Unique cell adhesion and invasion properties of yersinia enterocolitica O:3, the most frequent cause of human yersiniosis

PLoS Pathogens

Volumn 7, Issue 7, 2011, Pages

  Uliczka, Frank ^a,b   Pisano, Fabio ^a   Schaake, Julia ^a,b   Stolz, Tatjana ^a,b   Rohde, Manfred ^a   Fruth, Angelika ^c   Strauch, Eckhard ^d   Skurnik, Mikael ^e   Batzilla, Julia ^f   Rakin, Alexander ^f   Heesemann, Jürgen ^f   Dersch, Petra ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

^d Bundesinstitut für Risikoforschung   (Germany)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^f UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; INVA PROTEIN; INVASIN; O ANTIGEN; ROVA PROTEIN; UNCLASSIFIED DRUG; YADA PROTEIN; ADHESIN; INVASIN, YERSINIA; VIRULENCE FACTOR; YADA PROTEIN, YERSINIA;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL STRAIN; BINDING SITE; CELL ADHESION; CELL INVASION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; FEMALE; GENE INSERTION; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SEROTYPE; TEMPERATURE; THERMOREGULATION; TRANSCRIPTION INITIATION SITE; YERSINIA ENTEROCOLITICA; YERSINIOSIS; ADAPTATION; ANIMAL; BACTERIUM ADHERENCE; BAGG ALBINO MOUSE; CELL CULTURE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HEAT; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; YERSINIA INFECTION;

BACTERIA (MICROORGANISMS); MURINAE; YERSINIA; YERSINIA ENTEROCOLITICA;

ADAPTATION, PHYSIOLOGICAL; ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HOT TEMPERATURE; HUMANS; MICE; MICE, INBRED BALB C; O ANTIGENS; VIRULENCE FACTORS; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

EID: 79960959125     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002117     Document Type: Article

References (78)

1. Bottone EJ, (1997) Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10: 257-276.
2. Hanski C, Naumann M, Hahn H, Riecken EO, (1989) Determinants of invasion and survival of Yersinia enterocolitica in intestinal tissue. An in vivo study. Med Microbiol Immunol 178: 289-296.
3. Grutzkau A, Hanski C, Hahn H, Riecken EO, (1990) Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 31: 1011-1015.
4. Pepe JC, Miller VL, (1993) Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A 90: 6473-6477.
5. Carter PB, (1975) Pathogenecity of Yersinia enterocolitica for mice. Infect Immun 11: 164-170.
6. Handley SA, Dube PH, Revell PA, Miller VL, (2004) Characterization of oral Yersinia enterocolitica infection in three different strains of inbred mice. Infect Immun 72: 1645-1656.
7. Handley SA, Newberry RD, Miller VL, (2005) Yersinia enterocolitica invasin-dependent and invasin-independent mechanisms of systemic dissemination. Infect Immun 73: 8453-8455.
8. Barnes PD, Bergman MA, Mecsas J, Isberg RR, (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203: 1591-1601.
9. Trulzsch K, Sporleder T, Igwe EI, Russmann H, Heesemann J, (2004) Contribution of the major secreted yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect Immun 72: 5227-5234.
10. Miller VL, Falkow S, (1988) Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56: 1242-1248.
11. Miller VL, Finlay BB, Falkow S, (1988) Factors essential for the penetration of mammalian cells by Yersinia. Curr Top Microbiol Immunol 138: 15-39.
12. Pepe JC, Wachtel MR, Wagar E, Miller VL, (1995) Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection. Infect Immun 63: 4837-4848.
13. 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.
14. Young VB, Falkow S, Schoolnik GK, (1992) The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J Cell Biol 116: 197-207.
15. Pepe JC, Badger JL, Miller VL, (1994) Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol Microbiol 11: 123-135.
16. Marra A, Isberg RR, (1997) Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer's patch intestinal epithelium. Infect Immun 65: 3412-3421.
17. Straley SC, Perry RD, (1995) Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol 3: 310-317.
18. Herbst K, Bujara M, Heroven AK, Opitz W, Weichert M, et al. (2009) Intrinsic thermal sensing controls proteolysis of Yersinia virulence regulator RovA. PLoS Pathog 5: e1000435.
19. Heise T, Dersch P, (2006) Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci U S A 103: 3375-3380.
20. Biedzka-Sarek M, Salmenlinna S, Gruber M, Lupas AN, Meri S, et al. (2008) Functional mapping of YadA- and Ail-mediated binding of human factor H to Yersinia enterocolitica serotype O:3. Infect Immun 76: 5016-5027.
21. Biedzka-Sarek M, Jarva H, Hyytiainen H, Meri S, Skurnik M, (2008) Characterization of complement factor H binding to Yersinia enterocolitica serotype O:3. Infect Immun 76: 4100-4109.
22. Felek S, Krukonis ES, (2009) The Yersinia pestis Ail protein mediates binding and Yop delivery to host cells required for plague virulence. Infect Immun 77: 825-836.
23. Tsang TM, Felek S, Krukonis ES, (2010) Ail binding to fibronectin facilitates Yersinia pestis binding to host cells and Yop delivery. Infect Immun 78: 3358-3368.
24. Pederson KJ, Pierson DE, (1995) Ail expression in Yersinia enterocolitica is affected by oxygen tension. Infect Immun 63: 4199-4201.
25. Pierson DE, Falkow S, (1993) The ail gene of Yersinia enterocolitica has a role in the ability of the organism to survive serum killing. Infect Immun 61: 1846-1852.
26. Skurnik M, Toivanen P, (1992) LcrF is the temperature-regulated activator of the yadA gene of Yersinia enterocolitica and Yersinia pseudotuberculosis. J Bacteriol 174: 2047-2051.
27. Lambert de Rouvroit C, Sluiters C, Cornelis GR, (1992) Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol Microbiol 6: 395-409.
28. Skurnik M, Toivanen P, (1993) Yersinia enterocolitica lipopolysaccharide: genetics and virulence. Trends Microbiol 1: 148-152.
29. Skurnik M, Venho R, Bengoechea JA, Moriyon I, (1999) The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31: 1443-1462.
30. al-Hendy A, Toivanen P, Skurnik M, (1992) Lipopolysaccharide O side chain of Yersinia enterocolitica O:3 is an essential virulence factor in an orally infected murine model. Infect Immun 60: 870-875.
31. Bengoechea JA, Najdenski H, Skurnik M, (2004) Lipopolysaccharide O antigen status of Yersinia enterocolitica O:8 is essential for virulence and absence of O antigen affects the expression of other Yersinia virulence factors. Mol Microbiol 52: 451-469.
32. al-Hendy A, Toivanen P, Skurnik M, (1991) The effect of growth temperature on the biosynthesis of Yersinia enterocolitica O:3 lipopolysaccharide: temperature regulates the transcription of the rfb but not of the rfa region. Microb Pathog 10: 81-86.
33. Bengoechea JA, Zhang L, Toivanen P, Skurnik M, (2002) Regulatory network of lipopolysaccharide O-antigen biosynthesis in Yersinia enterocolitica includes cell envelope-dependent signals. Mol Microbiol 44: 1045-1062.
34. Young GM, Badger JL, Miller VL, (2000) Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect Immun 68: 4323-4326.
35. Lee LA, Gerber AR, Lonsway DR, Smith JD, Carter GP, et al. (1990) Yersinia enterocolitica O:3 infections in infants and children, associated with the household preparation of chitterlings. N Engl J Med 322: 984-987.
36. Tauxe RV, (2002) Emerging foodborne pathogens. Int J Food Microbiol 78: 31-41.
37. ECDC, (2009) Annual Centre for Disease Prevention and Control. Available:http://www.ecdc.europa.eu.
38. Jones TF, (2003) From pig to pacifier: chitterling-associated yersiniosis outbreak among black infants. Emerg Infect Dis 9: 1007-1009.
39. Fredriksson-Ahomaa M, Stolle A, Siitonen A, Korkeala H, (2006) Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O: 3 originate mainly from pigs. J Med Microbiol 55: 747-749.
40. Gurtler M, Alter T, Kasimir S, Linnebur M, Fehlhaber K, (2005) Prevalence of Yersinia enterocolitica in fattening pigs. J Food Prot 68: 850-854.
41. Kapatral V, Campbell JW, Minnich SA, Thomson NR, Matsumura P, et al. (2004) Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150: 2289-2300.
42. Biedzka-Sarek M, Venho R, Skurnik M, (2005) Role of YadA, Ail, and Lipopolysaccharide in Serum Resistance of Yersinia enterocolitica Serotype O:3. Infect Immun 73: 2232-2244.
43. El Tahir Y, Skurnik M, (2001) YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291: 209-218.
44. Nagel G, Lahrz A, Dersch P, (2001) Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family. Mol Microbiol 41: 1249-1269.
45. Ellison DW, Miller VL, (2006) H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J Bacteriol 188: 5101-5112.
46. Heroven AK, Nagel G, Tran HJ, Parr S, Dersch P, (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53: 871-888.
47. Lawrenz MB, Miller VL, (2007) Comparative analysis of the regulation of rovA from the pathogenic yersiniae. J Bacteriol 189: 5963-5975.
48. Dube PH, Handley SA, Revell PA, Miller VL, (2003) The rovA mutant of Yersinia enterocolitica displays differential degrees of virulence depending on the route of infection. Infect Immun 71: 3512-3520.
49. Trcek J, Fuchs TM, Trulzsch K, (2010) Analysis of Yersinia enterocolitica invasin expression in vitro and in vivo using a novel luxCDABE reporter system. Microbiology 156: 2734-2745.
50. Mahillon J, Chandler M, (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
51. Chandler M, Mahilon J, (2002) Insertions sequences revised. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II Washington DC ASM Press pp. 305-366.
52. Singh J, Mukerji M, Mahadevan S, (1995) Transcriptional activation of the Escherichia coli bgl operon: negative regulation by DNA structural elements near the promoter. Mol Microbiol 17: 1085-1092.
53. Schnetz K, Rak B, (1992) IS5: a mobile enhancer of transcription in Escherichia coli. Proc Natl Acad Sci U S A 89: 1244-1248.
54. Zhang Z, Saier MH Jr, (2009) A novel mechanism of transposon-mediated gene activation. PLoS Genet 5: e1000689.
55. Tran HJ, Heroven AK, Winkler L, Spreter T, Beatrix B, et al. (2005) Analysis of RovA, a transcriptional regulator of Yersinia pseudotuberculosis virulence that acts through antirepression and direct transcriptional activation. J Biol Chem 280: 42423-42432.
56. Revell PA, Miller VL, (2000) A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 35: 677-685.
57. Cathelyn JS, Ellison DW, Hinchliffe SJ, Wren BW, Miller VL, (2007) The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome. Mol Microbiol 66: 189-205.
58. Bengoechea JA, (2003) Regulation of O-antigen biosynthesis in Yersinia enterocolitica. Adv Exp Med Biol 529: 267-274.
59. Kirjavainen V, Jarva H, Biedzka-Sarek M, Blom AM, Skurnik M, et al. (2008) Yersinia enterocolitica serum resistance proteins YadA and Ail bind the complement regulator C4b-binding protein. PLoS Pathog 4: e1000140.
60. Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J, (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19: 5989-5999.
61. Heesemann J, Gruter L, (1987) Genetic evidence that the outer membrane protein YOP1 of Yersinia enterocolitica mediates adherence and phagocytosis resistance to human epithelial cells. FEBS Microbiol Lett 40: 37-41.
62. Eitel J, Dersch P, (2002) The YadA protein of Yersinia pseudotuberculosis mediates high-efficiency uptake into human cells under environmental conditions in which invasin is repressed. Infect Immun 70: 4880-4891.
63. Dersch P, Isberg RR, (1999) A region of the Yersinia pseudotuberculosis invasin protein enhances integrin-mediated uptake into mammalian cells and promotes self-association. EMBO J 18: 1199-1213.
64. Tran Van Nhieu G, Isberg RR, (1993) Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J 12: 1887-1895.
65. Dersch P, Isberg RR, (2000) An immunoglobulin superfamily-like domain unique to the Yersinia pseudotuberculosis invasin protein is required for stimulation of bacterial uptake via integrin receptors. Infect Immun 68: 2930-2938.
66. Sambrook J, (2001) Molecular Cloning: A Laboratory Manual,: Cold Spring Harbor Laboratories, Cold Spring Harbor, NY.
67. Miller JH, (1992) A short course in bacterial genetic: a laboratory manual and handbook for Escherichia coli and related bacteria; In: Laboratories CSH, editors. Cold Spring Habor, New York.
68. Heroven AK, Bohme K, Rohde M, Dersch P, (2008) A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 68: 1179-1195.
69. Tisa LS, Adler J, (1995) Chemotactic properties of Escherichia coli mutants having abnormal Ca2+ content. J Bacteriol 177: 7112-7118.
70. Valentine RC, Shapiro BM, Stadtman ER, (1968) Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7: 2143-2152.
71. Uliczka F, Kornprobst T, Eitel J, Schneider D, Dersch P, (2009) Cell invasion of Yersinia pseudotuberculosis by invasin and YadA requires protein kinase C, phospholipase C-gamma1 and Akt kinase. Cell Microbiol 11: 1782-1801.
72. Robins-Browne RM, Prpic JK, (1985) Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun 47: 774-779.
73. Simon R, Priefer U, Puehler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1: 784-791.
74. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW, (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 158: 60-89.
75. Skurnik M, (1984) Lack of correlation between the presence of plasmids and fimbriae in Yersinia enterocolitica and Yersinia pseudotuberculosis. J Appl Bacteriol 56: 355-363.
76. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
77. Lutz R, Bujard H, (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203-1210.
78. Monk IR, Casey PG, Cronin M, Gahan CG, Hill C, (2008) Development of multiple strain competitive index assays for Listeria monocytogenes using pIMC; a new site-specific integrative vector. BMC Microbiol 8: 96.