Unique Cell Adhesion and Invasion Properties of O:3, the Most Frequent Cause of Human Yersiniosis
Many enteric pathogens are equipped with multiple cell adhesion factors which are important for host tissue colonization and virulence. Y. enterocolitica, a common food-borne pathogen with invasive properties, uses the surface proteins invasin and YadA for host cell binding and entry. In this study, we demonstrate unique cell adhesion and invasion properties of Y. enterocolitica serotype O:3 strains, the most frequent cause of human yersiniosis, and show that these differences are mainly attributable to variations affecting the function and expression of invasin in response to temperature. In contrast to other enteric Yersinia strains, invasin production in O:3 strains is constitutive and largely enhanced compared to other Y. enterocolitica serotypes, in which invA expression is temperature-regulated and significantly reduced at 37°C. Increase of invasin levels is caused by (i) an IS1667 insertion into the invA promoter region, which includes an additional promoter and RovA and H-NS binding sites, and (ii) a P98S substitution in the invA activator protein RovA rendering the regulator less susceptible to proteolysis. Both variations were shown to influence bacterial colonization in a murine infection model. Furthermore, we found that co-expression of YadA and down-regulation of the O-antigen at 37°C is required to allow efficient internalization by the InvA protein. We conclude that even small variations in the expression of virulence factors can provoke a major difference in the virulence properties of closely related pathogens which may confer better survival or a higher pathogenic potential in a certain host or host environment.
Vyšlo v časopise:
Unique Cell Adhesion and Invasion Properties of O:3, the Most Frequent Cause of Human Yersiniosis. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002117
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002117
Souhrn
Many enteric pathogens are equipped with multiple cell adhesion factors which are important for host tissue colonization and virulence. Y. enterocolitica, a common food-borne pathogen with invasive properties, uses the surface proteins invasin and YadA for host cell binding and entry. In this study, we demonstrate unique cell adhesion and invasion properties of Y. enterocolitica serotype O:3 strains, the most frequent cause of human yersiniosis, and show that these differences are mainly attributable to variations affecting the function and expression of invasin in response to temperature. In contrast to other enteric Yersinia strains, invasin production in O:3 strains is constitutive and largely enhanced compared to other Y. enterocolitica serotypes, in which invA expression is temperature-regulated and significantly reduced at 37°C. Increase of invasin levels is caused by (i) an IS1667 insertion into the invA promoter region, which includes an additional promoter and RovA and H-NS binding sites, and (ii) a P98S substitution in the invA activator protein RovA rendering the regulator less susceptible to proteolysis. Both variations were shown to influence bacterial colonization in a murine infection model. Furthermore, we found that co-expression of YadA and down-regulation of the O-antigen at 37°C is required to allow efficient internalization by the InvA protein. We conclude that even small variations in the expression of virulence factors can provoke a major difference in the virulence properties of closely related pathogens which may confer better survival or a higher pathogenic potential in a certain host or host environment.
Zdroje
1. BottoneEJ 1997 Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10 257 276
2. HanskiCNaumannMHahnHRieckenEO 1989 Determinants of invasion and survival of Yersinia enterocolitica in intestinal tissue. An in vivo study. Med Microbiol Immunol 178 289 296
3. GrutzkauAHanskiCHahnHRieckenEO 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. PepeJCMillerVL 1993 Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A 90 6473 6477
5. CarterPB 1975 Pathogenecity of Yersinia enterocolitica for mice. Infect Immun 11 164 170
6. HandleySADubePHRevellPAMillerVL 2004 Characterization of oral Yersinia enterocolitica infection in three different strains of inbred mice. Infect Immun 72 1645 1656
7. HandleySANewberryRDMillerVL 2005 Yersinia enterocolitica invasin-dependent and invasin-independent mechanisms of systemic dissemination. Infect Immun 73 8453 8455
8. BarnesPDBergmanMAMecsasJIsbergRR 2006 Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203 1591 1601
9. TrulzschKSporlederTIgweEIRussmannHHeesemannJ 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. MillerVLFalkowS 1988 Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56 1242 1248
11. MillerVLFinlayBBFalkowS 1988 Factors essential for the penetration of mammalian cells by Yersinia. Curr Top Microbiol Immunol 138 15 39
12. PepeJCWachtelMRWagarEMillerVL 1995 Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection. Infect Immun 63 4837 4848
13. IsbergRRLeongJM 1990 Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60 861 871
14. YoungVBFalkowSSchoolnikGK 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. PepeJCBadgerJLMillerVL 1994 Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol Microbiol 11 123 135
16. MarraAIsbergRR 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. StraleySCPerryRD 1995 Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol 3 310 317
18. HerbstKBujaraMHerovenAKOpitzWWeichertM 2009 Intrinsic thermal sensing controls proteolysis of Yersinia virulence regulator RovA. PLoS Pathog 5 e1000435
19. HeiseTDerschP 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-SarekMSalmenlinnaSGruberMLupasANMeriS 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-SarekMJarvaHHyytiainenHMeriSSkurnikM 2008 Characterization of complement factor H binding to Yersinia enterocolitica serotype O:3. Infect Immun 76 4100 4109
22. FelekSKrukonisES 2009 The Yersinia pestis Ail protein mediates binding and Yop delivery to host cells required for plague virulence. Infect Immun 77 825 836
23. TsangTMFelekSKrukonisES 2010 Ail binding to fibronectin facilitates Yersinia pestis binding to host cells and Yop delivery. Infect Immun 78 3358 3368
24. PedersonKJPiersonDE 1995 Ail expression in Yersinia enterocolitica is affected by oxygen tension. Infect Immun 63 4199 4201
25. PiersonDEFalkowS 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. SkurnikMToivanenP 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 RouvroitCSluitersCCornelisGR 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. SkurnikMToivanenP 1993 Yersinia enterocolitica lipopolysaccharide: genetics and virulence. Trends Microbiol 1 148 152
29. SkurnikMVenhoRBengoecheaJAMoriyonI 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-HendyAToivanenPSkurnikM 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. BengoecheaJANajdenskiHSkurnikM 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-HendyAToivanenPSkurnikM 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. BengoecheaJAZhangLToivanenPSkurnikM 2002 Regulatory network of lipopolysaccharide O-antigen biosynthesis in Yersinia enterocolitica includes cell envelope-dependent signals. Mol Microbiol 44 1045 1062
34. YoungGMBadgerJLMillerVL 2000 Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect Immun 68 4323 4326
35. LeeLAGerberARLonswayDRSmithJDCarterGP 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. TauxeRV 2002 Emerging foodborne pathogens. Int J Food Microbiol 78 31 41
37. ECDC 2009 Annual Epidemiological Report on Communicable Diseases 2009. European Centre for Disease Prevention and Control. Available: http://www.ecdc.europa.eu
38. JonesTF 2003 From pig to pacifier: chitterling-associated yersiniosis outbreak among black infants. Emerg Infect Dis 9 1007 1009
39. Fredriksson-AhomaaMStolleASiitonenAKorkealaH 2006 Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O : 3 originate mainly from pigs. J Med Microbiol 55 747 749
40. GurtlerMAlterTKasimirSLinneburMFehlhaberK 2005 Prevalence of Yersinia enterocolitica in fattening pigs. J Food Prot 68 850 854
41. KapatralVCampbellJWMinnichSAThomsonNRMatsumuraP 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-SarekMVenhoRSkurnikM 2005 Role of YadA, Ail, and Lipopolysaccharide in Serum Resistance of Yersinia enterocolitica Serotype O:3. Infect Immun 73 2232 2244
43. El TahirYSkurnikM 2001 YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291 209 218
44. NagelGLahrzADerschP 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. EllisonDWMillerVL 2006 H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J Bacteriol 188 5101 5112
46. HerovenAKNagelGTranHJParrSDerschP 2004 RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53 871 888
47. LawrenzMBMillerVL 2007 Comparative analysis of the regulation of rovA from the pathogenic yersiniae. J Bacteriol 189 5963 5975
48. DubePHHandleySARevellPAMillerVL 2003 The rovA mutant of Yersinia enterocolitica displays differential degrees of virulence depending on the route of infection. Infect Immun 71 3512 3520
49. TrcekJFuchsTMTrulzschK 2010 Analysis of Yersinia enterocolitica invasin expression in vitro and in vivo using a novel luxCDABE reporter system. Microbiology 156 2734 2745
50. MahillonJChandlerM 1998 Insertion sequences. Microbiol Mol Biol Rev 62 725 774
51. ChandlerMMahilonJ 2002 Insertions sequences revised. CraigNLCraigieRGellertMLambowitzAM Mobile DNA II Washington DC ASM Press 305 366
52. SinghJMukerjiMMahadevanS 1995 Transcriptional activation of the Escherichia coli bgl operon: negative regulation by DNA structural elements near the promoter. Mol Microbiol 17 1085 1092
53. SchnetzKRakB 1992 IS5: a mobile enhancer of transcription in Escherichia coli. Proc Natl Acad Sci U S A 89 1244 1248
54. ZhangZSaierMHJr 2009 A novel mechanism of transposon-mediated gene activation. PLoS Genet 5 e1000689
55. TranHJHerovenAKWinklerLSpreterTBeatrixB 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. RevellPAMillerVL 2000 A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 35 677 685
57. CathelynJSEllisonDWHinchliffeSJWrenBWMillerVL 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. BengoecheaJA 2003 Regulation of O-antigen biosynthesis in Yersinia enterocolitica. Adv Exp Med Biol 529 267 274
59. KirjavainenVJarvaHBiedzka-SarekMBlomAMSkurnikM 2008 Yersinia enterocolitica serum resistance proteins YadA and Ail bind the complement regulator C4b-binding protein. PLoS Pathog 4 e1000140
60. HoiczykERoggenkampAReichenbecherMLupasAHeesemannJ 2000 Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19 5989 5999
61. HeesemannJGruterL 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. EitelJDerschP 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. DerschPIsbergRR 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 NhieuGIsbergRR 1993 Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J 12 1887 1895
65. DerschPIsbergRR 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. SambrookJ 2001 Molecular Cloning: A Laboratory Manual,: Cold Spring Harbor Laboratories, Cold Spring Harbor, NY
67. MillerJH 1992 A short course in bacterial genetic: a laboratory manual and handbook for Escherichia coli and related bacteria; LaboratoriesCSH Cold Spring Habor, New York
68. HerovenAKBohmeKRohdeMDerschP 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. TisaLSAdlerJ 1995 Chemotactic properties of Escherichia coli mutants having abnormal Ca2+ content. J Bacteriol 177 7112 7118
70. ValentineRCShapiroBMStadtmanER 1968 Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7 2143 2152
71. UliczkaFKornprobstTEitelJSchneiderDDerschP 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-BrowneRMPrpicJK 1985 Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun 47 774 779
73. SimonRPrieferUPuehlerA 1983 A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1 784 791
74. StudierFWRosenbergAHDunnJJDubendorffJW 1990 Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 158 60 89
75. SkurnikM 1984 Lack of correlation between the presence of plasmids and fimbriae in Yersinia enterocolitica and Yersinia pseudotuberculosis. J Appl Bacteriol 56 355 363
76. GuzmanLMBelinDCarsonMJBeckwithJ 1995 Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 4121 4130
77. LutzRBujardH 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. MonkIRCaseyPGCroninMGahanCGHillC 2008 Development of multiple strain competitive index assays for Listeria monocytogenes using pIMC; a new site-specific integrative vector. BMC Microbiol 8 96
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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