Skip to main content
SpringerLink
Log in

A novel C-type lectin identified by EST analysis in tissue migratory larvae of Ascaris suum

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

C-type lectins (CTLs) are a group of proteins which bind to carbohydrate epitopes in the presence of Ca2+, which have been described in a wide range of species. In this study, a cDNA sequence coding a putative CTL has been identified from the cDNA library constructed from the pig round worm Ascaris suum lung L3 (LL3) larvae, which was designated as A. suum C-type lectin-1 (As-CTL-1). The 510 nucleotide open reading frame of As-CTL-1 cDNA encoded the predicted 169 amino acid protein including a putative signal peptide of 23 residues and C-type lectin/C-type lectin-like domain (CLECT) at residue 26 to 167. As-CTL-1 was most similar to Toxocara canis C-type lectin-1 and 4 (Tc-CTL-1 and 4), and highly homologous to namatode CTLs and mammalian CTLs as well, such as human C-type lectin domain family 4 member G (CLECG4). In addition, As-CTL-1 was strongly expressed in tissue migrating LL3 and the L4 larvae, which were developmental larvae stages within the mammalian host. These results suggest that A. suum larvae might utilize As-CTL-1 to avoid pathogen recognition mechanisms in mammalian hosts due to it is similarity to host immune cell receptors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Anderson TJC (1995) Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110(2):215–219

    Article  PubMed  Google Scholar 

  • Arizono N, Yoshimura Y, Tohzaka N, Yamada M, Tegoshi T, Onishi K, Uchikawa R (2010) Ascariasis in Japan: is pig-derived Ascaris infecting humans? Jpn J Infect Dis 63(6):447–448

    PubMed  Google Scholar 

  • Brown AC, Harrison LM, Kapulkin W, Jones BF, Sinha A, Savage A, Villalon N, Cappello M (2006) Molecular cloning and characterization of a C-type lectin from Ancylostoma ceylanicum: evidence for a role in hookworm reproductive physiology. Mol Biochem Parasitol 151(2):141–147

    Article  PubMed  Google Scholar 

  • Cash HL, Whitham CV, Behrendt CL, Hooper LV (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313(5790):1126–1130

    Article  PubMed  CAS  Google Scholar 

  • Crompton DW (2001) Ascaris and ascariasis. Adv Parasitol 48:285–375

    Article  PubMed  CAS  Google Scholar 

  • Daub J, Loukas A, Pritchard DI, Blaxter M (2000) A survey of genes expressed in adults of the human hookworm, Necator americanus. Parasitology 120(2):171–184

    Article  PubMed  CAS  Google Scholar 

  • Dold C, Holland CV (2011) Ascaris and ascariasis. Microbes Infect 13(7):624–631

    Article  PubMed  CAS  Google Scholar 

  • Drickamer K (1988) Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem 263(20):9557–9560

    PubMed  CAS  Google Scholar 

  • Drickamer K (1996) Ca(2+)-dependent sugar recognition by animal lectins. Biochem Soc Trans 24(1):146–150

    PubMed  CAS  Google Scholar 

  • Drickamer K, Fadden AJ (2002) Genomic analysis of C-type lectins. Biochem Soc Symp 69:59–72

    PubMed  CAS  Google Scholar 

  • García-Vallejo JJ, van Kooyk Y (2009) Endogenous ligands for C-type lectin receptors: the true regulators of immune homeostasis. Immunol Rev 230(1):22–37

    Article  PubMed  Google Scholar 

  • Harcus Y, Nicoll G, Murray J, Filbey K, Gomez-Escobar N, Maizels RM (2009) C-type lectins from the nematode parasites Heligmosomoides polygyrus and Nippostrongylus brasiliensis. Parasitol Int 58(4):461–470

    Article  PubMed  CAS  Google Scholar 

  • Iobst ST, Drickamer K (1994) Binding of sugar ligands to Ca(2+)-dependent animal lectins: II. Generation of high-affinity galactose binding by site-directed mutagenesis. J Biol Chem 269(22):15512–15519

    PubMed  CAS  Google Scholar 

  • Islam MK, Miyoshi T, Yamada M, Alim MA, Huang X, Motobu M, Tsuji N (2006) Effect of piperazine (diethylenediamine) on the moulting, proteome express and pyrophosphate activity of Ascaris suum lung-stage larvae. Acta Trop 99:208–217

    Article  PubMed  CAS  Google Scholar 

  • Loukas A, Mullin NP, Tetteh KK, Moens L, Maizels RM (1999) A novel C-type lectin secreted by a tissue-dwelling parasitic nematode. Curr Biol 9(15):825–828

    Article  PubMed  CAS  Google Scholar 

  • Loukas A, Maizels RM (2000) Helminth C-type lectins and host–parasite interactions. Parasitol Today 16(8):333–339

    Article  PubMed  CAS  Google Scholar 

  • Loukas A, Doedens A, Hintz M, Maizels RM (2000) Identification of a new C-type lectin, TES-70, secreted by infective larvae of Toxocara canis, which binds to host ligands. Parasitology 121(5):545–554

    Article  PubMed  CAS  Google Scholar 

  • Loukas A, Prociv P (2001) Immune responses in hookworm infections. Clin Microbiol Rev 14:689–703

    Article  PubMed  CAS  Google Scholar 

  • Nejsum P, Parker ED Jr, Frydenberg J, Roepstorff A, Boes J, Haque R, Astrup I, Prag J, Skov Sørensen UB (2005) Ascariasis is a zoonosis in Denmark. J Clin Microbiol 43(3):1142–1148

    Article  PubMed  Google Scholar 

  • O'Rourke D, Baban D, Demidova M, Mott R, Hodgkin J (2006) Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 16(8):1005–1016

    Article  PubMed  Google Scholar 

  • Osorio F, Reis e Sousa C (2010) Myeloid C-type lectin receptors in pathogen recognition and host defense. Immunity 34(5):651–664

    Article  Google Scholar 

  • Schulenburg H, Hoeppner MP, Weiner J 3rd, Bornberg-Bauer E (2008) Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology 213(3–4):237–250

    Article  PubMed  CAS  Google Scholar 

  • Slotved HC, Eriksen L, Murrell KD, Nansen P (1998) Early Ascaris suum migration in mice as a model for pigs. J Parasitol 84(1):16–18

    Article  PubMed  CAS  Google Scholar 

  • Sun JC, Lanier LL (2011) NK cell development, homeostasis and function: parallels with CD8+ T cells. Nat Rev Immunol 11:645–657

    Article  PubMed  CAS  Google Scholar 

  • Takamiya S, Kita K, Wang H, Weinstein PP, Hiraishi A, Oya H, Aoki T (1993) Developmental changes in the respiratory chain of Ascaris mitochondria. Biochim Biophys Acta 1141:65–74

    Article  PubMed  CAS  Google Scholar 

  • Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol Plant Microbe Interact 15(8):747–752

    Article  PubMed  CAS  Google Scholar 

  • Weis WI, Drickamer K, Hendrickson WA (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360(6400):127–134

    Article  PubMed  CAS  Google Scholar 

  • Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163:19–34

    Article  PubMed  CAS  Google Scholar 

  • Zdobnov EM, Apweiler R (2001) InterProScan – an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848

    Article  PubMed  CAS  Google Scholar 

  • Zelensky AN, Gready JE (2003) Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD). Proteins 52:466–477

    Article  PubMed  CAS  Google Scholar 

  • Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272(24):6179–6217

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Hisako Kyan and Naomi Takeda for providing A. suum adult worm. This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant-in-Aid for Scientific Research C 21590466, Grant-in-Aid for Scientific Research on Priority Areas ‘Matrix of Infection Phenomena’ 21022041), the Ministry of Health, Labour and Welfare (H23-Shinko-Ippan-014, H23-Kokui-Shitei- 003, H22-Seisakusouyaku-Ippan-003) and grants from the University of Miyazaki (Support Program for Female Researchers M41D1123 and Integrated Research Project for Human and Veterinary Medicine).

Author information

Authors and Affiliations

  1. Department of Infectious Diseases, Division of Parasitology, Faculty of Medicine, University of Miyazaki, 5200 Kihara, Kiyotake, Miyazaki, 889-1692, Japan

    Ayako Yoshida, Eiji Nagayasu & Haruhiko Maruyama

  2. Laboratory of Veterinary Parasitic Diseases, Department of Veterinary Sciences, Faculty of Agriculture, University of Miyazaki, Miyazaki, Japan

    Yoichiro Horii

Authors
  1. Ayako Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eiji Nagayasu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoichiro Horii
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haruhiko Maruyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ayako Yoshida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshida, A., Nagayasu, E., Horii, Y. et al. A novel C-type lectin identified by EST analysis in tissue migratory larvae of Ascaris suum . Parasitol Res 110, 1583–1586 (2012). https://doi.org/10.1007/s00436-011-2677-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-011-2677-9

Keywords

Search

Navigation