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Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach

Published online by Cambridge University Press:  13 November 2006

A. BOUCHUT
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555, CNRS Université de Perpignan Perpignan, France
C. COUSTAU
Affiliation:
U547, INSERM Institut Pasteur de Lille, Lille, France
B. GOURBAL
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555, CNRS Université de Perpignan Perpignan, France
G. MITTA
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555, CNRS Université de Perpignan Perpignan, France

Abstract

In order to elucidate mechanisms underlying snail/echinostome compatibility, numerous molecular studies comparing transcripts and proteins of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni were undertaken. These studies focused on plasma and haemocytes of the two strains and revealed that some transcripts and/or proteins were differentially expressed between strains. The aim of the present study was to develop a complementary transcriptomic approach by constructing subtractive libraries. This work revealed some candidate transcripts already identified in previous studies (calcium-binding proteins and glycolytic enzymes) as well as novel candidate transcripts that were differentially represented between strains of B. glabrata. Among these newly identified genes, we revealed several genes potentially involved in immune processes encoding proteases, protease inhibitors, a lectin, an aplysianin-like molecule, and cell adhesion molecules.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abraham, E. G., Pinto, S. B., Ghosh, A., Vanlandingham, D. L., Budd, A., Higgs, S., Kafatos, F. C., Jacobs-Lorena, M. and Michel, K. ( 2005). An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proceedings of the National Academy of Sciences, USA 102, 1632716332. doi: 10.1073/pnas.0508335102.CrossRefGoogle Scholar
Apostolopoulos, J., Sparrow, R. L., McLeod, J. L., Collier, F. M., Darcy, P. K., Slater, H. R., Ngu, C., Gregorio-King, C. C. and Kirkland, M. A. ( 2001). Identification and characterization of a novel family of mammalian ependymin-related proteins (MERPs) in hematopoietic, nonhematopoietic, and malignant tissues. DNA and Cell Biology 20, 625635.CrossRefGoogle Scholar
Armstrong, P. B. ( 2006). Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 211, 263281. doi: 10.1016/j.imbio.2006.01.002.CrossRefGoogle Scholar
Ataev, G. L. and Coustau, C. ( 1999). Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility/resistance. Developmental and Comparative Immunology 23, 187198. doi: 10.1016/S0145-305X(99)00023-3.CrossRefGoogle Scholar
Bouchut, A., Roger, E., Coustau, C., Gourbal, B. and Mitta, G. ( 2006 a). Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. International Journal for Parasitology 36, 175184. doi: 10.1016/j.ijpara.2005.09.009.CrossRefGoogle Scholar
Bouchut, A., Sautiere, P. E., Coustau, C. and Mitta, G. ( 2006 b). Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Tropica 98, 234246. doi: 10.1016/j.actatropica.2006.05.007.CrossRefGoogle Scholar
Butzke, D., Hurwitz, R., Thiede, B., Goedert, S. and Rudel, T. ( 2005). Cloning and biochemical characterization of APIT, a new l-amino acid oxidase from Aplysia punctata. Toxicon 46, 479489. doi: 10.1016/j.toxicon.2005.06.005.CrossRefGoogle Scholar
Duclermortier, P., Lardans, V., Serra, E., Trottein, F. and Dissous, C. ( 2005). Biomphalaria glabrata embryonic cells express a protein with a domain homologous to the lectin domain of mammalian selectins. Parasitology Research 85, 481486.Google Scholar
Guillou, F., Mitta, G., Dissous, C., Pierce, R. and Coustau, C. ( 2004). Use of individual polymorphism to validate potential functional markers: case of a candidate lectin (BgSel) differentially expressed in susceptible and resistant strains of Biomphalaria glabrata. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 138, 175181. doi: 10.1016/j.cbpc.2004.03.010.CrossRefGoogle Scholar
Harada, Y., Hosoiri, Y. and Kuroda, R. ( 2004). Isolation and evaluation of dextral-specific and dextral-enriched cDNA clones as candidates for the handedness-determining gene in a freshwater gastropod, Lymnaea stagnalis. Development Genes and Evolution 214, 159169. doi: 10.1007/s00427-004-0392-6.CrossRefGoogle Scholar
Hoffmann, W. and Schwarz, H. ( 1996). Ependymins: meningeal-derived extracellular matrix proteins at the blood-brain barrier. International Review of Cytology 165, 121158.CrossRefGoogle Scholar
Humbert, E. and Coustau, C. ( 2001). Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata-Echinostoma caproni system. Parasitology 122, 651660.CrossRefGoogle Scholar
Jung, Y., Nowak, T. S., Zhang, S. M., Hertel, L. A., Loker, E. S. and Adema, C. M. ( 2005). Manganese superoxide dismutase from Biomphalaria glabrata. Journal of Invertebrate Pathology 90, 5963.CrossRefGoogle Scholar
Kanost, M. R. ( 1999). Serine proteinase inhibitors in arthropod immunity. Developmental and Comparative Immunology 23, 291301. doi: 10.1016/S0145-305(99)00012-9.CrossRefGoogle Scholar
Langand, J. and Morand, S. ( 1998). Heritable non-susceptibility in an allopatric host-parasite system: Biomphalaria glabrata (Mollusca)-Echinostoma caproni (platyhelminth Digenea). Journal of Parasitology 84, 739742.CrossRefGoogle Scholar
Langand, J., Jourdane, J., Coustau, C., Delay, B. and Morand, S. ( 1998). Cost of resistance, expressed as a delayed maturity, detected in the host-parasite system Biomphalaria glabrata/Echinostoma caproni. Heredity 80, 320325.CrossRefGoogle Scholar
Lewis, F. A., Richards, C. S., Knight, M., Cooper, L. A. and Clark, B. ( 1993). Schistosoma mansoni: analysis of an unusual infection phenotype in the intermediate host snail Biomphalaria glabrata. Experimental Parasitology 77, 349361. doi: 10.1006/expr.1993.1092.CrossRefGoogle Scholar
Lie, K. J. ( 1982). Swellengrebel lecture: survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata. A discussion of the interference theory. Tropical and Geographical Medicine 34, 111122.Google Scholar
Lockyer, A. E., Noble, L. R., Rollinson, D. and Jones, C. S. ( 2004). Schistosoma mansoni: resistant specific infection-induced gene expression in Biomphalaria glabrata identified by fluorescent-based differential display. Experimental Parasitology 107, 97104. doi: 10.1016/j.exppara.2004.04.004.CrossRefGoogle Scholar
Loukas, A., Mullin, N. P., Tetteh, K. K., Moens, L. and Maizels, R. M. ( 1999). A novel C-type lectin secreted by a tissue-dwelling parasitic nematode. Current Biology 9, 825828. doi: 10.1016/S0960-9822(99)80366-2.CrossRefGoogle Scholar
Luo, T., Zhang, X., Shao, Z. and Xu, X. ( 2003). PmAV, a novel gene involved in virus resistance of shrimp Penaeus monodon. FEBS Letters 551, 5357. doi: 10.1016/S0014-5793(03)00891-3.CrossRefGoogle Scholar
Miller, A. N., Raghavan, N., FitzGerald, P. C., Lewis, F. A. and Knight, M. ( 2001). Differential gene expression in haemocytes of the snail Biomphalaria glabrata: effects of Schistosoma mansoni infection. International Journal for Parasitology 31, 687696. doi: 10.1016/S0020-7519(01)00133-3.CrossRefGoogle Scholar
Nimmrich, I., Erdmann, S., Melchers, U., Chtarbova, S., Finke, U., Hentsch, S., Hoffmann, I., Oertel, M., Hoffmann, W. and Muller, O. ( 2001). The novel ependymin related gene UCC1 is highly expressed in colorectal tumor cells. Cancer Letters 165, 7179. doi: 10.1016/S0304-3835(01)00390-1.CrossRefGoogle Scholar
Nowak, T. S., Woodards, A. C., Jung, Y., Adema, C. M. and Loker, E. S. ( 2004). Identification of transcripts generated during the response of resistant Biomphalaria glabrata to Schistosoma mansoni infection using suppression subtractive hybridization. Journal of Parasitology 90, 10341040.CrossRefGoogle Scholar
Raghavan, N., Miller, A. N., Gardner, M., FitzGerald, P. C., Kerlavage, A. R., Johnston, D. A., Lewis, F. A. and Knight, M. ( 2003). Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Molecular and Biochemical Parasitology 126, 181191. doi: 10.1016/S0166-6851(02)00272-4.CrossRefGoogle Scholar
Richards, C. S. ( 1975). Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70, 231241.CrossRefGoogle Scholar
Richards, C. S. and Shade, P. C. ( 1987). The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. Journal of Parasitology 73, 11461151.CrossRefGoogle Scholar
Shagin, D. A., Barsova, E. V., Bogdanova, E., Britanova, O. V., Gurskaya, N., Lukyanov, K. A., Matz, M. V., Punkova, N. I., Usman, N. Y., Kopantzev, E. P., Salo, E. and Lukyanov, S. A. ( 2002). Identification and characterization of a new family of C-type lectin-like genes from planaria Girardia tigrina. Glycobiology 12, 463472.CrossRefGoogle Scholar
Takamatsu, N., Shiba, T., Muramoto, K. and Kamiya, H. ( 1995). Molecular cloning of the defense factor in the albumen gland of the sea hare Aplysia kurodai. FEBS Letters 377, 373376. doi: 10.1016/0014-5793(95)01375-X.CrossRefGoogle Scholar
Vergote, D., Bouchut, A., Sautiere, P. E., Roger, E., Galinier, R., Rognon, A., Coustau, C., Salzet, M. and Mitta, G. ( 2005). Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. International Journal for Parasitology 35, 215224. doi: 10.1016/j.ijpara.2004.11.006.CrossRefGoogle Scholar
Yuasa, H. J., Furuta, E., Nakamura, A. and Takagi, T. ( 1998). Cloning and sequencing of three C-type lectins from body surface mucus of the land slug, Incilaria fruhstorferi. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 119, 479484. doi: 10.1016/S0305-0491(98)00008-X.CrossRefGoogle Scholar