Oxidative Impact of Dietary Triclabendazole in Galleria mellonella

Recent studies have shown that anthelmintic and antifungal agents are recommended as alternative agents in chemical control of insectpests. In this study, first instar larvae of the greater wax moth, Galleria mellonella, were reared on artificial diets containing 0.001, 0.01, and0.1 g/100 g of triclabendazole, an anthelmintic benzimidazole. The eff ects of these triclabendazole concentrations on the lipid peroxidationproduct, malondialdehyde (MDA) and glutathione-S-transferase (GST) activity were investigated in all G. mellonella developmental stages,as well as in the midgut tissue of the insect. Compared to controls, the highest triclabendazole concentration (0.1%) increased MDA contentfrom 0.182±0.03 to 0.415±0.04 nmol/mg protein in the larvae, from 0.190±0.04 to 0.626±0.06 nmol/mg protein in the pupae, and from0.354±0.06 to 0.451±0.04 nmol/mg protein in the adults. MDA content was determined to be 0.141±0.02 to 0.835±0.13 nmol/mg protein inthe midgut. The highest concentration of triclabendazole was found to significantly increase GST activity in the larvae, pupae, adults, and inthe midgut tissue of G. mellonella in comparison to controls. The three dietary concentrations of triclabendazole resulted in a high degreeof oxidative stress and an increase in the activity of the detoxification enzyme GST following an increase in MDA levels in the midgut and inall developmental stages of G. mellonella.

Triklabendazolün Galleria mellonella’daki Oksidatif Etkisi

Son çalışmalarda, antihelmintik ve antifungal ajanların, böcek zararlılarının kimyasal kontrolünde alternatif kimyasallar olarak önerildiğini görülmektedir. Bu çalışmada, büyük bal mumu güvesi, Galleria mellonella, birinci evre larvaları 0.001, 0.01 ve 0.1 g/100 g benzimidazol grubu bir antihelmintik olan triklabendazol içeren yapay besinler ile beslendi. Belirlenen konsantrasyonların böceğin farklı gelişme evrelerinde (7. evre larva, pup ve ergin) ve orta bağırsağında oksidatif stresin önemli bir belirteci olan lipid peroksidasyonu ürünü malondialdehit (MDA) miktarı ve bir detoksifikasyon enzimi olan glutatyon-S-transferaz (GST) aktivitesi üzerine etkileri araştırıldı. Kontrol grubu ile en yüksek triklabendazol konsantrasyonu (0.1%) karşılaştırıldığında MDA miktarını böceğin larval evresinde 0.182±0.03’ten 0.415±0.04 nmol/mg proteine, pupal evrede 0.190±0.04’ten 0.626±0.06 nmol/mg proteine, ergin bireylerde 0.354±0.06’dan 0.451±0.04 nmol/mg proteine yükseldi. Orta bağırsağında MDA miktarı 0.141±0.02’den 0.835±0.13 nmol/mg protein olarak belirlendi. Triklabendazolün en yüksek konsantrasyonu kontrol grubuna göre böceğin larva, pup, ergin evreleri ve orta bağırsağında GST aktivitesini arttırdığı tespit edildi. Elde edilen bu sonuçlar ile triklabendazolun üç farklı konsantrasyonunun bulunduğu yapay besinler ile beslenen G. mellonella’nın tüm gelişme evrelerinde ve orta bağırsağında oksidatif stres belirteci MDA miktarındaki artışa bağlı olarak yüksek derecede oksidatif stres meydana geldiği ve detoksifikasyon enziminin aktivitesinin arttığı belirlendi.

PDF

___

1. Kılınçer N, Yiğit A, Kazak C, Er MK, Kurtuluş A, Uygun N: Teoriden pratiğe zararlılarla biyolojik mücadele. Türk Biyo Müc Derg, 1 (1): 15-60, 2010.

2. Ayubi A, Moravvej G, Karimi J, Jooyandeh A: Lethal effects of four insecticides on immature stages of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) in laboratory conditions. Turk Entomol Derg, 37 (4): 399-407, 2013.

3. Çalık G, Büyükgüzel K, Büyükgüzel E: Reduced fitness in adults from larval, Galleria mellonella (Lepidoptera: Pyralidae) reared on media amended with the antihelmintic, mebendazole. J Econ Entomol, 109 (1): 182-187, 2016. DOI: 10.1093/jee/tov305

4. Pereira, TC, de Barros PP, Fugisaki LRO, Rossoni RD, Ribeiro FC, de Menezes RT, Jungueira JC, Scorzoni L: Recent advances in the use of Galleria mellonella model to study immune responses against human pathogens. J Fungi (Basel), 4:128, 2018. DOI: 10.3390/jof4040128

5. Hernandez, RJ, Hesse E, Dowling AJ, Coyle NM, Feil EJ, Gaze WH, Vos M: Using the wax moth larva Galleria mellonella infection model to detect emerging bacterial pathogens. Peer J, 6:e6150, 2019. DOI: 10.7717/ peerj.6150

6. Büyükgüzel E, Kayaoğlu S: Niklozamidin Galleria mellonella L. (Lepidoptera: Pyralidae)’nın bazı biyolojik ve fizyolojik özelliklerine etkisi. Turk Entomol Derg, 38 (1): 83-99, 2014. DOI: 10.16970/ted.87976

7. Kılıç A, Büyükgüzel K, Büyükgüzel E: Antihelmintik triklabendazolun yapay besin ile beslenen Galleria mellonella (Lepidoptera: Pyralidae) larvalarının yaşama ve gelişimine etkisi. Kafkas Univ Vet Fak Derg, 21 (6): 841-847, 2015. DOI: 10.9775/kvfd.2015.13731

8. Sugeçti S, Büyükgüzel K: Effects of oxfendazole on metabolic enzymes in hemolymph of Galleria mellonella L. (Lepidoptera: Pyralidae) larvae reared on artificial diet. Karaelmas Fen Müh Derg, 8 (2): 590-594, 2018. DOI: 10.7212%2Fzkufbd.v8i2.1380

9. Sefer NE, Büyükgüzel K: Piperazinin Galleria mellonella’nın yaşama ve gelişimi üzerine etkisi. Karaelmas Fen Müh Derg, 8 (1): 365-372, 2018. DOI: 10.7212%2Fzkufbd.v8i1.1248

10. Çelik C, Büyükgüzel K, Büyükgüzel E: The effects of oxyclozanide on survival, development and total protein of Galleria mellonella L. (Lepidoptera: Pyralidae). J Entomol Res Soc, 21 (1): 95-108, 2019.

11. Farooqui T, Farooqui AA: Oxidative stress in vertebrates and invertebrates: Molecular Aspects of Cell Signaling. 261-270, John Wiley & Sons Inc., New Jersey, 2012.

12. Halliwell B, Gutteridge JM: Free Radicals in Biology and Medicine. 5th ed., 199-283, Oxford University Press, New York, 2015.

13. Özcan O, Erdal H, Çakırca G, Yönden Z: Oksidatif stres ve hücre içi lipit, protein ve DNA yapıları üzerine etkileri. J Clin Exp Invest, 6 (3): 331- 336, 2015. DOI: 10.5799/ahinjs.01.2015.03.0545

14. Kodrík D, Bednářová A, Zemanová M, Krishnan N: Hormonal regulation of response to oxidative stress in insects-an update. Int J Mol Sci, 16 (10): 25788-25816, 2015. DOI: 10.3390/ijms161025788

15. Büyükgüzel E, Kalender Y: Exposure to streptomycin alters oxidative and antioxidative response in larval midgut tissues of Galleria mellonella. Pestic Biochem Physiol, 94 (2-3): 112-118, 2009. DOI: 10.1016/j. pestbp.2009.04.008

16. Altuntaş H, Demirci SN, Duman E, Ergin E: Toxicological and physiological effects of ethephon on the model organism, Galleria mellonella L. 1758 (Lepidoptera: Pyralidae). Turk Entomol Derg, 40 (4): 413-423, 2016. DOI: 10.16970/ted.00995

17. Güneş E, Büyükgüzel E: Oxidative effects of boric acid on different developmental stages of Drosophila melanogaster Meigen, 1830 (Diptera: Drosophilidae). Turk Entomol Derg, 41 (1): 3-15, 2017. DOI: 10.16970/ ted.59163

18. Aslan N, Büyükgüzel E, Büyükgüzel K: Oxidative effects of gemifloxacin on some biological traits of Drosophila melanogaster (Diptera: Drosophilidae). Environ Entomol, 48 (3): 667-673, 2019. DOI: 10.1093/ee/ nvz039

19. Miguel-Aliaga I, Jasper H, Lemaitre B: Anatomy and physiology of the digestive tract of Drosophila melanogaster. Genetics, 210 (2): 357-396, 2018. DOI: 10.1534/genetics.118.300224

20. Dubovskiy IM, Martemyanov VV, Vorontsova YL, Rantala MJ, Gryzanova EV, Glupov VV: Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). Comp Biochem Physiol C Toxicol, 148 (1): 1-5, 2008. DOI: 10.1016/j.cbpc.2008.02.003

21. Ustundag G, Buyukguzel K, Buyukguzel E: The effect of niclosamide on certain biological and biochemical properties of Drosophila melanogaster. Eur J Biol, 78 (1): 29-39, 2019. DOI: 10.26650/EurJBiol.2019.0003

22. Kastamonuluoğlu S, Büyükgüzel K, Büyükgüzel E: The use of dietary antifungal agent terbinafine in artificial diet and its effects on some biological and biochemical parameters of the model organism Galleria mellonella (Lepidoptera: Pyralidae). J Econ Entomol, 113 (3): 1110- 1117, 2020. DOI: 10.1093/jee/toaa039

23. Calvopina HM, Guderian RH, Paredes WY, Cooper PJ: Comparison of two single day regimens of triclabendazole for the treatment of human pulmonary paragonimiasis. Trans R Soc Trop Med Hyg, 97, 451-454, 2003. DOI: 10.1016/S0035-9203(03)90088-5

24. Yüksek N, Altuğ N, Gül A: Koyunlarda endoparazit enfeksiyonlarında triklabendazol - levamizol kombinasyonunun tedavi etkinliği. Van Vet J, 18 (1): 19-24, 2007.

25. Bronskill J: A cage to simplify the rearing of the greater wax moth, Galleria mellonella (Pyralidae). J Lepid Soc, 15 (2): 102-104, 1961.

26. Jain SK, Levine SN: Elevated lipid peroxidation and vitamin E quinine levels in heart ventricles of streptozoticin-treated diabetic rats. Free Radic Biol Med, 18 (2): 337-341, 1995. DOI: 10.1016/0891-5849(94)00114-Y

27. Habig WH, Pabst MJ, Jakoby WB: Glutathione-S-transferases: The first enzymatic step in mercapturic acid formation. J Biol Chem, 249, 7130- 7139, 1974.

28. Lowry OH, Rosebroug NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem, 193, 265-275, 1951.

29. SPSS Inc: User’s Manual. Version 15.0 for Windows; SPSS Inc., Chicago, IL, USA, 2006.

30. Arrese EL, Soulages JL: Insect fat body: Energy, metabolism, and regulation. Annu Rev Entomol, 55, 207-225, 2010. DOI: 10.1146/annurevento-112408-085356

31. van Schoor T, Kelly ET, Tam N, Attardo GM: Impacts of dietary nutritional composition on larval development and adult body composition in the yellow fever mosquito (Aedes aegypti). Insects, 11 (8): 535, 2020. DOI: 10.3390/insects11080535

32. Büyükgüzel E, Kalender Y: Penicillin-induced oxidative stress: Effects on antioxidative response of midgut tissues in larval instars of Galleria mellonella. J Econ Entomol, 100 (5): 1533-1541, 2007. DOI: 10.1093/jee/ 100.5.1533

33. Büyükgüzel E, Kalender Y: Galleria mellonella survivorship, development and protein content in response to dietary antibiotics. J Entomol Sci, 43 (1): 27-40, 2008. DOI: 10.18474/0749-8004-43.1.27

34. Harmancı C, Büyükgüzel K, Büyükgüzel E: The effect of neomycin on survival and development of Pimpla turionellae L. (Hymenoptera: Ichneumonidae) reared on a natural host. J Econ Entomol, 112 (3): 1081- 1088, 2019. DOI: 10.1093/jee/toy419

35. Dmochowska-Ślęzak K, Giejdasz K, Fliszkiewicz M, Żołtowska K: Variations in antioxidant defense during the development of the solitary bee Osmia bicornis. Apidologie, 46, 432-444, 2015. DOI: 10.1007/s13592- 014-0333-y

36. Ventrella E, Adamski Z, Chudzińska E, Miądowicz-Kobielska M, Marciniak P, Buyukguzel E, Buyukguzel K, Erdem M, Falabella P, Scrano L, Bufo SA: Solanum tuberosum and Lycopersicon esculentum leaf extracts and single metabolites affect development and reproduction of Drosophila melanogaster. Plos One, 11 (5): e0155958, 2016. DOI: 10.1371/ journal.pone.0155958

37. Uwo MF, Ui-Tei K, Park P, Takeda M: Replacement of midgut epithelium in the greater wax moth, Galleria mellonela, during larval-pupal moult. Cell Tissue Res, 308 (2): 319-331, 2002. DOI: 10.1007/s00441-002-0515-1

38. Tettamanti G, Grimaldi A, Pennacchio F, de Eguileor M: Toxoneuron nigriceps parasitization delays midgut replacement in fifth-instar Heliothis virescens larvae. Cell Tissue Res, 332 (2): 371-379, 2008. DOI: 10.1007/ s00441-008-0579-7