Respiratory proteins contribute differentially to Campylobacter jejuni's survival and in vitro interaction with hosts' intestinal cells

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Kassem, Issmat I ^a   Khatri, Mahesh ^a   Esseili, Malak A ^a   Sanad, Yasser M ^a   Saif, Yehia M ^a   Olson, Jonathan W ^b   Rajashekara, Gireesh ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Adaptation; Biofilm; Campylobacter jejuni; Chicken intestinal epithelial cells; INT 407; Motility; Oxidative stress; Oxygen; Respiratory proteins; Survival; Temperature

Indexed keywords

FORMATE DEHYDROGENASE; FUMARIC ACID; HYDROGEN PEROXIDE; HYDROGENASE; NITRATE REDUCTASE; OXYGEN; PROTEIN DERIVATIVE; RESPIRATORY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BIOFILM; CAMPYLOBACTER JEJUNI; CELL INVASION; CELL SURVIVAL; CONTROLLED STUDY; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE CELL; MUTANT; NONHUMAN; OXYGEN CONCENTRATION; PHENOTYPE; PROTEIN FUNCTION; SCANNING ELECTRON MICROSCOPY; TEMPERATURE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CAMPYLOBACTER JEJUNI; CHICKENS; EPITHELIAL CELLS; GENE DELETION; HUMANS; HYDROGEN PEROXIDE; LOCOMOTION; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON, SCANNING; OXIDOREDUCTASES; TEMPERATURE; VIRULENCE FACTORS;

CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

EID: 84868655935     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-258     Document Type: Article

References (42)

1. Campylobacter jejuni Infections: update on emerging issues and trends. Allos BM, Clin Infect Dis 2001 32 1201 1206 10.1086/319760 11283810
2. Statistical comparison of Campylobacter jejuni subtypes from human cases and environmental sources. Garrett N, Devane ML, Hudson JA, Nicol C, Ball A, Klena JD, Scholes P, Baker MG, Gilpin BJ, Savill MG, J Appl Microbiol 2007 103 2113 2121 10.1111/j.1365-2672.2007.03437.x 18045395
3. Chickens and cattle as sources of sporadic domestically acquired Campylobacter jejuni infections in Finland. Hakkinen M, Nakari UM, Siitonen A, Appl Environ Microbiol 2009 75 5244 5249 10.1128/AEM.00374-09 19542336
4. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, Jagels K, Karlyshev AV, Moule S, Pallen MJ, Penn CW, Quail MA, Rajandream MA, Rutherford KM, van Vliet AH, Whitehead S, Barrell BG, Nature 2000 403 665 668 10.1038/35001088 10688204
5. Respiratory electron transport in Helicobacter and Campylobacter. Myers JD, Kelly DJ, Respiration in Archaea and Bacteria: Diversity of Prokaryotic Respiratory Systems Boston: Kluwer Academic Publishers, Zannoni D, 2004 63 77
6. Natural transformation in Campylobacter species. Wang Y, Taylor DE, J Bacteriol 1990 172 949 595 2404960
7. Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. Guccione E, Hitchcock A, Hall SJ, Mulholland F, Shearer N, van Vliet AH, Kelly DJ, Environ Microbiol 2010 12 576 591 10.1111/j.1462-2920.2009.02096.x 19919540
8. Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Weingarten RA, Grimes JL, Olson JW, Appl Environ Microbiol 2008 74 1367 1375 10.1128/AEM.02261-07 18192421
9. The dual-functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. Weingarten RA, Taveirne ME, Olson JW, J Bacteriol 2009 191 5293 5300 10.1128/JB.00166-09 19525346
10. The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Weerakoon DR, Borden NJ, Goodson CM, Grimes J, Olson JW, Microb Pathog 2009 47 8 15 10.1016/j.micpath.2009.04.009 19397993
11. Roles of the twin-arginine translocase and associated chaperones in the biogenesis of the electron transport chains of the human pathogen Campylobacter jejuni. Hitchcock A, Hall SJ, Myers JD, Mulholland F, Jones MA, Kelly DJ, Microbiology 2010 156 2994 3010 10.1099/mic.0.042788-0 20688826
12. Identification of Campylobacter jejuni genes contributing to acid adaptation by transcriptional profiling and genome-wide mutagenesis. Reid AN, Pandey R, Palyada K, Whitworth L, Doukhanine E, Stintzi A, Appl Environ Microbiol 2008 74 1598 1612 10.1128/AEM.01508-07 18192408
13. Gene expression profile of Campylobacter jejuni in response to growth temperature variation. Stintzi A, J Bacteriol 2003 185 2009 2016 10.1128/JB.185.6.2009-2016.2003 12618466
14. Campylobacter jejuni gene expression in the chick cecum: evidence for adaptation to a low-oxygen environment. Woodall CA, Jones MA, Barrow PA, Hinds J, Marsden GL, Kelly DJ, Dorrell N, Wren BW, Maskell DJ, Infect Immun 2005 73 5278 5285 10.1128/IAI.73.8.5278-5285.2005 16041056
15. Functional characterization of the twin-arginine translocation system in Campylobacter jejuni. Rajashekara G, Drozd M, Gangaiah D, Jeon B, Liu Z, Zhang Q, Foodborne Pathog Dis 2009 6 935 945 10.1089/fpd.2009.0298 19799526
16. Motility and chemotaxis in Campylobacter and Helicobacter. Lertsethtakarn P, Ottemann KM, Hendrixson DR, Annu Rev Microbiol 2011 65 389 410 10.1146/annurev-micro-090110-102908 21939377
17. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. Fields JA, Thompson SA, J Bacteriol 2008 190 3411 3416 10.1128/JB.01928-07 18310331
18. Respiratory physiology and energy conservation efficiency of Campylobacter jejuni. Hoffman PS, Goodman TG, J Bacteriol 1982 150 319 326 6277867
19. Bacterial motility on a surface: many ways to a common goal. Harshey RM, Annu Rev Microbiol 2003 57 249 273 10.1146/annurev.micro.57.030502.091014 14527279
20. Influences of temperature, salinity and starvation on the motility and chemotactic response of Vibrio anguillarum. Larsen MH, Blackburn N, Larsen JL, Olsen JE, Microbiology 2004 150 1283 1290 10.1099/mic.0.26379-0 15133091
21. Fumarate reductase is a major contributor to the of reactive oxygen species in the anaerobe Bacteroides fragilis. Meehan BM, Malamy MH, Microbiology 2012 158 539 546 10.1099/mic.0.054403-0 22075026
22. Role of the NiFe hydrogenase Hya in oxidative stress defense in Geobacter sulfurreducens. Tremblay PL, Lovley DR, J Bacteriol 2012 194 2248 2253 10.1128/JB.00044-12 22366414
23. Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Zhang W, Culley DE, Hogan M, Vitiritti L, Brockman FJ, Antonie Van Leeuwenhoek 2006 90 41 55 10.1007/s10482-006-9059-9 16680520
24. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. Palyada K, Sun YQ, Flint A, Butcher J, Naikare H, Stintzi A, BMC Genomics 2009 10 481 10.1186/1471-2164-10-481 19835633
25. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. Messner KR, Imlay JA, J Biol Chem 2002 277 42563 42571 10.1074/jbc.M204958200 12200425
26. Biofilm formation in Campylobacter jejuni. Joshua GW, Guthrie-Irons C, Karlyshev AV, Wren BW, Microbiology 2006 152 387 396 10.1099/mic.0.28358-0 16436427
27. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Resch A, Rosenstein R, Nerz C, Götz F, Appl Environ Microbiol 2005 71 2663 2676 10.1128/AEM.71.5.2663- 2676.2005 15870358
28. Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. Yoon MY, Lee KM, Park Y, Yoon SS, PLoS One 2011 6 16105 10.1371/journal.pone.0016105 21267455
29. Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. Konkel ME, Corwin MD, Joens LA, Cieplak W Jr, J Med Microbiol 1992 37 30 37 10.1099/00222615-37-1-30 1625313
30. Atypical roles for Campylobacter jejuni amino acid ATP binding cassette transporter components PaqP and PaqQ in bacterial stress tolerance and pathogen-host cell dynamics. Lin AE, Krastel K, Hobb RI, Thompson SA, Cvitkovitch DG, Gaynor EC, Infect Immun 2009 77 4912 4924 10.1128/IAI.00571-08 19703978
31. Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut. Van Deun K, Pasmans F, Ducatelle R, Flahou B, Vissenberg K, Martel A, Van den Broeck W, Van Immerseel F, Haesebrouck F, Vet Microbiol 2008 130 285 297 10.1016/j.vetmic.2007.11.027 18187272
32. The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling. Eucker TP, Konkel ME, Cell Microbiol 2012 14 226 238 10.1111/j.1462-5822.2011.01714.x 21999233
33. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Bernhardt TG, de Boer PA, Mol Microbiol 2003 48 1171 1182 10.1046/j.1365-2958.2003.03511.x 12787347
34. The twin-arginine translocation system: contributions to the pathobiology of Campylobacter jejuni. Kassem II, Zhang Q, Rajashekara G, Future Microbiol 2011 6 1315 1327 10.2217/fmb.11.107 22082291
35. Peptidoglycan-modifying enzyme Pgp1 is required for helical cell shape and pathogenicity traits in Campylobacter jejuni. Frirdich E, Biboy J, Adams C, Lee J, Ellermeier J, Gielda LD, Dirita VJ, Girardin SE, Vollmer W, Gaynor EC, PLoS Pathog 2012 8 1002602 10.1371/journal.ppat.1002602 22457624
36. Molybdenum and tungsten in Campylobacter jejuni: their physiological role and identification of separate transporters regulated by a single ModE-like protein. Taveirne ME, Sikes ML, Olson JW, Mol Microbiol 2009 74 758 771 10.1111/j.1365-2958.2009.06901.x 19919002
37. Variation of the natural transformation frequency of Campylobacter jejuni in liquid shake culture. Wilson DL, Bell JA, Young VB, Wilder SR, Mansfield LS, Linz JE, Microbiology 2003 149 3603 3615 10.1099/mic.0.26531-0 14663092
38. The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. Atack JM, Harvey P, Jones MA, Kelly DJ, J Bacteriol 2008 190 5279 5290 10.1128/JB.00100-08 18515414
39. Bacterial secreted proteins are required for the internaliztion of Campylobacter jejuni into cultured mammalian cells. Konkel ME, Kim BJ, Rivera-Amill V, Garvis SG, Mol Microbiol 1999 32 691 701 10.1046/j.1365-2958. 1999.01376.x 10361274
40. Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Monteville MR, Yoon JE, Konkel ME, Microbiology 2003 149 153 165 10.1099/mic.0.25820-0 12576589
41. Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Konkel ME, Hayes SF, Joens LA, Cieplak W Jr, Microb Pathog 1992 13 357 370 10.1016/0882-4010(92) 90079-4 1297914
42. Establishment and characterization of partially differentiated chicken enterocyte cell clones. Velge P, Bottreau E, Quéré P, Pardon P, Nicolle JC, Morisson M, Bout D, Dimier I, Eur J Cell Biol 2002 81 203 212 10.1078/0171-9335-00237 12018388