Adhesion to host cells is an important step in pathogenesis of Campylobacter jejuni, which is the most prevalent bacterial cause of human gastroenteritis worldwide. In contrast to other bacteria such as E. coli and Salmonella, adherence of C. jejuni is not mediated by fimbria or pili. A number of C. jejuni adhesion-related factors have been described. However, the results obtained by different researchers in different laboratories are often contradictory and inconclusive, with only some of the factors described being confirmed as true adhesins. In this review, we present the current state of studies on the mechanisms of attachment of C. jejuni to host cells.
1. P. Klemm M.A. Schembri 2000 Bacterial adhesins: function and structure Int J Med Microbiol 290 27–35.
2. J. Pizarro-Cerda P. Cossart 2006 Bacterial adhesion and entry into host cells Cell 124 715–727.
3. H.H. Niemann W.D. Schubert et al.2004 Adhesins and invasins of pathogenic bacteria: a structural view Microbes Infect 6 101–112.
4. K.A. Kline S. Falker et al.2009 Bacterial adhesins in host-microbe interactions Cell Host Microbe 5 580–592.
5. G.M. Ruiz-Palacios 2007 The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken Clin Infect Dis 44 701–703.
6. C.K. Olson S. Ethelberg et al.2008 Epidemiology of Campylobacter jejuni infections in industrialized nations I. Nachamkin C. Szymanski M.J. Blaser Campylobacter ASM Press Washigton, DC, USA 163–189.
7. B.M. Allos 2001 Campylobacter jejuni infections: update on emerging issues and trends Clin Infect Dis 32 1201–6.
8. K.T. Young L.M. Davis et al.2007 Campylobacter jejuni: molecular biology and pathogenesis Nat Rev Microbiol 5 665–679.
9. B. Jeon W.T. Muraoka et al.2010 Advances in Campylobacter biology and implications for biotechnological applications Microb Biotechnol 3 242–258.
10. R. Janssen K.A. Krogfelt et al.2008 Host-pathogen interactions in Campylobacter infections: the host perspective Clin Microbiol Rev 21 505–518.
11. R.L. Ziprin C.R. Young et al.1999 The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein Avian Dis 43 586–589.
12. L. Hu D.J. Kopecko 1999 Campylobacter jejuni 81–176 associates with microtubules and dynein during invasion of human intestinal cells Infect Immun 67 4171–4182.
13. J.L. Fauchere A. Rosenau et al.1986 Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces Infect Immun 54 283–287.
14. A.W. van der Velden A.J. Baumler et al.1998 Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice Infect Immun 66 2803–2808.
15. J.P. Nougayrede P.J. Fernandes et al.2003 Adhesion of enteropathogenic Escherichia coli to host cells Cell Microbiol 5 359–372.
16. M.R. Monteville J.E. Yoon et al.2003 Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization Microbiology 149 153–65.
17. R.C. Flanagan J.M. Neal-McKinney et al.2009 Examination of Campylobacter jejuni putative adhesins leads to the identification of a new protein, designated FlpA, required for chicken colonization Infect Immun 77 2399–2407.
18. M.E. Konkel C.L. Larson et al.2010 Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence J Bacteriol 192 68–76.
19. M.E. Konkel S.G. Garvis et al.1997 Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni Mol Microbiol 24 953–963.
20. S. Jin Y.C. Song et al.2003 JlpA of Campylobacter jejuni interacts with surface-exposed heat shock protein 90alpha and triggers signalling pathways leading to the activation of NF-kappaB and p38 MAP kinase in epithelial cells Cell Microbiol 5 165–174.
21. R. Pankov K.M. Yamada 2002 Fibronectin at a glance J Cell Sci 115 3861–3863.
22. M.E. Konkel J.E. Christensen et al.2005 Identification of a fibronectin-binding domain within the Campylobacter jejuni CadF protein Mol Microbiol 57 1022–1035.
23. S. Jin A. Joe et al.2001 JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells Mol Microbiol 39 1225–1236.
24. V. Novik D. Hofreuter et al.2010 Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells Infect Immun 78 3540–3553.
25. S.S. Ashgar N.J. Oldfield et al.2007 CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut J Bacteriol 189 1856–1865.
26. M. Oakland B. Jeon et al.2011 Functional characterization of a lipoprotein-encoding operon in Campylobacter jejuni PLoS One 6 e20084.
27. I. Moser W. Schroeder et al.1997 Campylobacter jejuni major outer membrane protein and a 59-kDa protein are involved in binding to fibronectin and INT 407 cell membranes FEMS Microbiol Lett 157 233–238.
28. Q. Zhang J.C. Meitzler et al.2000 Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein Infect Immun 68 5679–5689.
29. F. Goulhen E. De et al.2004 Functional refolding of the Campylobacter jejuni MOMP (major outer membrane protein) porin by GroEL from the same species Biochem J 378 851–856.
30. R. Yao D.H. Burr et al.1994 Isolation of motile and non-motile insertional mutants of Campylobacter jejuni: the role of motility in adherence and invasion of eukaryotic cells Mol Microbiol 14 883–893.
31. D.G. Newell H. McBride et al.1985 Investigations on the role of flagella in the colonization of infant mice with Campylobacter jejuni and attachment of Campylobacter jejuni to human epithelial cell lines J Hyg (Lond) 95 217–227.
32. M.E. Konkel J.D. Klena et al.2004 Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus J Bacteriol 186 3296–3303.
33. Y.C. Song S. Jin et al.2004 FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion Mol Microbiol 53 541–553.
34. E. McSweegan R.I. Walker 1986 Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates Infect Immun 53 141–148.
35. C.C. Grant M.E. Konkel et al.1993 Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures Infect Immun 61 1764–1771.
36. T.M. Wassenaar N.M. Bleumink-Pluym et al.1991 Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion EMBO J 10 2055–2061.
37. Y. Yanagawa M. Takahashi et al.1994 The role of flagella of Campylobacter jejuni in colonization in the intestinal tract in mice and the cultured-cell infectivity Nihon Saikingaku Zasshi 49 395–403.
38. A. Salamaszynska-Guz D. Klimuszko 2008 Functional analysis of the Campylobacter jejuni cj0183 and cj0588 genes Curr Microbiol 56 592–596.
39. M.C. Martino R.A. Stabler et al.2001 Helicobacter pylori poreforming cytolysin orthologue TlyA possesses in vitro hemolytic activity and has a role in colonization of the gastric mucosa Infect Immun 69 1697–1703.
40. Z.H. Pei R.T. Ellison 3rd et al.1991 Identification, purification, and characterization of major antigenic proteins of Campylobacter jejuni J Biol Chem 266 16363–16369.
41. M. Kervella J.M. Pages et al.1993 Isolation and characterization of two Campylobacter glycine-extracted proteins that bind to HeLa cell membranes Infect Immun 61 3440–3448.
42. Z. Pei M.J. Blaser 1993 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 18717–18725.
43. Z. Pei C. Burucoa et al.1998 Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice Infect Immun 66 938–943.
44. R. Leon-Kempis Mdel E. Guccione et al.2006 The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids Mol Microbiol 60 1262–1275.
45. L. Anton K. Majander et al.2010 Two distinct regions in the model protein Peb1 are critical for its heterologous transport out of Escherichia coli Microb Cell Fact 9 97.
46. D. Linton E. Allan et al.2002 Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni Mol Microbiol 43 497–508.
47. I. Batisson M.P. Guimond et al.2003 Characterization of the novel factor paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli Infect Immun 71 4516–4525.
48. K.M. Peterson J.J. Mekalanos 1988 Characterization of the EscVibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization Infect Immun 56 2822–2829.
49. E.S. Rangarajan S. Bhatia et al.2007 Structural context for protein N-glycosylation in bacteria: The structure of PEB3, an adhesin from Campylobacter jejuni Protein Sci 16 990–995.
50. T. Min M. Vedadi et al.2009 Specificity of Campylobacter jejuni adhesin PEB3 for phosphates and structural differences among its ligand complexes Biochemistry 48 3057–3067.
51. H. Asakura M. Yamasaki et al.2007 Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni FEMS Microbiol Lett 275 278–285.
52. K.M. Rathbun J.E. Hall et al.2009 Cj0596 is a periplasmic peptidyl prolyl cis-trans isomerase involved in Campylobacter jejuni motility, invasion, and colonization BMC Microbiol 9 160.
53. K. Kelle J.M. Pages et al.1998 A putative adhesin gene cloned from Campylobacter jejuni Res Microbiol 149 723–733.
54. M. Aspholm F.O. Olfat et al.2006 SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans PLoS Pathog 2 e110.
55. A. Magalhaes C.A. Reis 2010 Helicobacter pylori adhesion to gastric epithelial cells is mediated by glycan receptors Braz J Med Biol Res 43 611–618.
56. C.J. Day J. Tiralongo et al.2009 Differential carbohydrate recognition by Campylobacter jejuni strain 11168: influences of temperature and growth conditions PLoS One 4 e4927.
57. N.M. Young J.R. Brisson 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.
58. C.M. Szymanski D.H. Burr et al.2002 Campylobacter protein glycosylation affects host cell interactions Infect Immun 70 2242–2244.
59. D.R. Hendrixson V.J. DiRita 2004 Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract Mol Microbiol 52 471–484.
60. A.V. Karlyshev P. Everest et al.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.
61. N.M. van Sorge N.M. Bleumink et al.2009 N-glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL Cell Microbiol 11 1768–1781.
62. N.M. Iovine S. Pursnani et al.2008 Reactive nitrogen species contribute to innate host defense against Campylobacter jejuni Infect Immun 76 986–993.
63. Y. van Kooyk G.A. Rabinovich 2008 Protein-glycan interactions in the control of innate and adaptive immune responses Nat Immunol 9 593–601.
64. G. Lugo-Villarino D. Hudrisier et al.2011 C-type lectins with a sweet spot for Mycobacterium tuberculosis Eur J Microbiol Immunol 1 25–40.
65. P.R. Crocker 2005 Siglecs in innate immunity Curr Opin Pharmacol 5 431–437.
66. T. Avril E.R. Wagner et al.2006 Sialic acid-binding immunoglobulin-like lectin 7 mediates selective recognition of sialylated glycans expressed on Campylobacter jejuni lipooligosaccharides Infect Immun 74 4133–4141.
67. A.V. Karlyshev O.L. Champion et al.2005 Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses Mol Microbiol 55 90–103.
68. A.V. Karlyshev D. Linton et al.2000 Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity Mol Microbiol 35 529–541.
69. A.V. Karlyshev M.V. McCrossan et al.2001 Demonstration of polysaccharide capsule in Campylobacter jejuni using electron microscopy Infect Immun 69 5921–5924.
70. D.J. Bacon C.M. Szymanski et al.2001 A phase-variable capsule is involved in virulence of Campylobacter jejuni 81–176 Mol Microbiol 40 769–777.
71. B.M. Bachtiar P.J. Coloe et al.2007 Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions FEMS Immunol Med Microbiol 49 149–154.
72. A.V. Karlyshev B.W. Wren et al.2008 Campylobacter jejuni capsular polysaccharide I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC, USA 505–521.
73. G.M. Ruiz-Palacios L.E. Cervantes et al.2003 Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection J Biol Chem 278 14112–14120.
74. C.A. Weijers M.C. Franssen et al.2008 Glycosyltransferase-catalyzed synthesis of bioactive oligosaccharides Biotechnol Adv 26 436–456.
75. M. Christner G.C. Franke et al.2010 The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin Mol Microbiol 75 187–207.