Skip to main content
SpringerLink
Log in

Resveratrol- and α-viniferin-induced alterations of acetylcholinesterase and nitric oxide synthase in Raillietina echinobothrida

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Phytostilbenes, like resveratrol and α-viniferin, which occur mainly in the plants and belong to the families Cyperaceae, Vitaceae, and Gnetaceae are extensively popular for their medicinal and nutritional properties. In Northeast India, the Jaintia tribes consume these phytochemicals through aqueous extract of the medicinal plant Carex baccans to control helminthiasis. The present study aimed to investigate the inhibitory effect of the phytochemicals on neurotransmitters and its related enzymes in helminth parasite Raillietina echinobothrida. Viability of the parasites exposed to the phytostilbenes and extent of inhibition of cholinergic and nitrergic enzymes were evaluated in comparison to reference anthelmintic drug praziquantel and two known enzyme inhibitors, namely Nω-nitro-l-arginine and pyridostigmine. On exposure to resveratrol, α-viniferin, and reference drug praziquantel, the parasites ceased movement at 9.37, 11.38, and 0.24 h followed by death at 23.65, 34.13, and 1.87 h, respectively. Exposed parasites also showed a significant decrease in the activity of acetylcholinesterase (46.101, 65.935, and 63.645 %) and nitric oxide synthase (61.241, 55.046, and 29.618 %) in comparison to the controls. In addition, a decreased trend in nitric oxide (NO) level was also detected in the tissue of different phytochemical-exposed parasites compared to control. The present study suggests that anthelmintic potential of both the phytochemicals is mediated through inhibition of two vital enzymes which play diverse role in intracellular communications through neuromuscular system.

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

Similar content being viewed by others

Abbreviations

AChE:

Acetylcholinesterase

NOS:

Nitric oxide synthase

NO:

Nitric oxide

AVF:

α-Viniferin

RESV:

Resveratrol

NLA:

Nω-Nitro-l-arginine

PZQ:

Praziquantel

cGMP:

Cyclic guanosine monophosphate

References

  • Barua C, Hazarika S, Saikia B, Phukan A, Biswas A, Pathak D, Borah RS, Verma PK, Barua AG (2012) Evaluation of the effects of cholinergic drugs on the spontaneous muscular activity of isometrically mounted Paramphistomum cervi. J Vet Parasitol 26:127–133

    Google Scholar 

  • Benzi G, Moretti A (1998) Is there a rationale for the use of acetylcholinesterase inhibitors in the therapy of Alzheimer's disease? Eur J Pharmacol 346(1):1–13

    Article  CAS  PubMed  Google Scholar 

  • Bian X, Du L, Chen Z, Shi J, Liu F (2001) A quantitative pathological study on angiogenesis, vascular endothelial growth factor and inducible nitric oxide synthase in astrocytomas. Zhonghua Bing Li Xue Za Zhi Chin J Pathol 30(1):23–26

    CAS  Google Scholar 

  • Bryant C, Behm AC (1989) Biochemical adaptation in parasites. New York, Chapman and Hall Ltd, London

    Google Scholar 

  • Das B, Tandon V, Saha N (2006) Effect of isoflavone from Flemingia vestita (Fabaceae) on the Ca2+ homeostasis in Raillietina echinobothrida, the cestode of domestic fowl. Parasitol Int 55:17–21

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  PubMed  Google Scholar 

  • Evans AM, Martin RJ (1996) Activation and cooperative multi-ion block of single nicotinic-acetylcholine channel currents of Ascaris muscle by the tetrahydropyrimidine anthelmintic, morantel. Br J Pharmacol 118:1127–1140

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Giri BR, Roy B (2014) Resveratrol induced structural and biochemical alterations in the tegument of Raillietina echinobothrida. Parasitol Int 63:32–37

    Article  Google Scholar 

  • Gomori G (1952) Microscopic histochemistry. Principles and practice. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Greenberg RM (2005) Ca2+ signalling, voltage-gated Ca2+ channels and praziquantel in flatworm neuromusculature. Parasitology 131(S1):S97–S108

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson MKS, Lindholm AM, Terenina NB, Reuter M (1996) NO nerves in a tapeworm. NADPH-diaphorase histochemistry in adult Hymenolepis diminuta. Parasitology 113:559–565

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson MK, Terenina NB, Reuter M, Movsessian SO (2003) NO nerves and their targets in a tapeworm: an immunocytochemical study of cGMP in Hymenolepis diminuta. Parasitol Res 90(2):148–152

    PubMed  Google Scholar 

  • Hu Z, Chen Z, Yin Z, Jia R, Song X, Li L, Zou Y, Liang X, Li L, He C, Yin L, Lv C, Zhao L, Su G, Ye G, Shi F. 2015. In vitro acaricidal activity of 1, 8-cineole against Sarcoptes scabiei var. cuniculi and regulating effects on enzyme activity. Parasitol Res 1–9. doi: 10.1007/s00436-015-4498-8

  • Kar PK, Tandon V, Saha N (2002) Anthelmintic efficacy of Flemingia vestita: genistein-induced effect on the activity of nitric oxide synthase and nitric oxide in the trematode parasite, Fasciolopsis buski. Parasitol Int 51(3):249–257

    Article  PubMed  Google Scholar 

  • Karnovsky MJ, Roots L (1964) A direct coloring “thiocholin” method for cholinesterases. J Histochem Cytochem 12:219–221

    Article  CAS  PubMed  Google Scholar 

  • Kulke D, Krücken J, Demeler J, Harder A, Mehlhorn H, von Samson-Himmelstjerna G (2013) In vitro efficacy of cyclooctadepsipepdtides and aminophenylamidines alone and in combination against third-stage larvae and adult worms of Nippostrongylus brasiliensis and first-stage larvae of Trichinella spiralis. Parasitol Res 112(1):335–345

    Article  PubMed  Google Scholar 

  • Lefebvre RA (2002) Pharmacological characterization of the nitrergic innervation of the stomach. Verh K Acad Geneeskd Belg 64:151–166

    CAS  PubMed  Google Scholar 

  • Lindholm AM, Reuter M, Gustafsson MKS (1998) The NADPH-diaphorase staining reaction in relation to the aminergic and peptidergic nervous system and the musculature of adult Diphyllobothrium dendriticum. Parasitology 117:283–292

    Article  CAS  PubMed  Google Scholar 

  • Lipton SA, Stamler JS (1994) Actions of redox-related congeners of nitric oxide at the NMDA receptor. Neuropharmacology 33(11):1229–1233

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  • Martin RJ, Robertson AP (2007) Mode of action of levamisole and pyrantel, anthelmintic resistance, E153 and Q57. Parasitology 134(8):1093–1104

    Article  CAS  PubMed  Google Scholar 

  • Martin RJ, Verma S, Levandoski M, Clark CL, Qian H, Stewart M, Robertson AP (2005) Drug resistance and neurotransmitter receptors of nematodes: recent studies on the mode of action of levamisole. Parasitology 131(S1):S71–S84

    Article  CAS  PubMed  Google Scholar 

  • Matilde F, Paola F, Anna V, Gabriella T, Roberto G, Stefano B, Paolo G (2011) Importance of nitric oxide synthase in the anchoring structures of Neobenedenia girellae—an important fish parasite. Biochem Syst Ecol 39(4):841–845

    Article  CAS  Google Scholar 

  • McKay DM, Halton DW, Allen JM, Fairweather I (1989) The effects of cholinergic and serotoninergic drugs on motility in vitro of Haplometra cylindracea (Trematoda: Digenea). Parasitology 99(02):241–252

    Article  CAS  PubMed  Google Scholar 

  • Moore RB, Kauffman NG (1970) Simultaneous determination of citrulline and urea using diacetyl monoxime. Anal Biochem 33:263–272

    Article  CAS  PubMed  Google Scholar 

  • Onufriev MV, Gulyaeva NV, Terenina NB, Tolstenkov OO, Gustafsson MK (2005) The effects of nitric oxide donor on the synthesis of cGMP in Hymenolepis diminuta: a radiometric study. Parasitol Res 95(1):22–24

    Article  PubMed  Google Scholar 

  • Pearse AGE (1968) Histochemistry: theoretical and applied. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Roy B, Giri BR (2015) α-Viniferin-induced structural and functional alterations in Raillietina echinobothrida, a poultry tapeworm. Microsc Microanal 21:377–384

    Article  CAS  PubMed  Google Scholar 

  • Salter M, Knowles RG (1998) Measurement of NOS activity by conversion of radiolabelled arginine to citrulline using ion-exchange separation. In: Titheradge MA (ed) Nitric oxide protocols. Humana Press, New Jersey, pp 67–74

    Google Scholar 

  • Sermboonpaisarn T, Sawasdee P (2012) Potent and selective butyrylcholinesterase inhibitors from Ficus foveolata. Fitoterapia 83(4):780–784

    Article  CAS  PubMed  Google Scholar 

  • Sessa WC, Pritchart K, Seyedi N, Wang J, Hintz TH (1994) Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res 74:349–353

    Article  CAS  PubMed  Google Scholar 

  • Sung SH, Kang SY, Lee KY, Park MJ, Kim JH, Park JH, Kim YC, Kim J, Kim YC (2002) (+)-Alpha-viniferin, stilbene trimer from Caragana chamlague, inhibits acetylcholinesterase. Biol Pharm Bull 25(1):125–127

    Article  CAS  PubMed  Google Scholar 

  • Swargiary A, Roy B (2011) Kinetics of acetylcholinesterase inhibition in Fasciolopsis buski and Raillietina echinobothrida by shoot extract of Alpinia nigra, an indigenous medicinal plant. Med Plants Int J Phytomed Relat Ind 3(2):145–150

    Article  Google Scholar 

  • Terenina NB, Gustafsson MK (2003) Nitric oxide and its target cells in cercaria of Diplostomum chromatophorum: a histochemical and immunocytochemical study. Parasitol Res 89(3):199–206

    PubMed  Google Scholar 

  • Tran QK, Ohashi K, Watanabe H (2000) Calcium signaling in endothelial cells. Cardiovasc Res 48(1):13–22

    Article  CAS  PubMed  Google Scholar 

  • Veerakumari L, Lalhmingchhuanmawii K, Ashwini R (2012) Effect of Allium sativum and Punica granatum on the motility and acetylcholinesterase activity of Cotylophoron cotylophorum (Fischoeder, 1901). J Exp Zool 15(2):481–485

    Google Scholar 

  • Wolde Mussie E, Vande Waa J, Pax RA, Fetterer R, Bennett JL (1982) Schistosoma mansoni: calcium efflux and effects of calcium-free media on responses of the adult male musculature to praziquantel and other agents inducing contraction. Exp Parasitol 53:270–278

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a project grant from the Department of Science and Technology, New Delhi to BR. The authors also acknowledge UGC for infrastructural facilities provided in the form of DSA phase II to the Department of Zoology, North-Eastern Hill University, Shillong. UGC-BSR doctoral fellowship to BRG is also gratefully acknowledged.

Author information

Authors and Affiliations

  1. Parasitology Laboratory, Department of Zoology, North-Eastern Hill University, Shillong, 793022, Meghalaya, India

    Bikash Ranjan Giri & Bishnupada Roy

Authors
  1. Bikash Ranjan Giri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bishnupada Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bishnupada Roy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giri, B.R., Roy, B. Resveratrol- and α-viniferin-induced alterations of acetylcholinesterase and nitric oxide synthase in Raillietina echinobothrida . Parasitol Res 114, 3775–3781 (2015). https://doi.org/10.1007/s00436-015-4607-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4607-8

Keywords

Search

Navigation