Effect of polyphenols extracted from Punica granatum and Acacia saligna plants on glutathione S-transferase of the cattle tick Rhipicephalus (Boophilus) annulatus (Acari: Ixodidae)

Rasha A Guneidy; Mahmoud A Amer; Amr E El Hakim; Sobhy Abdel-Shafy; Shaimaa A Allam

doi:10.1007/s12639-020-01323-4

Effect of polyphenols extracted from Punica granatum and Acacia saligna plants on glutathione S-transferase of the cattle tick Rhipicephalus (Boophilus) annulatus (Acari: Ixodidae)

J Parasit Dis. 2021 Jun;45(2):524-538. doi: 10.1007/s12639-020-01323-4. Epub 2021 Jan 5.

Authors

Rasha A Guneidy¹, Mahmoud A Amer², Amr E El Hakim¹, Sobhy Abdel-Shafy³, Shaimaa A Allam¹

Affiliations

¹ Department of Molecular Biology, Genetic Engineering and Biotechnology Research Division, National Research Centre, 33 El Buhouth St, Ad Doqi, Dokki, Cairo, 12622 Cairo Governorate Egypt.
² Department of Cytology and Histology, Faculty of Science, Cairo University, Giza, Egypt.
³ Department of Parasitology and Animal Diseases, Division of Veterinary Research, National Research Centre, Cairo, Egypt.

Abstract

Ticks are hematophageal ectoparasites that transport major pathogens around the world. Glutathione S-transferases (GST) are involved in resistance to acaricide and redox balancing during the life cycle of the tick. The inhibition of tick GST enzymes by certain phenolic compounds, such as phenolic acids and tannins, can be a promising approach to tick control. The objective of this study was to evaluate the effects of Punica granatum red peel and Acacia saligna leaf extracts on Rhipicephalus (Boophilus) annulatus GST activity in order to reduce the resistance of cattle to acaricide. The results showed that P. granatum ethanol extract (70%) contained the highest total phenol content (350 ± 1.2 μM GAE g^-1), the highest condensed tannin content (270 ± 1.3 μM CE g^-1) and the highest hydrolysable tannin content (70 ± 5.0 μM TAE g^-1). Adult immersion test with a dosage of 100 mg ml^-1 of A. saligna ethanol extracts had a significant mortality of 50% and 75% after 24 h and 96 h, respectively (p < 0.01). A simple and reproducible procedure was established to purify the whole R. annulatus GST (wRaGST) while a full-length cDNA of GST was cloned from a cDNA library of the local Egyptian cattle tick R. (B.) annulatus (rRaGST). Aqueous extracts of P. granatum inhibited both wRaGST and rRaGST with values of IC₅₀ = 0.114 and 0.07 µg ml^-1, respectively, compared to A. saligna extracts (IC₅₀ values = 2.08 and 1.35 µg ml, respectively). These inhibitory effects were attributed to the presence of a high tannin concentration (≥ 80%). HPLC analysis indicated the presence of gallic acid and catechin in both extracts, in addition to the rutin, which was only observed in A. saligna extracts. The addition of a tannin inhibitor, polyethylene glycol, suggested the existence of other phenolic compounds in combination with catechins responsible for inhibiting the activity of these extracts. Non-competitive behaviour of catechins may be helpful in preventing, or at least delaying, the development of chemical acaricide resistance in R. annulatus.

Keywords: Glutathione S-transferases inhibition; Polyphenols; Rhipicephalus annulatus; Tannin; Tick control.