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Detection of O antigens in Escherichia coli

Published online by Cambridge University Press:  09 December 2011

Chitrita DebRoy ,
Elisabeth Roberts  and
Pina M. Fratamico
Chitrita DebRoy*
Affiliation:
E. coli Reference Center, Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA, USA
Elisabeth Roberts
Affiliation:
E. coli Reference Center, Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA, USA
Pina M. Fratamico
Affiliation:
Eastern Regional Research Center, U.S. Department of Agriculture, Agricultural Research Service, Wyndmoor, PA, USA
*
*Corresponding author. E-mail: rcd3@psu.edu
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Abstract

Lipopolysaccharide on the surface of Escherichia coli constitutes the O antigens which are important virulence factors that are targets of both the innate and adaptive immune systems and play a major role in host–pathogen interactions. O antigens are responsible for antigenic specificity of the strain and determine the O serogroup. The designation of O serogroups is important for classifying E. coli strains, for epidemiological studies, in tracing the source of outbreaks of gastrointestinal or other illness, and for linking the source to the infection. For conventional serogroup identification, serotyping by agglutination reactions against antisera developed for each of the O serogroups has been used. In the last decade, many O-antigen gene clusters that encode for the enzymes responsible for the synthesis of the variable oligosaccharide region on the surface of the bacteria have been sequenced and characterized. Unique gene sequences within the O-antigen gene clusters have been targeted for identification and detection of many O groups using the polymerase chain reaction and microarrays. This review summarizes current knowledge on the DNA sequences of the O-antigen gene clusters, genetic-based methods for O-group determination and detection of pathogenic E. coli based on O-antigen and virulence gene detection, and provides perspectives on future developments in the field.

Keywords

lipopolysaccharideserotypingagglutinationsequencing, RFLPPCRvirulencemicroarrays
Type
Review Article
Information
Animal Health Research Reviews , Volume 12 , Issue 2 , December 2011 , pp. 169 - 185
Copyright
Copyright © Cambridge University Press 2011

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References

Achtman, M and Pluschke, G (1986). Clonal analysis of descent and virulence among selected Escherichia coli. Annual Review of Microbiology 40: 185–210.CrossRefGoogle ScholarPubMed
Akira, S, Uematsu, S and Takeuchi, O (2006). Pathogen recognition and innate immunity. Cell 124: 783–801.CrossRefGoogle ScholarPubMed
Amor, PA and Whitfield, C (1997). Molecular and functional analysis of genes required for expression of group IB K antigens in Escherichia coli: characterization of the his-region containing gene clusters for multiple cell-surface polysaccharides. Molecular Microbiology 26: 145–161.CrossRefGoogle ScholarPubMed
Bastin, DA and Reeves, PR (1995). Sequence and analysis of the O antigen gene (rfb) cluster of Escherichia coli O111. Gene 164: 17–23.CrossRefGoogle ScholarPubMed
Bastin, DA, Stevenson, G, Brown, AH and Reeves, PR (1993). Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Molecular Microbiology 7: 725–734.CrossRefGoogle Scholar
Batchelor, RA, Alifano, P, Biffali, E, Hull, SI and Hull, RA (1992). Nucleotide sequences of the genes regulating O-polysaccharide antigen chain length (rol) from Escherichia coli and Salmonella typhimurium: protein homology and functional complementation. Journal of Bacteriology 174: 5228–5236.CrossRefGoogle ScholarPubMed
Bengoechea, JA, Najdenski, H and 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. Molecular Microbiology 52: 451–469.CrossRefGoogle Scholar
Beutin, L, Kong, Q, Feng, L, Wang, Q, Krause, G, Leomil, L, Jin, Q and Wang, L (2005a). Development of PCR assays targeting the genes involved in synthesis and assembly of the new Escherichia coli O 174 and O 177 O antigens. Journal of Clinical Microbiology 43: 5143–5149.CrossRefGoogle Scholar
Beutin, L, Tao, J, Feng, L, Krause, G, Zimmermann, S, Gleier, K, Xia, Q and Wang, L (2005b). Sequence analysis of the Escherichia coli O15 antigen gene cluster and development of a PCR assay for rapid detection of intestinal and extraintestinal pathogenic E. coli O15 strains. Journal of Clinical Microbiology 43: 703–710.CrossRefGoogle ScholarPubMed
Beutin, L, Wang, Q, Naumann, D, Han, W, Krause, G, Leomil, L, Wang, L and Feng, L (2007). Relationship between O-antigen subtypes, bacterial surface structures and O-antigen gene clusters in Escherichia coli O123 strains carrying genes for Shiga toxins and intimin. Journal of Medical Microbiology 56: 177–184.CrossRefGoogle ScholarPubMed
Bos, MP, Robert, V and Tommassen, J (2007). Biogenesis of Gram-negative bacterial outer membrane. Annual Review of Microbiology 61: 191–214.CrossRefGoogle ScholarPubMed
Bronner, D, Clarke, BR and Whitfield, C (1994). Identification of an ATP-binding cassette transport system required for translocation of lipopolysachharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumonia serotype O1. Molecular Microbiology 14: 505–519.CrossRefGoogle Scholar
Bugarel, M, Beutin, L, Martin, A, Gill, A and Fach, P (2010). Micro-array for the identification of Shiga toxin-producing Escherichia coli (STEC) seropathotypes associated with hemorrhagic colitis and hemolytic uremic syndrome in humans. International Journal of Food Microbiology 142: 318–329.CrossRefGoogle ScholarPubMed
Carvallo, F, DebRoy, C, Baeza, E, Hinckley, L and Gilbert, K (2010). Extraintestinal pathogenic Escherichia coli induced necrotizing pneumonia in a white tiger cub. Journal of Veterinary Diagnostic Investigation 22: 136–140.CrossRefGoogle Scholar
Chafchaouni-Moussaoui, I, Novikov, A, Bhrada, F, Perry, MB, Filali-Maltouf, A and Caroff, M (2011). A new rapid and micro-scale hydrolysis, using triethylamine citrate, for lipopolysaccharide characterization by mass spectrometry. Rapid Communication in Mass Spectrometry 14: 2043–2048.CrossRefGoogle Scholar
Cheng, J, Liu, B, Bastin, DA, Han, W, Wang, L and Feng, L (2007). Genetic characterization of the Escherichia coli O66 antigen and functional identification of its wzy gene. Journal of Microbiology 45: 69–74.Google ScholarPubMed
Cheng, J, Wang, Q, Wang, W, Wang, Y, Wang, L and Feng, L (2006). Characterization of E. coli O24 and O56 O antigen gene clusters reveals a complex evolutionary history of the O24 gene cluster. Current Microbiology 53: 470–476.CrossRefGoogle ScholarPubMed
Coimbra, RS, Grimont, F, Lenormand, P, Burguiere, P, Beutin, L and Grimont, PAD (2000). Identification of Escherichia coli O-serogroups by restriction of the amplified O-antigen gene cluster (rfb-RFLP). Research Microbiology 151: 639–654.CrossRefGoogle ScholarPubMed
Cunneen, MM and Reeves, PR (2007). The Yersinia kristensenii O11 O-antigen gene cluster was acquired by lateral gene transfer and incorporated at a novel chromosomal locus. Molecular Biology and Evolution 24: 1355–1365.CrossRefGoogle Scholar
Daniels, C, Vindurampulle, C and Morona, R (1998). Overexpression and topology of Shigella flexneri O antigen polymerase (Rfc/Wzy). Molecular Microbiology 28: 1211–1222.CrossRefGoogle ScholarPubMed
DebRoy, C, Fratamico, PM, Roberts, E, Davis, MA and Liu, Y (2005). Development of PCR assays targeting genes in O-antigen gene clusters for detection and identification of Escherichia coli O45 and O55 serogroups. Applied and Environmental Microbiology 71: 4919–4924.CrossRefGoogle ScholarPubMed
DebRoy, C, Roberts, E, Davis, MA and Bumbaugh, AC (2010). Detection of non-serotypable Shiga toxin-producing Escherichia coli strains derived from pigs by multiplex PCR assay. Foodborne Pathogen and Disease 7: 1407–1414.CrossRefGoogle Scholar
DebRoy, C, Roberts, E, Kundrat, J, Davis, MA, Briggs, CE and Fratamico, PM (2004). Detection of Escherichia coli serogroups O26 and O113 by PCR amplification of wzx and wzy genes. Applied and Environmental Microbiology 70: 1830–1832.CrossRefGoogle ScholarPubMed
DebRoy, C, Roberts, E, Valadez, AM, Dudley, EG and Cutter, CN (2011). Detection of Shiga toxin producing Escherichia coli O26, O45, O103, O111, O113, O121, O145, and O157 serogroups by multiplex PCR of the wzx gene of the O-antigen gene cluster. Foodborne Pathogen and Disease 8: 651–652.CrossRefGoogle ScholarPubMed
D'Souza, JM, Samuel, GN and Reeves, PR (2005). Evolutionary origins and sequence of the Escherichia coli O4 O-antigen gene cluster. FEMS Microbiology Letters 244: 27–32.CrossRefGoogle ScholarPubMed
D'Souza, JM, Wang, L and Reeves, PR (2002). Sequence of the Escherichia coli O26 O antigen gene cluster and identification of O26 specific genes. Gene 297: 123–127.CrossRefGoogle ScholarPubMed
Duda, KA, Lindner, B, Brade, H, Leimbach, A, Brzuszkiewicz, E, Dobrindt, U and Holst, O (2011). The lipopolysaccharide of the mastitis isolate Escherichia coli strain 1303 comprises a novel O-antigen and the rare K-12 core type. Microbiology 157: 1750–1760.CrossRefGoogle ScholarPubMed
Ewing, WH (1972). The genus Escherichia. In: Edwards, PR and Ewing, WH (eds) Identification of Enterobacteriaceae. Minneaopolis, MN: Burgess Publishing Co., pp. 67–107.Google Scholar
Ewing, WH, Tatum, HW, Davis, BR and Reavis, RW (1956). Studies on the Serology of the Escherichia coli Group. Atlanta, GA: Communicable Disease Center Publication, pp. 1–42.Google Scholar
Feng, L, Han, W, Wang, Q, Bastin, DA and Wang, L (2005a). Characterization of Escherichia coli O86 O-antigen gene cluster and identification of O86-specific genes. Veterinary Microbiology 106: 241–248.CrossRefGoogle ScholarPubMed
Feng, L, Perepelov, AV, Zhao, G, Shevelev, SD, Wang, Q, Senchenkova, SN, Shashkov, AS, Geng, Y, Reeves, PR, Knirel, YA and Wang, L (2007). Structural and genetic evidence that the Escherichia coli O148 O antigen is the precursor of the Shigella dysenteriae type 1 O antigen and identification of a glucosyltransferase gene. Microbiology 153: 139–147.CrossRefGoogle ScholarPubMed
Feng, L, Senchenkova, SN, Tao, J, Shashkov, AS, Liu, B, Shevelev, SD, Reeves, PR, Xu, J, Knirel, YA and Wang, L (2005b). Structural and genetic characterization of enterohemorrhagic Escherichia coli O145 O antigen and development of an O145 serogroup-specific PCR assay. Journal of Bacteriology 187: 758–764.CrossRefGoogle ScholarPubMed
Feng, L, Senchenkova, SN, Yang, J, Shashkov, AS, Tao, J, Guo, H, Cheng, J, Ren, Y, Knirel, YA, Reeves, PR and Wang, L (2004a). Synthesis of the heteropolysaccharide O antigen of Escherichia coli O52 requires an ABC transporter: structural and genetic evidence. Journal of Bacteriology 186: 4510–4519.CrossRefGoogle ScholarPubMed
Feng, L, Wang, W, Tao, J, Guo, H, Krause, G, Beutin, L and Wang, L (2004b). Identification of Escherichia coli O114 O-antigen gene cluster and development of an O114 serogroup-specific PCR assay. Journal of Clinical Microbiology 42: 3799–3804.CrossRefGoogle ScholarPubMed
Fratamico, PM, Bagi, LK, Cray, WC Jr., Narang, N, Yan, X, Medina, M and Liu, Y (2011). Detection by multiplex real-time polymerase chain reaction assays and isolation of Shiga toxin-producing Escherichia coli O26, O45, O103, O111, O121, and O145 in ground beef. Foodborne Pathogen and Disease 8: 601–607.CrossRefGoogle ScholarPubMed
Fratamico, PM, Briggs, CE, Needle, D, Chen, CY and DebRoy, C (2003). Sequence of the Escherichia coli O121 O-antigen gene cluster and detection of enterohemorrhagic E. coli O121 by PCR amplification of the wzx and wzy genes. Journal of Clinical Microbiology 41: 3379–3383.CrossRefGoogle ScholarPubMed
Fratamico, PM, DebRoy, C and Liu, Y (2009a). The DNA sequence of the Escherichia coli O22 O antigen gene cluster and detection of pathogenic strains belonging to E. coli serogroups O22 and O91 by multiplex PCR assays targeting virulence genes and genes in the respective O-antigen gene clusters. Food Analytical Methods 2: 169–179.CrossRefGoogle Scholar
Fratamico, PM, DebRoy, C, Miyamoto, T and Liu, Y (2009b). Detection of entero-hemorrhagic Escherichia coli O145 in food by PCR targeting genes in the E. coli O145 O antigen gene cluster and the Shiga toxins 1 and 2 genes. Foodborne Pathogen and Disease 6: 605–611.CrossRefGoogle Scholar
Fratamico, PM, DebRoy, C, Strobaugh, TP Jr. and Chen, CY (2005). DNA sequence of the Escherichia coli O103 O antigen gene cluster and detection of enterohemorrhagic E. coli O103 by PCR amplification of the wzx and wzy genes. Canadian Journal of Microbiology 51: 515–522.CrossRefGoogle ScholarPubMed
Fratamico, PM, Yan, X, Liu, Y, DebRoy, C, Byrne, B, Monaghan, A, Fanning, S and Bolton, D (2010). Escherichia coli serogroup O2 and O28ac O-antigen gene cluster sequences and detection of pathogenic E. coli O2 and O28ac by PCR. Canadian Journal of Microbiology 56: 308–316.CrossRefGoogle ScholarPubMed
Galanos, C, Luderitz, O, Rietschel, ET, Westphal, O, Brade, H, Brade, L, Freudenberg, M, Schade, U, Imoto, M, Yoshimura, H, Kusumoto, S and Shiba, T (1985). Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. European Journal of Biochemistry 148: 1–5.CrossRefGoogle ScholarPubMed
Golenbock, DT, Hampton, RY, Qureshi, N, Takayama, K and Raetz, CR (1991). Lipid A-like molecules that antagonize the effects of endotoxins on human nonocytes. Journal of Biological Chemistry 266: 19490–19498.CrossRefGoogle Scholar
Goswami, P, Gyles, C, Friendship, R, Poppe, C, Vinogradov, E and Boerlin, P (2010). The Escherichia coli O149 rfb gene cluster and its use for the detection of porcine E. coli O149 by real-time PCR. Veterinary Microbiology 141: 120–126.CrossRefGoogle ScholarPubMed
Grozdanov, L, Zahringer, U, Blum-Oehler, G, Brade, L, Henne, A, Knirel, YA, Schombel, U, Schulze, J, Sonnenborn, U, Gottschalk, G, Hacker, J, Rietschel, ET and Dobrindt, U (2002). A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. Journal of Bacteriology 184: 5912–5925.CrossRefGoogle ScholarPubMed
Guo, H, Feng, L, Tao, J, Zhang, C and Wang, L (2004). Identification of Escherichia coli O172 O-antigen gene cluster and development of a serogroup-specific PCR assay. Journal of Applied Microbiology 97: 181–190.CrossRefGoogle ScholarPubMed
Guo, H, Kong, Q, Cheng, J, Wang, L and Feng, L (2005). Characterization of the Escherichia coli O59 and O155 O-antigen gene clusters: the atypical wzx genes are evolutionary related. FEMS Microbiology Letters 248: 153–161.CrossRefGoogle ScholarPubMed
Gyles, CL (2007). Shiga toxin-producing Escherichia coli: an overview. Journal of Animal Science 85: E45–E62.CrossRefGoogle ScholarPubMed
Han, W, Liu, B, Cao, B, Beutin, L, Kruger, U, Liu, H, Li, Y, Liu, Y, Feng, L and Wang, L (2007). DNA microarray-based identification of serogroups and virulence gene patterns of Escherichia coli isolates associated with porcine postweaning diarrhea and edema disease. Applied and Environmental Microbiology 73: 4082–4088.CrossRefGoogle ScholarPubMed
Handt, LK, Stoffregen, DA, Prescott, JS, Pouch, WJ, Ngai, DTW, Anderson, CA, Gatto, NT, DebRoy, C, Fairbrother, JM, Motzel, SL and Klein, HJ (2003). Clinical and microbiologic characterization of hemorrhagic pneumonia due to extraintestinal pathogenic E. coli in four young dogs. Comparative Medicine 53: 663–670.Google ScholarPubMed
Hobbs, M and Reeves, PR (1994). The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Molecular Microbiology 12: 855–856.CrossRefGoogle ScholarPubMed
Hu, B, Perepelov, AV, Liu, B, Shevelev, SD, Guo, D, Senchenkova, SN, Shashkov, AS, Feng, L, Knirel, YA and Wang, L (2010). Structural and genetic evidence for the close relationship between Escherichia coli O71 and Salmonella enterica O28 O-antigens. FEMS Immunology and Medical Microbiology 59: 161–169.CrossRefGoogle ScholarPubMed
Kaper, JB and Nataro, JP (2004). Pathogenic Escherichia coli. Nature Review Microbiology 2: 123–140.CrossRefGoogle ScholarPubMed
Karmali, MA, Mascarenhas, M, Shen, S, Ziebell, K, Johnson, S, Reid-Smith, R, Isaac-Renton, J, Clark, C, Rahn, K and Kaper, JB (2003). Association of genomic O island 122 of Escherichia coli EDL933 with verotoxin producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease. Journal of Clinical Microbiology 41: 4930–4940.CrossRefGoogle ScholarPubMed
Kaufmann, F (1943). Ueber neue tthermolabile Körperantigen der Colibakterien. Acta Pathologica et Microbiologica Scandinavica 20: 21–44.Google Scholar
Kaufmann, F (1944). Zur Serologie der Coli-Gruppe. Acta Pathologica et Microbiologica Scandinavica 21: 20–45.CrossRefGoogle Scholar
Kaufmann, F (1947). The serology of E. coli group. Journal of Immunology 57: 71–100.CrossRefGoogle Scholar
Keenleyside, WJ and Whitfield, C (1996). A novel pathway for O polysaccharide biosynthesis in Salmonella enterica serovar Borreze. Journal of Biological Chemistry 271: 28581–28592.CrossRefGoogle ScholarPubMed
Knipschildt, HE (1945). Undersøgelser over Coligruppens Serologie. København: Nyt Nordisk Forlag Arnold Busck, pp. 21–126.Google Scholar
Krishnan, C, Fitzgerald, VA, Dakin, SJ and Behme, RJ (1987). Laboratory investigation of outbreak of hemorrhagic colitis caused by Escherichia coli O157:H7. Journal of Clinical Microbiology 25: 1043–1047.CrossRefGoogle ScholarPubMed
Kusecek, B, Wloch, H, Mercer, A, Vaisänen, V, Pluschke, G, Korhonen, T and Achtman, M (1984). Lipopolysaccharide, capsule, and fimbriae as virulence factors among O1, O7, O16, O18, or O75 and K1, K5, or K100 Escherichia coli. Infection and Immunity 43: 368–379.CrossRefGoogle ScholarPubMed
Li, D, Liu, B, Chen, M, Guo, D, Guo, X, Liu, F, Feng, L and Wang, L (2010a). A multiplex PCR method to detect 14 Escherichia coli serogroups associated with urinary tract infections. Journal of Microbiological Methods 82: 71–77.CrossRefGoogle ScholarPubMed
Li, X, Perepelov, AV, Wang, Q, Senchenkova, SN, Liu, B, Shevelev, SD, Guo, X, Shashkov, AS, Chen, W, Wang, L and Knirel, YA (2010b). Structural and genetic characterization of the O-antigen of Escherichia coli O161 containing a derivative of a higher acidic diamino sugar, legionaminic acid. Carbohydrate Research 345: 1581–1587.CrossRefGoogle ScholarPubMed
Li, Y, Liu, D, Cao, B, Han, W, Liu, Y, Liu, F, Guo, X, Bastin, DA, Feng, L and Wang, L (2006). Development of a serotype-specific DNA microarray for identification of some Shigella and pathogenic Escherichia coli strains. Journal of Clinical Microbiology 44: 4376–83.CrossRefGoogle ScholarPubMed
Linton, KJ and Higgins, CF (1998). The Escherichia coli ATP binding cassette (ABC) proteins. Molecular Microbiology 28: 5–13.CrossRefGoogle ScholarPubMed
Liu, B, Knirel, YA, Feng, L, Perepelov, AV, Senchenkova, SN, Wang, Q, Reeves, PR and Wang, L (2008). Structure and genetics of Shigella O antigens. FEMS Microobiological Reviews 32: 627–653.CrossRefGoogle ScholarPubMed
Liu, B, Wu, F, Li, D, Beutin, L, Chen, M, Cao, B and Wang, L (2010). Development of a serogroup-specific DNA microarray for identification of Escherichia coli strains associated with bovine septicemia and diarrhea. Veterinary Microbiology 142: 373–378.CrossRefGoogle ScholarPubMed
Liu, Y, DebRoy, C and Fratamico, PM (2007). Sequencing and analysis of the Escherichia coli serogroup O117, O126, and O146 O-antigen gene clusters and development of PCR assays targeting serogroup O117-, O126-, and O146-specific DNA sequences. Molecular and Cellular Probes 21: 295–302.CrossRefGoogle ScholarPubMed
Liu, Y and Fratamico, P (2006). Escherichia coli O antigen typing using DNA microarrays. Molecular and Cellular Probes 20: 239–244.CrossRefGoogle ScholarPubMed
Liu, Y, Fratamico, PM, DebRoy, C, Bumbaugh, AC and Allen, JW (2008). DNA sequencing and identification of serogroup-specific genes in the Escherichia coli O118 O antigen gene cluster and demonstration of antigenic diversity but only minor variation in DNA sequence of the O antigen clusters of E. coli O118 and O151. Foodborne Pathogen and Disease 5: 449–457.CrossRefGoogle ScholarPubMed
MacLean, LL, Liu, Y, Vinogradov, E and Perry, MB (2010). The structural characterization of the O-polysaccharide antigen of the lipopolysaccharide of Escherichia coli serotype O118 and its relation to the O-antigens of Escherichia coli O151 and Salmonella enterica O47. Carbohydrate Research 345: 2664–2669.CrossRefGoogle Scholar
MacLean, LL, Webb, AC and Perry, MB (2006). Structural elucidation of the O-antigenic polysaccharide from enterohemorrhagic (EHEC) Escherichia coli O48:H21. Carbohydrate Research 341: 2543–2549.CrossRefGoogle ScholarPubMed
Marolda, CL and Valvano, MA (1993). Identification, expression, and DNA sequence of the GDP-mannose biosynthesis genes encoded by the O7 rfb gene cluster of strain VW187 (Escherichia coli O7:K1). Journal of Bacteriology 175: 148–158.CrossRefGoogle ScholarPubMed
McGrath, BC and Osborn, MJ (1991). Localization of the terminal steps of O antigen synthesis in Salmonella Typhimurium. Journal of Bacteriology 173: 649–654.CrossRefGoogle Scholar
Mulford, CA and Osborn, MJ (1983). An intermediate step in translocation of lipopolysaccharide to outer membrane of Salmonella Typhimurium. Proceedings of the National Academy of Sciences USA 80: 1159–1163.CrossRefGoogle ScholarPubMed
Neill, MA, Tarr, PI, Clausen, CR, Christie, DL and Hickman, RO (1987). Escherichia coli O157:H7 as the predominant pathogen associated with the hemolytic uremic syndrome: a prospective study in the Pacific Northwest. Pediatrics 80: 37–40.CrossRefGoogle ScholarPubMed
Ørskov, F and Ørskov, I (1984). Serotyping of Escherichia coli. Methods in Microbiology 14: 43–112.CrossRefGoogle Scholar
Ørskov, I, Ørskov, F, Evans, DJ, Sack, RB, Sack, DA and Wadstrom, T (1976). Special Escherichia coli serotypes among enterotoxigenic strains from diarrhea in adults and children. Medical Microbiology and Immunology 162: 73–80.CrossRefGoogle ScholarPubMed
Ørskov, I, Ørskov, F, Jann, B and Jann, K (1977). Serology, Chemistry and genetics of O and K antigens of Escherichia coli. Bacteriological Review 41: 667–710.CrossRefGoogle Scholar
Ørskov, I, Ørskov, F and Rowe, B (1984). Six new E. coli O groups: O165, O166, O167, O168, O169 and O170. Acta Pathologica, Microbialogica et Immunologica Scandinavica Section B 92: 189–193.Google Scholar
Ørskov, I, Wachsmuth, IK, Taylor, DN, Echeverria, P, Rowe, B, Sakazaki, R et al. (1991). Two new Escherichia coli O groups: O172 from “Shiga-like” toxin II-producing strains (EHEC) and O173 from enteroinvasive E. coli (EIEC). Acta Pathologica, Microbialogica et Immunologica Scandinavica 99: 30–32.CrossRefGoogle ScholarPubMed
Paton, AW and Paton, JC (1999). Molecular characterization of the locus encoding biosynthesis of the lipopolysaccharide O antigen of Escherichia coli serotype O113. Infection and Immunity 67: 5930–5937.CrossRefGoogle ScholarPubMed
Perelle, S, Dilasser, F, Grout, J and Fach, P (2002). Identification of the O-antigen biosynthesis genes of Escherichia coli O91 and development of a O91 PCR serotyping test. Journal of Applied Microbiology 93: 758–764.CrossRefGoogle ScholarPubMed
Perelle, S, Dilasser, F, Grout, J and Fach, P (2004). Detection by 5′-nuclease PCR of Shiga-toxin producing Escherichia coli O26, O55, O91, O103, O111, O113, O145, and O157:H7. Molecular and Cellular Probes 18: 185–192.CrossRefGoogle Scholar
Perepelov, AV, Li, D, Liu, B, Senchenkova, SN, Guo, D, Shashkov, AS, Feng, L, Knirel, YA and Wang, L (2011a). Structural and genetic characterization of the closely related O-antigens of Escherichia coli O85 and Salmonella enterica O17. Innate Immunity 17: 164–173.CrossRefGoogle ScholarPubMed
Perepelov, AV, Li, D, Liu, B, Senchenkova, SN, Guo, D, Shevelev, SD, Shashkov, AS, Guo, X, Feng, L, Knirel, YA and Wang, L (2009). Structural and genetic characterization of Escherichia coli O99 antigen. FEMS Immunology and Medicinal Microbiology 57: 80–87.CrossRefGoogle ScholarPubMed
Perepelov, AV, Ni, Z, Wang, Q, Shevelev, SD, Senchenkova, SN, Shahskov, AS, Wang, L and Knirel, YA (2011b). Structure and gene cluster of the O-antigen of Escherichia coli O109; chemical and genetic evidences of the presence of L-RhaN3N derivatives in the O-antigens of E. coli O109 and O119. FEMS Immunology and Medicinal Microbiology 61: 47–53.CrossRefGoogle ScholarPubMed
Plainvert, C, Bidet, P, Peigne, C, Barbe, V, Médigue, C, Denamur, E, Bingen, E and Bonacorsi, S (2007). A new O-antigen gene cluster has a key role in the virulence of the Escherichia coli meningitis clone O45:K1:H7. Journal of Bacteriology 189: 8528–8536.CrossRefGoogle Scholar
Pluschke, G, Mayden, J, Achtman, M and Levine, RP (1983). Role of the capsule and the O-antigen in resistance of O18:K1 Escherichia coli to complement-mediated killing. Journal of Bacteriology 42: 907–913.Google ScholarPubMed
Poltorak, A, He, X, Smirnova, I, Liu, MY, Van Huffel, C and Du, X (1998). Defective LPS signaling in C#H/HeJ and C57BL/10ScCr mice. Mutations in TLR4 gene. Science 282: 2085–2088.CrossRefGoogle Scholar
Raetz, CRH, Reynolds, CM, Trent, MS and Bishop, RE (2007). Lipid A modification systems in Gram-negative bacteria. Annual Review of Biochemistry 76: 295–329.CrossRefGoogle ScholarPubMed
Raetz, CRH and Whitfield, C (2002). Lipopolysaccharide endotoxins. Annual Review of Biochemistry 71: 635–700.CrossRefGoogle ScholarPubMed
Reeves, PR (1994). Biosynthesis and assembly of lipopolysaccharide. New Comprehensive Biochemistry 27: 281–317.CrossRefGoogle Scholar
Reeves, PR, Hobbs, M, Valvano, MA, Skurnik, M, Whitfield, C, Coplin, D, Kido, N, Klena, J, Maskell, D, Raetz, CRH and Rick, PD (1996). Bacterial polysaccharide synthesis and gene nomenclature. Trends in Microbiology 4: 495–503.CrossRefGoogle ScholarPubMed
Reeves, PR and Wang, L (2002). Genomic organization of LPS-specific loci. Current Topics in Microbiological Immunology 264: 109–135.Google ScholarPubMed
Remis, RS, MacDonald, KL, Riley, LW, Puhr, ND, Wells, JG, Davis, BR, Blake, PA and Cohen, ML (1984). Sporadic cases of hemorrhagic colitis associated with Escherichia coli O157:H7. Annals of Internal Medicine 101: 624–626.CrossRefGoogle ScholarPubMed
Ren, Y, Liu, B, Cheng, J, Liu, F, Feng, L and Wang, L (2008). Characterization of Escherichia coli O3 and O21 O antigen gene clusters and development of serogroup-specific PCR assays. Journal of Microbiological Methods 75: 329–334.CrossRefGoogle ScholarPubMed
Riley, LW, Remis, RS, Helgerson, SD, McGee, HB, Wells, JG, Davis, BR, Hebert, RJ, Olcott, ES, Johnson, LM, Hargrett, NT, Blake, PA and Cohen, ML (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine 308: 681–685.CrossRefGoogle ScholarPubMed
Rump, LV, Beutin, L, Fischer, M and Feng, PC (2010b). Characterization of a gne::IS629 O rough:H7 Escherichia coli strain from a hemorrhagic colitis patient. Applied and Environmental Microbiology 76: 5290–5291.CrossRefGoogle ScholarPubMed
Rump, LV, Feng, PC, Fischer, M and Monday, SR (2010a). Genetic analysis for the lack of expression of the O157 antigen in an O Rough:H7 Escherichia coli strain. Applied and Environmental Microbiology 76: 945–957.CrossRefGoogle Scholar
Samuel, G and Reeves, PR (2003). Biosynthesis of O antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydrate Research 338: 2503–2519.CrossRefGoogle Scholar
Scheutz, F, Cheasty, T, Woodward, D and Smith, HR (2004). Designation of O174 and O175 to temporary O groups OX3 and OX7, and six new E. coli O groups that include verotoxin-producing E. coli (VTEC): O176, O177, O178, O179, O180 and O181. Acta Pathologica, Microbiologica et Immunologica Scandinavica 112: 569–584.CrossRefGoogle Scholar
Shao, J, Li, M, Jia, Q, Lu, Y and Wang, PG (2003). Sequence of Escherichia coli O128 antigen biosynthesis cluster and functional identification of an alpha-1,2-fucosyltransferase. FEBS Letters 553: 99–103.CrossRefGoogle ScholarPubMed
Shepherd, JG, Wang, L and Reeves, PR (2000). Comparison of O-antigen gene clusters of Escherichia coli (Shigella) sonnei and Plesiomonas shigelloides O17: sonnei gained its current plasmid-borne O-antigen genes from P. shigelloides in a recent event. Infection and Immunity 68: 6056–6061.CrossRefGoogle Scholar
Sura, R, Van Kruiningen, HJ, DebRoy, C, Hinckley, LS, Greenberg, KJ, Gordon, Z and French, RA (2007). Extraintestinal pathogenic E. coli (ExPEC) induced acute necrotizing pneumonia in cats. Zoonoses Public Health 54: 307–313.CrossRefGoogle ScholarPubMed
Tarr, PI, Schoening, LM, Yea, YL, Ward, TR, Jelacic, S and Whittam, TS (2000). Acquisition of the rfb-gnd cluster in evolution of Escherichia coli O55 and O157. Journal of Bacteriology 182: 6183–6191.CrossRefGoogle ScholarPubMed
Vigil, PD, Alteri, CJ and Mobley, HL (2011). Identification of in vivo induced antigens including a RTX family exoprotein required for uropathogenic Escherichia coli virulence. Infection and Immunity 79: 2335–2344.CrossRefGoogle ScholarPubMed
Wang, L, Briggs, CE, Rothemund, D, Fratamico, P, Luchansky, JB and Reeves, PR (2001). Sequence of the E. coli O104 antigen gene cluster and identification of O104 specific genes. Gene 270: 231–236.CrossRefGoogle Scholar
Wang, L, Curd, H, Qu, W and Reeves, PR (1998). Sequencing of Escherichia coli O111 O-antigen gene cluster and identification of O111-specific genes. Journal of Clinical Microbiology 36: 3182–3187.CrossRefGoogle ScholarPubMed
Wang, L, Huskic, S, Cisterne, A, Rothemund, D and Reeves, PR (2002). The O-antigen gene cluster of Escherichia coli O55:H7 and identification of a new UDP-GlcNAc C4 epimerase gene. Journal of Bacteriology 184: 2620–2625.CrossRefGoogle Scholar
Wang, L, Liu, B, Kong, Q, Steinruck, H, Krause, G, Beutin, L and Feng, L (2005). Molecular markers for detection of pathogenic Escherichia coli strains belonging to serogroups O138 and O139. Veterinary Microbiology 111: 181–190.CrossRefGoogle Scholar
Wang, L and Reeves, PR (1998). Organization of Escherichia coli O157 O antigen gene cluster and identification of its specific genes. Infection and Immunity 66: 3545–3551.CrossRefGoogle ScholarPubMed
Wang, L, Rothemund, D, Curd, H and Reeves, PR (2003). Species-wide variation in the Escherichia coli flagellin (H-antigen) gene. Journal of Bacteriology 185: 2936–2943.CrossRefGoogle ScholarPubMed
Wang, L, Wang, Q and Reeves, PR (2010). The variations of O antigens in gram negative bacteria. Subcellular Biochemistry 53: 123–152.CrossRefGoogle Scholar
Wang, Q, Perepelov, AV, Feng, L, Knirel, YA, Li, Y and Wang, L (2009). Genetic and structural analyses of Escherichia coli O107 and O117 O-antigens. FEMS Immunology and Medical Microbiology 55: 47–54.CrossRefGoogle ScholarPubMed
Wang, Q, Ruan, X, Wei, D, Hu, Z, Wu, L, Yu, T, Feng, L and Wang, L (2010a). Development of a serogroup-specific multiplex PCR assay to detect a set of Escherichia coli serogroups based on the identification of their O-antigen gene clusters. Molecular and Cellular Probes 24: 286–290.CrossRefGoogle ScholarPubMed
Wang, Q, Wang, S, Beutin, L, Cao, B, Feng, L and Wang, L (2010b). Development of a DNA microarray for detection and serotyping of enterotoxigenic Escherichia coli. Journal of Clinical Microbiology 48: 2066–2074.CrossRefGoogle ScholarPubMed
Wang, W, Perepelov, AV, Feng, L, Shevelev, SD, Wang, Q, Senchenkova, SN, Han, W, Li, Y, Shashkov, AS, Knirel, YA, Reeves, PR and Wang, L (2007). A group of Escherichia coli and Salmonella enterica O antigens sharing a common backbone structure. Microbiology 153: 2159–2167.CrossRefGoogle ScholarPubMed
Wang, X and Quinn, PJ (2010). Lipopolysaccharide: Biosynthetic pathway and structure modification. Progress in Lipid Research 49: 97–107.CrossRefGoogle ScholarPubMed
West, NP, Sansonetti, P, Mounier, J, Exley, RM, Parsot, C, Guadagnini, S, Pre´vost, M, Prochnicka-Chalufour, A, Delepierre, M, Tanguy, M and Tang, CM (2005). Optimization of virulence functions through glucosylation of Shigella LPS. Science 307: 1313–1317.CrossRefGoogle ScholarPubMed