The biosynthesis and biological role of lipopolysaccharide O-antigens of pathogenic Yersiniae.

Lipopolysaccharide (LPS) is the major component of the outer leaflet of the outer membrane of Gram-negative bacteria. The LPS molecule is composed of two biosynthetic entities: the lipid A--core and the O-polysaccharide (O-antigen). Most biological effects of LPS are due to the lipid A part, however, there is an increasing body of evidence indicating that O-antigen (O-ag) plays an important role in effective colonization of host tissues, resistance to complement-mediated killing and in the resistance to cationic antimicrobial peptides that are key elements of the innate immune system. In this review, we will discuss: (i) the work done on the genetics and biosynthesis of the O-ags in the genus Yersinia; (ii) the role of O-ag in virulence of these bacteria; (iii) the work done on regulation of the O-ag gene cluster expression and; (iv) the impact that the O-ag expression has on other bacterial surface and membrane components.

[1]  E. Wagar,et al.  Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection , 1995, Infection and immunity.

[2]  J. Thorson,et al.  Pathways and mechanisms in the biogenesis of novel deoxysugars by bacteria. , 1994, Annual review of microbiology.

[3]  A. Al-Hendy,et al.  Genetic organization and sequence of the rfb gene cluster of Yersinia enterocolitica serotype O:3: similarities to the dTDP‐L‐rhamnose biosynthesis pathway of Salmonella and to the bacterial polysaccharide transport systems , 1993, Molecular microbiology.

[4]  M. Skurnik,et al.  Expression cloning of Yersinia enterocolitica O:3 rfb gene cluster in Escherichia coli K12. , 1991, Microbial pathogenesis.

[5]  Y. Kawaoka,et al.  Growth temperature-dependent variation in the bacteriophage-inactivating capacity and antigenicity of Yersinia enterocolitica lipopolysaccharide. , 1983, Journal of general microbiology.

[6]  J. Hartley,et al.  Chemical and Physical Properties of Lipopolysaccharide of Yersinia pestis , 1974, Journal of bacteriology.

[7]  C. Whitfield,et al.  Modulation of the surface architecture of Gram‐negative bacteria by the action of surface polymer:lipid A–core ligase and by determinants of polymer chain length , 1997, Molecular microbiology.

[8]  R. Morona,et al.  Analysis of Shigella flexneri Wzz (Rol) function by mutagenesis and cross‐linking: Wzz is able to oligomerize , 1999, Molecular microbiology.

[9]  M. Skurnik,et al.  The gene cluster directing O-antigen biosynthesis in Yersinia enterocolitica serotype 0:8: identification of the genes for mannose and galactose biosynthesis and the gene for the O-antigen polymerase. , 1996, Microbiology.

[10]  N. Sternby,et al.  Yersinia enterocolitica (Pasteurella x) in human enteric infections. , 1966, British medical journal.

[11]  S. Falkow,et al.  Identification of Attenuated Yersinia pseudotuberculosis Strains and Characterization of an Orogastric Infection in BALB/c Mice on Day 5 Postinfection by Signature-Tagged Mutagenesis , 2001, Infection and Immunity.

[12]  Guy Plunkett,et al.  Genome Sequence of Yersinia pestis KIM , 2002, Journal of bacteriology.

[13]  M. Perry,et al.  Structure of the O-chain of the phenol-phase soluble cellular lipopolysaccharide of Yersinia enterocolitica serotype O:9. , 1984, European journal of biochemistry.

[14]  P. Hitchen,et al.  Structural characterization of lipo‐oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system , 2002, Molecular microbiology.

[15]  P. Reeves,et al.  Relationship of Yersinia pseudotuberculosis O Antigens IA, IIA, and IVB: the IIA Gene Cluster Was Derived from That of IVB , 2002, Infection and Immunity.

[16]  P. Reeves,et al.  The Wzz (Cld) Protein in Escherichia coli: Amino Acid Sequence Variation Determines O-Antigen Chain Length Specificity , 1998, Journal of bacteriology.

[17]  M. Skurnik,et al.  Mutations in the genes for synthesis of the outer core region of the lipopolysaccharide of Yersinia enterocolitica O:3. , 2003, Journal of applied microbiology.

[18]  V. L. Miller,et al.  Phospholipase A of Yersinia enterocolitica Contributes to Pathogenesis in a Mouse Model , 1998, Infection and Immunity.

[19]  Michael J. Smith,et al.  The Yersinia enterocolitica Motility Master Regulatory Operon, flhDC, Is Required for Flagellin Production, Swimming Motility, and Swarming Motility , 1999, Journal of bacteriology.

[20]  M. Skurnik,et al.  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. , 1991, Microbial pathogenesis.

[21]  M. Skurnik,et al.  Temperature‐regulated efflux pump/potassium antiporter system mediates resistance to cationic antimicrobial peptides in Yersinia , 2000, Molecular microbiology.

[22]  V. L. Miller,et al.  Yersinia enterocolitica invasin: a primary role in the initiation of infection. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Skurnik,et al.  Lipopolysaccharide O side chain of Yersinia enterocolitica O:3 is an essential virulence factor in an orally infected murine model , 1992, Infection and immunity.

[24]  G. Young,et al.  YplA Is Exported by the Ysc, Ysa, and Flagellar Type III Secretion Systems of Yersinia enterocolitica , 2002, Journal of bacteriology.

[25]  The failure of different strains of Yersinia pestis to produce lipopolysaccharide O-antigen under different growth conditions is due to mutations in the O-antigen gene cluster. , 2001, FEMS microbiology letters.

[26]  R. Brubaker,et al.  Structural studies of the O-specific side-chains of the lipopolysaccharide from Yersinia enterocolitica Ye 128. , 1980, Carbohydrate research.

[27]  R. Hancock,et al.  Effects of growth temperature, 47-megadalton plasmid, and calcium deficiency on the outer membrane protein porin and lipopolysaccharide composition of Yersinia pestis EV76 , 1983, Infection and immunity.

[28]  D. Pierson,et al.  Identification of the galE gene and a galE homolog and characterization of their roles in the biosynthesis of lipopolysaccharide in a serotype O:8 strain of Yersinia enterocolitica , 1996, Journal of bacteriology.

[29]  M. Skurnik,et al.  Regulatory network of lipopolysaccharide O‐antigen biosynthesis in Yersinia enterocolitica includes cell envelope‐dependent signals , 2002, Molecular microbiology.

[30]  M. Skurnik,et al.  The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity , 1999, Molecular microbiology.

[31]  M. Skurnik,et al.  Characterization of the O‐antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O‐antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b , 2000, Molecular microbiology.

[32]  J. Goldberg Genetics of Bacterial Polysaccharides , 1999 .

[33]  M. Skurnik,et al.  Molecular and chemical characterization of the lipopolysaccharide O‐antigen and its role in the virulence of Yersinia enterocolitica serotype O:8 , 1997, Molecular microbiology.

[34]  A. Darwin,et al.  Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature‐tagged transposon mutagenesis , 1999, Molecular microbiology.

[35]  M. Skurnik,et al.  A novel locus of Yersinia enterocolitica serotype O:3 involved in lipopolysaccharide outer core biosynthesis , 1995, Molecular microbiology.

[36]  M. Skurnik,et al.  Molecular genetics and biochemistry of Yersinia lipopolysaccharide , 1996, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[37]  T. Salminen,et al.  Functional Characterization of Gne (UDP-N-Acetylglucosamine- 4-Epimerase), Wzz (Chain Length Determinant), and Wzy (O-Antigen Polymerase) of Yersinia enterocolitica Serotype O:8 , 2002, Journal of bacteriology.

[38]  H. Mayer,et al.  Localization of enterobacterial common antigen in Yersinia enterocolitica by the immunoferritin technique , 1981, Journal of bacteriology.

[39]  M. Simmonds,et al.  Genome sequence of Yersinia pestis, the causative agent of plague , 2001, Nature.

[40]  M. Skurnik,et al.  Expression of heterologous O-antigen in Yersinia pestis KIM does not affect virulence by the intravenous route. , 2003, Journal of medical microbiology.