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Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract
dc.contributor.authorHendrixson, David R.en_US
dc.contributor.authorDiRita, Victor J.en_US
dc.date.accessioned2010-06-01T19:13:10Z
dc.date.available2010-06-01T19:13:10Z
dc.date.issued2004-04en_US
dc.identifier.citationHendrixson, David R.; DiRita, Victor J. (2004). "Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract." Molecular Microbiology 52(2): 471-484. <http://hdl.handle.net/2027.42/72403>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/72403
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=15066034&dopt=citationen_US
dc.description.abstractCampylobacter jejuni is the leading cause of bacterial gastroenteritis in humans in developed countries throughout the world. This bacterium frequently promotes a commensal lifestyle in the gastrointestinal tracts of many animals including birds and consumption or handling of poultry meats is a prevalent source of C. jejuni for infection in humans. To understand how the bacterium promotes commensalism, we used signature-tagged transposon mutagenesis and identified 29 mutants representing 22 different genes of C. jejuni strain 81–176 involved in colonization of the chick gastrointestinal tract. Among the determinants identified were two adjacent genes, one encoding a methyl-accepting chemotaxis protein (MCP), presumably required for proper chemotaxis to a specific environmental component, and another gene encoding a putative cytochrome c peroxidase that may function to reduce periplasmic hydrogen peroxide stress during in vivo growth. Deletion of either gene resulted in attenuation for growth throughout the gastrointestinal tract. Further examination of 10 other putative MCPs or MCP-domain containing proteins of C. jejuni revealed one other required for wild-type levels of caecal colonization. This study represents one of the first genetic screens focusing on the bacterial requirements necessary for promoting commensalism in a vertebrate host.en_US
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dc.publisherBlackwell Science Ltden_US
dc.rightsBlackwell Publishing Ltd, 2004en_US
dc.titleIdentification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tracten_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumUnit for Laboratory Animal Medicine, University of Michigan Medical School, Ann Arbor, MI 48109–0620, USA.en_US
dc.contributor.affiliationumDepartment of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109–0620, USA.en_US
dc.identifier.pmid15066034en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/72403/1/j.1365-2958.2004.03988.x.pdf
dc.identifier.doi10.1111/j.1365-2958.2004.03988.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceAkerley, B. J., and Lampe, D. J. ( 2002 ) Analysis of gene function in bacterial pathogens by GAMBIT. Methods Enzymol 0: 100 – 108.en_US
dc.identifier.citedreferenceAltekruse, S. F., Stern, N. J., Fields, P. I., and Swerdlow, D. L. ( 1999 ) Campylobacter jejuni – an emerging foodborne pathogen. Emerg Infect Dis 5: 28 – 35.en_US
dc.identifier.citedreferenceAmes, P., Studdert, C. A., Reiser, R. H., and Parkinson, J. S. ( 2002 ) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060 – 7065.en_US
dc.identifier.citedreferenceBeery, J. T., Hugdahl, M. B., and Doyle, M. P. ( 1988 ) Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54: 2365 – 2370.en_US
dc.identifier.citedreferenceBlack, R. E., Levine, M. M., Clements, M. L., Hughes, T. P., and Blaser, M. J. ( 1988 ) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157: 472 – 479.en_US
dc.identifier.citedreferenceBlair, D. F. ( 1995 ) How bacteria sense and swim. Annu Rev Microbiol 49: 489 – 522.en_US
dc.identifier.citedreferenceBras, A. M., Chatterjee, S., Wren, B. W., Newell, D. G., and Ketley, J. M. ( 1999 ) A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J Bacteriol 181: 3298 – 3302.en_US
dc.identifier.citedreferenceBry, L., Falk, P. G., Midtvedt, T., and Gordon, J. I. ( 1996 ) A model of host–microbial interactions in an open mammalian ecosystem. Science 273: 1380 – 1383.en_US
dc.identifier.citedreferenceDoig, P., Yao, R., Burr, D. H., Guerry, P., and Trust, T. J. ( 1996 ) An environmentally regulated pilus-like appendage involved in Campylobacter pathogenesis. Mol Microbiol 20: 885 – 894.en_US
dc.identifier.citedreferenceEllfolk, N., RÖnnberg, M., Aasa, R., AndrÉasson, L. E., and VÄnngÅrd, T. ( 1983 ) Properties and function of the two hemes in Pseudomonas cytochrome c peroxidase. Biochim Biophys Acta 743: 23 – 30.en_US
dc.identifier.citedreferenceFalke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A., and Danielson, M. A. ( 1997 ) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol 13: 457 – 512.en_US
dc.identifier.citedreferenceFalke, J. J., and Hazelbauer, G. L. ( 2001 ) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257 – 265.en_US
dc.identifier.citedreferenceFox, J. G., Ackerman, J. I., Talyor, N., Claps, M., and Murphy, J. C. ( 1987 ) Campylobacter jejuni infection in the ferret: an animal model of human campylobacteriosis. Am J Vet Res 48: 85 – 90.en_US
dc.identifier.citedreferenceFriedman, C. R., Neimann, J., Wegener, H. C., and Tauxe, R. V. ( 2000 ) Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter. Nachamkin, I., and Blaser, M. J. (eds). Washington, DC: American Society for Microbiology Press, pp. 121 – 138.en_US
dc.identifier.citedreferenceGoodhew, C. F., Wilson, I. B. H., Hunter, D. J. B., and Pettigrew, G. W. ( 1990 ) The cellular location and specificity of bacterial cytochrome c peroxidases. Biochem J 271: 707 – 712.en_US
dc.identifier.citedreferenceGraf, J., and Ruby, E. G. ( 1998 ) Host-derived amino acid support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 95: 1818 – 1822.en_US
dc.identifier.citedreferenceHazelbauer, G. L., Park, C., and Nowlin, D. M. ( 1989 ) Adaptational ‘crosstalk’ and the crucial role of methlyation in chemotactic migration by Escherichia coli. Proc Natl Acad Sci USA 86: 1448 – 1452.en_US
dc.identifier.citedreferenceHendrixson, D. R., and DiRita, V. J. ( 2003 ) Transcription of σ 54 -dependent but not σ 28 -dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol 50: 687 – 702.en_US
dc.identifier.citedreferenceHendrixson, D. R., Akerley, B. J., and DiRita, V. J. ( 2001 ) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40: 214 – 224.en_US
dc.identifier.citedreferenceHensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E., and Holden, D. W. ( 1995 ) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400 – 403.en_US
dc.identifier.citedreferenceHeungens, K., Cowles, C. E., and Goodrich-Blair, H. ( 2002 ) Identification of Xenorhabdus nematophila genes required for mutualistic colonization of Steinernema carpocapsae nematodes. Mol Microbiol 45: 1337 – 1353.en_US
dc.identifier.citedreferenceHooper, L. V., Xu, J., Falk, P. G., Midtvedt, T., and Gordon, J. I. ( 1999 ) A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci USA 96: 9833 – 9838.en_US
dc.identifier.citedreferenceHooper, L. V., Wong, M. H., Thelin, A., Hansson, L., Falk, P. G., and Gordon, J. I. ( 2001 ) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881 – 884.en_US
dc.identifier.citedreferenceHooper, L. V., Stappenbeck, T. S., Hong, C. V., and Gordon, J. I. ( 2003 ) Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nature Immun 4: 269 – 273.en_US
dc.identifier.citedreferenceKendall, E. J. C., and Tanner, E. I. ( 1982 ) Campylobacter enteritis in general practice. J Hyg 88: 155 – 163.en_US
dc.identifier.citedreferenceKim, K. K., Yokota, H., and Kim, S. -H. ( 1999 ) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400: 787 – 792.en_US
dc.identifier.citedreferenceKorlath, J. A., Osterholm, M. T., Judy, L. A., Forfang, J. C., and Robinson, R. A. ( 1985 ) A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152: 592 – 596.en_US
dc.identifier.citedreferenceLindblom, G. -B., SjÖgren, E., and Kaijser, B. ( 1986 ) Natural campylobacter colonization in chickens raised under different environmental conditions. J Hyg 96: 385 – 391.en_US
dc.identifier.citedreferenceLinton, D., Allan, E., Karlyshev, A. V., Cronshaw, A. D., and Wren, B. W. ( 2002 ) Identification of N -acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol Microbiol 43: 497 – 508.en_US
dc.identifier.citedreferenceMarchant, J., Wren, B., and Ketley, J. ( 2002 ) Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol 10: 155 – 159.en_US
dc.identifier.citedreferenceMartindale, J., Stroud, D., Moxon, E. R., and Tang, C. M. ( 2000 ) Genetic analysis of Escherichia coli K1 gastrointestinal colonization. Mol Microbiol 37: 1293 – 1305.en_US
dc.identifier.citedreferenceMerrell, D. S., Hava, D. L., and Camilli, A. ( 2002 ) Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol Microbiol 43: 1471 – 1491.en_US
dc.identifier.citedreferenceNachamkin, I., Yang, X. -H., and Stern, N. J. ( 1993 ) Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl Environ Microbiol 59: 1269 – 1273.en_US
dc.identifier.citedreferenceParkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., et al. ( 2000 ) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665 – 668.en_US
dc.identifier.citedreferencePerret, X., Staehelin, C., and Broughton, W. J. ( 2000 ) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180 – 201.en_US
dc.identifier.citedreferencePerry, R. ( 1999 ) Signature-tagged mutagenesis and the hunt for virulence factors. Trends Microbiol 7: 385 – 388.en_US
dc.identifier.citedreferencePokamunski, S., Kass, N., Borochovich, E., Marantz, B., and Rogol, M. ( 1986 ) Incidence of Campylobacter spp. in broiler flocks monitored from hatching to slaughter. Avian Path 15: 83 – 92.en_US
dc.identifier.citedreferenceRÖnnberg, M., and Ellfolk, N. ( 1979 ) Heme-linked properties of Pseudomonas cytochrome c peroxidase. Evidence for non-equivalence of hemes. Biochim Biophys Acta 581: 325 – 333.en_US
dc.identifier.citedreferenceRuby, E. G. ( 1996 ) Lessons from a cooperative, bacterial–animal association: The Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50: 591 – 624.en_US
dc.identifier.citedreferenceShea, J. E., Santangelo, J. D., and Feldman, R. G. ( 2000 ) Signature-tagged mutagenesis in the identification of virulence genes in pathogens. Curr Opin Microbiol 3: 451 – 458.en_US
dc.identifier.citedreferenceStappenbeck, T. S., Hooper, L. V., and Gordon, J. I. ( 2002 ) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99: 15451 – 15455.en_US
dc.identifier.citedreferenceStern, N. J., and Line, J. E. ( 1992 ) Comparison of three methods for recovery of Campylobacter spp. from broiler carcasses. J Food Prot 55: 663 – 666.en_US
dc.identifier.citedreferenceStern, N. J., Bailey, J. S., Blankenship, L. C., Cox, N. A., and McHan, F. ( 1988 ) Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Dis 32: 330 – 334.en_US
dc.identifier.citedreferenceSzymanksi, C. M., Yao, R., Ewing, C. P., Trust, T. J., and Guerry, P. ( 1999 ) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32: 1022 – 1030.en_US
dc.identifier.citedreferenceVisick, K. L., and McFall-Ngai, M. J. ( 2000 ) An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J Bacteriol 182: 1779 – 1787.en_US
dc.identifier.citedreferenceWassenaar, T. M., van der Zeijst, B. A. M., Ayling, R., and Newell, D. G. ( 1993 ) Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139: 1171 – 1175.en_US
dc.identifier.citedreferenceWempe, J. M., Genigeorgis, C. A., Farver, T. B., and Yusufu, H. I. ( 1983 ) Prevalence of Campylobacter jejuni in two California chicken processing plants. Appl Environ Microbiol 45: 355 – 359.en_US
dc.identifier.citedreferenceYao, R., Burr, D. H., Doig, P., Trust, T. J., Niu, H., and Guerry, P. ( 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.en_US
dc.identifier.citedreferenceYao, R., Burr, D. H., and Guerry, P. ( 1997 ) CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23: 1021 – 1031.en_US
dc.identifier.citedreferenceZiprin, R. L., Young, C. R., Stanker, L. H., Hume, M. E., and Konkel, M. E. ( 1999 ) The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding proteins. Avian Dis 43: 586 – 589.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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