Skip to main content
SpringerLink
Log in

Effects of infection by larvae of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) on the lipid metabolism of the experimental intermediate host Biomphalaria glabrata (Mollusca: Gastropoda)

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

Abstract

Experimental infection of Biomphalaria glabrata by Angiostrongylus cantonensis induces significant changes in the concentrations of triacylglycerol and cholesterol in the hemolymph and of neutral lipids in the digestive gonad–gland (DGG) complex of the host snail. In this study, snails were dissected after 1, 2, and 3 weeks of infection to collect the hemolymph and DGG and to measure the levels of cholesterol and triacylglycerol in the hemolymph and neutral lipid fractions in the tissues. The results show that infection by this nematode resulted in a significant decrease in the concentrations of both cholesterol and triacylglycerol in the hemolymph of B. glabrata during the parasite’s initial ontogenic development period. This reduction indicates the possible use of these molecules by both parasite and host not only as energy substrates but also as structural factors required during development of the parasite’s larval stages. In parallel, changes in the neutral lipid profile in the DGG and lipase activity of the infected snails were observed, indicating the importance of these molecules for successful infection.

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
Fig. 2
Fig. 3

References

  • Bandstra SR, Fried B, Sherma J (2006) High-performance thin-layer chromatographic analysis of neutral lipids and phospholipids in Biomphalaria glabrata patently infected with Echinostoma caproni. Parasitol Res 99:414–418

    Article  PubMed  Google Scholar 

  • Barrett J, Cain GD, Fairbairn D (1970) Sterols in Ascaris lumbricoides (Nematoda), Macracanthorhynchus hirudinaceus and Moniliformis dubius (Acanthocephala) and Echinostoma revolutum (Trematoda). J Parasitol 56:1004–1008

    Article  PubMed  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. J Physiol Biochem 37:911–913

    Article  CAS  Google Scholar 

  • Choi S, Hwang JM, Kim SI (2003) A colorimetric microplate assay method for high throughput analysis of lipase activity. J Biochem Mol Biol 36:417–420

    Article  PubMed  CAS  Google Scholar 

  • Choubisa SL (1988) Histological and histochemical observations on the digestive gland of Melanoides tuberculatus (Gastropoda) infected with certain larval trematodes and focus on their mode of nutrition. Indian Acad Sci (Anim Sci) 97:251–262

    Article  Google Scholar 

  • Fried B, Shapiro IL (1975) Accumulation and excretion of neutral lipids in the metacercaria of Leucochloridiomorpha constantiae (Trematoda), maintained in vitro. J Parasitol 61:906–909

    Article  PubMed  CAS  Google Scholar 

  • Fried B, Sherma J (1990) Thin layer chromatography of lipids found in snails (Gastropoda: Mollusca). J Planar Chromatogr 3:290–299

    CAS  Google Scholar 

  • Fried B, Schafer S, Kim S (1989) Effects of Echinostoma caproni infection on the lipid-composition of Biomphalaria glabrata. Int J Parasitol 19:353–354

    Article  PubMed  CAS  Google Scholar 

  • Fried B, Frazer BA, Lee MS, Sherma J (1998) Thin layer chromatography and histochemistry analyses of neutral lipids in Helisoma trivolvis infected with four species of larval trematodes. Parasitol Res 84:369–373

    Article  PubMed  CAS  Google Scholar 

  • Grewal PS, Grewal SK, Tan L, Adams BJ (2003) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. J Nematol 35:146–156

    PubMed  CAS  Google Scholar 

  • Guilhon J, Gaalon A (1969) Évolution larvaired´ un nematode parasite de pappariel circulatoire du chien dans l´ organisme de mollusques dulçaquicoles. Comp Rend Acad Sci 268:612–615

    CAS  Google Scholar 

  • Humiczewska M, Rajski K (2005) Lipids in the host–parasite system: digestive gland of Lymnaea truncatula infected the developmental stages of Fasciola hepatica. Acta Parasitol 50:235–239

    Google Scholar 

  • Kwong AYH (1989) Lipid composition and lipases of Angiostrongylus cantonensis (Nematoda: Metastrongyloidea). Thesis, University of Hong Kong

  • Lustrino D, Tunholi-Alves VM, Tunholi VM, Marassi MP, Pinheiro J (2010) Lipids analysis in hemolymph of Achatina fulica (Bowdich, 1822) exposed to different photoperiods. Braz J Biol 70:631–637

    Article  Google Scholar 

  • Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206–210

    Article  PubMed  CAS  Google Scholar 

  • Muller EE, Fried B, Sherma J (2000) HPTLC analysis of neutral lipids in Biomphalaria glabrata snails infected with Schistosoma mansoni (Trematoda). J Planar Chromatogr- Mod TLC 13:228–231

    CAS  Google Scholar 

  • Stewart GL, Ubelaker JE, Curtis D (1985) Pathophysiologic alterations in Biomphalaria glabrata infected with Angiostrongylus costaricensis. J Invertebr Pathol 45:152–157

    Article  PubMed  CAS  Google Scholar 

  • Tang P, Wang LC (2011) Uptake and utilization of arachidonic acid in infective larvae of Angiostrongylus cantonensis. J Helminthol 85:395–400

    Article  PubMed  CAS  Google Scholar 

  • Thiengo SC, Maldonado A, Mota EM, Torres EJ, Caldeira R, Carvalho OS, Oliveira AP, Simões RO, Fernandez MA, Lanfredi RM (2010) The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernanbuco, northeast Brazil. Acta Trop 115:194–199

    Article  PubMed  CAS  Google Scholar 

  • Trinder P (1969) Determination of glucose in blood using glucose oxidase with alternative oxygen acceptor. Ann Clin Biochem 6:24–27

    CAS  Google Scholar 

  • Tripathi PK, Singh A (2002) Toxic effects of dimethoate and carbaryl pesticides on carbohydrate metabolism of freshwater snail Lymnaea acuminata. Bull Environ Contam Toxicol 68:606–611

    Article  PubMed  CAS  Google Scholar 

  • Tunholi-Alves VM, Tunholi VM, Gôlo P, Lustrino D, Maldonado A Jr, Bittencourt VRP, Rodrigues MLA, Pinheiro J (2011a) Lipid levels in Biomphalaria glabrata infected with different doses of Echinostoma paraensei miracidia. Exp Parasitol 128:112–116

    Article  Google Scholar 

  • Tunholi-Alves VM, Tunholi VM, Lustrino D, Amaral LS, Thiengo SC, Pinheiro J (2011b) Changes in the reproductive biology of Biomphalaria glabrata experimentally infected with the nematode Angiostrongylus cantonensis. J Invertebr Pathol 108:220–223

    Article  PubMed  Google Scholar 

  • Tunholi-Alves VM, Tunholi VM, Pinheiro J, Thiengo SC (2012) Effects of infection by larvae of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) on the metabolism of the experimental intermediate host Biomphalaria glabrata. Exp Parasitol 131:143–147

    Article  PubMed  CAS  Google Scholar 

  • Wang QP, De-Hua L, Xing-Quan Z, Xiao-Guang C, Zhao-Rong L (2007) Human angiostrongyliasis. Lancet Infect Dis 8:621–630

    Article  Google Scholar 

  • WHO—World Health Organization (1983) Report of a Scientific Working Group on Plant Molluscicide and Guildelines for Evaluation of Plant Molluscicide. Geneva: World Health Organization (TDR/SCH-SWE (4)/83.3)

  • Willcox HP, Coura JR (1989) Nova concepção para o método de Baermann–Moraes–Coutinho na pesquisa de larvas de nematódeos. Mem Inst Oswaldo Cruz 84:539–565

    Google Scholar 

  • Yamoka T, Satoh K, Katoh S (1978) Preparation of thylakoid membranes active in oxygen evolution at high temperature from a thermophilic blue green alga. In: Metzner H (ed) Photosynthetic oxygen evolution. Academic Press, New York, pp 104–116

    Google Scholar 

  • Zhu N, Dai X, Lin DS, Connor WE (1994) The lipids of slugs and snails: evolution, feed and biosynthesis. Lipids 29:869–887

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by Conselho Nacional para o Desenvolvimento Científico e Tecnológico (CNPq) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Author information

Authors and Affiliations

  1. Departamento de Ciências Fisiológicas, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro (UFRuralRJ), Seropédica, Rio de Janeiro, Brazil

    Vinícius Menezes Tunholi-Alves, Victor Menezes Tunholi, Mariana Lima & Jairo Pinheiro

  2. Curso de Pós-Graduação em Ciências Veterinárias, Departamento de Parasitologia Animal, Instituto de Veterinária, UFRuralRJ, Seropédica, Brazil

    Vinícius Menezes Tunholi-Alves, Victor Menezes Tunholi, Patrícia Gôlo, Mariana Lima & Vânia Rita Elias Pinheiro Bittencourt

  3. Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil, 4365-Manguinhos, 21040-900, Rio de Janeiro, Rio de Janeiro, Brazil

    Juberlan Garcia & Arnaldo Maldonado Júnior

  4. Departamento de Química, Instituto de Ciências Exatas, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, 23890-000, Seropédica, Rio de Janeiro, Brazil

    Emerson Guedes Pontes

  5. Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil

    Vânia Rita Elias Pinheiro Bittencourt

Authors
  1. Vinícius Menezes Tunholi-Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Victor Menezes Tunholi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrícia Gôlo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariana Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juberlan Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arnaldo Maldonado Júnior
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emerson Guedes Pontes
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vânia Rita Elias Pinheiro Bittencourt
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jairo Pinheiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jairo Pinheiro.

Additional information

Vânia Rita Elias Pinheiro Bittencourt, Arnaldo Maldonado Júnior and Jairo Pinheiro are research fellows at CNPq.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tunholi-Alves, V.M., Tunholi, V.M., Gôlo, P. et al. Effects of infection by larvae of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) on the lipid metabolism of the experimental intermediate host Biomphalaria glabrata (Mollusca: Gastropoda). Parasitol Res 112, 2111–2116 (2013). https://doi.org/10.1007/s00436-013-3308-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3308-4

Keywords

Search

Navigation