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Identification and sequence comparison of a cuticular collagen of Brugia pahangi

Published online by Cambridge University Press:  06 April 2009

M. Bisoffi  and
B. Betschart
M. Bisoffi
Affiliation:
Department of Medical Parasitology, Swiss Tropical Institute, 4051 Basel, Switzerland
B. Betschart*
Affiliation:
Institute of Zoology, University of Neuchâtel, 2007 Neuchâtel, Switzerland
*
*Corresponding author. University of Neuchâtel, Institute of Zoology, Rue Emile-Argand 11, 2007 Neuchâtel, Switzerland. Tel: + + 41 38 23 30 45. Fax: + + 41 38 23 30 01. E-mail: bruno.betschart@zool.unine.ch.
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Summary

The cuticle of filarial nematodes is a specialized extracellular matrix that covers the parasite and protects it from adverse conditions of the environment. As a surface structure it is in direct contact with the host defence mechanisms and therefore plays an important role in the molecular host-parasite relationship. Using polyclonal antisera raised against the insoluble components of the cuticle of the adult filarial parasite Brugia pahangi, we have isolated cDNA clones encoding collagen molecules of the cuticle. The protein domain structure of cDNA clone Bpcol-1 was compared with the known structures of cuticular collagens of the nematodes Brugia malayi, Caenorhabditis elegans, Ascaris suum and Haemonchus contortus, confirming interspecies similarities. Using affinity-purified anti-Bpcol-1 antibodies we identified Bpcol-1 antigenic determinants in different nematode extracts, and determined the localization of such epitopes within the cuticle of B. pahangi.

Keywords

Brugia pahangifilarial nematodecuticlecollagensequence comparisonimmunolocalization
Type
Research Article
Information
Parasitology , Volume 113 , Issue 2 , August 1996 , pp. 145 - 155
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Altmann, M., Handschin, C. & Trachsel, H. (1987). mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae. Molecular Cell Biology 7, 998–1003.Google ScholarPubMed
Betschart, B. & Wyss, K. (1990). Analysis of the cuticular collagens of Ascaris suum. Acta Tropica 47, 297–305.CrossRefGoogle ScholarPubMed
Bird, A. F. & Bird, J. (1991). The Structure of Nematodes. Academic Press, San Diego.Google Scholar
Boisvenue, R. J., Stiff, M. I., Tonkinson, L. V. & Cox, G. N. (1991). Protective studies in sheep immunized with cuticular collagen proteins and peptides of Haemonchus contortus. Parasite Immunology 13, 227–240.CrossRefGoogle ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Caulagi, V. R. & Rajan, T. V. (1995). The structural organization of an α2 (type IV) basement membrane collagene gene from the filarial nematode Brugia malayi. Molecular and Biochemical Parasitology 70, 227–229.CrossRefGoogle Scholar
Caulagi, V. R., Werner, C. & Rajan, T. V. (1991). Isolation and partial sequence of a collagen gene from the human filarial parasite Brugia malayi. Molecular and Biochemical Parasitology 45, 57–64.CrossRefGoogle ScholarPubMed
Corden, J., Wasylyk, B., Buchwalder, A., Sassone-Corsi, P., Kedinger, C. & Chambon, P. (1980). Promoter sequences of eukaryotic protein-coding genes. Science 209, 1406–1414.CrossRefGoogle ScholarPubMed
Cox, G. N., Kusch, M. & Edgar, R. S. (1981). Cuticle of Caenorhabditis elegans: Its isolation and partial characterization. Journal of Cell Biology 90, 7–17.CrossRefGoogle ScholarPubMed
Cox, G. N., Fields, C., Kramer, J. M., Rosenzweig, B. & Hirsh, D. (1989). Sequence comparison of developmentally regulated collagen genes of Caenorhabditis elegans. Gene 76, 331–344.CrossRefGoogle ScholarPubMed
cox, G. N. (1990). Molecular biology of the cuticle collagen gene families of Caenorhabditis elegans and Haemonchus contortus. Acta Tropica 47, 269–281.CrossRefGoogle ScholarPubMed
cox, G. N. (1992). Molecular and biochemical aspects of nematode collagens. Journal of Parasitology 78, 1–15.CrossRefGoogle Scholar
Devereux, J., Haeberli, P. & Smithies, O. (1984). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Research 12, 387–395.CrossRefGoogle ScholarPubMed
Feinberg, A. P. & Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132, 6–13.CrossRefGoogle ScholarPubMed
Fetterer, R. H. (1989). The cuticular proteins from freeliving and parasitic stages of Haemonchus contortus-I. Isolation and partial characterization. Comparative Biochemistry and Physiology 94B, 383–388.Google ScholarPubMed
Fujimoto, D. & Kanaya, S. (1973). Cuticlin: a noncollagen structural protein from Ascaris cuticle. Archives of Biochemistry and Biophysics 157, 1–6.CrossRefGoogle ScholarPubMed
Guo, X. & Kramer, J. M. (1989). The two Caenorhabditis elegans basement membrane (type IV) collagen genes are located on separate chromosomes. Journal of Biological Chemistry 264, 17574–17582.CrossRefGoogle ScholarPubMed
Ho, N. F. H., Geary, T. G., Raub, T. J., Barsuhn, C. L. & Thompson, D. P. (1990). Biophysical transport properties of the cuticle of Ascaris suum. Molecular and Biochemical Parasitology 41, 153–166.CrossRefGoogle ScholarPubMed
Josse, J. & Harrington, W. F. (1964). Role of pyrrolidine residues in the structure and stabilization of collagen. Journal of Molecular Biology 9, 269–287.CrossRefGoogle ScholarPubMed
Kiefer, E., Rudin, W., Betschart, B., Weiss, N. & Hecker, H. (1986). Demonstration of anti-cuticular antibodies by immunoelectron microscopy in sera of mice immunized with cuticular extracts and isolated cuticles of Dipetalonema viteae (Filarioidea). Acta Tropical, 43 99–112.Google ScholarPubMed
Kingston, I. B., Wainwright, S. M. & Cooper, D. (1989). Comparison of collagen gene sequences in Ascaris suum and Caenorhabditis elegans. Molecular and Biochemical Parasitology 37, 137–146.CrossRefGoogle ScholarPubMed
Leushner, J., Semple, N. L. & Pasternak, J. (1979). Isolation and characterization of the cuticle from the free-living nematode Panagrellus silusiae. Biochimica et Biophysica Acta 580, 166–174.CrossRefGoogle ScholarPubMed
Maniatis, T., Fritsch, E. F. & Sambrook, J. (1982). Molecular Cloning: A Laboratory Manual, 2nd edn.New York: Cold Spring Harbor Laboratory Press.Google Scholar
McCall, J. W., Malone, J. B., Ah, H. S. & Thompson, P. E. (1973). Mongolian jirds (Meriones unguiculatus). infected with Brugia pahangi by the intraperitoneal route: a rich source of developing larvae, adult filariae and microfilariae. Journal of Parasitology 59, 436.CrossRefGoogle ScholarPubMed
Miller, E. J. & Gay, S. (1987). The collagens: an overview and update. Methods in Enzymology 144, 3–41.CrossRefGoogle ScholarPubMed
Ogilvie, B. M., Philipp, M., Jungery, M., Maizels, R. M., Worms, M. J. & Parkhouse, R. M. E. (1980). The surface of nematodes and the immune response of the host. In The Host Invader Interplay (ed. Van den Bossche, H.), pp. 99–104. Elsevier, Amsterdam.Google Scholar
Pettitt, J. & Kingston, I. B. (1991). The complete primary structure of a nematode α2 (IV) collagen and partial structural organization of its gene. Journal of Biological Chemistry 266, 16149–16156.CrossRefGoogle Scholar
Petralanda, I. & Piessens, W. (1991). Onchocerca volvulus, O. gutturosa, Brugia malayi and Dirofilaria immitis: A comparative study of the immunochemical properties of the cuticular proteins from filarial parasites. Experimental Parasitology 72, 164–173.CrossRefGoogle ScholarPubMed
Politz, S. M. & Philipp, M. (1992). Caenorhabditis elegans as a model for parasitic nematodes: A focus on the cuticle. Parasitology Today 8, 6–12.CrossRefGoogle Scholar
Pritchard, D. I., Mckean, P. G. & Rogan, M. T. (1988). Cuticular collagens – a concealed target for immune attack in hookworms. Parasitology Today 4, 239–241.CrossRefGoogle ScholarPubMed
Proudfoot, N. J. & Brownlee, G. G. (1976). 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature, London 263, 211–214.CrossRefGoogle ScholarPubMed
Reddigari, S. R., Jansma, P. L., Prmachandran, D. & Hussey, R. H. (1986). Cuticular collagenous proteins of second-stage juveniles and adult females of Meloidogyne incognita: Isolation and partial characterization. Journal of Nematology 18, 294–302.Google ScholarPubMed
Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463–5467.CrossRefGoogle ScholarPubMed
Scott, A. L., Yenbutr, P., Eisinger, S. W. & Raghavan, N. (1995). Molecular cloning of the cuticular collagen gene Bmcol-2 from Brugia malayi. Molecular and Biochemical Parasitology 70, 221–225.CrossRefGoogle ScholarPubMed
Selkirk, M. E., Nielsen, L., Kelly, C., Partono, F., Sayers, G. & Maizels, R. M. (1989 a). Identification, synthesis and immunogenicity of cuticular collagens from the filarial nematodes Brugia malayi and Brugia pahangi. Molecular and Biochemical Parasitology 59, 229–246.CrossRefGoogle Scholar
Selkirk, M. E., Denham, D. A., Partono, F. & Maizels, R. M. (1989 b). Heat shock cognate 70 is a prominent immunogen in brugian filariasis. Journal of Immunology 143, 299–308.CrossRefGoogle ScholarPubMed
Shamansky, L. M., Pratt, D., Boisvenue, J. & Cox, G. N. (1989). Cuticle collagen genes of Haemonchus contortus and Caenorhabditis elegans are highly conserved. Molecular and Biochemical Parasitology 37, 73–86.CrossRefGoogle ScholarPubMed
Sulston, J. E. & Brenner, S. (1974). The DNA of Caenorhabditis elegans. Genetics 77, 95–104.CrossRefGoogle ScholarPubMed
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4354.CrossRefGoogle ScholarPubMed
Wharton, D. A. (1986). A Functional Biology of Nematodes. Croom Helm, London & Sydney.CrossRefGoogle Scholar
Young, R. A. & Davis, R. W. (1983). Efficient isolation of genes using antibody probes. Proceedings of the National Academy of Sciences, USA 80, 1194–1198.CrossRefGoogle ScholarPubMed