Inhibition of Salmonella enterica serovar typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin a antibody

Infection and Immunity

Volumn 76, Issue 9, 2008, Pages 4137-4144

  Forbes, Stephen J ^a   Eschmann, Marisa ^a,c   Mantis, Nicholas J ^a,b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b WADSWORTH CENTER   (United States)

^c PLUM ISLAND ANIMAL DISEASE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL IMMUNOGLOBULIN A ANTIBODY; POLYCLONAL ANTIBODY; SECRETORY IMMUNOGLOBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BRIGHT FIELD MICROSCOPY; CELL CYCLE ARREST; CELL MOTILITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOGENICITY; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; CELL LINE; DOGS; EPITHELIAL CELLS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN FAB FRAGMENTS; LOCOMOTION; MACROPHAGES; MICE; MICROSCOPY, VIDEO; SALMONELLA TYPHIMURIUM;

EID: 51949090627     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00416-08     Document Type: Article

References (54)

1. Adler, J. 1966. Chemotaxis in bacteria. Science 153:708-716.
2. Alba, B. M., and C. A. Gross. 2004. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52:613-619.
3. Apter, F. M., P. Michetti, L. S. D. Winner, J. A. Mack, J. J. Mekalanos, and M. R. Neutra. 1993. Analysis of the roles of antilipopolysaccharide and anti-cholera toxin immunoglobulin A (IgA) antibodies in protection against Vibrio choleras and cholera toxin by use of monoclonal IgA antibodies in vivo. Infect. Immun. 61:5279-5285.
4. Berg, H. C. 2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19-54.
5. Berg, H. C., and R. A. Anderson. 1973. Bacteria swim by rotating their flagellar filaments. Nature 245:380-382.
6. Berg, H. C., and L. Turner. 1993. Torque generated by the flagellar motor of Escherichia coli. Biophys. J. 65:2201-2216.
7. Boehm, M. K., J. M. Woof, M. A. Kerr, and S. J. Perkins. 1999. The Fab and Fc fragments of IgA1 exhibit a different arrangement from that in IgG: a study by X-ray and neutron solution scattering and homology modelling. J. Mol. Biol. 286:1421-1447.
8. Booth, I. R., M. D. Edwards, S. Black, U. Schumann, and S. Miller. 2007. Mechanosensitive channels in bacteria: signs of closure? Nat. Rev. Microbiol. 5:431-440.
9. Brandtzaeg, P. 2007. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25:5467-5484.
10. Buchmeier, N. A., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect. Immun. 57:1-7.
11. Chau, P. Y., R. S. Tsang, S. K. Lam, J. T. La Brooy, and D. Rowley. 1981. Antibody response to the lipopolysaccharide and protein antigens of Salmonella typhi during typhoid infection. II. Measurement of intestinal antibodies by radioimmunoassay. Clin. Exp. Immunol. 46:515-520.
12. Chowers, Y., J. Kirschner, N. Keller, I. Barshack, S. Bar-Meir, S. Ashkenazi, R. Schneerson, J. Robbins, and J. H. Passwell. 2007. Specific polysaccharide conjugate vaccine-induced IgG antibodies prevent invasion of Shigella into Caco-2 cells and may be curative. Proc. Natl. Acad. Sci. USA 104:2396-2401.
13. Connolly, S. E., and J. L. Benach. 2005. The versatile roles of antibodies in Borrelia infections. Nat. Rev. Microbiol. 3:411-420.
14. Cossart, P., and P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248.
15. Dann, S. M., and L. Eckmann. 2007. Innate immune defenses in the intestinal tract. Curr. Opin. Gastroenterol. 23:115-120.
16. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
17. Ellenneier, C. D., J. R. Ellermeier, and J. M. Slauch. 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.
18. Fuerst, J. A., and J. W. Perry. 1988. Demonstration of lipopolysaccharide on sheathed flagella of Vibrio cholerae O:1 by protein A-gold immunoelectron microscopy. J. Bacteriol. 170:1488-1494.
19. Gabel, C. V., and H. C. Berg. 2003. The speed of the flagellar rotary motor of Escherichia coli varies linearly with protonmotive force. Proc. Natl. Acad. Sci. USA 100:8748-8751.
20. Galan, J. E. 2008. Energizing type III secretion machines: what is the fuel? Nat. Struct. Mol. Biol. 15:127-128.
21. Galan, J. E., and H. Wolf-Watz. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573.
22. Gustafsson. B., and T. Holme. 1985. Rapid detection of Vibrio cholerae O:1 by motility inhibition and immunofluorescence with monoclonal antibodies. Eur. J. Clin. Microbiol. 4:291-294.
23. Haraga, A., M. B. Ohlson, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66.
24. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Iankov, I. D., D. P. Petrov, I. V. Mladenov, I. H. Haralambieva, R. Ivanova, V. R. Velev, and I. G. Mitov. 2002. Production and characterization of monoclonal immunoglobulin A. antibodies directed against Salmonella H:g,m flagellar antigen. FEMS Immunol. Med. Microbiol. 33:107-113.
26. Iankov, I. D., D. P. Petrov, I. V. Mladenov, I. H. Haralambieva, O. K. Kalev, M. S. Balabanova, and I. G. Mitov. 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.
27. Iankov, I. D., D. P. Petrov, I. V. Mladenov, I. H. Haralambieva, and I. G. Mitov. 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.
28. lino, T. 1974. Assembly of Salmonella flagellin in vitro and in vivo. J. Supramol. Struct. 2:372-384.
29. Jones, B., N. Ghori, and S. Falkow. 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.
30. Jones, B. D., C. A. Lee, and S. Falkow. 1992. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60:2475-2480.
31. Kim, M. L., and J. M. Slauch. 1999. Effect of acetylation (O-factor 5) on the polyclonal antibody response to Salmonella typhimurium O-antigen. FEMS Immunol. Med. Microbiol. 26:83-92.
32. Kraehenbuhl, J. P., and M. R. Neutra. 1992. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 72:853-879.
33. LaRocca, T. J., L. I. Katona, D. G. Thanassi, and J. L. Benach. 2008. Bactericidal action of a complement-independent antibody against relapsing fever Borrelia resides in its variable region. J. Immunol. 180:6222- 6228.
34. Lin, D., C. V. Rao, and J. M. Stench. 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.
35. Mackaness, G. B., R. V. Blanden, and F. M. Collins. 1966. Host-parasite relations in mouse typhoid. J. Exp. Med. 124:573-583.
36. Michetti, P., M. J. Mahan, J. M. Slauch, J. J. Mekalanos, and M. R. Neutra. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60:1786-1792.
37. Michetti, P., N. Porta, M. J. Mahan, J. M. Slauch, J. J. Mekalanos, A. Blum, J. P. Kraehenbuhl, and M. R. Neutra. 1994. Monoclonal immunoglobulin A. prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107:915-923.
38. Nelson, M. B., T. F. Murphy, H. van Keulen, D. Rekosh, and M. A. Apicella. 1988. Studies on P6, an important outer-membrane protein antigen of Haemophilus influenzae. Rev. Infect. Dis. 10(Suppl. 2):S331-S336.
39. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593-656.
40. Nikaido, H. 1996. Outer membrane. In F. C. Neidhardt, R. I. Curtiss, J. In-graham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, vol. 1. ASM Press, Washington, DC.
41. Peterson, D. A., N. P. McNulty, J. L. Guruge, and J. I. Gordon. 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328-339.
42. Phalipon, A., A. Cardona, J. P. Kraehenbuhl, L. Edelman, P. J. Sansonetti, and B. Corthesy. 2002. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 17:107-115.
43. Phalipon, A., and B. Corthesy. 2003. Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends Immunol. 24: 55-58.
44. Phalipon, A., P. Michetti, M. Kaufmann, J. M. Cavaillon, M. Huerre. J. P. Kraehenbuhl, and P. J. Sansonetti. 1994. Protection against invasion of the mouse pulmonary epithelium by a monoclonal IgA directed against Shigella flexneri lipopolysaccharide. Ann. N. Y. Acad. Sci. 730:356-358.
45. Rowley, G., M. Spector, J. Kormanec, and M. Roberts. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4:383-394.
46. Ruiz, N., D. Kahne, and T. J. Silhavy. 2006. Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4:57-66.
47. Sarasombath, S., N. Banchuin, T. SukosoL B. Rungpitarangsi, and S. Manasatit. 1987. Systemic and intestinal immunities after natural typhoid infection. J. Clin. Microbiol. 25:1088-1093.
48. Schmitt, C. K., J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
49. Shibuya, A., N. Sakamoto, Y. Shimizu, K. Shibuya, M. Osawa, T. Hiroyama, H. J. Eyre, G. R. Sutherland, Y. Endo, T. Fujita, T. Miyabayashi, S. Sakano, T. Tsuji, E. Nakayama, J. H. Phillips, L. L. Lanier, and H. Nakauchi. 2000. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat. Immunol. 1:441-446.
50. Slauch, J. M., M. J. Mahan, P. Michetti, M. R. Neutra, and J. J. Mekalanos. 1995. Acetylation (O-factor 5) affects the structural and immunological properties of Salmonella typhimurium lipopolysaccharide O antigen. Infect. Immun. 63:437-441.
51. Turner, L., W. S. Ryu, and H. C. Berg. 2000. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182:2793-2801.
52. Wilharm, G., V. Lehmann, K. Krauss, B. Lehnert, S. Richter, K. Ruckde-schel, J. Heesemann, and K. Trulzsch. 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.
53. Winner, L. D., J. Mack, R. Weltzin, J. J. Mekalanos, J. P. Kraehenbuhl, and M. R. Neutra. 1991. New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A. from hybridoma tumors protects against Vibrio cholerae infection. Infect. Immun. 59:977-982.
54. Woof, J. M., and M. A. Kerr. 2006. The function of immunoglobulin A. in immunity. J. Pathol. 208:270-282.