Association of a protective monoclonal iga with the O antigen of Salmonella enterica serovar typhimurium impacts type 3 secretion and outer membrane integrity

Infection and Immunity

Volumn 80, Issue 7, 2012, Pages 2454-2463

  Forbes, Stephen J ^a,b,c   Martinelli, Daniel ^a   Hsieh, Chyongere ^a   Ault, Jeffrey G ^a   Marko, Michael ^a   Mannella, Carmen A ^a   Mantis, Nicholas J ^a,b  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITY AT ALBANY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; IMMUNOGLOBULIN A ANTIBODY; O ANTIGEN; SAL4 ANTIBODY; TRANSLOCON; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CULTURE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CROSS LINKING; CRYOELECTRON MICROSCOPY; EPITHELIUM CELL; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; TRANSMISSION ELECTRON MICROSCOPY; TYPE III SECRETION SYSTEM;

ANIMALS; ANTIBODIES, BACTERIAL; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; IMMUNOGLOBULIN A; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON; O ANTIGENS; PROTEIN BINDING; SALMONELLA TYPHIMURIUM;

EID: 84864808601     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00018-12     Document Type: Article

References (69)

1. Bakowski MA, et al. 2010. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonellacontaining vacuole. Cell Host Microbe 7:453- 462.
2. Becker LA, Bang IS, Crouch ML, Fang FC. 2005. Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium. Mol. Microbiol. 56:1004 -1016.
3. Berg HC. 2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19 -54.
4. Bernal-Bayard J, Ramos-Morales F. 2009. Salmonella type III secretion effector SlrP is an E3 ubiquitin ligase for mammalian thioredoxin. J. Biol. Chem. 284:27587-27595.
5. Blocker A, Komoriya K, Aizawa S. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. U. S. A. 100:3027-3030.
6. Booth IR, Edwards MD, Black S, Schumann U, Miller S. 2007. Mechanosensitive channels in bacteria: signs of closure. Nat. Rev. Microbiol. 5:431- 440.
7. Cossart P, Sansonetti PJ. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248.
8. de Rezende CE, Anriany Y, Carr LE, Joseph SW, Weiner RM. 2005. Capsular polysaccharide surrounds smooth and rugose types of Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 71:7345-7351.
9. Ellermeier CD, Ellermeier JR, Slauch JM. 2005. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 57:691-705.
10. Ellermeier CD, Slauch JM. 2003. RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185:5096 -5108.
11. Faulk WP, Taylor GM. 1971. An immunocolloid method for the electron microscope. Immunochemistry. 8:1081-1083.
12. Forbes SJ, Bumpus T, McCarthy EA, Corthesy B, Mantis NJ. 2011. Transient suppression of Shigella flexneri type 3 secretion by a protective O-antigen-specific monoclonal IgA. mBio 2(3):e00042-11. doi:10.1128/ mBio.00042-11.
13. Forbes SJ, Eschmann M, Mantis NJ. 2008. Inhibition of Salmonella enterica serovar Typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun. 76:4137- 4144.
14. Galan JE. 2008. Energizing type III secretion machines: what is the fuel? Nat. Struct. Mol. Biol. 15:127-128.
15. Galan JE, Wolf-Watz H. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573.
16. Gibson DL, et al. 2006. Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J. Bacteriol. 188:7722-7730.
17. Griffin AJ, McSorley SJ. 2011. Development of protective immunity to Salmonella, a mucosal pathogen with a systemic agenda. Mucosal Immunol. 4:371-382.
18. Gunn JS, Belden WJ, Miller SI. 1998. Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb. Pathog. 25:77-90.
19. Haraga A, Ohlson MB, Miller SI. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53- 66.
20. Holzer SU, Schlumberger MC, Jackel D, Hensel M. 2009. Effect of the O-antigen length of lipopolysaccharide on the functions of Type III secretion systems in Salmonella enterica. Infect. Immun. 77:5458 -5470.
21. Hsu HS. 1989. Pathogenesis and immunity in murine salmonellosis. Microbiol. Rev. 53:390-409.
22. Iankov ID, et al. 2004. Protective efficacy of IgA monoclonal antibodies to O and H antigens in a mouse model of intranasal challenge with Salmonella enterica serotype Enteritidis. Microbes Infect. 6:901-910.
23. Iankov ID, Petrov DP, Mladenov IV, Haralambieva IH, Mitov IG. 2002. Lipopolysaccharide-specific but not anti-flagellar immunoglobulin A monoclonal antibodies prevent Salmonella enterica serotype Enteritidis invasion and replication within HEp-2 cell monolayers. Infect. Immun. 70:1615-1618.
24. Jones B, Ghori N, Falkow S. 1994. Salmonella typhimurium initiated murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J. Exp. Med. 180:15-23.
25. Jovanovic G, Lloyd LJ, Stumpf MP, Mayhew AJ, Buck M. 2006. Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J. Biol. Chem. 281:21147-21161.
26. Kastowsky M, Gutberlet T, Bradaczek H. 1992. Molecular modelling of the three-dimensional structure and conformational flexibility of bacterial lipopolysaccharide. J. Bacteriol. 174:4798-4806.
27. Kim ML, Slauch JM. 1999. Effect of acetylation (O-factor 5) on the polyclonal antibody response to Salmonella typhimurium O-antigen. FEMS Immunol. Med. Microbiol. 26:83-92.
28. Labischinski H, et al. 1985. High state of order of isolated bacterial lipopolysaccharide and its possible contribution to the permeation barrier property of the outer membrane. J. Bacteriol. 162:9 -20.
29. Leive L. 1965. Release of lipopolysaccharide by EDTA treatment of E. coli. Biochem. Biophys. Res. Commun. 21:290 -296.
30. Lin D, Rao CV, Slauch JM. 2008. The Salmonella SPI1 type three secretion system responds to periplasmic disulfide bond status via the flagellar apparatus and the RcsCDB system. J. Bacteriol. 190:87-97.
31. Loeb MR. 1974. Bacteriophage T4-mediated release of envelope components from Escherichia coli. J. Virol. 13:631- 641.
32. Loeb MR, Kilner J. 1978. Release of a special fraction of the outer membrane from both growing and phage T4-infected Escherichia coli B. Biochim. Biophys. Acta 514:117-127.
33. Mantis NJ, Forbes SJ. 2010. Secretory IgA: arresting microbial pathogens at epithelial borders. Immunol. Invest. 39:383- 406.
34. Mantis NJ, McGuinness CR, Sonuyi O, Edwards G, Farrant SA. 2006. Immunoglobulin A antibodies against ricin A and B subunits protect epithelial cells from ricin intoxication. Infect. Immun. 74:3455-3462.
35. Mantis NJ, Rol N, Corthesy B. 2011. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4:603- 611.
36. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545-558.
37. McGuckin MA, Linden SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9:265-278.
38. Michetti P, et al. 1991. Production and use of monoclonal IgA antibodies complexed with recombinant secretory component for passive mucosal protection. Adv. Exp. Med. Biol. 310:183-185.
39. Michetti P, Mahan MJ, Slauch JM, Mekalanos JJ, Neutra MR. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60:1786 -1792.
40. Michetti P, et al. 1994. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107:915-923.
41. Miki T, Okada N, Shimada Y, Danbara H. 2004. Characterization of Salmonella pathogenicity island 1 type III secretion-dependent hemolytic activity in Salmonella enterica serovar Typhimurium. Microb. Pathog. 37:65-72.
42. Minamino T, Pugsley AP. 2005. Measure for measure in the control of type III secretion hook and needle length. Mol. Microbiol. 56:303-308.
43. Morrison DC, Leive L. 1975. Fractions of lipopolysaccharide from Escherichia coli O111:B4 prepared by two extraction procedures. J. Biol. Chem. 250:2911-2919.
44. Murata T, Tseng W, Guina T, Miller SI, Nikaido H. 2007. PhoPQmediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:7213-7222.
45. Murray GL, Attridge SR, Morona R. 2006. 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. 188:2735-2739.
46. Murray GL, Attridge SR, Morona R. 2003. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol. Microbiol. 47: 1395-1406.
47. Nikaido H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593- 656.
48. Nikaido H. 1996. Outer membrane, p 29-47. In Neidhardt FC, Curtiss RI, Ingraham J, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, vol 1. ASM Press, Washington, DC.
49. Pilhofer M, Ladinsky MS, McDowall AW, Jensen GJ. 2010. Bacterial TEM: new insights from cryo-microscopy. Methods Cell Biol. 96:21- 45.
50. Prouty AM, Gunn JS. 2003. Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect. Immun. 71:7154 -7158.
51. Prouty AM, Schwesinger WH, Gunn JS. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70:2640 -2649.
52. Rathinavelan T, et al. 2010. A repulsive electrostatic mechanism for protein export through the type III secretion apparatus. Biophys. J. 98: 452-461.
53. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4:383-394.
54. Ruiz N, Silhavy TJ. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8:122-126.
55. Schlumberger MC, et al. 2005. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc. Natl. Acad. Sci. U. S. A. 102:12548 -12553.
56. Sherry AE, et al. 2011. Characterisation of proteins extracted from the surface of Salmonella Typhimurium grown under SPI-2-inducing conditions by LC-ESI/MS/MS sequencing. Proteomics 11:361-370.
57. Singh SP, et al. 1999. Recognition specificity of monoclonal antibodies which protect mice against Salmonella typhimurium infection. Res. Microbiol. 150:385-394.
58. Slauch JM, Lee AA, Mahan MJ, Mekalanos JJ. 1996. Molecular characterization of the oafA locus responsible for acetylation of Salmonella typhimurium O-antigen: OafA is a member of a family of integral membrane trans-acylases. J. Bacteriol. 178:5904 -5909.
59. Slauch JM, Mahan MJ, Michetti P, Neutra MR, Mekalanos JJ. 1995. Acetylation (O-factor 5) affects the structural and immunological properties of Salmonella typhimurium lipopolysaccharide O antigen. Infect. Immun. 63:437- 441.
60. Snyder DS, Gibson D, Heiss C, Kay W, Azadi P. 2006. Structure of a capsular polysaccharide isolated from Salmonella enteritidis. Carbohydr Res. 341:2388 -2397.
61. Strugnell RA, Wijburg OL. 2010. The role of secretory antibodies in infection immunity. Nat. Rev. Microbiol. 8:656-667.
62. Tsolis RM, et al. 1999. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect. Immun. 67:6385- 6393.
63. Vaara M. 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56:395- 411.
64. Vaara M, Vaara T. 1983. Polycations as outer membrane-disorganizing agents. Antimicrob. Agents Chemother. 24:114 -122.
65. van der Velden AW, Lindgren SW, Worley MJ, Heffron F. 2000. Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype Typhimurium. Infect. Immun. 68:5702-5709.
66. Waldo FB, Cochran AM. 1989. Mixed IgA-IgG aggregates as a model of immune complexes in IgA nephropathy. J. Immunol. 142:3841-3846.
67. West NP, et al. 2005. Optimization of virulence functions through glucosylation of Shigella LPS. Science 307:1313-1317.
68. Wilharm G, et al. 2004. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72:4004-4009.
69. Woof JM, Kerr MA. 2006. The function of immunoglobulin A in immunity. J. Pathol. 208:270 -282.