Sodium nitroprusside toxicity in drosophila melanogaster: Delayed pupation, reduced adult emergence, and induced oxidative/nitrosative stress in eclosed flies

Archives of Insect Biochemistry and Physiology

Volumn 80, Issue 3, 2012, Pages 166-185

  Lozinsky, Oleksandr V ^a   Lushchak, Oleh V ^a   Storey, Janet M ^b   Storey, Kenneth B ^b   Lushchak, Volodymyr I ^a  

^a VASYL STEFANYK PRECARPATHIAN NATIONAL UNIVERSITY   (Ukraine)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

Aconitase; Antioxidant enzymes; Drosophila melanogaster; Oxidative stress; Reactive nitrogen species; Reactive oxygen species; Sodium nitroprusside

Indexed keywords

ANTIOXIDANT; DROSOPHILA PROTEIN; IRON; NITRIC OXIDE DONOR; NITRITE; NITROPRUSSIDE SODIUM;

ANIMAL; ARTICLE; DOSE RESPONSE; DROSOPHILA MELANOGASTER; DRUG EFFECT; FEMALE; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; METABOLISM; OXIDATIVE STRESS;

ANIMALS; ANTIOXIDANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; IRON; LARVA; MALE; NITRIC OXIDE DONORS; NITRITES; NITROPRUSSIDE; OXIDATIVE STRESS;

DROSOPHILA MELANOGASTER;

EID: 84863780609     PISSN: 07394462     EISSN: 15206327     Source Type: Journal    
DOI: 10.1002/arch.21033     Document Type: Article

References (66)

1. Andersson U, Leighton B, Young ME, Blomstrand E, Newsholme EA. 1998. Inactivation of aconitase and oxoglutarate dehydrogenase in skeletal muscle in vitro by superoxide anions and/or nitric oxide. Biochem Biophys Res Commun 249(2):512-516.
2. Arnér ES, Zhong L, Holmgren A. 1999. Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol 300:226-239.
3. Ashburner M, Golic KG, Hawley RS. 2005. Drosophila: a laboratory handbook. 2nd ed. NY: Cold Spring Harbor Laboratory Press. xxviii + 1409 pp.
4. Babich H, Zuckerbraun HL, Ricklis AS, Blau L. 1998. In vitro toxicity of sodium nitroprusside to human endothelial ECV304 cells. Environ Toxicol Pharmacol 5(2):135-144.
5. Bagnyukova TV, Chahrak OI, Lushchak VI. 2006. Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat toxicol 78(4):325-331.
6. Bates JN, Baker MT, Guerra R, Jr, Harrison DG. 1991. Nitric oxide generation from nitroprusside by vascular tissue. Evidence that reduction of the nitroprusside anion and cyanide loss are required. Biochem Pharmacol 42(Suppl):S157-165.
7. Bayliak M, Semchyshyn H, Lushchak V. 2006. Effect of hydrogen peroxide on antioxidant enzyme activities in Saccharomyces cerevisiae is strain-specific. Biochemistry (Moscow) 71(9):1013-1020.
8. Beda N, Nedospasov A. 2005. A spectrophotometric assay for nitrate in an excess of nitrite. Nitric Oxide 13(2):93-97.
9. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
10. Broderick KE, Balasubramanian M, Chan A, Potluri P, Feala J, Belke DD, McCulloch A, Sharma VS, Pilz RB, Bigby TD, Boss, GR. 2007. The cobalamin precursor cobinamide detoxifies nitroprusside-generated cyanide. Exp Biol Med (Maywood) 232(6):789-798.
11. Brooks SP. 1992. A simple computer program with statistical tests for the analysis of enzyme kinetics. BioTechniques 13(6):906-911.
12. Cáceres L, Necakov AS, Schwartz C, Kimber S, Roberts IJH, Krause HM. 2011. Nitric oxide coordinates metabolism, growth, and development via the nuclear receptor E75. Genes Dev 25(14):1476-1485.
13. Canteros G, Rettori V, Genaro A, Suburo A, Gimeno M, McCann S. 1996. Nitric oxide synthase content of hypothalamic explants: increase by norepinephrine and inactivated by NO and cGMP. Proc Natl Acad Sci USA 93(9):4246-4250.
14. Cardaci S, Filomeni G, Rotilio G, Ciriolo MR. 2008. Reactive oxygen species mediate p53 activation and apoptosis induced by sodium nitroprusside in SH-SY5Y cells. Mol Pharmacol 74(5):1234-1245.
15. Cho S-G, Lee YH, Park H-S, Ryoo K, Kang KW, Park J, Eom S-J, Kim MJ, Chang T-S, Choi S-Y, Shim J, Kim Y, Dong M-S, Lee M-J, Kim SG, Ichijo H, Choi E-J. 2001. Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J Biol Chem 276(16):12749-12755.
16. Clancy RM, Levartovsky D, Leszczynska-Piziak J, Yegudin J, Abramson SB. 1994. Nitric oxide reacts with intracellular glutathione and activates the hexose monophosphate shunt in human neutrophils: evidence for S-nitrosoglutathione as a bioactive intermediary. Proc Natl Acad Sci USA 91(9):3680-3684.
17. Curran RD, Ferrari FK, Kispert PH, Stadler J, Stuehr DJ, Simmons RL, Billiar TR. 1991. Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB J 5(7):2085-2092.
18. Emptage MH, Dreyers JL, Kennedy MC, Beinert H. 1983. Optical and EPR characterization of different species of active and inactive aconitase. J Biol Chem 258(18):11106-11111.
19. Fass U, Panickar K, Williams K, Nevels K, Personett D, McKinney M. 2004. The role of glutathione in nitric oxide donor toxicity to SN56 cholinergic neuron-like cells. Brain Res 1005(1-2):90-100.
20. Felton GW, Summers CB. 1995. Antioxidant systems in insects. Arch Insect Biochem Physiol 29(2):187-197.
21. Gardner PR, Fridovich I. 1991. Superoxide sensitivity of the Escherichia coli aconitase. J Biol Chem 266(29):19328-19328.
22. Gardner PR, Costantino G, Szabó C, Salzman AL. 1997. Nitric oxide sensitivity of the aconitases. J Biol Chem 272(40):25071-25076.
23. Gutteridge J. 1986. Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Lett 201(2):291-295.
24. Halliwell B, Gutteridge JMC. 1989. Free radicals in biology and medicine. 2nd ed. Oxford: Clarendon Press.
25. Hannas BR, Das PC, Li H, LeBlanc GA. 2010. Intracellular conversion of environmental nitrate and nitrite to nitric oxide with resulting developmental toxicity to the crustacean Daphnia magna. PloS One 5(8):e12453-e12453.
26. Hyršl P, Büyükgüzel E, Büyükgüzel K. 2007. The effects of boric acid-induced oxidative stress on antioxidant enzymes and survivorship in Galleria mellonella. Arch Insect Biochem Physiol 66(1):23-31.
27. Kanzok SM, Fechner A, Bauer H, Ulschmid JK, Müller HM, Botella-Munoz J, Schneuwly S, Schirmer R, Becker K. 2001. Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster. Science 291(5504):643-646.
28. Karamanev DG, Nikolov LN, Mamatarkova V. 2002. Rapid simultaneous quantitative determination of ferric and ferrous ions in drainage waters and similar solutions. Miner Eng 15(5):341-346.
29. Kim H-G, Kim B-C, Park E-H, Ahn K, Lim C-J. 2004. Differential regulation of three genes encoding glutathione S-transferases in S. pombe. Mol Cells 18(3):332-339.
30. Kim HJ, Tsoy I, Park MK, Lee YS, Lee JH, Seo HG, Chang KC. 2006. Iron released by sodium nitroprusside contributes to heme oxygenase-1 induction via the cAMP-protein kinase A-mitogen-activated protein kinase pathway in RAW 264.7 cells. Mol Pharmacol 69(5):1633-1640.
31. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER. 1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464-478.
32. Liu Y, Wu R, Wan Q, Xie G, Bi Y. 2007. Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol 48(3):511-511.
33. Luperchio S, Tamir S, Tannenbaum SR. 1996. NO-induced oxidative stress and glutathione metabolism in rodent and human cells. Free Radic Biol Med 21(4):513-519.
34. Lushchak VI. 2007. Free radical oxidation of proteins and its relationship with functional state of organisms. Biochemistry (Mosc) 72(8):809-827.
35. Lushchak VI. 2011. Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13-30.
36. Lushchak VI. 2012. Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids: Article ID 736837, 26 p., doi:10.1155/2012/736837.
37. Lushchak VI, Bagnyukova TV. 2006. Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comp Biochem Physiol C Toxicol Pharmacol 143(1):36-41.
38. Lushchak OV, Lushchak VI. 2008a. Catalase modifies yeast Saccharomyces cerevisiae response towards S-nitrosoglutathione-induced stress. Redox Rep 13(6):283-291.
39. Lushchak OV, Lushchak VI. 2008b. Sodium nitroprusside induces mild oxidative stress in Saccharomyces cerevisiae. Redox Rep 13(4):144-152.
40. Lushchak OV, Kubrak OI, Lozinsky OV, Storey JM, Storey KB, Lushchak VI. 2009. Chromium(III) induces oxidative stress in goldfish liver and kidney. Aquat Toxicol 93(1):45-52.
41. Lushchak OV, Rovenko BM, Gospodaryov DV, Lushchak VI. 2011. Drosophila melanogaster larvae fed by glucose and fructose demonstrate difference in oxidative stress markers and antioxidant enzymes of adult flies. Comp Biochem Physiol A Mol Integr Physiol 160(1):27-34.
42. Massie HR, Aiello VR, Williams TR. 1985. Iron accumulation during development and ageing of Drosophila. Mech Ageing Dev 29(2):215-220.
43. Massie HR, Aiello VR, Williams TR. 1993. Inhibition of iron absorption prolongs the life span of Drosophila. Mech Ageing Dev 67(3):227-237.
44. Mendjan S, Akhtar A. 2007. The right dose for every sex. Chromosoma 116(2):95-106.
45. Miyashita NT. 1990. Molecular and phenotypic variation of the Zw locus region in Drosophila melanogaster. Genetics 125(2):407-419.
46. Mogren CL, Trumble JT. 2010. The impacts of metals and metalloids on insect behavior. Entomol Exp Appl 135(1):1-17.
47. Nazir A, Mukhopadhyay I, Saxena DK, Siddiqui MS, Chowdhuri DK. 2003. Evaluation of toxic potential of captan: induction of hsp70 and tissue damage in transgenic Drosophila melanogaster (hsp70-lacZ) Bg9. J Biochem Mol Toxicol 17(2):98-107.
48. Olcott MH, Henkels MD, Rosen KL, Walker FL, Sneh B, Loper JE, Taylor BJ. 2010. Lethality and developmental delay in Drosophila melanogaster larvae after ingestion of selected Pseudomonas fluorescens strains. PloS One 5(9):e12504--e12504.
49. Padalko VI, Leonova IS, Kozlova EV. 2008. The protein oxidative damage level and lifespan modulation by xenobiotics in Drosophila melanogaster. Adv Gerontol 21(2):212-217.
50. Peranovich TM, da Silva AM, Fries DM, Stern A, Monteiro HP. 1995. Nitric oxide stimulates tyrosine phosphorylation in murine fibroblasts in the absence and presence of epidermal growth factor. Biochem J 305(Pt 2):613-619.
51. Pritsos CA, Ahmad S, Elliott AJ, Pardini RS.1990. Antioxidant enzyme level response to prooxidant allelochemicals in larvae of the southern armyworm moth, Spodoptera eridania. Free Radic Res Commun 9(2):127-133.
52. Radyuk SN, Klichko VI, Orr WC. 2000. Catalase expression in Drosophila melanogaster is responsive to ecdysone and exhibits both transcriptional and post-transcriptional regulation. Arch Insect Biochem Physiol 45(2):79-93.
53. Rowe JD, Patskovsky YV, Patskovska LN, Novikova E, Listowsky I. 1998. Rationale for reclassification of a distinctive subdivision of mammalian class Mu glutathione S-transferases that are primarily expressed in testis. J Biol Chem 273(16):9593-9601.
54. Ruan RS, Leong SK, Yeoh KH. 1999. Ototoxicity of sodium nitroprusside is not due to nitric oxide. Exp Neurol 158(1):192-201.
55. Semchyshyn HM, Lushchak VI. 2004. Effect of protonofore 2, 4-dinitrophenol on catalase activity of intact Escherichia coli bacteria. Ukr Biokhim Zh. 76(3):42-48.
56. Sies H. 1991. Role of reactive oxygen species in biological processes. Klin Wochenschr 69(21-23):965-968.
57. Singh MP, Reddy MMK, Mathur N, Saxena DK, Chowdhuri DK. 2009. Induction of hsp70, hsp60, hsp83 and hsp26 and oxidative stress markers in benzene, toluene and xylene exposed Drosophila melanogaster: role of ROS generation. Toxicol Appl Pharmacol 235(2):226-243.
58. Singh MP, Ram KR, Mishra M, Shrivastava M, Saxena DK, Chowdhuri DK. 2010. Effects of co-exposure of benzene, toluene and xylene to Drosophila melanogaster: alteration in hsp70, hsp60, hsp83, hsp26, ROS generation and oxidative stress markers. Chemosphere 79(5):577-587.
59. Terashima J, Takaki K, Sakurai S, Bownes M. 2005. Nutritional status affects 20-hydroxyecdysone concentration and progression of oogenesis in Drosophila melanogaster. J Endocrinol. 187(1):69-79.
60. Toba G, Aigaki T. 2000. Disruption of the microsomal glutathione S-transferase-like gene reduces life span of Drosophila melanogaster. Gene 253(2):179-187.
61. Tsuji Y, Unno N, Menconi MJ, Smith M, Fink MP. 1996. Nitric oxide donors increase cytosolic ionized calcium in cultured human intestinal epithelial cells. Shock 6(1):19-24.
62. Urig S, Becker K. 2006. On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin Cancer Biol 16(6):452-465.
63. Williamson JH, Bentley MM. 1983. Dosage compensation in Drosophila: NADP-enzyme activities and cross-reacting material. Genetics 103(4):649-658.
64. Winterbourn CC. 1995. Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol lett 82:969-974.
65. Yamada M, Momose K, Richelson E. 1996. Sodium nitroprusside-induced apoptotic cellular death via production of hydrogen peroxide in murine neuroblastoma N1E-115 cells. J Pharmacol Toxicol Methods 35(1):11-17.
66. Zinke I, Kirchner C, Chao LC, Tetzlaff MT, Pankratz MJ. 1999. Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 126(23):5275-5284.