012. FdhTUmodulated formate dehydrogenase expression and electron donor availability enhance recovery of Campylobacter jejuni following host cell infection. J. Bacteriol. 194:3803-3813.
33. Liu X, Gao B, Novik V, Galan JE. 2012. Quantitative proteomics of intracellular Campylobacter jejuni reveals metabolic reprogramming. PLoS Pathog. 8:e1002562. doi:10.1371/journal.ppat.1002562.
34. Kadhim K, Zuki ABZ, Noordin MM, Babjee SMA, Zamri-Saad M. 2011. Activities of amylase, trypsin and chymotrypsin of pancreas and small intestinal contents in the red jungle fowl and broiler breed. Afr. J. Biotechnol. 10:108-115.
35. Iji PA, Saki A, Tivey DR. 2001. Body and intestinal growth of broiler chicks on a commercial starter diet. 3. Development and characteristics of tryptophan transport. Br. Poult. Sci. 42:523-529.
36. Gielda LM, Dirita VJ. 2012. Zinc competition among the intestinal microbiota. mBio 3(4):e00171-12. doi:10.1128/mBio.00171-12.
37. Connell S, Meade KG, Allan B, Lloyd AT, Kenny E, Cormican P, Morris DW, Bradley DG, O'Farrelly C. 2012. Avian resistance to Campylobacter jejuni colonization is associated with an intestinal immunogene expression signature identified by mRNA sequencing. PLoS One 7:e40409. doi: 10.1371/journal.pone.0040409.
38. Jones MA, Marston KL, Woodall CA, Maskell DJ, Linton D, Karlyshev AV, Dorrell N, Wren BW, Barrow PA. 2004. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72:3769-3776.
39. Karlyshev AV, Everest P, Linton D, Cawthraw S, Newell DG, Wren BW. 2004. The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150:1957-1964.
40. Ghareeb K, Awad WA, Mohnl M, Porta R, Biarnes M, Bohm J, Schatzmayr G. 2012. Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poult. Sci. 91:1825-1832.
41. Kergourlay G, Messaoudi S, Dousset X, Prevost H. 2012. Genome sequence of Lactobacillus salivarius SMXD51, a potential probiotic strain isolated from chicken cecum, showing anti-campylobacter activity. J. Bacteriol. 194:3008-3009.
42. Zhang G, Ma L, Doyle MP. 2007. Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and Salmonella. J. Food Prot. 70:867-873.
43. Sell JL, Angel CR, Piquer FJ, Mallarino EG, al-Batshan HA. 1991. Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poult. Sci. 70:1200-1205.
44. Holt PR, Tierney AR, Kotler DP. 1985. Delayed enzyme expression: a defect of aging rat gut. Gastroenterology 89:1026-1034.
45. Gross BJ, Swoboda JG, Walker S. 2008. A strategy to discover inhibitors of O-linked glycosylation. J. Am. Chem. Soc. 130:440-441.
46. Han I, Kudlow JE. 1997. Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17:2550-2558.