The Natural Antimicrobial Carvacrol Inhibits Campylobacter jejuni Motility and Infection of Epithelial Cells

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  van Alphen, Lieke B ^a,c   Burt, Sara A ^b   Veenendaal, Andreas K J ^a   Bleumink Pluym, Nancy M C ^a   van Putten, Jos P M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARVACROL;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GROWTH; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; CAMPYLOBACTER ENTERITIS; CAMPYLOBACTER JEJUNI; CELL MOTILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; DRUG RESEARCH; ELECTRON MICROSCOPY; EPITHELIUM CELL; ESCHERICHIA COLI; IMMUNOBLOTTING; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; SPECIES INVASION;

ADENOSINE TRIPHOSPHATE; ANTI-BACTERIAL AGENTS; BIOLOGICAL AGENTS; CAMPYLOBACTER JEJUNI; CELL LINE; EPITHELIAL CELLS; ESCHERICHIA COLI; FLAGELLA; HUMANS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON; MONOTERPENES; MOVEMENT; MUTATION; TIME-LAPSE IMAGING;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; EUKARYOTA; ORIGANUM;

EID: 84866726938     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045343     Document Type: Article

References (51)

1. Allos BM, (2001) Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32: 1201-1206.
2. Gascon J, (2006) Epidemiology, etiology and pathophysiology of traveler's diarrhea. Digestion 73Suppl 1: 102-108.
3. Havelaar AH, van Pelt W, Ang CW, Wagenaar JA, van Putten JP, et al. (2009) Immunity to Campylobacter: its role in risk assessment and epidemiology. Crit Rev Microbiol. 35: 1-22.
4. Hughes RA, Cornblath DR, (2005) Guillain-Barré syndrome. Lancet 366: 1653-1666.
5. Hannu T, Mattila L, Rautelin H, Pelkonen P, Lahdenne P, et al. (2002) Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology 41: 312-318.
6. Coker AO, Isokpehi RD, Thomas BN, Amisu KO, Obi CL, (2002) Human campylobacteriosis in developing countries. Emerg Infect Dis 8: 237-244.
7. DuPont HL, (2007) The growing threat of foodborne bacterial enteropathogens of animal origin. Clin Infect Dis 45: 1353-1361.
8. Griggs DJ, Peake L, Johnson MM, Ghori S, Mott A, et al. (2009) Beta-lactamase-mediated beta-lactam resistance in Campylobacter species: prevalence of Cj0299 (bla OXA-61) and evidence for a novel beta-Lactamase in C. jejuni. Antimicrob Agents Chemother 53: 3357-3364.
9. Butzler JP, Oosterom J, (1991) Campylobacter: pathogenicity and significance in foods. Int J Food Microbiol 12: 1-8.
10. Till D, McBride G, Ball A, Taylor K, Pyle E, (2008) Large-scale freshwater microbiological study: rationale, results and risks. J Water Health 6: 443-460.
11. Szymanski CM, King M, Haardt M, Armstrong GD, (1995) Campylobacter jejuni motility and invasion of Caco-2 cells. Infect Immun 63: 4295-4300.
12. Yao R, Burr DH, Doig P, Trust TJ, Niu H, 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.
13. Grant CC, Konkel ME, Cieplak Jr W, Tompkins LS, (1993) Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect Immun 61: 1764-1771.
14. Wassenaar TM, Bleumink-Pluym NM, van der Zeijst BA, (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.
15. Fernando U, Biswas D, Allan B, Willson P, Potter AA, (2007) Influence of Campylobacter jejuni fliA, rpoN and flgK genes on colonization of the chicken gut. Int J Food Microbiol 118: 194-200.
16. Jin S, Joe A, Lynett J, Hani EK, Sherman P, et al. (2001) JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39: 1225-1236.
17. Monteville MR, Yoon JE, Konkel ME, (2003) Maximal adherence and invasion of INT-407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149: 153-165.
18. Moser I, Schroeder W, Salnikow J, (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.
19. Pei Z, Burucoa C, Grignon B, Baqar S, Huang XZ, 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.
20. Bachtiar BM, Coloe PJ, Fry BN, (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.
21. Bacon DJ, Szymanski CM, Burr DH, Silver RP, Alm RA, et al. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol Microbiol 40: 769-777.
22. Szymanski CM, Burr DH, Guerry P, (2002) Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70: 2242-2244.
23. Guerry P, Szymanski CM, Prendergast MM, Hickey TE, Ewing CP, et al. (2002) Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect Immun 70: 787-793.
24. Louwen R, Heikema A, van Belkum A, Ott A, Gilbert M, et al. (2008) The sialylated lipo-oligosaccharide outer core of Campylobacter jejuni is an important determinant for epithelial cell invasion. Infect Immun 76: 4431-4438.
25. McSweegan E, Walker RI, (1986) Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect Immun 53: 141-148.
26. van Putten JP, van Alphen LB, Wösten MM, de Zoete MR, (2009) Molecular mechanisms of campylobacter infection. Curr Top Microbiol Immunol 337: 197-229.
27. Burt S, (2004) Essential oils: their antibacterial properties and potential applications in foods-a review. Int J Food Microbiol 94: 223-253.
28. Di Pasqua R, Betts G, Hoskins N, Edwards M, Ercolini D, et al. (2007) Membrane toxicity of antimicrobial compounds from essential oils. J Agric Food Chem 55: 4863-4870.
29. Di Pasqua R, Hoskins N, Betts G, Mauriello G, (2006) Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem 54: 2745-2749.
30. Helander IM, Alakomi H-L, Latva-Kala K, Mattila-Sandholm T, Pol I, et al. (1998) Characterization of the action of selected essential oil components on Gram-negative bacteria. J Agric Food Chem 46: 3590-3595.
31. Gill AO, Holley RA, (2006) Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int J Food Microbiol 108: 1-9.
32. Gill AO, Holley RA, (2006) Inhibition of membrane bound ATPases of Escherichia coli and Listeria monocytogenes by plant oil aromatics. Int J Food Microbiol 111: 170-174.
33. Ultee A, Kets EP, Smid EJ, (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65: 4606-4610.
34. Ultee A, Smid EJ, (2001) Influence of carvacrol on growth and toxin production by Bacillus cereus. Int J Food Microbiol 64: 373-378.
35. Endtz HP, Giesendorf BA, van Belkum A, Lauwers SJ, Jansen WH, et al. (1993) PCR-mediated DNA typing of Campylobacter jejuni isolated from patients with recurrent infections. Res Microbiol 144: 703-708.
36. Palmer SR, Gully PR, White JM, Pearson AD, Suckling WG, et al. (1983) Water-borne outbreak of Campylobacter gastroenteritis. Lancet 1: 287-290.
37. Isberg RR, Voorhis DL, Falkow S, (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769-778.
38. Wösten MM, Wagenaar JA, van Putten JPM, (2004) The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni. J Biol Chem 279: 16214-16222.
39. Wösten MM, van Dijk L, Veenendaal AK, de Zoete MR, Bleumink-Pluijm NM, et al. (2010) Temperature-dependent FlgM/FliA complex formation regulates Campylobacter jejuni flagella length. Mol Microbiol 75: 1577-1591.
40. Gill AO, Holley RA, (2006) Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int J Food Microbiol 108: 1-9.
41. van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW, Wösten MM, et al. (2008) Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell Microbiol 10: 53-66.
42. Friedman M, Henika PR, Mandrell RE, (2002) Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J Food Prot 65: 1545-1560.
43. Ravishankar S, Zhu L, Law B, Joens L, Friedman M, (2008) Plant-derived compounds inactivate antibiotic-resistant Campylobacter jejuni strains. J Food Prot 71: 1145-1149.
44. Ultee A, Bennik MH, Moezelaar R, (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 68: 1561-1568.
45. Isberg RR, Leong JM, (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861-871.
46. Burt SA, van der Zee R, Koets AP, de Graaff AM, van Knapen F, et al. (2007) Carvacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157:H7. Appl Environ Microbiol 73: 4484-4490.
47. Oussalah M, Callet S, Lacroix M, (2006) Mechanism of action of Spanish oregano, Chinese cinnamon, and savory essential oils against cell membranes and walls of Escherichia coli O157:H7 and Listeria monocytogenes. J Food Prot 69: 1046-1055.
48. Xu H, Delling M, Jun JC, Clapham DE, (2006) Oregano, thyme and clone-derived flavors and skin sensitizes activate specific TRP channels. Nat Neuroscience 9: 628-635.
49. Fabian D, Sabol M, Domaracka K, Bujnakova D, (2006) Essential oils- their antimicrobial activity against Escherichia coli and effect on intestinal cell viability. Toxicol In Vitro 20: 1435-1445.
50. Hagmüller W, Jugl-Chizzola M, Zitterl-Eglseer K, Gabler C, Spergser J, (2006) The use of Thymi Herba as feed additive (0.1%, 0.5%, 1.0%) in weanling piglets with assessment of the shedding of haemolysing E. coli and the detection of thymol in the blood plasma. Berl Munch Tierarztl Wochenschr 119: 50-54.
51. Manzanilla EG, Nofrarías M, Anguita M, Castillo M, Perez JF, (2006) Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. J Anim Sci 84: 2743-2751.