Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Dec 22;267(1461):2511–2516. doi: 10.1098/rspb.2000.1313

Antigenic role of the endosymbionts of filarial nematodes: IgG response against the Wolbachia surface protein in cats infected with Dirofilaria immitis.

C Bazzocchi 1, F Ceciliani 1, J W McCall 1, I Ricci 1, C Genchi 1, C Bandi 1
PMCID: PMC1690852  PMID: 11197127

Abstract

Filarial nematodes harbour intracellular endosymbiotic bacteria, which have been assigned to the genus Wolbachia. These bacteria appear to play an important role in the pathogenesis of filarial diseases through their lipopolysaccharides. In view of the presence of Wolbachia endosymbionts in the body of filarial nematodes, one might also expect that proteins from these bacteria play an antigenic role in humans and animals affected by filariases. To test this hypothesis, we produced in recombinant form the surface protein WSP and a portion of the cell-cycle protein FTSZ from the Wolbachia of Dirofilaria immitis. Western immunoblot assays were then performed using cat sera to test the immunogenicity of these proteins. Sera were collected from owners' cats, which were either sero-negative or sero-positive for D. immitis and from cats before and after experimental infection with D. immitis. FTSZ was recognized in Western blots by sera from both positive and negative cats and from both uninfected and experimentally infected cats. WSP was recognized only by sera from positive cats and from cats experimentally infected with D. immitis; this protein was not recognized by sera from negative cats and from cats before experimental infection with D. immitis. The results of Western blot assays on WSP thus support the hypothesis that infection with filarial nematodes induces the production of antibodies against Wolbachia proteins.

Full Text

The Full Text of this article is available as a PDF (495.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bandi C., Anderson T. J., Genchi C., Blaxter M. L. Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci. 1998 Dec 22;265(1413):2407–2413. doi: 10.1098/rspb.1998.0591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bandi C., McCall J. W., Genchi C., Corona S., Venco L., Sacchi L. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol. 1999 Feb;29(2):357–364. doi: 10.1016/s0020-7519(98)00200-8. [DOI] [PubMed] [Google Scholar]
  3. Bazzocchi C., Jamnongluk W., O'Neill S. L., Anderson T. J., Genchi C., Bandi C. wsp gene sequences from the Wolbachia of filarial nematodes. Curr Microbiol. 2000 Aug;41(2):96–100. doi: 10.1007/s002840010100. [DOI] [PubMed] [Google Scholar]
  4. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Garraud O., Nkenfou C., Bradley J. E., Perler F. B., Nutman T. B. Identification of recombinant filarial proteins capable of inducing polyclonal and antigen-specific IgE and IgG4 antibodies. J Immunol. 1995 Aug 1;155(3):1316–1325. [PubMed] [Google Scholar]
  6. Genchi C., Sacchi L., Bandi C., Venco L. Preliminary results on the effect of tetracycline on the embryogenesis and symbiotic bacteria (Wolbachia) of Dirofilaria immitis. An update and discussion. Parassitologia. 1998 Sep;40(3):247–249. [PubMed] [Google Scholar]
  7. Hoerauf A., Nissen-Pähle K., Schmetz C., Henkle-Dührsen K., Blaxter M. L., Büttner D. W., Gallin M. Y., Al-Qaoud K. M., Lucius R., Fleischer B. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest. 1999 Jan;103(1):11–18. doi: 10.1172/JCI4768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hong X. Q., Santiago Mejia J., Kumar S., Perler F. B., Carlow C. K. Cloning and expression of DiT33 from Dirofilaria immitis: a specific and early marker of heartworm infection. Parasitology. 1996 Mar;112(Pt 3):331–338. doi: 10.1017/s0031182000065859. [DOI] [PubMed] [Google Scholar]
  9. Kozek W. J., Marroquin H. F. Intracytoplasmic bacteria in Onchocerca volvulus. Am J Trop Med Hyg. 1977 Jul;26(4):663–678. doi: 10.4269/ajtmh.1977.26.663. [DOI] [PubMed] [Google Scholar]
  10. Kozek W. J. Transovarially-transmitted intracellular microorganisms in adult and larval stages of Brugia malayi. J Parasitol. 1977 Dec;63(6):992–1000. [PubMed] [Google Scholar]
  11. Langworthy N. G., Renz A., Mackenstedt U., Henkle-Dührsen K., de Bronsvoort M. B., Tanya V. N., Donnelly M. J., Trees A. J. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc Biol Sci. 2000 Jun 7;267(1448):1063–1069. doi: 10.1098/rspb.2000.1110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McLaren D. J., Worms M. J., Laurence B. R., Simpson M. G. Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg. 1975;69(5-6):509–514. doi: 10.1016/0035-9203(75)90110-8. [DOI] [PubMed] [Google Scholar]
  13. Nygren P. A., Ståhl S., Uhlén M. Engineering proteins to facilitate bioprocessing. Trends Biotechnol. 1994 May;12(5):184–188. doi: 10.1016/0167-7799(94)90080-9. [DOI] [PubMed] [Google Scholar]
  14. Ohashi N., Unver A., Zhi N., Rikihisa Y. Cloning and characterization of multigenes encoding the immunodominant 30-kilodalton major outer membrane proteins of Ehrlichia canis and application of the recombinant protein for serodiagnosis. J Clin Microbiol. 1998 Sep;36(9):2671–2680. doi: 10.1128/jcm.36.9.2671-2680.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Osteryoung K. W., Vierling E. Conserved cell and organelle division. Nature. 1995 Aug 10;376(6540):473–474. doi: 10.1038/376473b0. [DOI] [PubMed] [Google Scholar]
  16. Ottesen E. A. Immune responsiveness and the pathogenesis of human onchocerciasis. J Infect Dis. 1995 Mar;171(3):659–671. doi: 10.1093/infdis/171.3.659. [DOI] [PubMed] [Google Scholar]
  17. Ottesen E. A. The Wellcome Trust Lecture. Infection and disease in lymphatic filariasis: an immunological perspective. Parasitology. 1992;104 (Suppl):S71–S79. doi: 10.1017/s0031182000075259. [DOI] [PubMed] [Google Scholar]
  18. Padmalayam I., Anderson B., Kron M., Kelly T., Baumstark B. The 75-kilodalton antigen of Bartonella bacilliformis is a structural homolog of the cell division protein FtsZ. J Bacteriol. 1997 Jul;179(14):4545–4552. doi: 10.1128/jb.179.14.4545-4552.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Prieto C., Venco L., Simon F., Genchi C. Feline heartworm (Dirofilaria immitis) infection: detection of specific IgG for the diagnosis of occult infections. Vet Parasitol. 1997 Jul 1;70(4):209–217. doi: 10.1016/s0304-4017(97)00008-3. [DOI] [PubMed] [Google Scholar]
  20. Prieto G., Simón F., Genchi C., McCall J. W., Venco L. Utility of adult antigens of Dirofilaria immitis for the early detection of dirofilariosis and for the evaluation of chemoprophylactic treatment in experimentally infected cats. Vet Parasitol. 1999 Sep 15;86(1):5–13. doi: 10.1016/s0304-4017(99)00116-8. [DOI] [PubMed] [Google Scholar]
  21. Rao U. R., Nasarre C., Coleman S. U., Horohov D. W., Klei T. R. Granulomatous inflammatory response to recombinant filarial proteins of Brugia species. Am J Trop Med Hyg. 1999 Feb;60(2):251–254. doi: 10.4269/ajtmh.1999.60.251. [DOI] [PubMed] [Google Scholar]
  22. Santiago Mejia J., Nkenfou C., Southworth M. W., Perler F. B., Carlow C. K. Expression of an Onchocerca volvulus Ov33 homolog in Dirofilaria immitis: potential in immunodiagnosis of heartworm infection. Parasite Immunol. 1994 Jun;16(6):297–303. doi: 10.1111/j.1365-3024.1994.tb00352.x. [DOI] [PubMed] [Google Scholar]
  23. Sironi M., Bandi C., Sacchi L., Di Sacco B., Damiani G., Genchi C. Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol Biochem Parasitol. 1995 Nov;74(2):223–227. doi: 10.1016/0166-6851(95)02494-8. [DOI] [PubMed] [Google Scholar]
  24. Taylor M. J., Cross H. F., Bilo K. Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J Exp Med. 2000 Apr 17;191(8):1429–1436. doi: 10.1084/jem.191.8.1429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Taylor M. J., Hoerauf A. Wolbachia bacteria of filarial nematodes. Parasitol Today. 1999 Nov;15(11):437–442. doi: 10.1016/s0169-4758(99)01533-1. [DOI] [PubMed] [Google Scholar]
  26. Webb J. R., Vedvick T. S., Alderson M. R., Guderian J. A., Jen S. S., Ovendale P. J., Johnson S. M., Reed S. G., Skeiky Y. A. Molecular cloning, expression, and immunogenicity of MTB12, a novel low-molecular-weight antigen secreted by Mycobacterium tuberculosis. Infect Immun. 1998 Sep;66(9):4208–4214. doi: 10.1128/iai.66.9.4208-4214.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES