Chapter 17 : Cell Biology of Human Host Cell Entry by

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Cell Biology of Human Host Cell Entry by , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap17-1.gif /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap17-2.gif


This chapter presents an overview of the interaction of with intestinal host cells and focuses on bacterial adherence and invasion into the intestinal epithelium, transcytosis across the epithelial mucosa, and ensuing damage to host cells. invasion into the epithelial mucosa appears to be an essential process leading to colitis. Although many researchers would agree with this general summary of invasion events, there still remains considerable confusion regarding how enter and cross the intestinal mucosa. In fact, researchers concluded, after treating T-84 cells with EGTA, that CadF-dependent invasion of epithelial cells occurs preferentially at the basolateral surface, which normally interacts with fibronectin. In the above study, the number of internalized F38011 increased approximately threefold after EGTA treatment and was then reduced ~80% by treating with anti-fibronectin antibody. A common theme among pathogenic invasive microorganisms is their ability to usurp the eukaryotic cell signaling systems both to allow for invasion and to trigger disease pathogenesis. The current data on signal transduction events involved in invasion suggest that host cell ‘’invasion receptors’’ reside in filipin III-sensitive membrane microdomains (i.e., lipid rafts). Clinical infections, experimental infections in humans and animals, and in vitro analyses in cultured human cells have now clearly demonstrated that cell adherence and invasiveness are necessary steps in -induced inflammatory diarrhea. Much progress has been made in the past 10 years in the understanding of the cell biology of these events.

Citation: Hu L, Kopecko D. 2008. Cell Biology of Human Host Cell Entry by , p 297-313. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch17

Key Concept Ranking

Bacterial Proteins
Bacterial Diseases
Two-Component Signal Transduction Systems
Programmed Cell Death
Cellular Processes
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1.
Figure 1.

Effects of calcium chelators, stimulator, or inhibitors on invasion of INT407 cells by 81-176 or serovar Typhi Ty2w. INT407 cells were grown in complete culture medium containing 10% fetal bovine serum to ~80% confluence in wells of a 24-well plate coated with poly--lysine. The host cells were washed and incubated in Ca-free, serum-free minimal essential medium (S-MEM) before pretreatment for 30 min with the various compounds before a 2-h invasion period with at a multiplicity of infection of 20. After invasion, the monolayer was washed and incubated with 100 μg/ml gentamicin in fresh S-MEM for 2 h before enumeration of intracellular bacteria. (A) Effect of extracellular cationic chelators on host cell invasion. (B) Effect of intracellular Ca chelator, BAPTA/AM, or BayK8644, a plasma membrane Ca channel agonist, on bacterial invasion. (C) Effect of dantrolene or U73122, which act in different ways to inhibit release of Ca from intracellular stores. Bacterial invasion over a 2-h period in the presence of inhibitors or stimulator was compared with invasion without stimulator or inhibitor compounds and is presented as percentage of invasion relative to the no inhibitor/stimulator control (from ).

Citation: Hu L, Kopecko D. 2008. Cell Biology of Human Host Cell Entry by , p 297-313. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch17
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2.
Figure 2.

Schematic diagram depicting the processes involved in regulating intracellular free Ca levels in the host cell and the steps affected by inhibitory/stimulatory compounds. Typically, interaction of a specific bacterial ligand (e.g., protein) with a tyrosine kinase receptor (TKR) located in the host plasma membrane can activate an associated messenger G protein, which in turn can activate phospholipase C (PLC). PLC cleaves membrane-bound phosphatidylinositol 4,5-bisphosphate (PIP 2) to diffusible inositol triphosphate (IP 3) and diacylglycerol (DAG). IP 3 interacts with cognate receptors (i.e., IP 3R) in the endoplasmic reticulum (ER) and causes the release of Ca from intracellular stores. The released Ca in turn activates ryanodine receptors (RyR) on the ER, resulting in augmented Ca release. Membrane-bound DAG causes activation of PKC, which ultimately modulates diverse cellular responses. External free Ca can be internalized through Ca channels in the plasma membrane, a process that is stimulated by the slow channel agonist Bay K8644. U73122 blocks the activity of PLC, and dantrolene blocks the activation of RyRs, both of which result in reduced release of Ca from intracellular stores. BAPTA/AM enters host cells, is cleaved to BAPTA, and then can effectively chelate all intracellular free Ca. W7 inhibits the activation of calmodulin, and calphostin C blocks the activation of PKC.

Citation: Hu L, Kopecko D. 2008. Cell Biology of Human Host Cell Entry by , p 297-313. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch17
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3.
Figure 3.

Schematic representation of host receptors in membrane caveolae/lipid rafts and signal transduction events initiated during invasion and showing the steps blocked by inhibitors. Abbreviations: AKT, anti-protein kinase; CT, cholera toxin; ERK-1/2, extracellular signal-regulated kinase 1 and 2; GDP, guanosine 5′-diphosphate; MAPK, mitogen-activated protein kinase; ERK and p38, MAPK; MEK-1, MAPK/ERK kinase; MKK3, MAPK 3; PDK, 3-phosphoinositide-dependent protein kinase; PI-3 kinase, phosphoinositide 3-kinase; PKA, protein kinase A; PTX, pertussis toxin; RTK, receptor tyrosine kinase. Ras, Rac, and Raf1 are family members of small, monometric GTP-binding proteins; filipin III disrupts lipid rafts; wortmannin and LY294002 are specific inhibitors of PI-3 kinase; staurosporine and genistein are general protein phosphorylation inhibitors. apparently interact with receptors located in lipid rafts/caveolae, which results in a cascade of host signaling pathways as shown.

Citation: Hu L, Kopecko D. 2008. Cell Biology of Human Host Cell Entry by , p 297-313. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch17
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abrahams, G. L., and, M. Hensel. 2006. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell. Microbiol. 8:728737.
2. AbuOun, M.,, G. Manning,, S. A. Cawthraw,, A. Ridley,, I. H. Ahmed,, T. M. Wassenaar, and, D. G. Newell. 2005. Cytolethal distending toxin (CDT)-negative Campylobacter jejuni strains and anti-CDT neutralizing antibodies are induced during human infection but not during colonization in chickens. Infect. Immun. 73:30533062.
3. Ahmed, I. H.,, G. Manning,, T. M. Wassenaar,, S. Cawthraw, and, D. G. Newell. 2002. Identification of genetic differences between two Campylobacter jejuni strains with different colonization potentials. Microbiolog. 148:12031212.
4. Alm, R. A.,, P. Guerry, and, T. J. Trust. 1993. The Campylobacter sigma 54 flaB flagellin promoter is subject to environmental regulation. J. Bacteriol. 175:44484455.
5. Allos, B. M. 1997. Association between Campylobacter infection and Guillain-Barré syndrome. J. Infect. Dis. 176(Suppl. 2):S125S128.
6. Al-Salloom, F. S.,, A. Al Mahmeed,, A. Ismaeel,, G. A. Botta, and, M. Bakhiet. 2003. Campylobacter-stimulated INT407 cells produce dissociated cytokine profiles. J. Infect. 47:217224.
7. Bacon, D. J.,, R. A. Alm,, D. H. Burr,, L. Hu,, D. J. Kopecko,, C. P. Ewing,, T. J. Trust, and, P. Guerry. 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68:43844390.
8. Bacon, D. J.,, R. A. Alm,, L. Hu,, T. E. Hickey,, C. P. Ewing,, R. A. Batchelor,, T. J. Trust, and, P. Guerry. 2002. DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81-176. Infect. Immun. 70:62426250.
9. Bacon, D. J.,, C. M. Szymanski,, D. H. Burr,, R. P. Silver,, R. A. Alm, and, P. Guerry. 2001. A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40:769777.
10. Bakhiet, M., F., S. Al-Salloom,, A. Qareiballa,, K. Bindayna,, I. Farid, and, G. A. Botta. 2004. Induction of alpha and beta chemokines by intestinal epithelial cells stimulated with Campylobacter jejuni. J. Infect. 48:236244.
11. Barnes, I. H.,, M. C. Bagnall,, D. D. Browning,, S. A. Thompson,, G. Manning, and, D. G. Newell. 2007. Gamma-glutamyl transpeptidase has a role in the persistent colonization of the avian gut by Campylobacter jejuni. Microb. Pathog. 43:198207.
12. Bierne, H.,, S. Dramsi,, M. P. Gratacap,, C. Randriamampita,, G. Carpenter,, B. Payrastre, and, P. Cossart. 2000. The invasion protein InlB from Listeria monocytogenes activates PLC-gamma1 downstream from PI 3-kinase. Cell. Microbiol. 2:465476.
13. Biswas, D.,, U. Fernando,, C. Reiman,, P. Willson,, A. Potter, and, B. Allan. 2006. Effect of cytolethal distending toxin of Campylobacter jejuni on adhesion and internalization in cultured cells and in colonization of the chicken gut. Avian Dis. 50:586593.
14. Biswas, D.,, K. Itoh, and, C. Sasakawa. 2000. Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT407 cells. FEMS Immunol. Med. Microbiol. 29:203211.
15. Biswas, D.,, K. Itoh, and, C. Sasakawa. 2003. Role of Microfilaments and microtubules in the Invasion of INT407 Cells by Campylobacter jejuni. Microbiol. Immunol. 47:469473.
16. Biswas D.,, H. Niwa, and, K. Itoh. 2004. Infection with Campylobacter jejuni induces tyrosine-phosphorylated proteins into INT-407 cells. Microbiol. Immunol. 48:221228.
17. Black, R. E.,, M. M. Levine,, M. L. Clements,, T. P. Hughes, and, M. J. Blaser. 1988. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157:472479.
18. Boucrot, E.,, T. Henry,, J. P. Borg,, J. P. Gorvel, and, S. Meresse. 2005. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308:11741178.
19. Bras, A. M., and, J. M. Ketley. 1999. Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol. Lett. 179:209215.
20. Brumell, J. H.,, D. L. Goosney, and, B. B. Finlay. 2002. SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3:407415.
21. Byrd, J.,, R. H. Bailey,, R. Wills, and, D. Nisbet. 2007. Recovery of Campylobacter from commercial broiler hatchery trayliners. Poult. Sci. 86:2629.
22. Cawthraw, S. A., Wassenaar,, T. M., Ayling, R., and, D. G. Newell. 1996. Increased colonization potential of Campylobacter jejuni strain 81116 after passage through chickens and its implication on the rate of transmission within flocks. Epidemiol. Infect. 117:213215.
23. Chen, M. L.,, Z. Ge,, J. G. Fox, and, D. B. Schauer. 2006. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect. Immun. 74:65816589.
24. Clapham, D. E. 1995. Calcium signaling. Cell 80:259268.
25. Clausen, J. D.,, G. Christiansen,, H. U. Holst, and, S. Birkelund. 1997. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol. Microbiol. 25:441449.
26. de Melo, M. A.,, G. Gabbiani, and, J. C. Pechere. 1989. Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect. Immun. 57:22142222.
27. Elsinghorst, E. A.,, L. S. Baron, and, D. J. Kopecko. 1989. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli. Proc. Natl. Acad. Sci. USA 86:51735177.
28. Eppinger, M.,, C. Baar,, G. Raddatz,, D. H. Huson, and, S. C. Schuster. 2004. Comparative analysis of four campylobacterales. Nat. Rev. Microbiol. 2:872885.
29. Everest, P. H.,, H. Goossens,, J. P. Butzler,, D. Lloyd,, S. Knutton,, J. M. Ketley, and, P. H. Williams. 1992. Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J. Med. Microbiol. 37:319325.
30. Fauchere, J. L.,, A. Rosenau,, M. Veron,, E. N. Moyen,, S. Richard, and, A. Pfister. 1986. Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces. Infect. Immun. 54:283287.
31. Finlay, B. B., and, S. Falkow. 1989. Common themes in microbial pathogenicity. Microbiol. Rev. 53:210230.
32. Finlay, B. B., and, S. Falkow. 1988. Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie 70:10891099.
33. Finlay, B. B., and, S. Falkow. 1990. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis. 162:10961106.
34. Finlay, B. B.,, S. Ruschkowski, and, S. Dedhar. 1991. Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. J. Cell. Sci. 99:283296.
35. Florin, I., and, F. Antillon. 1992. Production of enterotoxin and cytotoxin in Campylobacter jejuni strains isolated in Costa Rica. J. Med. Microbiol. 37:2229.
36. Fouts, D. E.,, E. F. Mongodin,, R. E. Mandrell,, W. G. Miller,, D. A. Rasko,, J. Ravel,, L. M. Brinkac,, R. T. DeBoy,, C. T. Parker,, S. C. Daugherty,, R. J. Dodson,, A. S. Durkin,, R. Madupu,, S. A. Sullivan,, J. U. Shetty,, M. A. Ayodeji,, A. Shvartsbeyn,, M. C. Schatz,, J. H. Badger,, C. M. Fraser, and, K. E. Nelson. 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PloS Biol. 3:e15.
37. Fox, J. G.,, A. B. Rogers,, M. T. Whary,, Z. Ge,, N. S. Taylor,, S. Xu,, B. H. Horwitz, and, S. E. Erdman. 2004. Gastroenteritis in NF-kappaB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infect. Immun. 72:11161125.
38. Frisan, T.,, X. Cortes-Bratti, and, M. Thelestam. 2002. Cytolethal distending toxins and activation of DNA damage-dependent checkpoint responses. Int. J. Med. Microbiol. 291:495499.
39. Garcia-del Portillo, F.,, M. B. Zwick,, K. Y. Leung, and, B. B. Finlay. 1993. Intracellular replication of Salmonella within epithelial cells is associated with filamentous structures containing lysosomal membrane glycoproteins. Infect. Agents Dis. 2:227231.
40. Garvis, S. G.,, G. J. Puzon, and, M. E. Konkel. 1996. Molecular characterization of a Campylobacter jejuni 29-kilodalton periplasmic binding protein. Infect. Immun. 64:35373543.
41. Grant, C. C.,, M. E. Konkel,, W. Cieplak, Jr., and, L. S. Tompkins. 1993. Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect. Immun. 61:17641771.
42. Grieshaber, S. S.,, N. A. Grieshaber, and, T. Hackstadt. 2003. Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process. J. Cell Sci. 116:37933802.
43. Guignot, J.,, E. Caron,, C. Beuzon,, C. Bucci,, J. Kagan,, C. Roy, and, D. W. Holden. 2004. Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J. Cell Sci. 117:10331045.
44. Hänel, I.,, J. Muller,, W. Muller, and, F. Schulze. 2004. Correlation between invasion of Caco-2 eukaryotic cells and colonization ability in the chick gut in Campylobacter jejuni. Vet. Microbiol. 101:7582.
45. Hardwidge, P. R.,, W. Deng,, B. A. Vallance,, I. Rodriguez-Escudero,, V. J. Cid,, M. Molina, and, B. B. Finlay. 2005. Modulation of host cytoskeleton function by the enteropathogenic Escherichia coli and Citrobacter rodentium effector protein EspG. Infect. Immun. 73:25862594.
46. Harrison, R. E.,, J. H. Brumell,, A. Khandani,, C. Bucci,, C. C. Scott,, X. Jiang,, B. B. Finlay, and, S. Grinstein. 2004. Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles. Mol. Biol. Cell. 15:31463154.
47. Harvey, P., Battle, T., and, S. Leach. 1999. Different invasion phenotypes of Campylobacter isolates in Caco-2 cell monolayers. J. Med. Microbiol. 48:46169.
48. Hendrixson, D. R., and, V. J. DiRita. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52:471484.
49. Henry, T.,, J. P. Gorvel, and, S. Meresse. 2006. Molecular motors hijacking by intracellular pathogens. Cell. Microbiol. 8:2332.
50. Hickey, T. E.,, S. Baqar,, A. L. Bourgeois,, C. P. Ewing, and, P. Guerry. 1999. Campylobacter jejuni–stimulated secretion of interleukin-8 by INT407 cells. Infect. Immun. 67:8893.
51. Hickey, T. E.,, G. Majam, and, P. Guerry. 2005. Intracellular survival of Campylobacter jejuni in human monocytic cells and induction of apoptotic death by cytholethal distending toxin. Infect. Immun. 73:51945197.
52. Hickey, T. E.,, A. L. McVeigh,, D. A. Scott,, R. E. Michielutti,, A. Bixby,, S. A. Carroll,, A. L. Bourgeois, and, P. Guerry. 2000. Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect. Immun. 68:65356541.
53. Hofreuter, D.,, J. Tsai,, R. O. Watson,, V. Novik,, B. Altman,, M. Benitez,, C. Clark,, C. Perbost,, T. Jarvie,, L. Du, and, J. E. Galan. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74:46944707.
54. Hu, L.,, M. D. Bray,, M. Osorio, and, D. J. Kopecko. 2006a. Campylobacter jejuni induces maturation and cytokine production in human dendritic cells. Infect. Immun. 74:26972705.
55. Hu, L., and, T. E. Hickey. 2005. Campylobacter jejuni induces secretion of proinflammatory chemokines from human intestinal epithelial cells. Infect. Immun. 73:44374440.
56. Hu, L., and, D. J. Kopecko. 1999. Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun. 67:41714182.
57. Hu, L., and, D. J. Kopecko. 2000. Interactions of Campylobacter with eukaryotic cells: gut luminal colonization and mucosal invasion mechanisms, p. 191215. In I. Nachamkin and, M. J. Blaser (ed.), Campylobacter, 2nd ed. American Society for Microbiology, Washington, DC.
58. Hu, L.,, J. P. McDaniel, and, D. J. Kopecko. 2006b. Signal transduction events involved in human epithelial cell invasion by Campylobacter jejuni 81-176. Microb. Pathog. 40:91100.
59. Hu, L,, R. B. Raybourne, and, D. J. Kopecko. 2005. Ca2+ release from host intracellular stores and related signal transduction during Campylobacter jejuni 81-176 internalization into human intestinal cells. Microbiology 151:30973105.
60. Huang, X. Z.,, B. Tall,, W. R. Schwan, and, D. J. Kopecko. 1998. Physical limitations on Salmonella typhi entry into cultured human intestinal epithelial cells. Infect. Immun. 66:29282937.
61. Ilangumaran, S., and, D. C. Hoessli. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335(Pt. 2):433440.
62. Isberg, R. R.,, D. L. Voorhis, and, S. Falkow. 1987. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50:769778.
63. Jacob, R. 1990. Calcium oscillations in electrically non-excitable cells erratum appears. Biochim. Biophys. Acta 1052:427438.
64. Jin, S.,, A. Joe,, J. Lynett,, E. K. Hani,, P. Sherman, and, V. L. Chan. 2001. JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol. Microbiol. 39:12251236.
65. Jin, S., Song,, Y. C., Emil,, A., Sherman,, P. A., and, V. L. Chan. 2003. JplA of Campylobacter jejuni interacts with surface-exposed heat shoch protein 90alpha and triggers signaling pathways leading to the activation of NF-kappaB and p38 MAP kinase in epithelial cells. Cell. Microbiol. 5:165174.
66. Johanesen, P. A., and, M. B. Dwinell. 2006. Flagellin-independent regulation of chemokine host defense in Campylobacter jejuni–infected intestinal epithelium. Infect. Immun. 74:34373447.
67. Johnson, W. M., and, H. Lior. 1988a. A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb. Pathog. 4:115126.
68. Johnson, W. M., and, H. Lior. 1988b. A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. Microb. Pathog. 4:103113.
69. Jones, M. A.,, K. L. Marston,, C. A. Woodall,, D. J. Maskell,, D. Linton,, A. V. Karlyshev,, N. Dorrell,, B. W. Wren, and, P. A. Barrow. 2004. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72:37693776.
70. Jones, M. A.,, S. Totemeyer,, D. J. Maskell,, C. E. Bryant, and, P. A. Barrow. 2003. Induction of proinflammatory responses in the human monocytic cell line THP-1 by Campylobacter jejuni. Infect. Immun. 71:26262633.
71. Kanipes, M. I.,, L. C. Holder,, A. T. Corcoran,, A. P. Moran, and, P. Guerry. 2004. A deep-rough mutant of Campylobacter jejuni 81-176 is noninvasive for intestinal epithelial cells. Infect. Immun. 72:24524255.
72. Kanwar, R. K.,, N. K. Ganguly,, L. Kumar,, J. Rakesh,, D. Panigrahi, and, B. N. S. Walia. 1995. Calcium and protein kinase C play an important role in Campylobacter jejuni–induced changes in Na+ and Cl2 transport in rat ileum in vitro. Biochim. Biophys. Acta 1270:179192.
73. Karlyshev, A. V.,, P. Everest,, D. Linton,, S. Cawthraw,, D. G. Newell, and, B. W. Wren. 2004. The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150:19571964.
74. Karlyshev, A. V.,, D. Linton,, N. A. Gregson,, A. J. Lastovica, and, B. W. Wren. 2000. Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol. Microbiol. 35:529541.
75. Ketley, J. M. 1997. Pathogenesis of enteric infection by Campylobacter. Microbiology 143(Pt. 1):521.
76. Kihlstrom, E., and, L. Nilsson. 1977. Endocytosis of Salmonella typhimurium 395 MS and MR10 by HeLa cells. Acta Pathol. Microbiol. Scand. B 85B:322328.
77. Klipstein, F. A., and, R. F. Engert. 1984a. Properties of crude Campylobacter jejuni heat-labile enterotoxin. Infect. Immun. 45:314319.
78. Klipstein, F. A., and, R. F. Engert. 1984b. Purification of Campylobacter jejuni enterotoxin. Lancet i:11231124.
79. Konkel, M. E.,, M. D. Corwin,, L. A. Joens, and, W. Cieplak. 1992a. Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. J. Med. Microbiol. 37:3037.
80. Konkel, M. E.,, S. A. Gray,, B. J. Kim,, S. G. Garvis, and, J. Yoon. 1999. Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J. Clin. Microbiol. 37:510517.
81. Konkel, M. E.,, S. F., Hayes,, L. A. Joens, and, W. Cieplak. Jr. 1992b. Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb. Pathog. 13:357370.
82. Konkel, M. E., and, L. A. Joens. 1989. Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect. Immun. 57:29842990.
83. Konkel, M. E.,, J. D. Klena,, V. Rivera-Amill,, M. R. Monteville,, D. Biswas,, B. Raphael, and, J. Mickelson. 2004. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J. Bacteriol. 186:32963303.
84. Konkel, M. E.,, D. J. Mead,, S. F. Hayes, and, W. Cieplak, Jr. 1992c. Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J. Infect. Dis. 166:308315.
85. Kopecko, D. J.,, Hu, L., and, K. J. M. Zaal. 2001. Campylobacter jejuni —microtubule-dependent invasion. Trends Microbiol. 9:389396.
86. Krause-Gruszczynska, M.,, M. Rohde,, R. Hartig,, H. Genth,, G. Schmidt,, T. Keo,, W. Konig,, W. G. Miller,, M. E. Konkel, and, S. Backert. 2007. Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell. Microbiol. 9:24312444.
87. Kuhle, V.,, G. L. Abrahams, and, M. Hensel. 2006. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7:716730.
88. Kuhle, V.,, D. Jackel, and, M. Hensel. 2004. Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 5:356570.
89. Lara-Tejero, M., and, J. E. Galan. 2000. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290:354357.
90. Lara-Tejero, M., and, J. E. Galan. 2001. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect. Immun. 69:43584365.
91. Lee, A.,, J. O’Rourke,, M. B. Phillips, and, P. Barrington. 1983. Campylobacter jejuni as a Mucosa Associated Organism: An Ecological Study. Public Health Laboratory Service, London, United Kindom.
92. MacCallum, A.,, S. P. Hardy, and, P. H. Everest. 2005. Campylobacter jejuni inhibits the absorptive transport functions of Caco-2 cells and disrupts cellular tight junctions. Microbiology 151:24512458.
93. MacCallum, A. J.,, D. Harris,, G. Haddock, and, P. H. Everest. 2006. 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 152:36613665.
94. MacKichan, J. K.,, E. C. Gaynor,, C. Chang,, S. Cawthraw,, D. G. Newell,, J. F. Miller, and, S. Falkow. 2004. The Campylobacter jejuni dccRS two-component system is required for optimal in vivo colonization but is dispensable for in vitro growth. Mol. Microbiol. 54:12691286.
95. Marks, P. W., and, F. R. Maxfield. 1990a. Local and global changes in cytosolic free calcium in neutrophils during chemotaxis and phagocytosis. Cell Calcium 11:181190.
96. Marks, P. W., and, F. R. Maxfield. 1990b. Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J. Cell Biol. 110:4352.
97. McSweegan, E.,, D. H. Burr, and, R. I. Walker. 1987. Intestinal mucus gel and secretory antibody are barriers to Campylobacter jejuni adherence to INT 407 cells. Infect. Immun. 55:14311435.
98. McSweegan, E., and, R. I. Walker. 1986. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect. Immun. 53:141148.
99. Meldolesi, J.,, E. Clementi,, C. Fasolato,, D. Zacchetti, and, T. Pozzan. 1991. Ca2+ influx following receptor activation. Trends Pharmacol. Sci. 12:289292.
100. Mellits, K. H.,, J. Mullen,, M. Wand,, G. Armbruster,, A. Patel,, P. L. Connerton,, M. Skelly, and, I. F. Connerton. 2002. Activation of the transcription factor NF-kappaB by Campylobacter jejuni. Microbiology 148:27532763.
101. Miller, V. L.,, B. B. Finlay, and, S. Falkow. 1988. Factors essential for the penetration of mammalian cells by Yersinia. Curr. Top. Microbiol. Immunol. 138:1539.
102. Misawa, N.,, T. Ohnishi,, K. Itoh, and, E. Takahashi. 1994. Development of a tissue culture assay system for Campylobacter jejuni cytotoxin and the influence of culture conditions on cytotoxin production. J. Med. Microbiol. 41:224230.
103. Monteville, M. R., and, M. E. Konkel. 2002. Fibronectin-facilitated invasion of T84 eukaryotic cells by Campylobacter jejuni occurs preferentially at the basolateral cell surface. Infect. Immun. 70:66656671.
104. Monteville, M. R.,, J. E. Yoon, and, M. E. Konkel. 2003. Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149:153165.
105. Norris, V.,, S. Grant,, P. Freestone,, J. Canvin,, F. N. Sheikh,, I. Toth,, M. Trinei,, K. Modha, and, R. I. Norman. 1996. Calcium signalling in bacteria. J. Bacteriol. 178:36773682.
106. Oelschlaeger, T. A.,, P. Guerry, and, D. J. Kopecko. 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA. 90:68846888.
107. Parkhill, J.,, B. W. Wren,, K. Mungall,, J. M. Ketley,, C. Churcher,, D. Basham,, T. Chillingworth,, R. M. Davies,, T. Feltwell,, S. Holroyd,, K. Jagels,, A. V. Karlyshev,, S. Moule,, M. J. Pallen,, C. W. Penn,, M. A. Quail,, M. A. Rajandream,, K. M. Rutherford,, A. H. van Vliet,, S. Whitehead, and, B. G. Barréll. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665668.
108. Pei, Z., and, 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. 268:1871718725.
109. Pei, Z.,, C. Burucoa,, B. Grignon,, S. Baqar,, X. Z. Huang,, D. J. Kopecko,, A. L. Bourgeois,, J. L. Fauchere, and, M. J. Blaser. 1998. Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun. 66:938943.
110. Pei, Z. H.,, R. T. Ellison, III, and, M. J. Blaser. 1991. Identification, purification, and characterization of major antigenic proteins of Campylobacter jejuni. J. Biol. Chem. 266:1636316369.
111. Poly, F.,, C. Ewing,, S. Goon,, T. E. Hickey,, D. Rockabrand,, G. Majam,, L. Lee,, J. Phan,, N. J. Savarino, and, P. Guerry. 2007. Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect. Immun. 75:38593867.
112. Purdy, D.,, C. M. Buswell,, A. E. Hodgson,, K. McAlpine,, I. Henderson, and, S. A. Leach. 2000. Characterisation of cytolethal distending toxin (CDT) mutants of Campylobacter jejuni. J. Med. Microbiol. 49:473479.
113. Ringoir, D. D., and, V. Korolik. 2003. Colonisation phenotype and colonization potential differences in Campylobacter jejuni strains in chickens before and after passage in vivo. Vet. Microbiol. 92:225235.
114. Rosenquist, H.,, N. L. Nielsen,, H. M. Sommer,, B. Norrung, and, B. B. Christensen. 2003. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int. J. Food Microbiol. 83:87103.
115. Ruiz-Palacios, G. M.,, J. Torres,, N. I. Torres,, E. Escamilla,, B. R. Ruiz-Palacios, and, J. Tamayo. 1983. Cholera-like enterotoxin produced by Campylobacter jejuni. Characterisation and clinical significance. Lancet ii:250253.
116. Ruschkowski, S.,, I. Rosenshine, and, B. B. Finlay. 1992. Salmonella typhimurium induces an inositol phosphate flux in infected epithelial cells. FEMS Microbiol. Lett. 95:121126.
117. Russell, R. G., and, D. C. Blake, Jr. 1994. Cell association and invasion of Caco-2 cells by Campylobacter jejuni. Infect. Immun. 62:37733779.
118. Siegesmund, A. M.,, M. E. Konkel,, J. D. Klena, and, P. F. Mixter. 2004. Campylobacter jejuni infection of differentiated THP-1 macrophages results in interleukin 1 beta release and caspase-1-independent apoptosis. Microbiology 150:561569.
119. Simons, K., and, D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:3139.
120. Stern, N. J.,, J. S. Bailey,, L. C. Blankenship,, N. A. Cox, and, F. McHan. 1988. Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Dis. 32:330334.
121. Tanaka, T.,, T. Ohmura,, T. Yamakado, and, H. Hidaka. 1982. Two types of calcium-dependent protein phosphorylations modulated by calmodulin antagonists. Naphthalenesulfonamide derivatives. Mol. Pharmacol. 22:408412.
122. Tran Van Nhieu, G.,, C. Clair,, G. Grompone, and, P. Sansonetti. 2004. Calcium signalling during cell interactions with bacterial pathogens. Biol. Cell. 96:93101.
123. Tsien, R. W., and, R. Y. Tsien. 1990. Calcium channels, stores, and oscillations. Annu. Rev. Cell Biol. 6:715760.
124. Uchiya, K.,, M. A. Barbieri,, K. Funato,, A. H. Shah,, P. D. Stahl, and, E. A. Groisman. 1999. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18:39243933.
125. Van Alphen, L. B., Bleumink-Pluym,, N. M. C., Rochat,, K. D., van Balkom,, B. W. M., Wosten,, M. M. S. M., and, J. P. M. van Putten. 2008. Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell. Microbiol. 10:5366.
126. van Spreeuwel, J. P.,, G. C. Duursma,, C. J. Meijer,, R. Bax,, P. C. Rosekrans, and, J. Lindeman. 1985. Campylobacter colitis: histological. immunohistochemical and ultrastructural findings. Gut. 26:945951.
127. Vazquez-Torres, A.,, Y. Xu,, J. Jones-Carson,, D. W. Holden,, S. M. Lucia,, M. C. Dinauer,, P. Mastroeni, and, F. C. Fang. 2000. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287:16551658.
128. Walker, R. I.,, M. B. Caldwell,, E. C. Lee,, P. Guerry,, T. J. Trust, and, G. M. Ruiz-Palacios. 1986. Pathophysiology of Campylobacter enteritis. Microbiol. Rev. 50:8194.
129. Wallis, M. R. 1994. The pathogenesis of Campylobacter jejuni. Br. J. Biomed. Sci. 51:5764.
130. Wassenaar, T. M., and, M. J. Blaser. 1999. Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect. 1:10231033.
131. Wassenaar, T. M.,, N. M. Bleumink-Pluym, and, B. A. van der Zeijst. 1991. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J. 10:20552061.
132. Watson, R. O., and, J. E. Galan. 2005. Signal transduction in Campylobacter jejuni–induced cytokine production. Cell. Microbiol. 7:655665.
133. Whitehouse, C. A.,, P. B. Balbo,, E. C. Pesci,, D. L. Cottle,, P. M. Mirabito, and, C. L. Pickett. 1998. Campylobacter jejuni cyto-lethal distending toxin causes a G2-phase cell cycle block. Infect. Immun. 66:19341940.
134. Wooldridge, K. G., and, J. M. Ketley. 1997. Campylobacter–host cell interactions. Trends Microbiol. 5:96102.
135. Wooldridge, K. G.,, P. H. Williams, and, J. M. Ketley. 1996. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 21:299305.
136. Yanagawa, Y.,, M. Takahashi, and, T. Itoh. 1994. The role of flagella of Campylobacter jejuni in colonization in the intestinal tract in mice and the cultured-cell infectivity. Nippon Saikingaku Zasshi 49:395403.
137. Yao, R.,, D. H. Burr,, P. Doig,, T. J. Trust,, H. Niu, and, P. Guerry. 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. 14:883893.
138. Yoshida, S.,, Y. Handa,, T. Suzuki,, M. Ogawa,, M. Suzuki,, A. Tamai,, A. Abe,, E. Katayama, and, C. Sasakawa. 2006. Micro-tubule-severing activity of Shigella is pivotal for intercellular spreading. Science 314:985989.
139. Yoshida, S., and, C. Sasakawa. 2003. Exploiting host microtubule dynamics: a new aspect of bacterial invasion. Trends Microbiol. 11:139143.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error