European Journal of Microbiology and Immunology
Volume/Issue:
Volume 5: Issue 1
Campylobacter jejuni serine protease HtrA plays an important role in heat tolerance, oxygen resistance, host cell adhesion, invasion, and transmigration
Authors: Manja Boehm 1 , Judith Lind 1 , Steffen Backert 1 , and Nicole Tegtmeyer 1
View More View Less
  • 1 Friedrich Alexander University Erlangen/Nuremberg Department of Biology, Division of Microbiology Staudtstr. 5 D-91058 Erlangen Germany
DOI:
https://doi.org/10.1556/eujmi-d-15-00003
Page Count:
68–80
Publication Date:
01 Mar 2015
Online Publication Date:
26 Mar 2015
Article Category:
Research Article
Open access

Campylobacter jejuni is an important pathogen of foodborne illness. Transmigration across the intestinal epithelial barrier and invasion are considered as primary reasons for tissue damage triggered by C. jejuni. Using knockout mutants, it was shown that the serine protease HtrA may be important for stress tolerance and physiology of C. jejuni. HtrA is also secreted in the extracellular environment, where it can cleave junctional host cell proteins such as E-cadherin. Aim of the present study was to establish a genetic complementation system in two C. jejuni strains in order to introduce the wild-type htrA gene in trans, test known htrA phenotypes, and provide the basis to perform further mutagenesis. We confirm that reexpression of the htrA wild-type gene in ΔhtrA mutants restored the following phenotypes: 1) C. jejuni growth at high temperature (44 °C), 2) growth under high oxygen stress conditions, 3) expression of proteolytically active HtrA oligomers, 4) secretion of HtrA into the supernatant, 5) cell attachment and invasion, and 6) transmigration across polarized epithelial cells. These results establish a genetic complementation system for htrA in C. jejuni, exclude polar effects in the ΔhtrA mutants, confirm important HtrA properties, and permit the discovery and dissection of new functions.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • World Health Organization: Foodborne Diseases. WHO 2014, Geneva, Switzerland (http://www.who.int/foodsafety/areas_work/foodborne-diseases/en/)

  • Young KT, Davis LM, DiRita VJ: Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5, 665–679 (2007)

    DiRita VJ , 'Campylobacter jejuni: molecular biology and pathogenesis ' (2007 ) 5 Nat Rev Microbiol : 665 -679.

    • Search Google Scholar

  • Nachamkin I, Szymanski CM, Blaser MJ (2008): Campylobacter. ASM Press, Washington, DC

    Blaser MJ , '', in Campylobacter , (2008 ) -.

  • Oyarzabal OA, Backert S (2011): Microbial Food Safety. Springer, New York

    Backert S , '', in Microbial Food Safety , (2011 ) -.

  • Talukder RK, Sutradhar SR, Rahman KM, Uddin MJ, Akhter H: Guillian–Barre syndrome. Mymensingh Med J 20, 748–756 (2011)

    Akhter H , 'Guillian–Barre syndrome ' (2011 ) 20 Mymensingh Med J : 748 -756.

  • Wakerley BR, Uncini A, Yuki N, GBS Classification Group, GBS Classification Group: Guillain–Barré and Miller Fisher syndromes—new diagnostic classification. Nat Rev Neurol 10, 537–544 (2014)

    Yuki N , 'Guillain–Barré and Miller Fisher syndromes—new diagnostic classification ' (2014 ) 10 Nat Rev Neurol : 537 -544.

    • Search Google Scholar

  • Hofreuter D: Defining the metabolic requirements for the growth and colonization capacity of Campylobacter jejuni. Front Cell Infect Microbiol 4, 137 (2014)

    Hofreuter D , 'Defining the metabolic requirements for the growth and colonization capacity of Campylobacter jejuni ' (2014 ) 4 Front Cell Infect Microbiol : 137 -.

    • Search Google Scholar

  • Wassenaar TM, Blaser MJ: Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1, 1023–1033 (1999)

    Blaser MJ , 'Pathophysiology of Campylobacter jejuni infections of humans ' (1999 ) 1 Microbes Infect : 1023 -1033.

    • Search Google Scholar

  • Gölz G, Sharbati S, Backert S, Alter T: Quorum sensing dependent phenotypes and their molecular mechanisms in Campylobacterales. Eur J Microbiol Immunol (Bp) 2, 50–60 (2012)

    Alter T , 'Quorum sensing dependent phenotypes and their molecular mechanisms in Campylobacterales ' (2012 ) 2 Eur J Microbiol Immunol (Bp) : 50 -60.

    • Search Google Scholar

  • Ó Cróinín T, Backert S: Host epithelial cell invasion by Campylobacter jejuni: trigger or zipper mechanism? Front Cell Infect Microbiol 2, 25 (2012)

    Backert S , 'Host epithelial cell invasion by Campylobacter jejuni: trigger or zipper mechanism ' (2012 ) 2 Front Cell Infect Microbiol : 25 -.

    • Search Google Scholar

  • Szymanski CM, King M, Haardt M, Armstrong GD: Campylobacter jejuni motility and invasion of Caco-2 cells. Infect Immun 63, 4295–4300 (1995)

    Armstrong GD , 'Campylobacter jejuni motility and invasion of Caco-2 cells ' (1995 ) 63 Infect Immun : 4295 -4300.

    • Search Google Scholar

  • Young GM, Schmiel DH, Miller VL: A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA 96, 6456–6461 (1999)

    Miller VL , 'A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system ' (1999 ) 96 Proc Natl Acad Sci USA : 6456 -6461.

    • Search Google Scholar

  • Konkel ME, Gray SA, Kim BJ, Garvis SG, Yoon JJ: Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. Clin Microbiol 37, 510–517 (1999)

    Yoon JJ , 'Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product ' (1999 ) 37 Clin Microbiol : 510 -517.

    • Search Google Scholar

  • Christensen JE, Pacheco SA, Konkel ME: Identification of a Campylobacter jejuni — secreted protein required for maximal invasion of host cells. Mol Microbiol 73, 650–662 (2009)

    Konkel ME , 'Identification of a Campylobacter jejuni — secreted protein required for maximal invasion of host cells ' (2009 ) 73 Mol Microbiol : 650 -662.

    • Search Google Scholar

  • Neal-McKinney JM, Christensen JE, Konkel ME: Aminoterminal residues dictate the export efficiency of the Campylobacter jejuni filament proteins via the flagellum. Mol Microbiol 76, 918–931 (2010)

    Konkel ME , 'Aminoterminal residues dictate the export efficiency of the Campylobacter jejuni filament proteins via the flagellum ' (2010 ) 76 Mol Microbiol : 918 -931.

    • Search Google Scholar

  • Euker TP, Konkel ME: The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling. Cell Microbiol 14, 226–238 (2012)

    Konkel ME , 'The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling ' (2012 ) 14 Cell Microbiol : 226 -238.

    • Search Google Scholar

  • Barrero-Tobon AM, Hendrixson DR: Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization. Mol Microbiol 84, 352–369 (2012)

    Hendrixson DR , 'Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization ' (2012 ) 84 Mol Microbiol : 352 -369.

    • Search Google Scholar

  • Barrero-Tobon AM, Hendrixson DR: Flagellar biosynthesis exerts temporal regulation of secretion of specific Campylobacter jejuni colonization and virulence determinants. Mol Microbiol 93, 957–974 (2014)

    Hendrixson DR , 'Flagellar biosynthesis exerts temporal regulation of secretion of specific Campylobacter jejuni colonization and virulence determinants ' (2014 ) 93 Mol Microbiol : 957 -974.

    • Search Google Scholar

  • Pei Z, Burucoa C, Grignon B, Baqar S, Huang XZ, Kopecko DJ, Bourgeois AL, Fauchere JL, Blaser MJ: Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 66, 938–943 (1998)

    Blaser MJ , 'Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice ' (1998 ) 66 Infect Immun : 938 -943.

    • Search Google Scholar

  • Konkel ME, Monteville MR, Rivera-Amill V, Joens LA: The pathogenesis of Campylobacter jejuni-mediated enteritis. Curr Issues Intest Microbiol 2, 55–71 (2001)

    Joens LA , 'The pathogenesis of Campylobacter jejuni-mediated enteritis ' (2001 ) 2 Curr Issues Intest Microbiol : 55 -71.

    • Search Google Scholar

  • Poly F, Guerry P: Pathogenesis of Campylobacter. Curr Opin Gastroenterol 24, 27–31 (2008)

    Guerry P , 'Pathogenesis of Campylobacter ' (2008 ) 24 Curr Opin Gastroenterol : 27 -31.

  • Brøndsted L, Andersen MT, Parker M, Jørgensen K, Ingmer H: The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Appl Environ Micro biol 71, 3205–3212 (2005)

    Ingmer H , 'The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells ' (2005 ) 71 Appl Environ Micro biol : 3205 -3212.

    • Search Google Scholar

  • Bæk KT, Vegge CS, Brøndsted L: HtrA chaperone activity contributes to host cell binding in Campylobacter jejuni. Gut Pathog 3, 13 (2011)

    Brøndsted L , 'HtrA chaperone activity contributes to host cell binding in Campylobacter jejuni ' (2011 ) 3 Gut Pathog : 13 -.

    • Search Google Scholar

  • Krause-Gruszczynska M, Rohde M, Hartig R, Genth H, Schmidt G, Keo T, Koenig W, Miller WG, Konkel ME, Backert S: Role of small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell Microbiol 9, 2431–2444 (2007)

    Backert S , 'Role of small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni ' (2007 ) 9 Cell Microbiol : 2431 -2444.

    • Search Google Scholar

  • Krause-Gruszczynska M, Boehm M, Rohde M, Tegtmeyer N, Takahashi S, Buday L, Oyarzabal OA, Backert S: The signaling pathway of Campylobacter jejuni-induced Cdc42 activation: Role of fibronectin, integrin beta1, tyrosine kinases and guanine exchange factor Vav2. Cell Commun Signal 9, 32 (2011)

    Backert S , 'The signaling pathway of Campylobacter jejuni-induced Cdc42 activation: Role of fibronectin, integrin beta1, tyrosine kinases and guanine exchange factor Vav2 ' (2011 ) 9 Cell Commun Signal : 32 -.

    • Search Google Scholar

  • Boehm M, Hoy B, Rohde M, Tegtmeyer N, Bæk KT, Oyarzabal OA, Brøndsted L, Wessler S, Backert S: Rapid paracellular transmigration of Campylobacter jejuni across polarized epithelial cells without affecting TER: role of proteolytic-active HtrA cleaving E-cadherin but not fibronectin. Gut Pathog 4, 3 (2012)

    Backert S , 'Rapid paracellular transmigration of Campylobacter jejuni across polarized epithelial cells without affecting TER: role of proteolytic-active HtrA cleaving E-cadherin but not fibronectin ' (2012 ) 4 Gut Pathog : 3 -.

    • Search Google Scholar

  • Ingmer H, Brøndsted L: Proteases in bacterial pathogenesis. Res Microbiol 160, 704–710 (2009)

    Brøndsted L , 'Proteases in bacterial pathogenesis ' (2009 ) 160 Res Microbiol : 704 -710.

  • Frees D, Brøndsted L, Ingmer H: Bacterial proteases and virulence. Subcell Biochem 66, 161–192 (2013)

    Ingmer H , 'Bacterial proteases and virulence ' (2013 ) 66 Subcell Biochem : 161 -192.

  • Backert S, Boehm M, Wessler S, Tegtmeyer N: Transmigration route of Campylobacter jejuni across polarized intestinal epithelial cells: paracellular, transcellular or both? Cell Commun Signal 11, 72 (2013)

    Tegtmeyer N , 'Transmigration route of Campylobacter jejuni across polarized intestinal epithelial cells: paracellular, transcellular or both ' (2013 ) 11 Cell Commun Signal : 72 -.

    • Search Google Scholar

  • Skorko-Glonek J, Zurawa-Janicka D, Koper T, Jarzab M, Figaj D, Glaza P, Lipinska B: HtrA protease family as therapeutic targets. Curr Pharm Des 19, 977–1009 (2013)

    Lipinska B , 'HtrA protease family as therapeutic targets ' (2013 ) 19 Curr Pharm Des : 977 -1009.

    • Search Google Scholar

  • Kim DY, Kim KK: Structure and function of HtrA family proteins, the key players in protein quality control. J Biochem Mol Biol 38, 266–274 (2005)

    Kim KK , 'Structure and function of HtrA family proteins, the key players in protein quality control ' (2005 ) 38 J Biochem Mol Biol : 266 -274.

    • Search Google Scholar

  • Clausen T, Southan C, Ehrmann M: The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10, 443–455 (2002)

    Ehrmann M , 'The HtrA family of proteases: implications for protein composition and cell fate ' (2002 ) 10 Mol Cell : 443 -455.

    • Search Google Scholar

  • Clausen T, Kaiser M, Huber R, Ehrmann M: HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12, 152–162 (2011)

    Ehrmann M , 'HTRA proteases: regulated proteolysis in protein quality control ' (2011 ) 12 Nat Rev Mol Cell Biol : 152 -162.

    • Search Google Scholar

  • Hoy B, Löwer M, Weydig C, Carra G, Tegtmeyer N, Geppert T, Schröder P, Sewald N, Backert S, Schneider G, Wessler S: Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep 11, 798–804 (2010)

    Wessler S , 'Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion ' (2010 ) 11 EMBO Rep : 798 -804.

    • Search Google Scholar

  • Hoy B, Geppert T, Boehm M, Reisen F, Plattner P, Gadermaier G, Sewald N, Ferreira F, Briza P, Schneider G, Backert S, Wessler S: Distinct roles of secreted HtrA proteases from gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin. J Biol Chem 23, 10115–10120 (2012)

    Wessler S , 'Distinct roles of secreted HtrA proteases from gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin ' (2012 ) 23 J Biol Chem : 10115 -10120.

    • Search Google Scholar

  • Champion OL, Karlyshev AV, Senior NJ, Woodward M, La Ragione R, Howard SL, Wren BW, Titball RW: Insect infection model for Campylobacter jejuni reveals that Omethyl phosphoramidate has insecticidal activity. J Infect Dis 201, 776–782 (2010)

    Titball RW , 'Insect infection model for Campylobacter jejuni reveals that Omethyl phosphoramidate has insecticidal activity ' (2010 ) 201 J Infect Dis : 776 -782.

    • Search Google Scholar

  • Heimesaat MM, Alutis M, Grundmann U, Fischer A, Tegtmeyer N, Böhm M, Kühl AA, Göbel UB, Backert S, Bereswill S: The role of serine protease HtrA in acute ulcerative enterocolitis and extra-intestinal immune responses during Campylobacter jejuni infection of gnotobiotic IL-10 deficient mice. Front Cell Infect Microbiol 4, 77 (2014)

    Bereswill S , 'The role of serine protease HtrA in acute ulcerative enterocolitis and extra-intestinal immune responses during Campylobacter jejuni infection of gnotobiotic IL-10 deficient mice ' (2014 ) 4 Front Cell Infect Microbiol : 77 -.

    • Search Google Scholar

  • Heimesaat MM, Fischer A, Alutis M, Grundmann U, Boehm M, Tegtmeyer N, Göbel UB, Kühl AA, Bereswill S, Backert S: The impact of serine protease HtrA in apoptosis, intestinal immune responses and extra-intestinal histopathology during Campylobacter jejuni infection of infant mice. Gut Pathog 6, 16 (2014)

    Backert S , 'The impact of serine protease HtrA in apoptosis, intestinal immune responses and extra-intestinal histopathology during Campylobacter jejuni infection of infant mice ' (2014 ) 6 Gut Pathog : 16 -.

    • Search Google Scholar

  • Boehm M, Haenel I, Hoy B, Brøndsted L, Smith TG, Hoover T, Wessler S, Tegtmeyer N: Extracellular secretion of protease HtrA from Campylobacter jejuni is highly efficient and independent of its protease activity and flagellum. Eur J Microbiol Immunol (Bp) 3, 163–173 (2013)

    Tegtmeyer N , 'Extracellular secretion of protease HtrA from Campylobacter jejuni is highly efficient and independent of its protease activity and flagellum ' (2013 ) 3 Eur J Microbiol Immunol (Bp) : 163 -173.

    • Search Google Scholar

  • Wroblewski LE, Shen L, Ogden S, Romero-Gallo J, Lapierre LA, Israel DA, Turner JR, Peek RM Jr: Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation. Gastroenterology 136, 236–246 (2009)

    Peek RM , 'Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation ' (2009 ) 136 Gastroenterology : 236 -246.

    • Search Google Scholar

  • Li SR, Dorrell N, Everest PH, Dougan G, Wren BW: Construction and characterization of a Yersinia enterocolitica O:8 high-temperature requirement (htrA) isogenic mutant. Infect Immun, 64, 2088–2094 (1996)

    Wren BW , 'Construction and characterization of a Yersinia enterocolitica O:8 high-temperature requirement (htrA) isogenic mutant ' (1996 ) 64 Infect Immun : 2088 -2094.

    • Search Google Scholar

  • Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M: The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67, 1560–1568 (1999)

    Roberts M , 'The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium ' (1999 ) 67 Infect Immun : 1560 -1568.

    • Search Google Scholar

  • Cortes G, de Astorza B, Benedi VJ, Alberti S: Role of the htrA gene in Klebsiella pneumoniae virulence. Infect Immun 70, 4772–4776 (2002)

    Alberti S , 'Role of the htrA gene in Klebsiella pneumoniae virulence ' (2002 ) 70 Infect Immun : 4772 -4776.

    • Search Google Scholar

  • Purdy GE, Hong M, Payne SM: Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect Immun. 70, 6355–6364 (2002)

    Payne SM , 'Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread ' (2002 ) 70 Infect Immun. : 6355 -6364.

    • Search Google Scholar

  • Wilson RL, Brown LL, Kirkwood-watts D, Warren TK, Lund SA, King DS, Jones KF, Hruby DE: Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence. Microbiology 74, 765–768 (2006)

    Hruby DE , 'Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence ' (2006 ) 74 Microbiology : 765 -768.

    • Search Google Scholar

  • Gloeckl S, Ong VA, Patel P, Tyndall JD, Timms P, Beagley KW, Allan JA, Armitage CW, Turnbull L, Whitchurch CB, Merdanovic M, Ehrmann M, Powers JC, Oleksyszyn J, Verdoes M, Bogyo M, Huston WM: Identification of a serine protease inhibitor which causes inclusion vacuole reduction and is lethal to Chlamydia trachomatis. Mol Microbiol 89, 676–689 (2013)

    Huston WM , 'Identification of a serine protease inhibitor which causes inclusion vacuole reduction and is lethal to Chlamydia trachomatis ' (2013 ) 89 Mol Microbiol : 676 -689.

    • Search Google Scholar

  • Weibezahn J, Schlieker C, Tessarz P, Mogk A, Bukau B: Novel insights into the mechanism of chaperone-assisted protein disaggregation. Biol Chem 386, 739–744 (2005)

    Bukau B , 'Novel insights into the mechanism of chaperone-assisted protein disaggregation ' (2005 ) 386 Biol Chem : 739 -744.

    • Search Google Scholar

  • Doyle SM, Wickner S: Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34, 40–48 (2009)

    Wickner S , 'Hsp104 and ClpB: protein disaggregating machines ' (2009 ) 34 Trends Biochem Sci : 40 -48.

    • Search Google Scholar

  • Johnson, K., I. Charles, G. Dougan, D. Pickard, P. O’Gaora, G. Costa, T. Ali, I. Miller, Hormaeche C: The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol 5, 401–407 (1991)

    Miller I , 'The role of a stress-response protein in Salmonella typhimurium virulence ' (1991 ) 5 Mol Microbiol : 401 -407.

    • Search Google Scholar

  • Elzer, PH, Phillips RW, Robertson GT, Roop RM: The HtrA stress response protease contributes to resistance of Brucella abortus to killing by murine phagocytes. Infect Immun 64, 4838–4841 (1996)

    Roop RM , 'The HtrA stress response protease contributes to resistance of Brucella abortus to killing by murine phagocytes ' (1996 ) 64 Infect Immun : 4838 -4841.

    • Search Google Scholar

  • Smith MA, Finel M, Korolik V, Mendz GL: Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori. Arch Microbiol 174, 1–10 (2000)

    Mendz GL , 'Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori ' (2000 ) 174 Arch Microbiol : 1 -10.

    • Search Google Scholar

  • Krojer T, Sawa J, Schäfer E, Saibil HR, Ehrmann M, Clausen T: Structural basis for the regulated protease and chaperone function of DegP. Nature 453, 885–890 (2008)

    Clausen T , 'Structural basis for the regulated protease and chaperone function of DegP ' (2008 ) 453 Nature : 885 -890.

    • Search Google Scholar

  • 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: The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668 (2000)

    Barrell BG , 'The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences ' (2000 ) 403 Nature : 665 -668.

    • Search Google Scholar

  • Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, Ravel J, Brinkac LM, DeBoy RT, Parker CT, Daugherty SC, Dodson RJ, Durkin AS, Madupu R, Sullivan SA, Shetty JU, Ayodeji MA, Shvartsbeyn A, Schatz MC, Badger JH, Fraser CM, Nelson KE: Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3, e15 (2005)

    Nelson KE , 'Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species ' (2005 ) 3 PLoS Biol : 15 -.

    • Search Google Scholar

  • Hofreuter D, Tsai J, Watson RO, Novik V, Altman B, Benitez M, Clark C, Perbost C, Jarvie T, Du L, Galán JE: Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74, 4694–4707 (2006)

    Galán JE , 'Unique features of a highly pathogenic Campylobacter jejuni strain ' (2006 ) 74 Infect Immun : 4694 -4707.

    • Search Google Scholar

  • Wiesner RS, Hendrixson DR, DiRita VJ: Natural transformation of Campylobacter jejuni requires components of a type II secretion system. J Bacteriol 185, 5408–5418 (2003)

    DiRita VJ , 'Natural transformation of Campylobacter jejuni requires components of a type II secretion system ' (2003 ) 185 J Bacteriol : 5408 -5418.

    • Search Google Scholar

  • Novik V, Hofreuter D, Galan JE: Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells. Infect Immun 78, 3540–3553 (2010)

    Galan JE , 'Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells ' (2010 ) 78 Infect Immun : 3540 -3553.

    • Search Google Scholar

  • Boehm M, Krause-Gruszczynska M, Rohde M, Tegtmeyer N, Takahashi S, Oyarzabal OA, Backert S: Major host factors involved in epithelial cell invasion of Campylobacter jejuni: Role of fibronectin, integrin beta1, FAK, Tiam-1 and DOCK180 in activating Rho GTPase Rac1. Front Cell Infect Microbiol 1, 17 (2011)

    Backert S , 'Major host factors involved in epithelial cell invasion of Campylobacter jejuni: Role of fibronectin, integrin beta1, FAK, Tiam-1 and DOCK180 in activating Rho GTPase Rac1 ' (2011 ) 1 Front Cell Infect Microbiol : 17 -.

    • Search Google Scholar

  • Ashgar SS, Oldfield NJ, Wooldridge KG, Jones MA, Irving GJ, Turner DP, Ala’Aldeen DA: CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut. J Bacteriol 189, 1856–1865 (2007)

    Ala’Aldeen DA , 'CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut ' (2007 ) 189 J Bacteriol : 1856 -1865.

    • Search Google Scholar

  • Jin S, Joe A, Lynett J, Hani EK, Sherman P, Chan VL: JlpA, a novel surface exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39, 1225–1236 (2001)

    Chan VL , 'JlpA, a novel surface exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells ' (2001 ) 39 Mol Microbiol : 1225 -1236.

    • Search Google Scholar

  • Szymanski CM, Burr DH, Guerry P: Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70, 2242–2244 (2002)

    Guerry P , 'Campylobacter protein glycosylation affects host cell interactions ' (2002 ) 70 Infect Immun : 2242 -2244.

    • Search Google Scholar

  • Vuckovic D, Abram M, Doric M: Primary Campylobacter jejuni infection in different mice strains. Microb Pathog 24, 263–268 (1998)

    Doric M , 'Primary Campylobacter jejuni infection in different mice strains ' (1998 ) 24 Microb Pathog : 263 -268.

    • Search Google Scholar

  • Watson RO, Novik V, Hofreuter D, Lara-Tejero M, Galan JE: A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection. Infect Immun 75, 1994–2003 (2007)

    Galan JE , 'A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection ' (2007 ) 75 Infect Immun : 1994 -2003.

    • Search Google Scholar

  • Lamb-Rosteski JM, Kalischuk LD, Inglis GD, Buret AG: Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect Immun 76, 3390–3398 (2008)

    Buret AG , 'Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation ' (2008 ) 76 Infect Immun : 3390 -3398.

    • Search Google Scholar

  • Nemelka KW, Brown AW, Wallace SM, Jones E, Asher LV, Pattarini D, Applebee L, Gilliland TC Jr, Guerry P, Baqar S: Immune response to and histopathology of Campylobacter jejuni infection in ferrets (Mustela putorius furo). Comp Med 59, 363–371 (2009)

    Baqar S , 'Immune response to and histopathology of Campylobacter jejuni infection in ferrets (Mustela putorius furo) ' (2009 ) 59 Comp Med : 363 -371.

    • Search Google Scholar

  • Everest PH, Goossens H, Sibbons P, Lloyd DR, Knutton S, Leece R, Ketley JM, Williams PH: Pathological changes in the rabbit ileal loop model caused by Campylobacter jejuni from human colitis. J Med Microbiol 38, 316–321 (1993)

    Williams PH , 'Pathological changes in the rabbit ileal loop model caused by Campylobacter jejuni from human colitis ' (1993 ) 38 J Med Microbiol : 316 -321.

    • Search Google Scholar

  • Zhou P, Hussain SK, Liles MR, Arias CR, Backert S, Kieninger J, Oyarzabal OA. A simplified and cost-effective enrichment protocol for the isolation of Campylobacter spp. from retail broiler meat without microaerobic incubation. BMC Microbiol 11, 175 (2011)

    Oyarzabal OA , 'A simplified and cost-effective enrichment protocol for the isolation of Campylobacter spp. from retail broiler meat without microaerobic incubation ' (2011 ) 11 BMC Microbiol : 175 -.

    • Search Google Scholar

  • Speegle L, Miller ME, Backert S, Oyarzabal OA: Use of cellulose filters to isolate Campylobacter spp. from naturally contaminated retail broiler meat. J Food Prot 72, 2592–2596 (2009)

    Oyarzabal OA , 'Use of cellulose filters to isolate Campylobacter spp. from naturally contaminated retail broiler meat ' (2009 ) 72 J Food Prot : 2592 -2596.

    • Search Google Scholar

  • Backert S, Hofreuter D: Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen Campylobacter jejuni. J Microbiol Methods 95, 8–23 (2013)

    Hofreuter D , 'Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen Campylobacter jejuni ' (2013 ) 95 J Microbiol Methods : 8 -23.

    • Search Google Scholar

  • Tegtmeyer N, Rivas Traverso F, Rohde M, Oyarzabal OA, Lehn N, Schneider-Brachert W, Ferrero RL, Fox JG, Berg DE, Backert S: Electron microscopic, genetic and protein expression analyses of Helicobacter acinonychis strains from a Bengal tiger. PLoS One 8, e71220 (2013)

    Backert S , 'Electron microscopic, genetic and protein expression analyses of Helicobacter acinonychis strains from a Bengal tiger ' (2013 ) 8 PLoS One : 71220 -.

    • Search Google Scholar

  • Tegtmeyer N, Wittelsberger R, Hartig R, Wessler S, Martinez-Quiles, Backert S: Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori. Cell Host Microbe 9, 520–531 (2011)

    Martinez-Quiles B S , 'Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori ' (2011 ) 9 Cell Host Microbe : 520 -531.

    • Search Google Scholar

  • Mueller D, Tegtmeyer N, Brandt S, Yamaoka Y, De Poire E, Sgouras D, Wessler S, Torres J, Smolka A, Backert S: c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 122, 1553–1566 (2012)

    Backert S , 'c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains ' (2012 ) 122 J Clin Invest : 1553 -1566.

    • Search Google Scholar
Cover European Journal of Microbiology and Immunology
European Journal of Microbiology and Immunology
Online ISSN:
2062-8633
Keywords:
HtrA; secretion; chaperone; flagellum; E-cadherin; molecular pathogenesis; cellular invasion; signaling; transwell; paracellular; virulence; stress response

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Sep 2020 0 5 2
Oct 2020 0 5 4
Nov 2020 0 13 6
Dec 2020 0 4 4
Jan 2021 0 15 15
Feb 2021 0 6 3
Mar 2021 0 2 1