Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-20T00:42:50.101Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification of stage-specifically expressed genes of Trichinella spiralis by suppression subtractive hybridization

Published online by Cambridge University Press:  03 May 2007

M. Y. LIU ,
X. L. WANG ,
B. Q. FU ,
C. Y. LI ,
X. P. WU ,
D. Le RHUN ,
Q. J. CHEN  and
P. BOIREAU
M. Y. LIU
Affiliation:
Key Laboratory of Zoonoses, Ministry of Education, Institute of Zoonoses, Jilin University, 5333 Xian Road, 130062 Changchun, P. R. China
X. L. WANG
Affiliation:
Key Laboratory of Zoonoses, Ministry of Education, Institute of Zoonoses, Jilin University, 5333 Xian Road, 130062 Changchun, P. R. China
B. Q. FU
Affiliation:
AFSSA, INRA, ENYA, UPUM, UMR 956Biologie Moléculaire et Immunologie Parasitaires et fongiques, 23 av du Général de Gaulle, 94703 Maisons-Alfort, France Key Laboratory of Veterinary Parasitology of Gansu Province, State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, 730046, Lanzhou, P. R. China
C. Y. LI
Affiliation:
AFSSA, INRA, ENYA, UPUM, UMR 956Biologie Moléculaire et Immunologie Parasitaires et fongiques, 23 av du Général de Gaulle, 94703 Maisons-Alfort, France
X. P. WU
Affiliation:
Key Laboratory of Zoonoses, Ministry of Education, Institute of Zoonoses, Jilin University, 5333 Xian Road, 130062 Changchun, P. R. China
D. Le RHUN
Affiliation:
AFSSA, INRA, ENYA, UPUM, UMR 956Biologie Moléculaire et Immunologie Parasitaires et fongiques, 23 av du Général de Gaulle, 94703 Maisons-Alfort, France
Q. J. CHEN
Affiliation:
Key Laboratory of Zoonoses, Ministry of Education, Institute of Zoonoses, Jilin University, 5333 Xian Road, 130062 Changchun, P. R. China Swedish Institute for Infectious Disease Control, Nobels väg 18, 171 82 StockholmSweden
P. BOIREAU*
Affiliation:
AFSSA, INRA, ENYA, UPUM, UMR 956Biologie Moléculaire et Immunologie Parasitaires et fongiques, 23 av du Général de Gaulle, 94703 Maisons-Alfort, France
*
*Corresponding author: UMR 956 INRA-AFSSA-ENVA-UPVM, Biologie Moléculaire et Immunologie Parasitaires et fongiques, 23 av du Général de Gaulle, 94703 Maisons-Alfort, France. Tel: +33 149771328. Fax: +33 149771316. E-mail: pboireau@vet-alfort.fr.
Get access Rights & Permissions [Opens in a new window]

Summary

Newborn larvae (NBL) and adult (Ad) stage-specifically expressed genes or members of gene families of Trichinella spiralis were identified by suppression subtractive hybridization (SSH)†. Six cDNA clones were identified as NBL stage-specific, including 1 member of the T. spiralis gene family encoding glutamic acid-rich proteins, 2 clones encoding novel serine proteases, 2 closely related clones encoding proteins that are members of a deoxyribonuclease II (DNase II)-like family and 1 clone with no similarity to known genes. Four stage-specific clones encoding homologues of retinoid X receptor, caveolin, C2H2 type zinc finger protein and a putative protein with no homology to known sequences were obtained from 3-day-old adult worms. One gene specifically up-regulated in the 5-day-old adult worms encoding a putative cuticle collagen was also identified.

Keywords

Trichinella spiralisstage-specifically expressed genesnewborn larvaeadultssuppression subtractive hybridization
Type
Research Article
Information
Parasitology , Volume 134 , Issue 10 , September 2007 , pp. 1443 - 1455
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Arasu, P., Ellis, L. A., Iglesias, R., Ubeira, F. M. and Appleton, J. A. (1994). Molecular analysis of antigens targeted by protective antibodies in rapid expulsion of Trichinella spiralis. Molecular and Biochemical Parasitology 65, 201–211.CrossRefGoogle ScholarPubMed
Armas-Serra, C., Gimenez-Pardo, C., Jimenez-Gonzalez, A., Bernadina, W. E. and Rodriguez-Caabeiro, F. (1995). Purification and preliminary characterization of a protease from the excretion-secretion products of Trichinella spiralis muscle-stage larvae. Veterinary Parasitology 59, 157–168.CrossRefGoogle ScholarPubMed
Bellatin, J. A., Murray, A. S., Zhao, M. and McMaster, W. R. (2002). Leishmania mexicana: identification of genes that are preferentially expressed in amastigotes. Experimental Parasitology 100, 44–53.CrossRefGoogle ScholarPubMed
Blair, L. (1983). Laboratory techniques. In Trichinella and Trichinosis (ed. Campbell, W. C.), pp. 560–570. Plenum Press, New York.Google Scholar
Boireau, P., Vallée, I., Le Guerhier, F., Blaga, R., Fu, B. Q., Hernandez-Bello, R., Ortega Pierres, G. and Liu, M. Y. (2004). Trichinella antigens and immunodominant epitopes. In Proceedings of IX European Multicolloquium of Parasitology – EMOP, pp. 181–188. Valencia, Spain.Google Scholar
Boireau, P., Vayssier, M., Fabien, J. F., Perret, C., Calamel, M. and Soule, C. (1997). Characterization of eleven antigenic groups in Trichinella genus and identification of stage and species markers. Parasitology 115, 641–651.CrossRefGoogle Scholar
Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Cottee, P. A., Nisbet, A. J., Abs El-Osta, Y. G., Webster, T. L. and Gasser, R. B. (2006). Construction of gender-enriched cDNA archives for adult Oesophagostomum dentatum by suppressive-subtractive hybridization and a microarray analysis of expressed sequence tags. Parasitology 132, 691–708.CrossRefGoogle Scholar
Criado-Fornelio, A., Armas-Serra, C., Gimenez-Pardo, C., Casado-Escribano, N., Jimenez-Gonzalez, A. and Rodriguez-Caabeiro, F. (1992). Proteolytic enzymes from Trichinella spiralis larvae. Veterinary Parasitology 45, 133–140.CrossRefGoogle ScholarPubMed
Dabrowska, M., Jagielska, E., Ciesla, J., Plucienniczak, A., Kwiatowski, J., Wranicz, M., Boireau, P. and Rode, W. (2004). Trichinella spiralis thymidylate synthase: cDNA cloning and sequencing, and developmental pattern of mRNA expression. Parasitology 128, 209–221.CrossRefGoogle ScholarPubMed
Despommier, D. D. (2000). Trichinella spiralis. In Parasitic Diseases, 4th Edn (ed. Despommier, D. D., Gwadz, R. W., Hotez, P. J. and Knirsch, C. A.), pp. 125–132. Apple Trees Productions, New York, USA.Google Scholar
Dessens, J. T., Margos, G., Rodriguez, M. C. and Sinden, R. E. (2000). Identification of differentially regulated genes of Plasmodium by suppression subtractive hybridization. Parasitology Today 16, 354–356.CrossRefGoogle ScholarPubMed
Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D. and Siebert, P. D. (1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences, USA 93, 6025–6030.CrossRefGoogle ScholarPubMed
Fu, B. Q., Liu, M. Y., Kapel, C. M., Meng, X. P., Lu, Q., Wu, X. P., Chen, Q. J. and Boireau, P. (2005 a). Cloning and analysis of a novel cDNA from Trichinella spiralis encoding a protein with an FYVE zinc finger domain. Veterinary Parasitology 132, 27–30.CrossRefGoogle ScholarPubMed
Fu, B. Q., Liu, M. Y., Kapel, C. M., Meng, X. P., Lu, Q., Wu, X. P., Chen, Q. J. and Boireau, P. (2005 b). Molecular cloning of a cDNA encoding a putative cuticle collagen of Trichinella spiralis. Veterinary Parasitology 132, 31–35.CrossRefGoogle ScholarPubMed
Gao, B., Allen, R., Maier, T., Davis, E. L., Baum, T. J. and Hussey, R. S. (2001). Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Molecular Plant-Microbe Interactions 14, 1247–1254.CrossRefGoogle ScholarPubMed
Gare, D., Boyd, J. and Connolly, B. (2004). Developmental regulation and secretion of nematode-specific cysteine-glycine domain proteins in Trichinella spiralis. Molecular and Biochemical Parasitology 134, 257–266.CrossRefGoogle ScholarPubMed
Krishna, S. S., Majumdar, I. and Grishin, N. V. (2003). Structural classification of zinc fingers: survey and summary. Nucleic Acids Research 31, 532–550.CrossRefGoogle ScholarPubMed
Liu, M. Y., Zhu, X. P., Xu, K. C., Lu, Q. and Boireau, P. (2001). Biological and genetic characteristics of two Trichinella isolates in China; comparison with European species. Parasite 8, S34–S38.CrossRefGoogle Scholar
Luo, H. L., Nie, P., Chang, M. X., Song, Y. and Yao, W. J. (2004). Characterization of development-related genes for the cestode Bothriocephalus acheilognathi. Parasitology Research 94, 265–274.CrossRefGoogle ScholarPubMed
Mak, C. H., Chung, Y. Y. and Ko, R. C. (2000). Single-stranded endonuclease activity in the excretory-secretory products of Trichinella spiralis and Trichinella pseudospiralis. Parasitology 120, 527–533.CrossRefGoogle ScholarPubMed
Mak, C. H. and Ko, R. C. (1999). Characterization of endonuclease activity from excretory/secretory products of a parasitic nematode, Trichinella spiralis. European Journal of Biochemistry 260, 477–481.CrossRefGoogle ScholarPubMed
Mak, C. H., Su, K. W. and Ko, R. C. (2001). Identification of some heat-induced genes of Trichinella spiralis. Parasitology 123, 293–300.CrossRefGoogle ScholarPubMed
Mitreva, M., Appleton, J., McCarter, J. P. and Jasmer, D. P. (2005). Expressed sequence tags from life cycle stages of Trichinella spiralis: application to biology and parasite control. Veterinary Parasitology 132, 13–17.CrossRefGoogle ScholarPubMed
Mitreva, M., Jasmer, D. P., Appleton, J., Martin, J., Dante, M., Wylie, T., Clifton, S. W., Waterston, R. H. and McCarter, J. P. (2004). Gene discovery in the adenophorean nematode Trichinella spiralis: an analysis of transcription from three life cycle stages. Molecular and Biochemical Parasitology 137, 277–291.CrossRefGoogle ScholarPubMed
Moczon, T. and Wranicz, M. (1999). Trichinella spiralis: proteinases in the larvae. Parasitology Research 85, 47–58.CrossRefGoogle ScholarPubMed
Nagano, I., Wu, Z., Nakada, T., Boonmars, T. and Takahashi, Y. (2003). Molecular cloning and characterization of a serine proteinase gene of Trichinella spiralis. Journal of Parasitology 89, 92–98.CrossRefGoogle ScholarPubMed
Okamoto, T., Schlegel, A., Scherer, P. E. and Lisanti, M. P. (1998). Caveolins, a family of scaffolding proteins for organizing “preassembled signaling complexes” at the plasma membrane. The Journal of Biological Chemistry 273, 5419–5422.CrossRefGoogle ScholarPubMed
Ortega-Pierres, M. G., Yepez-Mulia, L., Homan, W., Gamble, H. R., Lim, P. L., Takahashi, Y., Wassom, D. I. and Appleton, J. A. (1996). Workshop on a detailed characterization of Trichinella spiralis antigens: a platform for future studies on antigens and antibodies to this parasite. Parasite Immunology 18, 273–284.CrossRefGoogle ScholarPubMed
Parkhouse, R. M. and Ortega-Pierres, G. (1984). Stage-specific antigens of Trichinella spiralis. Parasitology 88, 623–630.CrossRefGoogle ScholarPubMed
Rehm, B. H. (2001). Bioinformatic tools for DNA/protein sequence analysis, functional assignment of genes and protein classification. Applied Microbiological Biotechnology 57, 579–592.CrossRefGoogle ScholarPubMed
Romaris, F., North, S. J., Gagliardo, L. F., Butcher, B. A., Ghosh, K., Beiting, D. P., Panico, M., Arasu, P., Dell, A., Morris, H. R. and Appleton, J. A. (2002). A putative serine protease among the excretory-secretory glycoproteins of L1 Trichinella spiralis. Molecular and Biochemical Parasitology 122, 149–160.CrossRefGoogle ScholarPubMed
Spielmann, T. and Beck, H. P. (2000). Analysis of stage-specific transcription in Plasmodium falciparum reveals a set of genes exclusively transcribed in ring stage parasites. Molecular and Biochemical Parasitology 111, 453–458.CrossRefGoogle ScholarPubMed
Tang, Z., Okamoto, T., Boontrakulpoontawee, P., Katada, T., Otsuka, A. J. and Lisanti, M. P. (1997). Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. Journal of Biological Chemistry 272, 2437–2445.CrossRefGoogle ScholarPubMed
The C. elegans Sequencing Consortium (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018.CrossRefGoogle Scholar
Todorova, V. K. (2000). Proteolytic enzymes secreted by larval stage of the parasitic nematode Trichinella spiralis. Folia Parasitologica 47, 141–145.CrossRefGoogle ScholarPubMed
Todorova, V. K., Knox, D. P. and Kennedy, M. W. (1995). Proteinases in the excretory/secretory products (ES) of adult Trichinella spiralis. Parasitology 111, 201–208.CrossRefGoogle ScholarPubMed
Todorova, V. K. and Stoyanov, D. I. (2000). Partial characterization of serine proteinases secreted by adult Trichinella spiralis. Parasitology Research 86, 684–687.CrossRefGoogle ScholarPubMed
Trap, C., Fu, B. Q., Le Guerhier, F., Liu, M., Le Rhun, D., Romand, T., Perret, C., Blaga, R. and Boireau, P. (2006). Cloning and analysis of a cDNA encoding a putative serine protease comprising two trypsin-like domains of Trichinella spiralis. Parasitology Research 98, 288–294.CrossRefGoogle ScholarPubMed
Vassilatis, D. K., Despommier, D., Misek, D. E., Polvere, R. I., Gold, A. M. and Van der Ploeg, L. H. (1992). Analysis of a 43-kDa glycoprotein from the intracellular parasitic nematode Trichinella spiralis. Journal of Biological Chemistry 267, 18459–18465.CrossRefGoogle ScholarPubMed
Vayssier, M., Le Guerhier, F., Fabien, J. F., Philippe, H., Vallet, C., Ortega-Pierres, G., Soule, C., Perret, C., Liu, M., Vega-Lopez, M. and Boireau, P. (1999). Cloning and analysis of a Trichinella britovi gene encoding a cytoplasmic heat shock protein of 72 kDa. Parasitology 119, 81–93.CrossRefGoogle Scholar
Weston, D., Patel, B. and Van Voorhis, W. C. (1999). Virulence in Trypanosoma cruzi infection correlates with the expression of a distinct family of sialidase superfamily genes. Molecular and Biochemical Parasitology 98, 105–116.CrossRefGoogle ScholarPubMed
Zarlenga, D. S., Boyd, P., Lichtenfels, J. R., Hill, D. and Ray, G. H. (2002). Identification and characterisation of a cDNA sequence encoding a glutamic acid-rich protein specifically transcribed in Trichinella spiralis newborn larvae and recognised by infected swine serum. International Journal for Parasitology 32, 1361–1370.CrossRefGoogle ScholarPubMed
Zhu, X. P., Garcia-Reyna, P., Fu, B. Q., Yang, J., Li, C. V., Yang, Y. P., Liu, M. Y., Ortega-Pierres, G. and Boireau, P. (2005). A stage-specific open reading frame from three-day old adult worms of Trichinella spiralis encodes zinc-finger motifs. Parasite 12, 151–157.CrossRefGoogle ScholarPubMed