The Effect of Niclosamide on Certain Biological and Biochemical Properties of Drosophila melanogaster

Abstract

ABSTRACT

Objective: Laboratory research on management strategies such as biological and chemical control usually demands rearing high numbers of high-quality insects. For this reason, there is a need for detailed information about which antimicrobial agents should be added to their diets in order to obtain high quality insects. Materials and methods: Niclosamide, which is an anthelmintic derivative of salisilanilid, was added in amounts of 100, 200, 400 and 800 mg/L into artificial diets of Drosophila melanogaster (Meigen). The effects on survival rate, developmental time and adult longevity of the insects were examined. Furthermore, the effect of this anthelmintic antibiotic on important oxidative stress indicators; lipid peroxidation product, malondialdehyde (MDA) and protein oxidation products; protein carbonyl (PCO) contents and a detoxification enzyme, glutathione S-transferase (GST) activity in 3rd instar larvae, pupae and adult stage of the insect were also investigated. Results: Compared with those insects on the control diet, the tested concentrations of niclosamide significantly decreased survival rate in all developmental stages of the insect. The control diet produced 94.0 ± 1.0 % of 3rd stage larvae whereas in the highest concentration (800 mg/L) this ratio decreased to 14.00 % ± 1.73. While 42.08 ± 0.50 % of the adults survived in the control diet, longevity decreased to 2.30 ± 0.15 days in the highest concentration. All concentrations of niclosamide resulted in increased MDA contents in the last larval stage of D. melanogaster and concentrations of 100, 200 and 800 mg/L niclosamide increased pupal MDA content in comparison to the control group. At low concentrations of niclosamide, PCO decreased in the last stage of larvae.  The diet with 400 mg/L niclosamide concentration significiantly increased GST activity in pupal stage. Conclusion: The results of this work indicated that the negative effects of niclosamide on biological characteristics of D. melanogaster are due to an increase in the oxidative stress and crippled detoxification capacity of the insect. 

Keywords

• Drosophila melanogaster,oxidative stress,niclosamide,survival,development

Supporting Institution

This study was supported by Research Fund of Zonguldak Bülent Ecevit University

Project Number

201550737594-0

References

1. 1. Ozparlak H. The structure of cuticle, moulting and effects of diflubenzuron (DFB) in insects. J Sci Fac Art Sci. Selçuk Uni 2003; 21: 7-19.
2. 2. Singh P, House HL. Antimicrobials safe levels in a synthetic diet of an insect, Agria affinis. J Insect Physiol 1970; 16: 1769-82.
3. 3. Grenier S, Liu WH. Antifungals: Mold control and safe levels in artificial media for Trichogramma (Hymenoptera: Trichogrammatidae). Entomophaga 1990; 35: 283-91.
4. 4. Pearson B, Raybould AF. The Effects of antibiotics on the development of larvae and the possible role of bacterial load in caste determination and diapause in Myrmicarubra (Hymenoptera: Formicidae). Sociobiol 1998; 31: 77-90.
5. 5. Büyükgüzel K. DNA gyrase inhibitors: Novobiocin enhances the survial of Pimpla turionellae larvae reared on an arftifical diet but other antibiotics do not. J Appl Entomol 2001; 125: 583-87.
6. 6. Büyükgüzel K, Yazgan Ş. Effects of antimicrobial agents on survival and development of larvae of Pimpla turionellae L. (Hymenoptera: Ichneumonidae) reared on an artificial diet. Turk J Zool 2002; 26: 111-19.
7. 7. Alverson J, Cohen AC. Effect of antifungal agents on biological fitness of Lygus hesperus (Heteroptera: Miridae). J Econ Entomol 2002; 65: 256-60.
8. 8. Inglis GD, Cohen AC. Influence of antimicrobial agents on the spoilage of a meat-based entomophage diet. J Econ Entomol 2004; 97: 235-250.

9. 9. Büyükgüzel E, Kalender Y. Penicillin-Induced Oxidative Stress: Effects on Antioxidative Response of Midgut Tissues in Larval Instars of G. mellonella. J Econ Entomol 2007; 100: 1533-41.
10. 10. Büyükgüzel E, Kalender Y. Galleria mellonella survivorship, development and protein content in response to dietary antibiotics. J Entomol Sci 2008; 43: 27-40.
11. 11. Büyükgüzel E, Kalender Y. Exposure to streptomycin alters oxidative and Antioxidative response in larval midgut tissues of Galleria mellonella. Pestic Biochem Physiol 2009; 94: 112-18.
12. 12. Büyükgüzel E, Büyükgüzel K. Effect of acyclovir on the microbial contamination in the artifical and natural diets for rearing of Galleria mellonella L. Karaelmas Sci Eng J 2016a; 6: 105-10.
13. 13. Büyükgüzel E, Büyükgüzel K. Effects of antiviral agent, acyclovir, on the biological fitness of Galleria mellonella (Lepidoptera: Pyralidae) adults. J Econ Entomol 2016b; 109: 2090-95.
14. 14. Çalık G, Büyükgüzel K, Büyükgüzel E. Reduced fitness in adults from larval, Galleria mellonella (Lepidoptera: Pyralidae) reared on media amended with the anthelmintic, mebendazole. J Econ Entomol 2016; 109: 1-6.
15. 15. Büyükgüzel E, Erdem M, Tunaz H, Küçük C, Atılgan UC, Stanley D, et al. Inhibition of eicosanoid signaling leads to increased lipid peroxidation in a host/parasitoid system. Comp Biochem Physiol Part A: Mol Integ Physiol 2017; 204: 121-28.
16. 16. Kelly J, Kavanagh K. Caspofungi.n primes the immune response of the larvae of Galleria mellonella and induces a non-specific antimicrobial response. J Med Microbiol 2011; 60: 189-96. 17. Ashburner M. Drosophila a Laboratory Handbook, New York: Cold Spring Harbor Press; 1989.
17. 18. Tennessen, J M, Barry, WE, Cox, J, Thummel, CS. Methods for studying metabolism in Drosophila. Methods 2014; 68: 105-15.
18. 19. Çakır Ş, Sarıkaya R. Effects of some organophosphate insecticides on percentage of survival of Drosophila melanogaster. J Gazi Educ Fac 2004; 24: 71-80.
19. 20. Sarıkaya R, Selvi M, Akkaya N, Acar M, Erkoç F. Effects of food dyes in different concentrations on percentage of survival in Drosophila melanogaster (mwh x flr), SDU J Sci (E- Journal) 2010; 5: 38-46.
20. 21. Zhou J, Jin B, Jin Y, Liu Y, Pan J. The antihelminthic drug niclosamide effectively inhibits the malignant phenotypes of uveal melanoma in vitro and in vivo. Theranostics 2017; 7: 1447-62.
21. 22. Öztop AY, Saygı G, Öztop HN. In vitro effects of some anthelminthics on the malate dehydrogenase and lactate dehydrogenase enzyme activities of Taenia Saginata. Tr J Med Sci 1999; 29: 365-70.
22. 23. Şanlı Y, Kaya S. Veteriner Farmakoloji ve İlaçla Sağıtım Seçenekleri kitabı, 2.Baskı. Ankara: Medisan Yayınevi; 1994.p.651-69.
23. 24. Lobo, V, Patil, A, Phatak, A, Chandra, N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy reviews 4(8), 118-26.
24. 25. Petersen, RC. Free-radicals and advanced chemistries involved in cell membrane organization influence oxygen diffusion and pathology treatment. AIMS Biophysics, 2017; 4: 240-83.
25. 26. Birben, E., Sahiner, U M., Sackesen, C, Erzurum, S, Kalayci, O. (2012). Oxidative stress and antioxidant defense. WAO Journal, 2010; 51: 9-19.
26. 27. Zhu, YC, Gordon, LS, Ming,SC. Comparative study on glutathione S-transferase activity, cDNA, and gene expression between malathion susceptible and resistant strains of the tarnished plant bug, Lygus lineolaris. Pest. Biochem. Physiol 2007; 87: 62-72.
27. 28. Rogina B, Reenan RA, Nilsen SP, Helfand SL. Helfand, Extended lifespan conferred by contransporter gene mutations in Drosophila. Biogerontol Sci 2000; 290: 2137-40.
28. 29. Lesch C, Goto A, Lindgren M, Bidla G, Dushay MS, Theopold U. A role for Hemolectin in coagulation and immunity in Drosophila melonagaster. Develop Com Immun 2007; 31: 1255-63.
29. 30. Jain SK, Levine SN. Levine, Elevated lipid peroxidation and vitamin e-quinone levels in heart ventricles of streptozotocin-treated diabetic rats. Free Rad Biol Med 18: 337-41.
30. 31. Levine RL, Williams JA, Stadtman ER., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Meth Enzymol 1994; 233: 346-57.
31. 32. Krishnan N, Kodrík D. Antioxidant enzymes in Spodoptera littoralis (Boisduval): Are they enhanced to protect gut tissues during oxidative stress? J Insect Physiol 2006; 52: 11-20.
32. 33. Habig HW, Pabst MJ, Jakoby WB. Glutathione-S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249: 7130-39.
33. 34. Lowry OH, Rosebrough NL, Farr AL. Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 19: 265.
34. 35. Pajot P. Fluorescence of proteins in 6-M Guanidine Hydrochloride. Euro J Biochem 1976; 63: 263-69.
35. 36. Snedecor GS, Cochran WG. Cochran, Statistical methods, 8th edn., Iowa State University Press Ames IA 1989.
36. 37. Grenier S, Delobel B, Bannot G. Physiological considerations of importance to the success of in vitro culture. J Insect Physiol 1986; 32: 403–8.
37. 38. Sak O, Uçkan F. Effects of cypermethrin exposed to host on the developmental biology of Pimpla turionellae (Hymenoptera: Ichneumonidae). Ann Entomol Soc Am 2009; 102: 288-94.
38. 39. Sak O, Uçkan F. Boric acid dust as a component of an integrated cockroach management program in confined swine production. J Econ Entomol 2003; 96: 1362-66.
39. 40. Xue RD, Barnard DR. Barnard, Boric acid bait kills adult mosquitoes (Diptera: Culicidae). J Econ Entomol 2003; 96: 1559-62.
40. 41. Gore JC, Schal C. Laboratory evaluation of boric acid-sugar solutions as baits for management of German cockroach infestiation. J Econ Entomol 2004; 97: 581-87.
41. 42. Gore JC, Zurek L, Santangelo RG, Stringham MS, Watson DW, Schal C. Water solutions of boric acid and sugar for management of German cocroach populations in livestock production system. J Econ Entomol 2004; 97: 715-20.
42. 43. Hyršl P, Büyükgüzel E, Büyükgüzel K. The effects of boric acidinduced oxidative stress on antioxidant enzymes and survivorship in Galleria mellonella. Arch Insect Biochem Physiol 2007; 66: 23-31.
43. 44. Wadhwa R, Sharma SP. Studies on catalase in ageing Zaprionus paravittiger (Diptera) with special reference to an antioxidant feding. Mech Ageing Dev 1987; 40: 139-147.
44. 45. Bains JS, Stephane HR, Baimoukhametova DV, Piet R. Retrograde regulation of GABA transmission by the tonic release of oxytocin and endocannabinoids governs postsynaptic firing. J Neurosci 2007; 27: 1325–33.
45. 46. Büyükgüzel E, Kayaoğlu S. The effect of niclosamide on some biological and physiological aspects of Galleria mellonella L. (Lepidoptera: Pyralidae). Turk J Entomol 2014; 38: 83-99.
46. 47. Muller FL, Lustgarten MS, Jang Y, Richardson A, Remmen HV. Trends in oxidative aging theories. Free Rad Biol Medic 2007; 43: 477-503.
47. 48. Cruz SA, Silva ECM, Bueno OC, Malaspina O. Malaspina, Morphological alterations induced by boric acid and fipronil in the midgut of worker honey bee (Apis mellifera) larvae. Cell Biol Tox 2009; 26: 165-176.
48. 49. Şahin N, Türkoğlu Ş. The effects of some textile dyes on the percentage of survival, longevity and number of offspring individuals of Drosophila melanogaster Cumhuriyet Un Fac Sci J 2014; 35: 1300-1949.
49. 50. Wu KC,  Liu J, Klaassen CD. Role of Nrf2 in preventing ethanol induced oxidative stress and lipid accumulation. Toxicol Appl Pharmacol 2012; 262: 321-29.
50. 51. Erdem M, Büyükgüzel E. The Effects of Xanthotoxın on the biology and biochemıstry of Galleria mellonella L. (Lepidoptera: Pyralidae). Arch Insect Biochem Physiol 2015; 89: 193-203.
51. 52. Büyükgüzel E, Erdem M, Tunaz H, Küçük C, Atılgan UC, Stanley D, et al. Inhibition of eicosanoid signaling leads to increased lipid peroxidation in a host/parasitoid system. Comp Biochem Physiol Part A: Mol Integ Physiol 2017; 204: 121-128.
52. 53. Güneş E, Büyükgüzel E. Oxidative effects of boric acid on different developmental stages of Drosophila melanogaster meigen (Diptera: Drosophilidae). Turk J Entomol 2017; 41: 3-15.
53. 54. Agianian B, Tucker PA, Schouten A, Leonard K, Bullard B, Gros P. GrosStructure of a Drosophila Sigma class Glutathione S-transferase reveals a novel active site topography suited for lipid peroxidation products. J Mol Biol 2003; 326: 151-65.
54. 55. Hunaiti AA, Elbettieha AM. Developmental studies on Drosophila melanogaster Glutathione –S-transferase and its induction by oxadiazolone. Insect Biochem Mol Biol 1995; 25: 1115-1119.
55. 56. Rajurkar RB, Khan ZH, Gujar GT. Studies on levels of Glutathione-S- Transferase, its isolation and purification from Helicoverpa armigera. Current Sci 2003; 85: 1355-60.
56. 57. Slepneva IA, Glupov VV, Sergeeya SV, Khramtsov VV. Detection of reactive oxygen species in hemolymph of Galleria mellonella and Dendrolimus superans sibiricus (Lepidoptera) larvae. Biochem Biophys Res Commun 1999; 264: 215-5.
57. 58. Glupov VV, Khyosheyskaya MF, Lozinskaya YL, Dubovski IM, Martemyanov VV, Sokolova JY. Application of the nitroblue tetrazoliumreduction method for studies on the production of reactive oxygen species in insect haemocytes. Cytobios 2001; 106: 165-78.
58. 59. Lozinskaya YL, Slepneva IA, Khramtsov VV, Glupov VV. Changes of the antioxidant status and system of generation of free radicals in hemolymph of Galleria mellonella Larvae at Microsporidiosis. J Evol Biochem Phsycol 2004; 40: 119–25.
59. 60. Aucoin JS, Jiang P, Aznavour N, Tong XK, Buttini M, Descarries L, et al. Selective cholinergic denervation, independent from oxidative stress, in a mouse model of Alzheimer’s disease. Neurosci 2005; 132: 73–86.
60. 61. Kayış T, Emre İ, Coşkun M. Effects of diazinon on antioxidant enzymes and adult emergence of the parasitoid Pimpla turionellae L. (Hymenoptera: Ichneumonidae). Turk J Entomol 2012; 36: 463-71.
61. 62. Sezer B, Ozalp P. Effect of juvenile hormone analogue, pyriproxyfen on antioxidant enzymes of greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae: Galleriinae) Larvae. Pak J Zool 2015; 47: 665-69.
62. 63. Adamski Z, Ziemnicki K, Fila K, Zikic RV, Stajn A. Stajn, Effects of long-term exposure to fenitrothion on Spodoptera exigua and Tenebrio molitor larval development and antioxidant enzyme activity. Biol Lett 2003; 40: 43-52
63. 64. Cervera A, Maymo AC, Pardo RM, Garcera MD. Antiooxidant enzymes in Oncopeltus fasciatus (Heteroptera: Lygaeidae) exposed to cadmium. Environ Entomol 2003; 32: 705-10.