Skip to main content
Log in

O-Antigen modifications providing antigenic diversity of Shigella flexneri and underlying genetic mechanisms

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

O-Antigens (O-specific polysaccharides) of Shigella flexneri, a primary cause of shigellosis, are distinguished by a wide diversity of chemical modifications following the oligosaccharide O-unit assembly. The present review is devoted to structural, serological, and genetic aspects of these modifications, including O-acetylation and phosphorylation with phosphoethanolamine that have been identified recently. The modifications confer the host with specific immunodeterminants (O-factors or O-antigen epitopes), which accounts for the antigenic diversity of S. flexneri considered as a virulence factor of the pathogen. Totally, 30 O-antigen variants have been recognized in these bacteria, the corresponding O-factors characterized using specific antibodies, and a significant extension of the serotyping scheme of S. flexneri on this basis is suggested. Multiple genes responsible for the O-antigen modifications and the resultant serotype conversions of S. flexneri have been identified. The genetic mechanisms of the O-antigen diversification by acquisition of mobile genetic elements, including prophages and plasmids, followed occasionally by gene mobilization and inactivation have been revealed. These findings further our understanding of the genetics and antigenicity of S. flexneri and assist control of shigellosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Receive 10 units per month
  • Download 1 article/chapter for 1 unit
  • Get selected eBooks for 7 units
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

GalA:

galacturonic acid

GalNAc:

2-acetamido-2-deoxygalactose

GlcNAc:

2-acetamido-2-deoxyglucose

IS:

insertion sequence

LPS:

lipopolysaccharide

PEtN:

phosphoethanolamine

Rha:

rhamnose

Sf:

Shigella flexneri

References

  1. Bardhan, P., Faruque, A. S., Naheed, A., and Sack, D. A. (2010) Decrease in shigellosis-related deaths without Shigella spp.-specific interventions, Asia, Emerg. Infect. Dis., 16, 1718–1723.

    Article  PubMed  Google Scholar 

  2. Schroeder, G. N., and Hilbi, H. (2008) Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion, Clin. Microbiol. Rev., 21, 134–156.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Ewing, W. H., and Lindberg, A. A. (1984) Serology of Shigella, Methods Microbiol., 14, 113–142.

    Article  CAS  Google Scholar 

  4. Pupo, G. M., Lan, R., and Reeves, P. R. (2000) Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics, Proc. Natl. Acad. Sci. USA, 97, 10567–10572.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Kotloff, K. L., Winickoff, J. P., Ivanoff, B., Clemens, J. D., Swerdlow, D. L., Sansonetti, P. J., Adak, G. K., and Levine, M. M. (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies, Bull. World Health Organ., 77, 651666.

    Google Scholar 

  6. Shiferaw, B., Shallow, S., Marcus, R., Segler, S., Soderlund, D., Hardnett, F. P., and Van Gilder, T (2004) Trends in population-based active surveillance for shigellosis and demographic variability in FoodNet sites, 19961999, Clin. Infect. Dis., 38 (Suppl. 3), S175–S180.

    Article  PubMed  Google Scholar 

  7. Livio, S., Strockbine, N., Panchalingam, S., Tennant, S. M., Barry, E. M., Marohn, M. E., Antonio, M., Hossain, A., Mandomando, I., Ochieng, J., B. Oundo, J. O., Qureshi, S., Ramamurthy, T, Tamboura, B., Adegbola, R. A., Hossain, M. J., Saha, D., Sen, S., Faruque, A. S., Alonso, P. L., Breiman, R. F., Zaidi, A. K., Sur, D., Sow, S. O., Berkeley, L. Y, O’Reilly, C., Mintz, E. D., Biswas, K., Cohen, D., Farag, T H., Nasrin, D., Wu, Y., Blackwelder, W. C., Kotloff, K. L., Nataro, J. P., and Levine, M. M. (2014) Shigella isolates from the Global Enteric Multicenter Study inform vaccine development, Clin. Infect. Dis., 59, 933–941.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Kenne, L., Lindberg, B., Petersson, K., Katzenellenbogen, E., and Romanowska, E. (1978) Structural studies of Shigella flexneri O-antigens, Eur. J. Biochem., 91, 279–284.

    Article  CAS  PubMed  Google Scholar 

  9. Simmons, D. A. R., and Romanowska, E. (1987) Structure and biology of Shigella flexneri O antigens, J. Med. Microbiol., 23, 289–302.

    Article  CAS  PubMed  Google Scholar 

  10. Perepelov, A. V., Shekht, M. E., Liu, B., Shevelev, S. D., Ledov, V. A., L’vov, V. L., Senchenkova, S. N., Shashkov, A. S., Feng, L., Aparin, P. G., Wang, L., and Knirel, Y. A. (2012) Shigella flexneri O-antigens revisited: final elucidation of the O-acetylation profiles and a survey of the Oantigen structure diversity, FEMS Immunol. Med. Microbiol., 66, 201–210.

    Article  CAS  PubMed  Google Scholar 

  11. Liu, B., Knirel, Y. A., Feng, L., Perepelov, A. V., Senchenkova, S. N., Wang, Q., Reeves, P. R., and Wang, L. (2008) Structure and genetics of Shigella O antigens, FEMS Microbiol. Rev., 32, 627–653.

    Article  PubMed  Google Scholar 

  12. Li, Y., Cao, B., Liu, B., Liu, D., Gao, Q., Peng, X., Wu, J., Bastin, D. A., Feng, L., and Wang, L. (2009) Molecular detection of all 34 distinct O-antigen forms of Shigella, J. Med. Microbiol., 58, 69–81.

    Article  CAS  PubMed  Google Scholar 

  13. Perepelov, A. V., Shevelev, S. D., Liu, B., Senchenkova, S. N., Shashkov, A. S., Feng, L., Knirel, Y. A., and Wang, L. (2010) Structures of the O-antigens of Escherichia coli O13, O129 and O135 related to the O-antigens of Shigella flexneri, Carbohydr. Res., 345, 1594–1599.

    Article  CAS  PubMed  Google Scholar 

  14. Allison, G. E., and Verma, N. K. (2000) Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri, Trends Microbiol., 8, 17–23.

    Article  CAS  PubMed  Google Scholar 

  15. Sun, Q., Lan, R., Wang, Y., Zhao, A., Zhang, S., Wang, J., Xia, S., Jin, D., Cui, Z., Zhao, H., Li, Z., Ye, C., Jing, H., and Xu, J. (2011) Development of a multiplex PCR assay targeting O-antigen modification genes for molecular serotyping of Shigella flexneri, J. Clin. Microbiol., 49, 3766–3770.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. West, N. P., Sansonetti, P., Mounier, J., Exley, R. M., Parsot, C., Guadagnini, S., Prevost, M. C., Prochnicka-Chalufour, A., Delepierre, M., Tanguy, M., and Tang, C. M. (2005) Optimization of virulence functions through glucosylation of Shigella LPS, Science, 307, 1313–1317.

    Article  CAS  PubMed  Google Scholar 

  17. Kohler, H., Rodrigues, S. P., and McCormick, B. A. (2002) Shigella flexneri interactions with the basolateral membrane domain of polarized model intestinal epithelium: role of lipopolysaccharide in cell invasion and in activation of the mitogen-activated protein kinase ERK, Infect. Immun., 70, 1150–1158.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Hong, M., and Payne, S. M. (1997) Effect of mutations in Shigella flexneri chromosomal and plasmid-encoded lipopolysaccharide genes on invasion and serum resistance, Mol. Microbiol., 24, 779–791.

    Article  CAS  PubMed  Google Scholar 

  19. Brahmbhatt, H. N., Lindberg, A. A., and Timmis, K. N. (1992) Shigella lipopolysaccharide: structure, genetics, and vaccine development, Curr. Top. Microbiol. Immunol., 180, 45–64.

    CAS  PubMed  Google Scholar 

  20. Kubler-Kielb, J., Vinogradov, E., Chu, C., and Schneerson, R. (2007) O-Acetylation in the O-specific polysaccharide isolated from Shigella flexneri serotype 2a, Carbohydr. Res., 342, 643–647.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Perepelov, A. V., L’vov, V. L., Liu, B., Senchenkova, S. N., Shekht, M. E., Shashkov, A. S., Feng, L., Aparin, P. G., Wang, L., and Knirel, Y. A. (2009) A similarity in the Oacetylation pattern of the O-antigens of Shigella flexneri types 1a, 1b and 2a, Carbohydr. Res., 344, 687–692.

    Article  CAS  PubMed  Google Scholar 

  22. Wang, J., Knirel, Y A., Lan, R., Senchenkova, S. N., Luo, X., Perepelov, A. V., Wang, Y, Shashkov, A. S., Xu, J., and Sun, Q. (2014) Identification of an O-acyltransferase gene (oacB) that mediates 3- and 4-O-acetylation of rhamnose III in Shigella flexneri O antigens, J. Bacteriol., 196, 15251531.

    Google Scholar 

  23. Knirel, Y. A., Luo, X., Wang, J., Senchenkova, S. N., Lan, R., Shpirt, A. M., Du, P., Shashkov, A. S., Xu, J., and Sun, Q. (2014) Genetic and structural identification of an Oacyltransferase gene (oacC) responsible for the 3/4-Oacetylation on rhamnose III in Shigella flexneri serotype 6, BMC Microbiol., 14, 266.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Sun, Q., Knirel, Y. A., Wang, J., Luo, X., Senchenkova, S. N., Lan, R., Shashkov, A. S., and Xu, J. (2014) Serotypeconverting bacteriophage SfII encodes an acyltransferase protein that mediates 6-O-acetylation of GlcNAc in Shigella flexneri O-antigens, conferring on the host a novel O-antigen epitope, J. Bacteriol., 196, 3656–3666.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Jakhetia, R., Marri, A., Stahle, J., Widmalm, G., and Verma, N. K. (2014) Serotype-conversion in Shigella flexneri: identification of a novel bacteriophage, Sf101, from a serotype 7a strain, BMC Genomics, 15, 742.

    PubMed  Google Scholar 

  26. Perepelov, A. V., L’vov, V. L., Liu, B., Senchenkova, S. N., Shekht, M. E., Shashkov, A. S., Feng, L., Aparin, P. G., Wang, L., and Knirel, Y. A. (2009) A new ethanolamine phosphate-containing variant of the O-antigen of Shigella flexneri type 4a, Carbohydr. Res., 344, 1588–1591.

    Article  CAS  PubMed  Google Scholar 

  27. Sun, Q., Knirel, Y. A., Lan, R., Wang, J., Senchenkova, S. N., Jin, D., Shashkov, A. S., Xia, S., Perepelov, A. V., Chen, Q., Wang, Y, Wang, H., and Xu, J. (2012) A novel plasmidencoded serotype conversion mechanism through addition of phosphoethanolamine to the O-antigen of Shigella flexneri, PLoS ONE, 7, e46095.

    Article  Google Scholar 

  28. Knirel, Y. A., Lan, R., Senchenkova, S. N., Wang, J., Shashkov, A. S., Wang, Y, Perepelov, A. V., Xiong, Y, Xu, J., and Sun, Q. (2013) O-antigen structure of Shigella flexneri serotype Yv and effect of the lpt-O gene variation on phosphoethanolamine modification of S. flexneri O-antigens, Glycobiology, 23, 475–485.

    Article  CAS  PubMed  Google Scholar 

  29. Sun, Q., Lan, R., Wang, J., Xia, S., Wang, Y, Wang, Y, Jin, D., Yu, B., Knirel, Y. A., and Xu, J. (2013) Identification and characterization of a novel Shigella flexneri serotype Yv in China, PLoS ONE, 8, e70238.

    Article  Google Scholar 

  30. Kenne, L., Lindberg, B., Petersson, K., and Romanowska, E. (1977) Basic structure of the oligosaccharide repeatingunit of the Shigella flexneri O-antigens, Carbohydr. Res., 56, 363–370.

    Article  CAS  PubMed  Google Scholar 

  31. Carlin, N. I. A., and Lindberg, A. A. (1987) Monoclonal antibodies specific for Shigella flexneri lipopolysaccharides: clones binding to type IV, V, and VI antigens, group 3,4 antigen, and an epitope common to all Shigella flexneri and Shigella dysenteriae type 1 strains, Infect. Immun., 55, 14121420.

    Google Scholar 

  32. Carlin, N. I. A., Bundle, D. R., and Lindberg, A. A. (1987) Characterization of five Shigella flexneri variant Y-specific monoclonal antibodies using defined saccharides and glycoconjugate antigens, J. Immunol., 138, 4419–4427.

    CAS  PubMed  Google Scholar 

  33. Wang, J., Lan, R., Knirel, Y. A., Luo, X., Senchenkova, S. N., Shashkov, A. S., Xu, J., and Sun, Q. (2014) Serological identification and prevalence of a novel O-antigen epitope linked to 3- and 4-O-acetylated rhamnose III of lipopolysaccharide in Shigella flexneri, J. Clin. Microbiol., 52, 2033–2038.

    Article  PubMed Central  PubMed  Google Scholar 

  34. Shashkov, A. S., Senchenkova, S. N., Sun, Q., Lan, R., Wang, J., Perepelov, A. V, Knirel, Y A., and Xu, J. (2013) Structure of the O-antigen of a novel Shigella flexneri serotype, 1d (I: 7,8), Carbohydr. Res., 373, 93–96.

    Article  CAS  PubMed  Google Scholar 

  35. Kenne, L., Lindberg, B., Petersson, K., Katzenellenbogen, E., and Romanowska, E. (1977) Structural studies of the Shigella flexneri variant X, type 5a and 5b O-antigens, Eur. J. Biochem., 76, 327–330.

    Article  CAS  PubMed  Google Scholar 

  36. Dmitriev, B. A., Knirel, Y A., Sheremet, O. K., Shashkov, A. S., Kochetkov, N. K., and Hofman, I. L. (1979) Somatic antigens of Shigella. The structure of the specific polysaccharide of Shigella newcastle (Sh. flexneri type 6) lipopolysaccharide, Eur. J. Biochem., 98, 309–316.

    Article  CAS  PubMed  Google Scholar 

  37. Wehler, T, and Carlin, N. I. A. (1988) Structural and immunochemical studies of the lipopolysaccharide from a new provisional serotype of Shigella flexneri, Eur. J. Biochem., 176, 471–476.

    Article  CAS  PubMed  Google Scholar 

  38. Foster, R. A., Carlin, N. I. A., Majcher, M., Tabor, H., Ng, L.-K., and Widmalm, G. (2011) Structural elucidation of the O-antigen of the Shigella flexneri provisional serotype 88-893: structural and serological similarities with Shigella flexneri provisional serotype Y394 (1c), Carbohydr. Res., 346, 872–876.

    Article  CAS  PubMed  Google Scholar 

  39. Kondakova, A. N., Vinogradov, E. V., Shekht, M. E., Markina, A. A., Lindner, B., L’vov, V. L., Aparin, P. G., and Knirel, Y. A. (2010) Structure of the oligosaccharide region (core) of the lipopolysaccharides of Shigella flexneri types 2a and 5b, Bioorg. Khim., 36, 396–399.

    CAS  Google Scholar 

  40. Kubler-Kielb, J., Vinogradov, E., Mocca, C., Pozsgay, V., Coxon, B., Robbins, J. B., and Schneerson, R. (2010) Immunochemical studies of Shigella flexneri 2a and 6, and Shigella dysenteriae type 1 O-specific polysaccharide-core fragments and their protein conjugates as vaccine candidates, Carbohydr. Res., 345, 1600–1608.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Guan, S., Bastin, D. A., and Verma, N. K. (1999) Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX, Microbiology, 145, 1263–1273.

    Article  CAS  PubMed  Google Scholar 

  42. Carlin, N. I. A., Wehler, T, and Lindberg, A. A. (1986) Shigella flexneri O-antigen epitopes: chemical and immunochemical analyses reveal that epitopes of type III and group 6 antigens are identical, Infect. Immun., 53, 110115.

    Google Scholar 

  43. Lugowski, C., Romanowska, E., Kenne, L., and Lindberg, B. (1983) Identification of a trisaccharide repeating-unit in the enterobacterial common-antigen, Carbohydr. Res., 118, 173–181.

    Article  CAS  Google Scholar 

  44. Dell, A., Oates, J., Lugowski, C., Romanowska, E., Kenne, L., and Lindberg, B. (1984) The enterobacterial commonantigen, a cyclic polysaccharide, Carbohydr. Res., 133, 95104.

    Article  Google Scholar 

  45. Carlin, N. I., Rahman, M., Sack, D. A., Zaman, A., Kay, B., and Lindberg, A. A. (1989) Use of monoclonal antibodies to type Shigella flexneri in Bangladesh, J. Clin. Microbiol., 27, 1163–1166.

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Talukder, K. A., Dutta, D. K., Safa, A., Ansaruzzaman, M., Hassan, F., Alam, K., Islam, K. M., Carlin, N. I., Nair, G. B., and Sack, D. A. (2001) Altering trends in the dominance of Shigella flexneri serotypes and emergence of serologically atypical S. flexneri strains in Dhaka, Bangladesh, J. Clin. Microbiol., 39, 3757–3759.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Rusden, A. D., Stephenson, D. P., and Verma, N. K. (2013) Topological investigation of glucosyltransferase V in Shigella flexneri using the substituted cysteine accessibility method, Biochemistry, 52, 2655–2661.

    Article  CAS  PubMed  Google Scholar 

  48. Markine-Goriaynoff, N., Gillet, L., Van Etten, J. L., Korres, H., Verma, N., and Vanderplasschen, A. (2004) Glycosyltransferases encoded by viruses, J. Gen. Virol., 85, 2741–2754.

    Article  CAS  PubMed  Google Scholar 

  49. Mavris, M., Manning, P. A., and Morona, R. (1997) Mechanism of bacteriophage SfII-mediated serotype conversion in Shigella flexneri, Mol. Microbiol., 26, 939–950.

    Article  CAS  PubMed  Google Scholar 

  50. Allison, G. E., Angeles, D., Tran-Dinh, N., and Verma, N. K. (2002) Complete genomic sequence of SfV, a serotypeconverting temperate bacteriophage of Shigella flexneri, J. Bacteriol., 184, 1974–1987.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Allison, G. E., Angeles, D. C., Huan, P. T, and Verma, N. K. (2003) Morphology of temperate bacteriophage SfV and characterization of the DNA packaging and capsid genes: the structural genes evolved from two different phage families, Virology, 308, 114–127.

    Article  CAS  PubMed  Google Scholar 

  52. Sun, Q., Lan, R., Wang, Y, Wang, J., Wang, Y, Li, P., Du, P., and Xu, J. (2013) Isolation and genomic characterization of SfI, a serotype-converting bacteriophage of Shigella flexneri, BMC Microbiol., 13, 39.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. George, D. T, Stephenson, D. P., Tran, E., Morona, R., and Verma, N. K. (2013) Complete genome sequence of SfII, a serotype-converting bacteriophage of the highly prevalent Shigella flexneri serotype 2a, Genome Announc., 1, e00626–13.

    Article  Google Scholar 

  54. Jakhetia, R., Talukder, K. A., and Verma, N. K. (2013) Isolation, characterization and comparative genomics of bacteriophage SfIV: a novel serotype converting phage from Shigella flexneri, BMC Genomics, 14, 677.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Sun, Q., Lan, R., Wang, Y, Wang, J., Luo, X., Zhang, S., Li, P., Wang, Y., Ye, C., Jing, H., and Xu, J. (2011) Genesis of a novel Shigella flexneri serotype by sequential infection of serotype-converting bacteriophages SfX and SfI, BMC Microbiol., 11, 269.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Stagg, R. M., Tang, S. S., Carlin, N. I., Talukder, K. A., Cam, P. D., and Verma, N. K. (2009) A novel glucosyltransferase involved in O-antigen modification of Shigella flexneri serotype 1c, J. Bacteriol., 191, 6612–6617.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Thanweer, F., Tahiliani, V., Korres, H., and Verma, N. K. (2008) Topology and identification of critical residues of the O-acetyltransferase of serotype-converting bacteriophage, SF6, of Shigella flexneri, Biochem. Biophys. Res. Commun., 375, 581–585.

    Article  CAS  PubMed  Google Scholar 

  58. Casjens, S., Winn-Stapley, D. A., Gilcrease, E. B., Morona, R., Kuhlewein, C., Chua, J. E., Manning, P. A., Inwood, W, and Clark, A. J. (2004) The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging, J. Mol. Biol., 339, 379–394.

    Article  CAS  PubMed  Google Scholar 

  59. Sun, Q., Lan, R., Wang, Y., Wang, J., Xia, S., Wang, Y, Zhang, J., Yu, D., Li, Z., Jing, H., and Xu, J. (2012) Identification of a divergent O-acetyltransferase gene oac1b from Shigella flexneri serotype 1b strains, Emerg. Microbes Infect., 1, e21.

    Article  CAS  Google Scholar 

  60. Sun, Q., Knirel, Y. A., Lan, R., Wang, J., Senchenkova, S. N., Shashkov, A. S., Wang, Y, Wang, Y, Luo, X., and Xu, J. (2014) Dissemination and serotype modification potential of pSFxv_2, an O-antigen PEtN modification plasmid in Shigella flexneri, Glycobiology, 24, 305–313.

    Article  CAS  PubMed  Google Scholar 

  61. Zhang, N., Lan, R., Sun, Q., Wang, J., Wang, Y, Zhang, J., Yu, D., Hu, W., Hu, S., Dai, H., Du, P., Wang, H., and Xu, J. (2014) Genomic portrait of the evolution and epidemic spread of a recently emerged multidrug-resistant Shigella flexneri clone in China, J. Clin. Microbiol., 52, 1119–1126.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Ye, C., Lan, R., Xia, S., Zhang, J., Sun, Q., Zhang, S., Jing, H., Wang, L., Li, Z., Zhou, Z., Zhao, A., Cui, Z., Cao, J., Jin, D., Huang, L., Wang, Y, Luo, X., Bai, X., Wang, P., Xu, Q., and Xu, J. (2010) Emergence of a new multidrug-resistant serotype X variant in an epidemic clone of Shigella flexneri, J. Clin. Microbiol., 48, 419426.

    Google Scholar 

  63. Qiu, S., Wang, Z., Chen, C., Liu, N., Jia, L., Liu, W., Wang, L., Hao, R., Zhang, L., Wang, Y, and Song, H. (2011) Emergence of a novel Shigella flexneri serotype 4s strain that evolved from a serotype X variant in China, J. Clin. Microbiol., 49, 1148–1150.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Y. A. Knirel, Qiangzheng Sun or Jianguo Xu.

Additional information

To whom correspondence should be addressed.

Published in Russian in Biokhimiya, 2015, Vol. 80, No. 7, pp. 1072-1087.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Knirel, Y.A., Sun, Q., Senchenkova, S.N. et al. O-Antigen modifications providing antigenic diversity of Shigella flexneri and underlying genetic mechanisms. Biochemistry Moscow 80, 901–914 (2015). https://doi.org/10.1134/S0006297915070093

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1134/S0006297915070093

Keywords