1887

Abstract

the cause of bacillary dysentery, belongs to Gram-negative enteropathogenic bacteria. contains a 210 kb virulence plasmid that encodes an O-antigen gene cluster of LPSs. However, this virulence plasmid is frequently lost during replication. It is well-documented that after losing the O-antigen and becoming rough strains, the Gram-negative bacteria may express an LPS core on its surface. Previous studies have suggested that by using the LPS core, Gram-negative bacteria can interact with several C-type lectin receptors that are expressed on antigen-presenting cells (APCs).

by losing the virulence plasmid may hijack APCs via the interactions of LPS-CD209/CD207.

This study aimed to investigate if the rough strain, by losing the virulence plasmid, interacted with APCs that express C-type lectins of human CD207, human CD209a and mouse CD209b.

SDS-PAGE silver staining was used to examine the O-antigen expression of WT and its rough strain. Invasion assays and inhibition assays were used to examine the ability of WT and its rough strain to invade APCs and investigate whether CD209 and CD207 are receptors for phagocytosis of rough . Animal assays were used to observe the dissemination of .

did not express O-antigens after losing the virulence plasmid. The rough strain invades with APCs, including human dendritic cells (DCs) and mouse macrophages. CD209 and CD207 are receptors for phagocytosis of rough . Expression of the O-antigen reduces the ability of the rough strain to be disseminated to mesenteric lymph nodes and spleens.

This work demonstrated that rough strains – by losing the virulence plasmid – invaded APCs through interactions with CD209 and CD207 receptors.

Funding
This study was supported by the:
  • the National Natural Science Foundation of China (Award 81471915)
    • Principle Award Recipient: TieChen
  • the National Natural Science Foundation of China (Award 81271780)
    • Principle Award Recipient: TieChen
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001297
2021-02-16
2021-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/3/jmm001297.html?itemId=/content/journal/jmm/10.1099/jmm.0.001297&mimeType=html&fmt=ahah

References

  1. Paciello I, Silipo A, Lembo-Fazio L, Curcurù L, Zumsteg A et al. Intracellular Shigella remodels its LPS to dampen the innate immune recognition and evade inflammasome activation. Proc Natl Acad Sci U S A 2013; 110:E4345–E4354 [View Article][PubMed]
    [Google Scholar]
  2. Anderson M, Sansonetti PJ, Marteyn BS. Shigella diversity and changing landscape: insights for the twenty-first century. Front Cell Infect Microbiol 2016; 6:45 [View Article][PubMed]
    [Google Scholar]
  3. Kahsay AG, Muthupandian S. A review on sero diversity and antimicrobial resistance patterns of Shigella species in Africa, Asia and South America, 2001-2014. BMC Res Notes 2016; 9:422 [View Article][PubMed]
    [Google Scholar]
  4. Gu B, Cao Y, Pan S, Zhuang L, Yu R et al. Comparison of the prevalence and changing resistance to nalidixic acid and ciprofloxacin of Shigella between Europe-America and Asia-Africa from 1998 to 2009. Int J Antimicrob Agents 2012; 40:9–17 [View Article][PubMed]
    [Google Scholar]
  5. The HC, Thanh DP, Holt KE, Thomson NR, Baker S. The genomic signatures of Shigella evolution, adaptation and geographical spread. Nat Rev Microbiol 2016; 14:235 [View Article][PubMed]
    [Google Scholar]
  6. Anderson MC, Vonaesch P, Saffarian A, Marteyn BS, Sansonetti PJ. Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche occupancy. Cell Host Microbe 2017; 21:769–776 [View Article][PubMed]
    [Google Scholar]
  7. Phalipon A, Sansonetti PJ, Armelle P, SP J. Shigella's ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival?. Immunol Cell Biol 2007; 85:119–129 [View Article][PubMed]
    [Google Scholar]
  8. Shepherd JG, Wang L, Reeves PR. 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. Infect Immun 2000; 68:6056–6061 [View Article][PubMed]
    [Google Scholar]
  9. Holst O. The structures of core regions from enterobacterial lipopolysaccharides - an update. FEMS Microbiol Lett 2007; 271:3–11 [View Article][PubMed]
    [Google Scholar]
  10. Kalynych S, Morona R, Cygler M. Progress in understanding the assembly process of bacterial O-antigen. FEMS Microbiol Rev 2014; 38:1048–1065 [View Article][PubMed]
    [Google Scholar]
  11. Murray GL, Attridge SR, Morona R. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol Microbiol 2003; 47:1395–1406 [View Article][PubMed]
    [Google Scholar]
  12. Murray GL, Attridge SR, Morona R. Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar typhimurium with macrophages and complement. J Bacteriol 2006; 188:2735–2739 [View Article][PubMed]
    [Google Scholar]
  13. Jiang Y, Yang F, Zhang X, Yang J, Chen L et al. The complete sequence and analysis of the large virulence plasmid pSS of Shigella sonnei . Plasmid 2005; 54:149–159 [View Article][PubMed]
    [Google Scholar]
  14. Sansonetti PJ, Kopecko DJ, Formal SB. Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infect Immun 1981; 34:75–83 [View Article][PubMed]
    [Google Scholar]
  15. McVicker G, Tang CM. Deletion of toxin-antitoxin systems in the evolution of Shigella sonnei as a host-adapted pathogen. Nat Microbiol 2016; 2:16204 [View Article][PubMed]
    [Google Scholar]
  16. Zhang P, Schwartz O, Pantelic M, Li G, Knazze Q et al. DC-SIGN (CD209) recognition of Neisseria gonorrhoeae is circumvented by lipooligosaccharide variation. J Leukoc Biol 2006; 79:731–738 [View Article][PubMed]
    [Google Scholar]
  17. Zhang P, Snyder S, Feng P, Azadi P, Zhang S et al. Role of N-acetylglucosamine within core lipopolysaccharide of several species of gram-negative bacteria in targeting the DC-SIGN (CD209). J Immunol 2006; 177:4002–4011 [View Article][PubMed]
    [Google Scholar]
  18. Zhang P, Skurnik M, Zhang SS, Schwartz O, Kalyanasundaram R et al. Human dendritic cell-specific intercellular adhesion molecule-grabbing nonintegrin (CD209) is a receptor for Yersinia pestis that promotes phagocytosis by dendritic cells. Infect Immun 2008; 76:2070–2079 [View Article][PubMed]
    [Google Scholar]
  19. Yang K, Park CG, Cheong C, Bulgheresi S, Zhang S et al. Host Langerin (CD207) is a receptor for Yersinia pestis phagocytosis and promotes dissemination. Immunol Cell Biol 2015; 93:815–824 [View Article][PubMed]
    [Google Scholar]
  20. He Y-X, Ye C-L, Zhang P, Li Q, Park CG et al. Yersinia pseudotuberculosis exploits CD209 receptors for promoting host dissemination and infection. Infect Immun 2019; 87:e00654–18 [View Article][PubMed]
    [Google Scholar]
  21. Yang K, He Y, Park CG, Kang YS, Zhang P et al. Yersinia pestis interacts with SIGNR1 (CD209b) for promoting host dissemination and infection. Front Immunol 2019; 10:96 [View Article][PubMed]
    [Google Scholar]
  22. Ye C, Li Q, Li X, Park CG, He Y et al. Salmonella enterica serovar typhimurium interacts with CD209 receptors to promote host dissemination and infection. Infect Immun 2019; 87:e00100–00119 [View Article][PubMed]
    [Google Scholar]
  23. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000; 100:587–597 [View Article][PubMed]
    [Google Scholar]
  24. Engering A, Van Vliet SJ, Geijtenbeek TB, Van Kooyk Y. Subset of DC-SIGN(+) dendritic cells in human blood transmits HIV-1 to T lymphocytes. Blood 2002; 100:1780–1786 [View Article][PubMed]
    [Google Scholar]
  25. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D et al. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 2003; 300:1295–1297 [View Article][PubMed]
    [Google Scholar]
  26. Nhieu GT, Sansonetti PJ. Mechanism of Shigella entry into epithelial cells. Curr Opin Microbiol 1999; 2:51–55 [View Article][PubMed]
    [Google Scholar]
  27. Schroeder GN, Hilbi H. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 2008; 21:134–156 [View Article][PubMed]
    [Google Scholar]
  28. Sansonetti PJ. Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella, making sense of prokaryote-eukaryote cross-talks. FEMS Microbiol Rev 2001; 25:3–14 [View Article][PubMed]
    [Google Scholar]
  29. Klena JD, Ashford RS, Schnaitman CA. Role of Escherichia coli K-12 rfa genes and the RFP gene of Shigella dysenteriae 1 in generation of lipopolysaccharide core heterogeneity and attachment of O antigen. J Bacteriol 1992; 174:7297–7307 [View Article][PubMed]
    [Google Scholar]
  30. Rosqvist R, Skurnik M, Wolf-Watz H. Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 1988; 334:522–525 [View Article][PubMed]
    [Google Scholar]
  31. Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 1990; 60:861–871 [View Article][PubMed]
    [Google Scholar]
  32. Skurnik M, Peippo A, Ervelä E. 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. Mol Microbiol 2000; 37:316–330 [View Article][PubMed]
    [Google Scholar]
  33. Chen T, Belland RJ, Wilson J, Swanson J. Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med 1995; 182:511–517 [View Article][PubMed]
    [Google Scholar]
  34. Qadri F, Hossain SA, Ciznár I, Haider K, Ljungh A et al. Congo red binding and salt aggregation as indicators of virulence in Shigella species. J Clin Microbiol 1988; 26:1343–1348 [View Article][PubMed]
    [Google Scholar]
  35. Kang YS, Yamazaki S, Iyoda T, Pack M, Bruening SA et al. Sign-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int Immunol 2003; 15:177–186 [View Article][PubMed]
    [Google Scholar]
  36. Bell SJ, Rigby R, English N, Mann SD, Knight SC et al. Migration and maturation of human colonic dendritic cells. J Immunol 2001; 166:4958–4967 [View Article][PubMed]
    [Google Scholar]
  37. Chen T, Grunert F, Medina-Marino A, Gotschlich EC. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J Exp Med 1997; 185:1557–1564 [View Article][PubMed]
    [Google Scholar]
  38. Yang JY, Lee SN, Chang SY, Ko H-J, Ryu S et al. A mouse model of shigellosis by intraperitoneal infection. J Infect Dis 2014; 209:203–215 [View Article][PubMed]
    [Google Scholar]
  39. Klena J, Zhang P, Schwartz O, Hull S, Chen T. The core lipopolysaccharide of Escherichia coli is a ligand for the dendritic-cell-specific intercellular adhesion molecule nonintegrin CD209 receptor. J Bacteriol 2005; 187:1710–1715 [View Article][PubMed]
    [Google Scholar]
  40. Kuwae A, Yoshida S, Tamano K, Mimuro H, Suzuki T et al. Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC. J Biol Chem 2001; 276:32230–32239 [View Article][PubMed]
    [Google Scholar]
  41. Mayer S, Raulf MK, Lepenies B. C-Type lectins: their network and roles in pathogen recognition and immunity. Histochem Cell Biol 2017; 147:223–237 [View Article][PubMed]
    [Google Scholar]
  42. Preza GC, Tanner K, Elliott J, Yang OO, Anton PA et al. Antigen-presenting cell candidates for HIV-1 transmission in human distal colonic mucosa defined by CD207 dendritic cells and CD209 macrophages. AIDS Res Hum Retroviruses 2014; 30:241–249 [View Article][PubMed]
    [Google Scholar]
  43. Loukas A, Maizels RM. Helminth C-type lectins and host-parasite interactions. Parasitol Today 2000; 16:333–339 [View Article][PubMed]
    [Google Scholar]
  44. de Witte L, Nabatov A, Geijtenbeek TB. Distinct roles for DC-SIGN+-dendritic cells and Langerhans cells in HIV-1 transmission. Trends Mol Med 2008; 14:12–19 [View Article][PubMed]
    [Google Scholar]
  45. Gurney KB, Elliott J, Nassanian H, Song C, Soilleux E et al. Binding and transfer of human immunodeficiency virus by DC-SIGN+ cells in human rectal mucosa. J Virol 2005; 79:5762–5773 [View Article][PubMed]
    [Google Scholar]
  46. Nasr N, Lai J, Botting RA, Mercier SK, Harman AN et al. Inhibition of two temporal phases of HIV-1 transfer from primary Langerhans cells to T cells: the role of langerin. J Immunol 2014; 193:2554–2564 [View Article][PubMed]
    [Google Scholar]
  47. Maeda N, Nigou J, Herrmann JL, Jackson M, Amara A et al. The cell surface receptor DC-SIGN discriminates between Mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J Biol Chem 2003; 278:5513–5516 [View Article][PubMed]
    [Google Scholar]
  48. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M et al. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 2003; 197:121–127 [View Article][PubMed]
    [Google Scholar]
  49. van Kooyk Y, Geijtenbeek TB. DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol 2003; 3:697–709 [View Article][PubMed]
    [Google Scholar]
  50. Sansonetti PJ. Microbes and microbial toxins: paradigms for microbial-mucosal interactions III. Shigellosis: from symptoms to molecular pathogenesis. Am J Physiol Gastrointest Liver Physiol 2001; 280:G319–323 [View Article][PubMed]
    [Google Scholar]
  51. Bernardini ML, Mounier J, d'Hauteville H, Coquis-Rondon M, Sansonetti PJ. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci U S A 1989; 86:3867–3871 [View Article][PubMed]
    [Google Scholar]
  52. Lugo-Villarino G, Troegeler A, Balboa L, Lastrucci C, Duval C et al. The C-Type Lectin receptor DC-SIGN has an anti-inflammatory role in human M(IL-4) macrophages in response to Mycobacterium tuberculosis . Front Immunol 2018; 9:1123 [View Article][PubMed]
    [Google Scholar]
  53. Schnaitman CA, Klena JD. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 1993; 57:655–682 [View Article][PubMed]
    [Google Scholar]
  54. Klena JD, Schnaitman CA. Function of the rfb gene cluster and the rfe gene in the synthesis of O antigen by Shigella dysenteriae 1. Mol Microbiol 1993; 9:393–402 [View Article][PubMed]
    [Google Scholar]
  55. Gillenius E, Urban CF. The adhesive protein invasin of Yersinia pseudotuberculosis induces neutrophil extracellular traps via β1 integrins. Microbes Infect 2015; 17:327–336 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001297
Loading
/content/journal/jmm/10.1099/jmm.0.001297
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error