Search for other papers by M. T. Le in
Current site
Google Scholar
PubMed
Search for other papers by I. Porcelli in
Current site
Google Scholar
PubMed
Search for other papers by C. M. Weight in
Current site
Google Scholar
PubMed
Search for other papers by D. J. H. Gaskin in
Current site
Google Scholar
PubMed
School of Medicine, Health Policy and Practice, University of East Anglia, Norwic, UK
Search for other papers by S. R. Carding in
Current site
Google Scholar
PubMed
Institute of Food Research, Norwich Research Park, Norwich, NR4 7UA, UK
Search for other papers by A. H. M. van Vliet in
Current site
Google Scholar
PubMed
Abstract
The bacterial pathogen Campylobacter jejuni is the leading cause of foodborne gastroenteritis in the developed world, with the organism being transmitted by ingestion of contaminated and undercooked poultry. Exposure to acid is an inevitable stressor for C. jejuni during gastric passage, yet the effect of low pH on C. jejuni virulence is still poorly understood. Here, we investigate the effect of acid-shock on C. jejuni viability, gene expression and host-cell invasion. C. jejuni strain NCTC 11168 survived acid exposure at pH 3.5 and above for up to 30 min without a drop in viability, and this exposure induced the expression of flagellar genes transcribed from σ54-dependent promoters. Furthermore, acid-shock resulted in increased C. jejuni invasion of m-ICcl2 mouse small intestine crypt cells grown on transwells, but not when the cells were grown on flat-bottomed wells. This suggests that C. jejuni might be invading intestinal epithelial cells at the basolateral side, possibly after paracellular passage. We hypothesize that acid-shock prior to intestinal entry may serve as a signal that primes C. jejuni to express its virulence gene repertoire including flagellar motility genes, but this requires further study in the context of an appropriate colonization or disease model.
-
1. R. Janssen K.A. Krogfelt S.A. Cawthraw W. van Pelt J.A. Wagenaar R.J. Owen 2008 Host-pathogen interactions in Campylobacter infections: the host perspective Clin Microbiol Rev 21 505–518.
-
2. DEFRA (2010): Zoonoses report. United Kingdom 2008.
-
3. S.M. Man 2011 The clinical importance of emerging Campylobacter species Nat Rev Gastroenterol Hepatol 8 669–685.
-
4. N. Yuki 2007 Campylobacter sialyltransferase gene polymorphism directs clinical features of Guillain-Barré syndrome J Neurochem 103 Suppl1 150–158.
-
5. J.B. Dressman R.R. Berardi L.C. Dermentzoglou T.L. Russell S.P. Schmaltz J.L. Barnett K.M. Jarvenpaa 1990 Upper gastrointestinal (GI) pH in young, healthy men and women Pharm Res 7 756–761.
-
6. J.A. Siegel J.L. Urbain L.P. Adler N.D. Charkes A.H. Maurer B. Krevsky L.C. Knight R.S. Fisher L.S. Malmud 1988 Biphasic nature of gastric emptying Gut 29 85–89.
-
7. J.P. Audia C.C. Webb J.W. Foster 2001 Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria Int J Med Microbiol 291 97–106.
-
8. N.A. Burton M.D. Johnson P. Antczak A. Robinson P.A. Lund 2010 Novel aspects of the acid response network of E. coli K-12 are revealed by a study of transcriptional dynamics J Mol Biol 401 726–742.
-
9. A.N. Reid R. Pandey K. Palyada H. Naikare A. Stintzi 2008 Identification of Campylobacter jejuni genes involved in the response to acidic pH and stomach transit Appl Environ Microbiol 74 1583–1597.
-
10. A.N. Reid R. Pandey K. Palyada L. Whitworth E. Doukhanine A. Stintzi 2008 Identification of Campylobacter jejuni genes contributing to acid adaptation by transcriptional profiling and genome-wide mutagenesis Appl Environ Microbiol 74 1598–1612.
-
11. S. Hwang B. Jeon J. Yun S. Ryu 2011 Roles of RpoN in the resistance of Campylobacter jejuni under various stress conditions BMC Microbiol 11 207.
-
12. Y. Ma H. Irene M. Slavik 2009 Stress-induced adaptive tolerance response and virulence gene expression in Campylobacter jejuni J Food Safety 29 126–143.
-
13. C. Murphy C. Carroll K.N. Jordan 2003 Identification of a novel stress resistance mechanism in Campylobacter jejuni J Appl Microbiol 95 704–708.
-
14. D.S. Merrell M.L. Goodrich G. Otto L.S. Tompkins S. Falkow 2003 pH-regulated gene expression of the gastric pathogen Helicobacter pylori Infect Immun 71 3529–3539.
-
15. T. Polen D. Rittmann V.F. Wendisch H. Sahm 2003 DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate Appl Environ Microbiol 69 1759–1774.
-
16. L.M. Maurer E. Yohannes S.S. Bondurant M. Radmacher J.L. Slonczewski 2005 pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12 J Bacteriol 187 304–319.
-
17. J. Parkhill 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 B.G. Barrell 2000 The genome sequence of the food borne pathogen Campylobacter jejuni reveals hypervariable sequences Nature 403 665–668.
-
18. K. Holmes F. Mulholland B.M. Pearson C. Pin J. McNicholl-Kennedy J.M. Ketley J.M. Wells 2005 Campylobacter jejuni gene expression in response to iron limitation and the role of Fur Microbiology 151 243–257.
-
19. S. Lucchini P. McDermott A. Thompson J.C. Hinton 2009 The HNS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium Mol Microbiol 74 1169–1186.
-
20. M. Bens A. Bogdanova F. Cluzeaud L. Miquerol S. Kerneis J.P. Kraehenbuhl A. Kahn E. Pringault A. Vandewalle 1996 Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype Am J Physiol 270 C1666–C1674.
-
21. L.M. Friis C. Pin B.M. Pearson J.M. Wells 2005 In vitro cell culture methods for investigating Campylobacter invasion mechanisms J Microbiol Meth 61 145–160.
-
22. C. Murphy C. Carroll K.N. Jordan 2003 Induction of an adaptive tolerance response in the foodborne pathogen, Campylobacter jejuni FEMS Microbiol Lett 223 89–93.
-
23. M.T. Thomas M. Shepherd R.K. Poole A.H. van Vliet D.J. Kelly B.M. Pearson 2011 Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on L-lactate Environ Microbiol 13 48–61.
-
24. M.M.S.M. Wösten J. Wagenaar J.P.M. Van Putten 2004 The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni J Biol Chem 279 16214–16222.
-
25. T.G. Smith T.R. Hoover 2009 Deciphering bacterial flagellar gene regulatory networks in the genomic era Adv Appl Microbiol 67 231–267.
-
26. R.E. Avila M.E. Semar S.P. de Fabro 1986 Ultrastructural differentiation of glandular stomach (proventriculus) in chick embryo Folia Histochem Cytobiol 24 227–231.
-
27. P. Chaveerach A.A.H.M. ter Huurne L.J.A. Lipman F. van Knapen 2003 Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions Appl Environ Microbiol 69 711–714.
-
28. S.N. Joslin D.R. Hendrixson 2009 Activation of the Campylobacter jejuni FlgSR two-component system is linked to the flagellar export apparatus J Bacteriol 191 2656–2667.
-
29. Y. Wen J. Feng D.R. Scott E.A. Marcus G. Sachs 2009 The pH-responsive regulon of HP0244 (FlgS), the cytoplasmic histidine kinase of Helicobacter pylori J Bacteriol 191 449–460.
-
30. L.B. van Alphen N.M.C. Bleumlnk-Pluym K.D. Rochat B.W.M. van Balkom M.S.M. Wösten J.P.M. van Putten 2008 Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells Cell Microbiol 10 53–66.
-
31. L. Hu B.D. Tall S.K. Curtis D.J. Kopecko 2008 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 76 5294–5304.
-
32. C.C. Grant M.E. Konkel W. Cieplak Jr 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 1764–1771.
-
33. S. Bereswill A. Fischer R. Plickert L.M. Haag B. Otto A.A. Kuhl J.I. Dasti A.E. Zautner M. Munoz C. Loddenkemper U. Gross U.B. Gobel M.M. Heimesaat 2011 Novel murine infection models provide deep insights into the “menage a trois” of Campylobacter jejuni, microbiota and host innate immunity PLoS One 6 20953.
-
34. R.O. Watson V. Novik D. Hofreuter M. Lara-Tejero J.E. Galan 2007 A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection Infect Immun 75 1994–2003.
-
35. C. Chang J.F. Miller 2006 Campylobacter jejuni colonization of mice with limited enteric flora Infect Immun 74 5261–5271.
-
36. M.E. Konkel M.R. Monteville V. Rivera-Amill L.A. Joens 2001 The pathogenesis of Campylobacter jejuni-mediated enteritis Curr Issues Intest Microbiol 2 55–71.
-
37. D. Axelsson-Olsson L. Svensson J. Olofsson P. Salomon J. Waldenström P. Ellström B. Olsen 2010 Increase in acid tolerance of Campylobacter jejuni through coincubation with amoebae Appl Environ Microbiol 76 4194–4200.
-
38. C.M. Szymanski M. King M. Haardt G.D. Armstrong 1995 Campylobacter jejuni motility and invasion of Caco-2 cells Infect Immun 63 4295–4300.
-
39. P. Guerry 2007 Campylobacter flagella: not just for motility Trends Microbiol 15 456–461.
-
40. K.T. Young L.M. Davis V.J. Di Rita 2007 Campylobacter jejuni: molecular biology and pathogenesis Nature Rev Microbiol 5 665–679.
-
41. D.R. Buelow J.E. Christensen J.M. Neal-McKinney M.E. Konkel 2011 Campylobacter jejuni, survival within human epithelial cells in enhanced by the secreted protein Cial Mol Microbiol 80 1296–1312.
Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de
Indexing and Abstracting Services:
- PubMed Central
- Scopus
- ESCI
- CABI
- CABELLS Journalytics
| 2024 | |
|---|---|
| Scopus | |
| CiteScore | |
| CiteScore rank | |
| SNIP | |
| Scimago | |
| SJR index | 0.569 |
| SJR Q rank | Q3 |
| 2023 | |
|---|---|
| Web of Science | |
| Total Cites WoS |
674 |
| Journal Impact Factor | 3.3 |
| Rank by Impact Factor |
Q2 |
| Impact Factor without Journal Self Cites |
3.1 |
| 5 Year Impact Factor |
3.2 |
| Scimago | |
| Scimago H-index |
15 |
| Scimago Journal Rank |
0.601 |
| Scimago Quartile Score | Microbiology (medical) (Q2) Microbiology (Q3) Immunology and Allergy (Q3) Immunology (Q3) |
| Scopus | |
| Scopus Cite Score |
5.0 |
| Scopus CIte Score Rank |
Microbiology (medical) Q2 |
| Scopus SNIP |
0.832 |
| European Journal of Microbiology and Immunology | |
|---|---|
| Publication Model | Gold Open Access Online only |
| Submission Fee | none |
| Article Processing Charge | 900 EUR/article |
| Regional discounts on country of the funding agency | World Bank Lower-middle-income economies: 50% World Bank Low-income economies: 100% |
| Further Discounts | Editorial Board / Advisory Board members: 50% Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100% |
| Subscription Information | Gold Open Access |
| Purchase per Title | |
| European Journal of Microbiology and Immunology | |
|---|---|
| Language | English |
| Size | A4 |
| Year of Foundation |
2011 |
| Volumes per Year |
1 |
| Issues per Year |
4 |
| Founder | Akadémiai Kiadó |
| Founder's Address |
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245. |
| Publisher | Akadémiai Kiadó |
| Publisher's Address |
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245. |
| Responsible Publisher |
Chief Executive Officer, Akadémiai Kiadó |
| ISSN | 2062-509X (Print) |
| ISSN | 2062-8633 (Online) |
Monthly Content Usage
| Abstract Views | Full Text Views | PDF Downloads | |
|---|---|---|---|
| Dec 2024 | 32 | 0 | 0 |
| Jan 2025 | 59 | 0 | 0 |
| Feb 2025 | 72 | 0 | 0 |
| Mar 2025 | 56 | 0 | 0 |
| Apr 2025 | 28 | 0 | 0 |
| May 2025 | 20 | 0 | 0 |
| Jun 2025 | 0 | 0 | 0 |
Copyright Akadémiai Kiadó AKJournals is the trademark of Akadémiai Kiadó's journal publishing business branch.