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Volume 56, Issue 7

Novel protein targets of the humoral immune response to infection in rabbits Free

Abstract

The role of the humoral immune response in protective immunity against listerial infection has been overlooked and is essentially unknown. This study aimed to discover the protein targets of that elicit an antibody response following infection in a rabbit model. A genomic expression library for was constructed and differentially screened to identify genes encoding proteins that reacted with antiserum from rabbits infected with live serotype 4b (RL), but not with that from animals immunized with heat-killed bacteria (RK). Thirty-one clones expressing proteins that reacted exclusively with RL were identified and sequenced. Sequence analysis, together with Western blot analysis of the proteins expressed from positive clones, led to the identification of eight proteins as targets of humoral immune responses during listerial infection: three internalin members (InlA, InlD and InlC2) and five novel proteins of unknown function (designated IspA, IspB, IspC, IspD and IspE, respectively). Exhibition of humoral immune responses to these proteins in actively infected rabbits but not in animals receiving heat-killed suggested that they were induced or significantly upregulated during infection and thus are important in pathogenesis. With the exception of antibodies to InlA, this is the first demonstration of antibodies to the other seven proteins in infected hosts. These immunogenic proteins may be useful candidates for elucidation of the role of antibodies in protective immunity in the context of listerial infection, as well as potential targets for serodiagnostic reagents and vaccine and drug development.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AP, alkaline phosphatase and Isp, immunogenic surface protein
Government of Canada
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2007-07-01
2024-05-01
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References

  1. Artiushin S., Timoney J. F., Nally J., Verma A. 2004; Host-inducible immunogenic sphingomyelinase-like protein, Lk73.5, of Leptospira interrogans. . Infect Immun 72:742–749 [CrossRef]
     [Google Scholar]
  2. Bannantine J. P., Stabel J. R. 2001; Identification of two Mycobacterium avium subspecies paratuberculosis gene products differentially recognised by sera from rabbits immunised with live mycobacteria but not heat-killed mycobacteria. J Med Microbiol 50:795–804
     [Google Scholar]
  3. Berche P., Reich K. A., Bonnichon M., Beretti J. L., Geoffroy C., Raveneau J., Cossart P., Gaillard J. L., Geslin P. other authors 1990; Detection of anti-listeriolysin O for serodiagnosis of human listeriosis. Lancet 335:624–627 [CrossRef]
     [Google Scholar]
  4. Bhunia A. K. 1997; Antibodies to Listeria monocytogenes . Crit Rev Microbiol 23:77–107 [CrossRef]
     [Google Scholar]
  5. Boerlin P., Boerlin-Petzold F., Jemmi T. 2003; Use of listeriolysin O and internalin A in a seroepidemiological study of listeriosis in Swiss dairy cows. J Clin Microbiol 41:1055–1061 [CrossRef]
     [Google Scholar]
  6. Braun L., Dramsi S., Dehoux P., Bierne H., Lindahl G., Cossart P. 1997; InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microbiol 25:285–294 [CrossRef]
     [Google Scholar]
  7. Braun L., Ghebrehiwet B., Cossart P. 2000; gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. . EMBO J 19:1458–1466 [CrossRef]
     [Google Scholar]
  8. Cabanes D., Dehoux P., Dussurget O., Frangeul L., Cossart P. 2002; Surface proteins and the pathogenic potential of Listeria monocytogenes . Trends Microbiol 10:238–245 [CrossRef]
     [Google Scholar]
  9. Cabanes D., Dussurget O., Dehoux P., Cossart P. 2004; Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol Microbiol 51:1601–1614 [CrossRef]
     [Google Scholar]
  10. Deb D. K., Dahiya P., Srivastava K. K., Srivastava R., Srivastava B. S. 2002; Selective identification of new therapeutic targets of Mycobacterium tuberculosis by IVIAT approach. Tuberculosis (Edinb 82:175–182 [CrossRef]
     [Google Scholar]
  11. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. 1995; Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 16:251–261 [CrossRef]
     [Google Scholar]
  12. Dramsi S., Dehoux P., Lebrun M., Goossens P. L., Cossart P. 1997; Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun 65:1615–1625
     [Google Scholar]
  13. Edelson B. T., Unanue E. R. 2000; Immunity to Listeria infection. Curr Opin Immunol 12:425–431 [CrossRef]
     [Google Scholar]
  14. Edelson B. T., Cossart P., Unanue E. R. 1999; Cutting edge: paradigm revisited: antibody provides resistance to Listeria infection. J Immunol 163:4087–4090
     [Google Scholar]
  15. Gentschev I., Sokolovic Z., Kohler S., Krohne G. F., Hof H., Wagner J., Goebel W. 1992; Identification of p60 antibodies in human sera and presentation of this listerial antigen on the surface of attenuated salmonellae by the HlyB-HlyD secretion system. Infect Immun 60:5091–5098
     [Google Scholar]
  16. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P. other authors 2001; Comparative genomics of Listeria species. Science 294:849–852
     [Google Scholar]
  17. Grenningloh R., Darji A., Wehland J., Chakraborty T., Weiss S. 1997; Listeriolysin and IrpA are major protein targets of the human humoral response against Listeria monocytogenes. . Infect Immun 65:3976–3980
     [Google Scholar]
  18. Handfield M., Brady L. J., Progulske-Fox A., Hillman J. D. 2000; IVIAT: a novel method to identify microbial genes expressed specifically during human infections. Trends Microbiol 8:336–339 [CrossRef]
     [Google Scholar]
  19. Hang L., John M., Asaduzzaman M., Bridges E. A., Vanderspurt C., Kirn T. J., Taylor R. K., Hillman J. D., Progulske-Fox A. other authors 2003; Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. . Proc Natl Acad Sci U S A 100:8508–8513 [CrossRef]
     [Google Scholar]
  20. Hoffman J. A., Badger J. L., Zhang Y., Huang S. H., Kim K. S. 2000; Escherichia coli K1 aslA contributes to invasion of brain microvascular endothelial cells in vitro and in vivo. Infect Immun 68:5062–5067 [CrossRef]
     [Google Scholar]
  21. Hughes J., Ward C. J., Peral B., Aspinwall R., Clark K., San Millan J. L., Gamble V., Harris P. C. 1995; The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151–160 [CrossRef]
     [Google Scholar]
  22. John M., Kudva I. T., Griffin R. W., Dodson A. W., McManus B., Krastins B., Sarracino D., Progulske-Fox A., Hillman J. D. other authors 2005; Use of in vivo-induced antigen technology for identification of Escherichia coli O157 : H7 proteins expressed during human infection. Infect Immun 73:2665–2679 [CrossRef]
     [Google Scholar]
  23. Kajava A. V. 1998; Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519–527 [CrossRef]
     [Google Scholar]
  24. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  25. Lazowska I., Trzeciak L., Godlewska R., Hennig E., Jagusztyn-Krynicka K., Popowski J., Regula J., Ostrowski J. 2000; In search of immunogenic Helicobacter pylori proteins by screening of expression library. Digestion 61:14–21 [CrossRef]
     [Google Scholar]
  26. Lin M. 1999; Molecular analysis of flaB, a periplasmic flagellar core protein gene in pathogenic leptospires. J Biochem Mol Biol Biophys 2:181–187
     [Google Scholar]
  27. Lodes M. J., Houghton R. L., Bruinsma E. S., Mohamath R., Reynolds L. D., Benson D. R., Krause P. J., Reed S. G., Persing D. H. 2000; Serological expression cloning of novel immunoreactive antigens of Babesia microti . Infect Immun 68:2783–2790 [CrossRef]
     [Google Scholar]
  28. Lorber B. 1997; Listeriosis. Clin Infect Dis 24:1–9 [CrossRef]
     [Google Scholar]
  29. Mackaness G. B. 1962; Cellular resistance to infection. J Exp Med 116:381–406 [CrossRef]
     [Google Scholar]
  30. McLaughlan A. M., Foster S. J. 1998; Molecular characterization of an autolytic amidase of Listeria monocytogenes EGD. Microbiology 144:1359–1367 [CrossRef]
     [Google Scholar]
  31. Meier J., Lopez L. 2001; Listeriosis: an emerging food-borne disease. Clin Lab Sci 14:187–192
     [Google Scholar]
  32. Mengaud J., Ohayon H., Gounon P., Mege R. M., Cossart P. 1996; E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923–932 [CrossRef]
     [Google Scholar]
  33. Ochsenbein A. F., Fehr T., Lutz C., Suter M., Brombacher F., Hengartner H., Zinkernagel R. M. 1999; Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156–2159 [CrossRef]
     [Google Scholar]
  34. Read T. D., Peterson S. N., Tourasse N., Baillie L. W., Paulsen I. T., Nelson K. E., Tettelin H., Fouts D. E., Eisen J. A. other authors 2003; The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81–86 [CrossRef]
     [Google Scholar]
  35. Rocourt J., Bille J. 1997; Foodborne listeriosis. World Health Stat Q 50:67–73
     [Google Scholar]
  36. Rollins S. M., Peppercorn A., Hang L., Hillman J. D., Calderwood S. B., Handfield M., Ryan E. T. 2005; In vivo induced antigen technology (IVIAT. Cell Microbiol 7:1–9
     [Google Scholar]
  37. Sambrook J., Russel D. W. 2000 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  38. Schlech W. F. III 1993; An animal model of foodborne Listeria monocytogenes virulence: effect of alterations in local and systemic immunity on invasive infection. Clin Invest Med 16:219–225
     [Google Scholar]
  39. Shen Y., Naujokas M., Park M., Ireton K. 2000; InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103:501–510 [CrossRef]
     [Google Scholar]
  40. Suk K., Das S., Sun W., Jwang B., Barthold S. W., Flavell R. A., Fikrig E. 1995; Borrelia burgdorferi genes selectively expressed in the infected host. Proc Natl Acad Sci U S A 92:4269–4273 [CrossRef]
     [Google Scholar]
  41. Vazquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., Gonzalez-Zorn B., Wehland J., Kreft J. 2001; Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584–640 [CrossRef]
     [Google Scholar]
  42. Yu W. 2004; The gene products of Listeria monocytogenes induced specifically during rabbit infection . MSc Thesis University of Ottawa; Ottawa, Canada:
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Novel protein targets of the humoral immune response to Listeria monocytogenes infection in rabbits
J. Med. Microbiol. 56, 888 (2007); https://doi.org/10.1099/jmm.0.46977-0
/content/journal/jmm/10.1099/jmm.0.46977-0
/content/journal/jmm/10.1099/jmm.0.46977-0
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