Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen campylobacter jejuni

Journal of Microbiological Methods

Volumn 95, Issue 1, 2013, Pages 8-23

  Backert, Steffen ^a   Hofreuter, Dirk ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cellular invasion; Molecular pathogenesis; Signalling; Virulence

Indexed keywords

SMALL INTERFERING RNA;

BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CAMPYLOBACTER JEJUNI; CELL ADHESION; COLONY FORMING UNIT; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENTAMICIN PROTECTION ASSAY; GTPASE ACTIVATION ASSAY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; INTERNALIZATION; INTRACELLULAR SURVIVAL ASSAY; LIVE DEAD STAINING; LUCIFERASE REPORTER ASSAY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGICAL PARAMETERS; MULTIPLICITY OF INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TRANSCELLULAR CELL MIGRATION; TRANSIENT EXPRESSION; TRANSWELL ASSAY;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; NEGIBACTERIA;

CELLULAR INVASION; MOLECULAR PATHOGENESIS; SIGNALLING; VIRULENCE;

ANIMALS; BACTERIAL ADHESION; BACTERIOLOGICAL TECHNIQUES; CAMPYLOBACTER JEJUNI; CYTOPLASM; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; LOCOMOTION; MICROBIAL VIABILITY; MOLECULAR BIOLOGY;

EID: 84884169299     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2013.06.031     Document Type: Review

References (188)

1. Ahmed I.H., Manning G., Wassenaar T.M., Cawthraw S., Newell D.G. Identification of genetic differences between two Campylobacter jejuni strains with different colonization potentials. Microbiology 2002, 148:1203-1212.
2. Alemka A., Clyne M., Shanahan F., Tompkins T., Corcionivoschi N., Bourke B. Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect. Immun. 2010, 78:2812-2822.
3. Alemka A., Corcionivoschi N., Bourke B. Defense and adaptation: the complex inter-relationship between Campylobacter jejuni and mucus. Front. Cell. Infect. Microbiol. 2012, 2:15.
4. Allos B.M. Campylobacter jejuni Infections: update on emerging issues and trends. Clin. Infect. Dis. 2001, 32:1201-1206.
5. Apel D., Ellermeier J., Pryjma M., Dirita V.J., Gaynor E.C. Characterization of Campylobacter jejuni RacRS reveals roles in the heat shock response, motility, and maintenance of cell length homogeneity. J. Bacteriol. 2012, 194:2342-2354.
6. Asakura H., Yamasaki M., Yamamoto S., Igimi S. Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol. Lett. 2007, 275:278-285.
7. Ashgar S.S., Oldfield N.J., Woolridge K.G., Jones M.A., Irving G.J., Turner D.P., Ala'Aldeen D.A. CapA, an autotransporter protein of Campylobacter jejuni mediates association with human epithelial cells and colonization of the chicken gut. J. Bacteriol. 2007, 189:1856-1865.
8. Babakhani F.K., Bradley G.A., Joens L.A. Newborn piglet model for campylobacteriosis. Infect. Immun. 1993, 61:3466-3475.
9. Bachtiar B.M., Coloe P.J., Fry B.N. Knockout mutagenesis of the KpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium host interactions. FEMS Immunol. Med. Microbiol. 2007, 49:149-154.
10. Bacon D.J., Alm R.A., Burr D.H., Hu L., Kopecko D.J., Ewing C.P., Trust T.J., Guerry P. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 2000, 68:4384-4390.
11. Bacon D.J., Szymanski C.M., Burr D.H., Silver R.P., Alm R.A., Guerry P. A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 2001, 40:769-777.
12. Bæk K.T., Vegge C.S., Brøndsted L. HtrA chaperone activity contributes to host cell binding in Campylobacter jejuni. Gut Pathog. 2011, 3:13.
13. Balkovetz D.F., Katz J. Bacterial invasion by a paracellular route: divide and conquer. Microbes Infect. 2003, 5:613-619.
14. Beery J.T., Hugdahl M.B., Doyle M.P. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 1988, 54:2365-2370.
15. Behrens I., Stenberg P., Artursson P., Kissel T. Transport of lipophilic drug molecules in a new mucus-secreting cell culture model based on HT29-MTX cells. Pharm. Res. 2001, 18:1138-1145.
16. Beltinger J., del Buono J., Skelly M.M., Thornley J., Spiller R.C., Stack W.A., Hawkey C.J. Disruption of colonic barrier function and induction of mediator release by strains of Campylobacter jejuni that invade epithelial cells. World J. Gastroenterol. 2008, 14:7345-7352.
17. Bereswill S., Fischer A., Plickert R., Haag L.M., Otto B., Kühl A.A., Dasti J.I., Zautner A.E., Muñoz M., Loddenkemper C., Gross U., Göbel U.B., Heimesaat M.M. Novel murine infection models provide deep insights into the "menage a trois" of Campylobacter jejuni, microbiota and host innate immunity. PLoS One 2011, 6:e20953.
18. Biswas D., Itoh K., Sasakawa C. Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol. Med. Microbiol. 2000, 29:203-211.
19. Biswas D., Itoh K., Sasakawa C. Role of microfilaments and microtubules in the invasion of INT-407 cells by Campylobacter jejuni. Microbiol. Immunol. 2003, 47:469-473.
20. Biswas D., Fernando U., Reimau C., Willson P., Potter A., Allau B. Effect of cytolethal distending toxin of Campylobacter jejuni on adhesion and internalization in cultured cells and in colonization of the chicken gut. Avian Dis. 2006, 50:586-593.
21. Black R.E., Levine M.M., Clements M.L., Hughes T.P., Blaser M.J. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 1988, 157:472-479.
22. Boehm M., Krause-Gruszczynska M., Rohde M., Tegtmeyer N., Takahashi S., Oyarzabal O.A., Backert S. Major host factors involved in epithelial cell invasion of Campylobacter jejuni: role of fibronectin, integrin beta1, FAK, Tiam-1, DOCK180 in activating Rho GTPase Rac1. Front. Cell. Infect. Microbiol. 2011, 1:17.
23. Boehm M., Hoy B., Rohde M., Tegtmeyer N., Baek K.T., Oyarzabal O.A., Brondsted L., Wessler S., Backert S. Rapid paracellular transmigration of Campylobacter jejuni across polarized epithelial cells without affecting TER: role of proteolytic-active HtrA cleaving E-cadherin but not fibronectin. Gut Pathog. 2012, 4:3.
24. Boquet P., Lemichez E. Bacterial virulence factors targeting Rho GTPases: parasitism or symbiosis?. Trends Cell Biol. 2003, 13:238-246.
25. Bouwman L.I., Niewold P., van Putten J.P. Basolateral invasion and trafficking of Campylobacter jejuni in polarized epithelial cells. PLoS One 2013, 8:e54759.
26. Brás A.M., Ketley J.M. Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol. Lett. 1999, 179:209-215.
27. Brøndsted L., Andersen M.T., Parker M., Jørgensen K., Ingmer H. The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Appl. Environ. Microbiol. 2005, 71:3205-3212.
28. Buelow D.R., Christentsen J.E., Neal-McKinney J.M., Konkel M.E. Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI. Mol. Microbiol. 2011, 80:1296-1312.
29. Byrne C.M., Clyne M., Bourke B. Campylobacter jejuni adhere to and invade chicken intestinal epithelial cells in vitro. Microbiology 2007, 153:561-569.
30. Caldwell M.B., Guerry P., Lee E.C., Burans J.P., Walker R.I. Reversible expression of flagella in Campylobacter jejuni. Infect. Immun. 1985, 50:941-943.
31. Cameron A., Frirdich E., Huynh S., Parker C.T., Gaynor E.C. Hyperosmotic stress response of Campylobacter jejuni. J. Bacteriol. 2012, 194:6116-6130.
32. Candon H.L., Allan B.J., Fraley C.D., Gaynor E.C. Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J. Bacteriol. 2007, 189:8099-8108.
33. Chen M.L., Ge Z., Fox J.G., Schauer D.B. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect. Immun. 2006, 74:6581-6589.
34. Christensen J.E., Pacheco S.A., Konkel M.E. Identification of a Campylobacter jejuni-secreted protein required for maximal invasion of host cells. Mol. Microbiol. 2009, 73:650-662.
35. Coote J.G., Stewart-Tull D.E., Owen R.J., Bolton F.J., Siemer B.L., Candlish D., Thompson D.H., Wardlaw A.C., On S.L., Candlish A., Billcliffe B., Jordan P.J., Kristiansen K., Borman P. Comparison of virulence-associated in vitro properties of typed strains of Campylobacter jejuni from different sources. J. Med. Microbiol. 2007, 56:722-732.
36. Dasti J.I., Tareen A.M., Lugert R., Zautner A.E., Gross U. Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int. J. Med. Microbiol. 2010, 300:205-211.
37. Day W.A., Sajecki J.L., Pitts T.M., Joens L.A. Role of catalase in Campylobacter jejuni intracellular survival. Infect. Immun. 2000, 68:6337-6345.
38. De Melo M.A., Gabbiani G., Pechere J.C. Cellular events and intracellular survival of Campylobacter jejuni during infection of Hep-2 cells. Infect. Immun. 1989, 57:2214-2222.
39. Drozd M., Gangaiah D., Liu Z., Rajashekara G. Contribution of TAT system translocated PhoX to Campylobacter jejuni phosphate metabolism and resilience to environmental stresses. PLoS One 2011, 6:e26336.
40. Ellson C.D., Andrews S., Stephens L.R., Hawkins P.T. The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 2002, 115:1099-1105.
41. Elmi A., Watson E., Sandu P., Gundogdu O., Mills D.C., Inglis N.F., Manson E., Imrie L., Bajaj-Elliott M., Wren B.W., Smith D.G., Dorrell N. Campylobacter jejuni outer membrane vesicles play an important role in bacterial interactions with human intestinal epithelial cells. Infect. Immun. 2012, 80:4089-4098.
42. Elsinghorst E.A. Measurement of invasion by gentamicin resistance. Methods Enzymol. 1994, 236:405-420.
43. Eucker T.P., Konkel M.E. The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling. Cell. Microbiol. 2012, 14:226-238.
44. Everest P.H., Goossens H., Butzler J.P., Lloyd D., Knutton S., Ketley J.M., Williams P.H. Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J. Med. Microbiol. 1992, 37:319-325.
45. Fauchere J.L., Rosenau A., Veron M., Moyen E.N., Richard S., Pfister A. Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces. Infect. Immun. 1986, 54:283-287.
46. Fearnley C., Manning G., Bagnall M., Javed M.A., Wassenaar T.M., Newell D.G. Identification of hyperinvasive Campylobacter jejuni strains isolated from poultry and human clinical sources. J. Med. Microbiol. 2008, 57:570-580.
47. Ferrero R.L., Lee A. Motility of Campylobacter jejuni in a viscous environment: comparison with conventional rod-shaped bacteria. J. Gen. Microbiol. 1988, 134:53-59.
48. Fields J.A., Thompson S.A. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J. Bacteriol. 2008, 190:3411-3416.
49. Flanagan R.C., Neal-McKinney J.M., Dhillon A.S., Miller W.G., Konkel M.E. Examination of Campylobacter jejuni putative adhesins leads to the identification of a new protein, designated FlpA, required for chicken colonization. Infect. Immun. 2009, 77:2399-23407.
50. Fouts D.E., Mongodin E.F., Mandrell R.E., Miller W.G., Rasko D.A., Ravel J., Brinkac L.M., DeBoy R.T., Parker C.T., Daugherty S.C., Dodson R.J., Durkin A.S., Madupu R., Sullivan S.A., Shetty J.U., Ayodeji M.A., Shvartsbeyn A., Schatz M.C., Badger J.H., Fraser C.M., Nelson K.E. Major structural differences and novel potential virulence mechanisms from the genomes of multiple campylobacter species. PLoS Biol. 2005, 3:e15.
51. Fry B.N., Feng S., Chen Y.Y., Newell D.G., Coloe P.J., Korolik V. The galE gene of Campylobacter jejuni is involved in lipopolysaccharide synthesis and virulence. Infect. Immun. 2000, 68:2594-2601.
52. Gaasbeek E.J., Wagenaar J.A., Guilhabert M.R., Wosten M.M., van Putten J.P., van der Graaf-van Bloois L., Parker C.T., van der Wal F.J. A DNase encoded by integrated element CJIE1 inhibits natural transformation of Campylobacter jejuni. J. Bacteriol. 2009, 191:2296-2306.
53. Gaasbeek E.J., Wagenaar J.A., Guilhabert M.R., van Putten J.P., Parker C.T., van der Wal F.J. Nucleases encoded by the integrated elements CJIE2 and CJIE4 inhibit natural transformation of Campylobacter jejuni. J. Bacteriol. 2010, 192:936-941.
54. Gangaiah D., Liu Z., Arcos J., Kassem I.I., Sanad Y., Torrelles J.B., Rajashekara G. Polyphosphate kinase 2: a novel determinant of stress responses and pathogenesis in Campylobacter jejuni. PLoS One 2010, 5:e12142.
55. Gaynor E.C., Cawthraw S., Manning G., MacKichan J.K., Falkow S., Newell D.G. The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J. Bacteriol. 2004, 186:503-517.
56. Gaynor E.C., Wells D.H., MacKichan J.K., Falkow S. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol. Microbiol. 2005, 56:8-27.
57. Gilbert M., Karwaski M.F., Bernatchez S., Young N.M., Taboada E., Michniewicz J., Cunningham A.M., Wakarchuk W.W. The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen, Campylobacter jejuni. J. Biol. Chem. 2002, 277:327-337.
58. Golden N.J., Acheson D.W. Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect. Immun. 2002, 70:1761-1771.
59. Goon S., Ewing C.P., Lorenzo M., Pattarini D., Majam G., Guerry P.A. sigma28-regulated nonflagella gene contributes to virulence of Campylobacter jejuni 81-176. Infect. Immun. 2006, 74:769-772.
60. Grant C.C.R., Konkel M.E., Cieplak W., Tompkins L.S. Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect. Immun. 1993, 61:1764-1771.
61. Gripp E., Hlahla D., Didelot X., Kops F., Maurischat S., Tedin K., Alter T., Ellerbroek L., Schreiber K., Schomburg D., Janssen T., Bartholomaus P., Hofreuter D., Woltemate S., Uhr M., Brenneke B., Gruning P., Gerlach G., Wieler L., Suerbaum S., Josenhans C. Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 2011, 12:584.
62. Guccione E., Leon-Kempis Mdel R., Pearson B.M., Hitchin E., Mulholland F., van Diemen P.M., Stevens M.P., Kelly D.J. Amino acid-dependent growth of Campylobacter jejuni: key roles for aspartase (AspA) under microaerobic and oxygen-limited conditions and identification of AspB (Cj0762), essential for growth on glutamate. Mol. Microbiol. 2008, 69:77-93.
63. Guerry P. Campylobacter flagella: not just for motility. Trends Microbiol. 2007, 15:456-461.
64. Guerry P., Ewing C.P., Schirm M., Lorenzo M., Kelly J., Pattarini D., Majam G., Thibault P., Logan S. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 2006, 60:299-311.
65. Gundogdu O., Bentley S.D., Holden M.T., Parkhill J., Dorrell N., Wren B.W. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 2007, 8:162.
66. -/- mice via Toll-like-receptor-2 and -4 signaling. PLoS One 2012, 7:e40761.
67. Harvey P., Battle T., Leach S. Different invasion phenotypes of Campylobacter isolates in Caco-2 cell monolayers. J. Med. Microbiol. 1999, 48:461-469.
68. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9:690-701.
69. Hendrixson D.R. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 2006, 61:1646-1659.
70. Hendrixson D.R. Restoration of flagellar biosynthesis by varied mutational events in Campylobacter jejuni. Mol. Microbiol. 2008, 70:519-536.
71. Hendrixson D.R., DiRita V.J. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 2004, 52:471-484.
72. Hermans D., Van Deun K., Martel A., Van Immerseel F., Messens W., Heyndrickx M., Haesebrouck F., Pasmans F. Colonization factors of Campylobacter jejuni in the chicken gut. Vet. Res. 2011, 42:82.
73. Hickey T.E., McVeigh A.L., Scott D.A., Michielutti R.E., Bixby A., Carroll S.A., Bourgeois A.L., Guerry P. Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect. Immun. 2000, 68:6535-6541.
74. Hickey T.E., Majam G., Guerry P. Intracellular survival of Campylobacter jejuni in human monocytic cells and induction of apoptotic death by cytholethal distending toxin. Infect. Immun. 2005, 73:5194-5197.
75. Hiett K.L., Stintzi A., Andacht T.M., Kuntz R.L., Seal B.S. Genomic differences between Campylobacter jejuni isolates identify surface membrane and flagellar function gene products potentially important for colonizing the chicken intestine. Funct. Integr. Genomics 2008, 8:407-420.
76. Hofreuter D., Tsai J., Watson R.O., Novik V., Altman B., Benitez M., Clark C., Perbost C., Jarvie T., Du L., Galan J.E. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 2006, 74:4694-4707.
77. Hofreuter D., Novik V., Galan J.E. Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe 2008, 4:425-433.
78. Hofreuter D., Mohr J., Wensel O., Rademacher S., Schreiber K., Schomburg D., Gao B., Galan J.E. Contribution of amino acid catabolism to the tissue specific persistence of Campylobacter jejuni in a murine colonization model. PLoS One 2012, 7:e50699.
79. Hoy B., Löwer M., Weydig C., Carra G., Tegtmeyer N., Geppert T., Schröder P., Sewald N., Backert S., Schneider G., Wessler S. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep. 2010, 11:798-804.
80. Hoy B., Geppert T., Boehm M., Reisen F., Plattner P., Gadermaier G., Sewald N., Ferreira F., Briza P., Schneider G., Backert S., Wessler S. Distinct roles of secreted HtrA proteases from Gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin. J. Biol. Chem. 2012, 287:10115-10120.
81. Hu L., Kopecko D.J. Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun. 1999, 67:4171-4182.
82. Hu L., Kopecko D.J. Cell biology of human host cell entry by Campylobacter jejuni. Campylobacter 2008, 297-313. ASM Press, Washington, DC. I. Nachamkin, Szymanski, M.J. Blaser (Eds.).
83. Hu L., Raybourne R.B., Kopecko D.J. Ca2+ release from host intracellular stores and related signal transduction during Campylobacter jejuni 81-176 internalization into human intestinal cells. Microbiology 2005, 151:3097-3105.
84. Hu L., McDaniel J.P., Kopecko D.J. Signal transduction events involved in human epithelial cell invasion by Campylobacter jejuni 81-176. Microb. Pathog. 2006, 40:91-100.
85. Hu L., Tall B.D., Curtis S.K., Kopecko D.J. Enhanced microscopic definition of Campylobacter jejuni 81-176 adherence to, invasion of, translocation across, and exocytosis from polarized human intestinal Caco-2 cells. Infect. Immun. 2008, 76:5294-5304.
86. Humphrey C.D., Montag D.M., Pittman F.E. Morphologic observations of experimental Campylobacter jejuni infection in the hamster intestinal tract. Am. J. Pathol. 1986, 122:152-159.
87. Ica T., Caner V., Istanbullu O., Nguyen H.D., Ahmed B., Call D.R., Beyenal H. Characterization of mono- and mixed-culture Campylobacter jejuni biofilms. Appl. Environ. Microbiol. 2012, 78:1033-1038.
88. Janssen R., Krogfelt K.A., Cawthraw S.A., van Pelt W., Wagenaar J.A., Owen R.J. Host-pathogen interactions in Campylobacter infections: the host perspective. Clin. Microbiol. Rev. 2008, 21:505-518.
89. Javed M.A., Grant A.J., Bagnall M.C., Maskell D.J., Newell D.G., Manning G. Transposon mutagenesis in a hyper-invasive clinical isolate of Campylobacter jejuni reveals a number of genes with potential roles in invasion. Microbiology 2010, 156:1134-1143.
90. Javed M.A., Cawthraw S.A., Baig A., Li J., McNally A., Oldfield N.J., Newell D.G., Manning G. Cj1136 is required for lipooligosaccharide biosynthesis, hyperinvasion, and chick colonization by Campylobacter jejuni. Infect. Immun. 2012, 80:2361-2370.
91. Jin S., Joe A., Lynett J., Hani E.K., Sherman P., Chan V.L. JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol. Microbiol. 2001, 39:1225-1236.
92. Jin S., Song Y.C., Emili A., Sherman P.M., Chan V.L. 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. 2003, 5:165-174.
93. Jones M.A., Marston K.L., Woodall C.A., Maskell D.J., Linton D., Karlyshev A.V., Dorrell N., Wren B.W., Barrow P.A. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 2004, 72:3769-3776.
94. Kakuda T., DiRita V.J. Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect. Immun. 2006, 74:4715-4723.
95. Kalischuk L.D., Inglis G.D., Buret A.G. Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni is correlated with invasion ability and is independent of cytolethal distending toxin. Microbiology 2007, 153:2952-2963.
96. Kalischuk L.D., Inglis G.D., Buret A.G. Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts. Gut Pathog. 2009, 1:2.
97. Karim Q.N., Logan R.P., Puels J., Karnholz A., Worku M.L. Measurement of motility of Helicobacter pylori, Campylobacter jejuni, and Escherichia coli by real time computer tracking using the Hobson BacTracker. J. Clin. Pathol. 1998, 51:623-628.
98. Karlyshev A.V., Linton D., Gregson N.A., Wren B.W. A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni. Microbiology 2002, 148:473-480.
99. Karlyshev A.V., Champion O.L., Churcher C., Brisson J.R., Jarrell H.C., Gilbert M., Brochu D., St Michael F., Li J., Wakarchuk W.W., Goodhead I., Sanders M., Stevens K., White B., Parkhill J., Wren B.W., Szymanski C.M. Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol. Microbiol. 2005, 55:90-103.
100. Kazmierczak B.I., Mostov K., Engel J.N. Interaction of bacterial pathogens with polarized epithelium. Annu. Rev. Microbiol. 2001, 55:407-435.
101. Kiehlbauch J.A., Albach R.A., Baum L.L., Chang K.P. Phagocytosis of Campylobacter jejuni and its intracellular survival in mononuclear phagocytes. Infect. Immun. 1985, 48:446-451.
102. Kim J.S., Li J., Barnes I.H., Baltzegar D.A., Pajaniappan M., Cullen T.W., Trent M.S., Burns C.M., Thompson S.A. Role of the Campylobacter jejuni Cj1461 DNA methyltransferase in regulating virulence characteristics. J. Bacteriol. 2008, 190:6524-6529.
103. Konkel M.E., Joens L.A. Adhesion to and invasion of Hep-2 cells by Campylobacter spp. Infect. Immun. 1989, 57:2984-2990.
104. Konkel M.E., Corwin M.D., Joens L.A., Cieplak W. Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. J. Med. Microbiol. 1992, 37:30-37.
105. Konkel M.E., Hayes S.F., Joens L.A., Cieplak W. Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb. Pathog. 1992, 13:357-370.
106. Konkel M.E., Mead D.J., Hayes S.F., Cieplak W. Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J. Infect. Dis. 1992, 166:308-315.
107. Konkel M.E., Kim B.J., Rivera-Amill V., Garvis S.G. Identification of proteins required for the internalization of Campylobacter jejuni into cultured mammalian cells. Adv. Exp. Med. Biol. 1999, 473:215-224.
108. Konkel M.E., Monteville M.R., Rivera-Amill V., Joens L.A. The pathogenesis of Campylobacter jejuni-mediated enteritis. Curr. Issues Intest. Microbiol. 2001, 2:55-71.
109. Konkel M.E., Christensen J.E., Keech A.M., Monteville M.R., Klena J.D., Garvis S.G. Identification of a fibronectin-binding domain within the Campylobacter jejuni CadF protein. Mol. Microbiol. 2005, 57:1022-1035.
110. Konkel M.E., Christensen J.E., Dhillon A.S., Lane A.B., Hare-Sanford R., Schaberg D.M., Larson C.L. Campylobacter jejuni strains compete for colonization in broiler chicks. Appl. Environ. Microbiol. 2007, 73:2297-2305.
111. Konkel M.E., Larson C.L., Flanagan R.C. Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J. Bacteriol. 2010, 192:68-76.
112. Krause-Gruszczynska M., Rohde M., Hartig R., Genth H., Schmidt G., Keo T., Koenig W., Miller W.G., Konkel M.E., Backert S. Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell. Microbiol. 2007, 9:2431-2444.
113. Krause-Gruszczynska M., van Alphen L.B., Oyarzabal O.A., Alter T., Hänel I., Schliephake A., König W., van Putten J.P., Konkel M.E., Backert S. Expression patterns and role of the CadF protein in Campylobacter jejuni and Campylobacter coli. FEMS Microbiol. Lett. 2007, 274:9-16.
114. Krause-Gruszczynska M., Boehm M., Rohde M., Tegtmeyer N., Takahashi S., Buday L., Oyarzabal O.A., Backert S. The signaling pathway of Campylobacter jejuni-induced Cdc42 activation: role of fibronectin, integrin beta1, tyrosine kinases and guanine exchange factor Vav2. Cell Commun. Signal. 2011, 9:32.
115. Larson C.L., Shah D.H., Dhillon A.S., Call D.R., Ahn S., Haldorson G.J., Davitt C., Konkel M.E. Campylobacter jejuni invade chicken LMH cells inefficiently and stimulate differential expression of the chicken CXCLi1 and CXCLi2 cytokines. Microbiology 2008, 154:3835-3847.
116. Lee A., O'Rourke J.L., Barrington P.J., Trust T.J. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect. Immun. 1986, 51:536-546.
117. Leon-Kempis Mdel R., Guccione E., Mulholland F., Williamson M.P., Kelly D.J. 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. 2006, 60:1262-1275.
118. Li Y.P., Vegge C.S., Brøndsted L., Madsen M., Ingmer H., Bang D.D. Campylobacter jejuni induces an anti-inflammatory response in human intestinal epithelial cells through activation of phosphatidylinositol 3-kinase/Akt pathway. Vet. Microbiol. 2011, 148:75-83.
119. Lin J., Sahin O., Michel L.O., Zhang Q. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 2003, 71:4250-4259.
120. Liu X., Gao B., Novik V., Galan J.E. Quantitative proteomics of intracellular Campylobacter jejuni reveals metabolic reprogramming. PLoS Pathog. 2012, 8:e1002562.
121. Louwen R., Heikema A., van Belkum A., Ott A., Gilbert M., Ang W., Endtz H.P., Bergman M.P., Nieuwenhuis E.E. The sialylated lipooligosaccharide outer core in Campylobacter jejuni is an important determinant for epithelial cell invasion. Infect. Immun. 2008, 76:4431-4438.
122. Louwen R., Nieuwenhuis E.E., van Marrewijk L., Horst-Kreft D., de Ruiter L., Heikema A.P., van Wamel W.J., Wagenaar J.A., Endtz H.P., Samsom J., van Baarlen P., Akhmanova A., van Belkum A. Campylobacter jejuni translocation across intestinal epithelial cells is facilitated by ganglioside-like lipooligosaccharide structures. Infect. Immun. 2012, 80:3307-3318.
123. MacCallum A., Hardy S.P., Everest P.H. Campylobacter jejuni inhibits the absorptive transport functions of Caco-2 cells and disrupts cellular tight junctions. Microbiology 2005, 151:2451-2458.
124. MacCallum A.J., Harris D., Haddock G., Everest P.H. Campylobacter jejuni-infected human epithelial cell lines vary in their ability to secrete interleukin-8 compared to in vitro-infected primary human intestinal tissue. Microbiology 2006, 152:3661-3665.
125. McSweegan E., Walker R.I. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect. Immun. 1986, 53:141-148.
126. Miller W.G., Bates A.H., Horn S.T., Brandl M.T., Wachtel M.R., Mandrell R.E. Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl. Environ. Microbiol. 2000, 66:5426-5436.
127. Misawa N., Blaser M.J. Detection and characterization of autoagglutination activity by Campylobacter jejuni. Infect. Immun. 2000, 68:6168-6175.
128. Mixter P.F., Klena J.D., Flom G.A., Siegesmund A.M., Konkel M.E. In vivo tracking of Campylobacter jejuni by using a novel recombinant expressing green fluorescent protein. Appl. Environ. Microbiol. 2003, 69:2864-2874.
129. Monteville M.R., Konkel M.E. Fibronectin-facilitated invasion of T84 eukaryotic cells by Campylobacter jejuni occurs preferentially at the basolateral cell surface. Infect. Immun. 2002, 70:6665-6671.
130. Monteville M.R., Yoon J.E., Konkel M.E. Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 2003, 149:153-165.
131. Morooka T., Umeda A., Amako K. Motility as an intestinal colonization factor for Campylobacter jejuni. J. Gen. Microbiol. 1985, 131:1973-1980.
132. Muller A., Leon-Kempis Mdel R., Dodson E., Wilson K.S., Wilkinson A.J., Kelly D.J. A bacterial virulence factor with a dual role as an adhesin and a solute-binding protein: the crystal structure at 1.5A resolution of the PEB1a protein from the food-borne human pathogen Campylobacter jejuni. J. Mol. Biol. 2007, 372:160-171.
133. Myers J.D., Kelly D.J. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 2005, 151:233-242.
134. Myszewski M.A., Stern N.J. Phagocytosis and intracellular killing of Campylobacter jejuni by elicited chicken peritoneal macrophages. Avian Dis. 1991, 35:750-755.
135. Nachamkin I., Yang X.H., Stern N.J. Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl. Environ. Microbiol. 1993, 59:1269-1273.
136. Nachamkin I., Allos B.M., Ho T. Campylobacter species and Guillain-Barre syndrome. Clin. Microbiol. Rev. 1998, 11:555-567.
137. Nachamkin I., Szymanski C.M., Blaser M.J. Campylobacter 2008, ASM Press, Washington, DC.
138. Naikare H., Palyada K., Panciera R., Marlow D., Stintzi A. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect. Immun. 2006, 74:5433-5444.
139. Naito M., Frirdich E., Fields J.A., Pryjma M., Li J., Cameron A., Gilbert M., Thompson S.A., Gaynor E.C. Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J. Bacteriol. 2010, 192:2182-2192.
140. Neal-McKinney J.M., Konkel M.E. The Campylobacter jejuni CiaC virulence protein is secreted from the flagellum and delivered to the cytosol of host cells. Front. Cell. Infect. Microbiol. 2012, 2:31.
141. Newell D.G., McBride H., Dolby J.M. 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. 1985, 95:217-227.
142. Newell D.G., McBride H., Saunders F., Dehele Y., Pearson A.D. The virulence of clinical and environmental isolates of Campylobacter jejuni. J. Hyg. 1985, 94:45-54.
143. Ng L.K., Sherburne R., Taylor D.E., Stiles M.E. Morphological forms and viability of Campylobacter species studied by electron microscopy. J. Bacteriol. 1985, 164:338-343.
144. Ng L.K., Stiles M.E., Taylor D.E. Comparison of basal media for culturing Campylobacter jejuni and Campylobacter coli. J. Clin. Microbiol. 1985, 21:226-230.
145. Novik V., Hofreuter D., Galan J.E. Characterization of a Campylobacter jejuni VirK protein homolog as a novel virulence determinant. Infect. Immun. 2009, 77:5428-5436.
146. Novik V., Hofreuter D., Galan J.E. Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells. Infect. Immun. 2010, 78:3540-3553.
147. Ó Cróinín T., Backert S. Host epithelial cell invasion by Campylobacter jejuni: trigger or zipper mechanism?. Front. Cell. Infect. Microbiol. 2012, 2:25.
148. Oelschlaeger T.A., Guerry P., Kopecko D.J. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:6884-6888.
149. Oyarzabal O.A., Backert S. Microbial Food Safety 2011, Springer, New York.
150. Parkhill J., Wren B.W., Mungall K., Ketley J.M., Churcher C., Basham D., Chillingworth T., Davies R.M., Feltwell T., Holroyd S., Jagels K., Karlyshev A.V., Moule S., Pallen M.J., Penn C.W., Quail M.A., Rajandream M.A., Rutherford K.M., van Vliet A.H., Whitehead S., Barrell B.G. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000, 403:665-668.
151. Pei Z., Burucoa C., Grignon B., Baqar S., Huang X.Z., Kopecko D.J., Bourgeois A.L., Fauchere J.L., Blaser M.J. Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun. 1998, 66:938-943.
152. Pesci E.C., Cottle D.L., Pickett C.L. Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect. Immun. 1994, 62:2687-2694.
153. Poly F., Read T., Tribble D.R., Baqar S., Lorenzo M., Guerry P. Genome sequence of a clinical isolate of Campylobacter jejuni from Thailand. Infect. Immun. 2007, 75:3425-3433.
154. Poly F., Read T.D., Chen Y.H., Monteiro M.A., Serichantalergs O., Pootong P., Bodhidatta L., Mason C.J., Rockabrand D., Baqar S., Porter C.K., Tribble D., Darsley M., Guerry P. Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies. Infect. Immun. 2008, 76:5655-5667.
155. Prendergast M.M., Tribble D.R., Baqar S., Scott D.A., Ferris J.A., Walker R.I., Moran A.P. In vivo phase variation and serologic response to lipooligosaccharide of Campylobacter jejuni in experimental human infection. Infect. Immun. 2004, 72:916-922.
156. Pryjma M., Apel D., Huynh S., Parker C.T., Gaynor E.C. FdhTU-modulated formate dehydrogenase expression and electron donor availability enhance recovery of Campylobacter jejuni following host cell infection. J. Bacteriol. 2012, 194:3803-3813.
157. Raphael B.H., Pereira S., Flom G.A., Zhang Q., Ketley J.M., Konkel M.E. The Campylobacter jejuni response regulator, CbrR, modulates sodium deoxycholate resistance and chicken colonization. J. Bacteriol. 2005, 187:3662-3670.
158. Rivera-Amill V., Kim B.J., Seshu J., Konkel M.E. Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J. Infect. Dis. 2001, 183:1607-1616.
159. Russell R.G., Blake D.C. Cell association and invasion of Caco-2 cells by Campylobacter jejuni. Infect. Immun. 1994, 62:3773-3779.
160. Russell R.G., O'Donnoghue M., Blake D.C., Zulty J., DeTolla L.J. Early colonic damage and invasion of Campylobacter jejuni in experimentally challenged infant Macaca mulatta. J. Infect. Dis. 1993, 168:210-215.
161. Seal B.S., Hiett K.L., Kuntz R.L., Woolsey R., Schegg K.M., Ard M., Stintzi A. Proteomic analyses of a robust versus a poor chicken gastrointestinal colonizing isolate of Campylobacter jejuni. J. Proteome Res. 2007, 6:4582-4591.
162. Sellars M.J., Hall S.J., Kelly D.J. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J. Bacteriol. 2002, 184:4187-4196.
163. Snelling W.J., McKenna J.P., Lecky D.M., Dooley J.S. Survival of Campylobacter jejuni in waterborne protozoa. Appl. Environ. Microbiol. 2005, 71:5560-5571.
164. Song Y.C., Jin S., Louie H., Ng D., Lau R., Zhang Y., Weerasekera R., Al Rashid S., Ward L.A., Der S.D., Chan V.L. FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol. Microbiol. 2004, 53:541-553.
165. Svensson S.L., Davis L.M., MacKichan J.K., Allan B.J., Pajaniappan M., Thompson S.A., Gaynor E.C. The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol. Microbiol. 2009, 71:253-272.
166. Szymanski C.M., King M., Haardt M., Armstrong G.D. Campylobacter jejuni motility and invasion of Caco-2 cells. Infect. Immun. 1995, 63:4295-4300.
167. Szymanski C.M., Burr D.H., Guerry P. Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 2002, 70:2242-2244.
168. Tamás P., Solti Z., Bauer P., Illés A., Sipeki S., Bauer A., Faragó A., Downward J., Buday L. Mechanism of epidermal growth factor regulation of Vav2, a guanine nucleotide exchange factor for Rac. J. Biol. Chem. 2003, 278:5163-5171.
169. Tareen A.M., Dasti J.I., Zautner A.E., Gross U., Lugert R. Campylobacter jejuni proteins Cj0952c and Cj0951c affect chemotactic behaviour towards formic acid and are important for invasion of host cells. Microbiology 2010, 156:3123-3135.
170. Tareen A.M., Dasti J.I., Zautner A.E., Gross U., Lugert R. Sulphite: cytochrome c oxidoreductase deficiency in Campylobacter jejuni reduces motility, host cell adherence and invasion. Microbiology 2011, 157:1776-1785.
171. Tegtmeyer N., Rohde M., Backert S. Clinical presentations and pathogenicity mechanisms of foodborne infections. Microbial Food Safety 2011, 13-31. Springer, New York, NY. O.A. Oyarzabal, S. Backert (Eds.).
172. Tribble D.R., Baqar S., Scott D.A., Oplinger M.L., Trespalacios F., Rollins D., Walker R.I., Clements J.D., Walz S., Gibbs P., Burg E.F., Moran A.P., Applebee L., Bourgeois A.L. Assessment of the duration of protection in Campylobacter jejuni experimental infection in humans. Infect. Immun. 2010, 78:1750-1759.
173. van Alphen L.B., Bleumink-Pluym N.M., Rochat K.D., van Balkom B.W., Wösten M.M., van Putten J.P. Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell. Microbiol. 2008, 10:53-66.
174. Van Deun K., Pasmans F., Ducatelle R., Flahou B., Vissenberg K., Martel A., Van den Broeck W., Van Immerseel F., Haesebrouck F. Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut. Vet. Microbiol. 2008, 130:285-297.
175. van Putten J.P., van Alphen L.B., Wosten M.M., de Zoete M.R. Molecular mechanisms of campylobacter infection. Curr. Top. Microbiol. Immunol. 2009, 337:197-229.
176. van Spreeuwel J.P., Duursma G.C., Meijer C.J., Bax R., Rosekrans P.C., Lindeman J. Campylobacter colitis: histological immunohistochemical and ultrastructural findings. Gut 1985, 26:945-951.
177. Walker R.I., Caldwell M.B., Lee E.C., Guerry P., Trust T.J., Ruiz-Palacios G.M. Pathophysiology of Campylobacter enteritis. Microbiol. Rev. 1986, 50:81-94.
178. Wassenaar T.M., Engelskirchen M., Park S., Lastovica A. Differential uptake and killing potential of Campylobacter jejuni by human peripheral monocytes/macrophages. Med. Microbiol. Immunol. 1997, 186:139-144.
179. Watson R.O., Galán J.E. Signal transduction in Campylobacter jejuni-induced cytokine production. Cell. Microbiol. 2005, 7:655-665.
180. Watson R.O., Galan J.E. Campylobacter jejuni survives within epithelial cells by avoiding delivery to lysosomes. PLoS Pathog. 2008, 4:e14.
181. Watson R.O., Novik V., Hofreuter D., Lara-Tejero M., Galan J.E. A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection. Infect. Immun. 2007, 75:1994-2003.
182. Wine E., Chan V.L., Sherman P.M. Campylobacter jejuni mediated disruption of polarized epithelial monolayers is cell-type specific, time dependent, and correlates with bacterial invasion. Pediatr. Res. 2008, 64:599-604.
183. Wooldridge K.G., Williams P.H., Ketley J.M. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 1996, 21:299-305.
184. Wösten M.M., Wagenaar J.A., van Putten J.P. The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni. J. Biol. Chem. 2004, 279:16214-16222.
185. Yao R., Burr D.H., Doig P., Trust T.J., Niu H., Guerry P. Isolation of motile and non-motile insertional mutants of Campylobacter jejuni: the role of motility in adherence and invasion of eukaryotic cells. Mol. Microbiol. 1994, 14:883-893.
186. Yao R., Burr D.H., Guerry P. CheY-mediated modulation of Campylobacter jejuni virulence. Mol. Microbiol. 1997, 23:1021-1031.
187. Young K.T., Davis L.M., Dirita V.J. Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 2007, 5:665-679.
188. Zheng J., Meng J., Zhao S., Singh R., Song W. Campylobacter-induced interleukin-8 secretion in polarized human intestinal epithelial cells requires Campylobacter-secreted cytolethal distending toxin- and Toll-like receptor-mediated activation of NF-kappaB. Infect. Immun. 2008, 76:4498-4508.