DOSE-DEPENDENT INFLUENCES OF VANILLIC ACID ON COGNITIVE FUNCTION AND REDOX HOMEOSTASIS STATUS IN N-NITROSODIETHYLAMINE TREATED DROSOPHILA MELANOGASTER
DOI:
https://doi.org/10.22159/ijcpr.2021v13i4.42750Keywords:
Cancer, Drosophila melanogaster, Vanillic acid, Behavioural assays, Free radical, Dose dependencyAbstract
Objective: To assess the dose-dependent effect of vanillic acid on cognitive behavior and indices of redox homeostasis in the fruit fly, Drosophila melanogaster.
Methods: In this study, flies were divided into five groups-group 1 control, group 2-treated with 0.01% NDEA through drinking water for 15 w, group 3-treated with NDEA and vanillic acid (VA) (0.005%) in culture medium, group 4-treated with NDEA and VA (0.01%) and group 5-treated with NDEA and VA (0.05%). Cognitive-behavioral assays and assessment of redox homeostasis indices were performed.
Results: Behavioural abnormalities (negative geotaxis, phototaxis, smell and taste chemotaxis, hypotaxis and thermotaxis) were quantitatively deviated in NDEA treated flies compared to control but were tend to be normalized in VA treated flies. The contents of protein carbonyl, thiobarbituric acid reactive substance (TBARS), protein thiol and lipid peroxides were noticeably augmented in NDEA treated flies than control flies and correspondingly tend to normalize in VA (0.01%) treated groups. Further, superoxide dismutase (SOD), catalase (CAT), glutathione-S-transferase (GST), glutathione peroxidise (GPX) and reduced glutathione (GSH) were decreased in NDEA treated group and were significantly increased (p<0.05) in VA treated (0.01%) groups.
Conclusion: Vanillic acid, a bioactive phytochemical could act as a potent antioxidant and as well exhibit antiproliferative characteristics. The dose lower than 0.01% could not be effective as the dose is low. Nevertheless, at 0.01% the maximum benefits could have been achieved, and beyond this saturation point, higher doses, such as 0.05% could not be effective.
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References
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31. Vinoth A, Kowsalya R. Chemopreventive potential of vanillic acid against 7,12-dimethylbenz(a)anthrazene-induced hamster buccal pouch carcinogenesis. J Cancer Res Ther 2018;14:1285-90.
32. Velli S, Sundaram J, Murugan M, Balaraman G, Thiruvengadam D. Protective effect of vanillic acid against benzo(a)pyrene induced lung cancer in swiss albino mice. J Biochem Mol Toxicol 2019;33:e22382.
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34. Pendergrass JC, Targum SD, Harrison JE. Cognitive impairment associated with cancer: a brief review. Innovations Clin Neurosci 2018;15:36-44.
35. Haddadi M, Jahromi SR, Sagar BK, Patil RK, Shivanandappa T, Ramesh SR. Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster. Behav Brain Res 2012;259:60-9.
36. Aleanizy FS, Alqahtani FH, Eltayb EK, Alrumikan N, Almebki R, Alhossan A, et al. Evaluating the effect of antibiotics sub-inhibitory dose on Pseudomonas aeruginosa quorum sensing dependent virulence and its phenotypes. Saudi J Biol Sci 2021;28:550-9.
37. Burrell Saward H, Harris AJ, LaFlor R, Sallam H, Alavijeh MS, Ward TH, et al. Dose-dependent effect and pharmacokinetics of fexinidabole and its metabolites in a mouse model of human African trypanosomiasis. Int J Antimic Agents 2017;50:203-9.
38. Subramanian P, Jayapalan JJ, Abdul Rahman PS, Manjula A, Hashim OH. Temporal regulation of proteome profile in the fruit fly, Drosophila melanogaster. Peer J 2016;4:2080.
39. Macmillan HA, Hughson BN. A high-throughput method of hemolymph collection from adult Drosophila without anesthesia. J Insect Physiol 2014;63:27-31.
40. Neckameyer WS, Bhatt P. Protocols to study behavior in Drosophila. In: Dahmann C. Ed. Drosophila: methods and protocols, Springer: New York; 2016. p. 303-20.
41. Feany MB, Bender WW. A Drosophila model of Parkinson’s disease. Nature 2000;404:394-8.
42. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Meth Enzymol 1990;186:464-78.
43. Niehaus WG, Samuelsson B. Formation of malondialdehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 1968;6:126-30.
44. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82:70-7.
45. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8.
46. Habig WH, Palst MJ, Jakpoly WB. Glutathione transferase: A first enzymatic step in mercapturic acid and formation. J Biol Chem 1974;249:7130-9.
47. Kakkar P, Das B, Viswanathan PN. A modified spectrophotometric assay of superoxide dismutase (SOD). Ind J Biochem Biophys 1984;21:130-2.
48. Sinha KA. Colorimetric assay of catalase. Anal Biochem 1972;7:389-94.
49. Rotruck JT, Pope A, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG. Selenium: biochemical roles as components of glutathione peroxidase. Science 1973;179:588–90.
50. Takahashi E, Marczylo TH, Watanabe T, Nagai S, Hayatsu H, Negishi T. Preventive effects of anthraquinone food pigments on the DNA damage induced by carcinogens in Drosophila. Mut Res 2001;1:139-45.
51. Hosamani R, Muralidhara. Neuroprotective efficacy of Bacopa monnieri against rotenone induced oxidative stress and neurotoxicity in Drosophila melanogaster. Neurotoxicology 2009;30:977-85.
52. Hill VM, O'Connor RM, Sissoko GB, Irobunda IS, Leong S, Canman JC, et al. A bidirectional relationship between sleep and oxidative stress in Drosophila. PLoS Biol 2018;16:e2005206.
53. Silveira TFF, Souza TC, Carvalho AV, Ribeiro AB, Kuhnle GCC, Godoy HT. White acai juice (Euterpe oleracea): phenolic composition by LC-ESI-MS/MS, antioxidant capacity and inhibition effect on the formation of colorectal cancer related compounds. J Func Foods 2017;36:215-23.
54. Huang X, Xi Y, Mao Z, Chu X, Ma RZ, Cheng H, et al. Vanillic acid attenuates cartilage degeneration by regulating the MAPK and PI3K/AKT/NF-?B pathways. Eur J Pharmacol 2019;859:172481.
55. Taqvi S, Bhat EA, Sajjad N, Sabir JSM, Quershi A, Rather IA, et al. Protective effect of vanillic acid in hydrogen-peroxide induced oxidative stress in D. mel-2 cell line. Saudi J Biol Sci 2021;28:1795-800.
56. Yang Y, Zhang G, Guo F, Li Q, Luo H, Shu Y, et al. Mitochondrial UQCC3 modulates hypoxia adaptation by orchestrating OXPHOS and glycolysis in hepatocellular carcinoma. Cell Rep 2020;33:108340.
57. Weinberg F, Ramnath N, Nagrath D. Reactive oxygen species in the tumor microenvironment: an overview. Cancers 2019;11:1191.
58. Kasapoglu M, Ozben T. Alterations of antioxidant enzymes and oxidative stress markers in aging. Exp Gerontol 2001;36:209-20.
59. Aguiar LM, Figueira FH, Gottschalk MS, Rosa CE. Glyphosphate-based herbicide exposure causes antioxidant defense responses in the fruit fly Drosophila melanogaster. Comp Biochem Physiol C: Toxicol Pharmacol 2016;185-186:94-101.
60. Kuo CL, Chou HY, Chiu YC, Cheng AN, Fan CC, Chang YN, et al. Mitochondrial oxidative stress by Lon-PYCR1 maintains an immunosuppressive tumor microenvironment that promotes cancer progression and metastasis. Cancer Lett 2020;474:138-50.
61. Gaya Bover A, Hernandez Lopez R, Alorda Clara M, Rosa JM, Fernandez T, Company MM, et al. Antioxidant enzymes change in different non-metastatic changes in tumoral and peritumoral tissues of colorectal cancer. Int J Biochem Cell Biol 2020;120:105698.
62. Ishii N, Homma T, Guo X, Yamada KI, Yamada S, Fujii J. Ascorbic acid prevents N-nitrosodiethylamine induced hepatic injury and hepatocarcinogenesis in Akr1a-knockout mice. Toxicol Lett 2020;333:192-201.
2. Millburn GH, Grosby MA, Gramates LS, Tweedie S, FlyBase C. FlyBase portals to human disease research using Drosophila models. Dis Models Mechan 2016;9:245-52.
3. Sonoshita M, Cagan RL. Modeling human cancers in Drosophila. Curr Topics Dev Biol 2017;121:287-309.
4. Adnan H, Adnan SM, Deng K, Yang C, Zhao W, Li K. Variation in insurance-mortality relationship amid macroeconomic shifts: a study of SEER female-specific cancer patients in USA. Public Health 2020;185:130-8.
5. Hoskins RA. Drosophila genome sequence, a model for the human. Biomed Pharmacother 2000;54:415-6.
6. Hussain M, Jabeen N, Shabbir S, Udin N, Aziz B, Amanullah A, et al. Dataset for homologous proteins in Drosophila melanogaster for SARS-CoV-2/human interactome. Data Brief 2020; 32:106082.
7. Vang LL, Medvedev AV, Adler J. Simple ways to measure behavioural responses of drosophila to stimuli and use of these methods to characterize a novel mutant, Plos One 2012;7:e37495.
8. Antoni MH, Lutgendorf SK, Cole SW, Dhabhar FS, Sephton SE, McDonald PG, et al. The influence of bio-behavioral factors in tumor biology: pathways and mechanisms. Nature Rev Cancer 2006;6:240-8.
9. Bonilla E, Contreras R, Medina Leendertz S, Mora M, Villalobos V, Bravo Y. Minocycline increases the life span and motor activity and decreases lipid peroxidation in manganese treated Drosophila melanogaster. Toxicology 2012;294:50-3.
10. Subramanian P, Prasanna V, Jayapalan JJ, Adbul Rahman PS, Hashim OH. Role of Bacopa monnieri in the temporal regulation of oxidative stress in clock mutant (cryb) of Drosophila melanogaster. J Insect Physiol 2014;65:37-44.
11. Hebels DGAJ, Jennen DGJ, Kleinjans JCS, de Kok TMCM. Molecular signatures of N-nitroso compounds in caco-2 cells: implications for colon carcinogenesis. Toxicol Sci 2009;108:290-300.
12. El-Din NKB, Ali DA, Othman R, French W, Ghoneum M. Chemopreventive role of arabinoxylan rice-bran, MGN-3/Biobran, on liver carcinogenesis in rats. Biomed Pharmacother 2020;126:110064.
13. Lu S, Li G, Lv Z, Gong P, Xia L, Sun Z, et al. Facile and sensitive determination of N-nitrosoamines in food samples by high performance liquid chromatography via combining fluorescent labelling with dispersive liquid-liquid microextraction. Food Chem 2017;234:408-15.
14. Stuff JE, Goh ET, Barrera SL, Bondy ML, Forman MR. Construction of an N-nitroso database for assessing dietary intake. J Food Comp Anal 2009;225:542-77.
15. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biol Int 2006;160:1-40.
16. Aiub CAF, Gadermeier G, Oliveira I, Felzenszwalb I, Ferreira F, Pinto LFR, et al. N-nitrosodiethylamine genotoxicity in primary rat hepatocytes: effects of cytochrome P450 induction by phenobarbital. Toxicol Lett 2011;206:139-43.
17. Pinto RLF. Differences between isoamylalcohol and ethanol on the metabolism and DNA ethylation of N-nitrosodiethylamine in the rat. Toxicology 2000;151:73–9.
18. Muller FL, Lustgarten MS, Jang Y, Richardson A, Remmen VH. Trends in oxidative aging theories. Free Radical Biol Med 2007;43:477-503.
19. Lin Y, Jiang M, Chen W, Zhao T, Wei Y. Cancer and ER stress: mutual crosstalk between autophagy, oxidative stress and inflammatory response. Biomed Pharmacother 2019;118:109249.
20. Wong KC, Sankaran S, Jayapalan JJ, Subramanian P, Abdul Rahman PS. Melatonin improves cognitive behaviour, oxidative stress and metabolism in tumor-prone lethal giant larvae mutant of Drosophila melanogaster. Arch Insect Biochem Physiol 2021;107:e21785.
21. Donohoe C, Senge MO, Arnaut LG, Gomes-de-Silva LC. Cell death in photodynamic therapy: from oxidative stress to anti-tumor immunity. Biochim Biophysica Acta Rev Cancer 2019;1872:188308.
22. Nimse SB, Pal D. Free radicals, natural antioxidants, and their reaction mechanisms. Royal Soc Chem Adv 2015;5:27986–8006.
23. Yan ZJ, Xiang X, Ying D, Hua ZX. Fermented barley extracts with Lactobacillus plantarum dy-1 rich in vanillic acid modulate glucose consumption in human HepG2 cells. Biomed Env Sci 2018;31:667-76.
24. Ahmadi N, Safari S, Mirazi N, Karimi SA, Komaki A. Effects of vanillic acid on A?1-40-induced oxidative stress and learining and memory deficit in male rats. Brain Res Bull 2021;170:264-73.
25. Mohan S, George G, Raghu KG. Vanillic acid retains redox status in HepG2 cells during hyperinsulinemic shock using the mitochondrial pathway. Food Biosci 2021;41:101016.
26. Sharma N, Khurana N, Muthuraman A, Utreja P. Pharmacological evaluation of vanillic acid in rotenone-induced Parkinson’s disease rat model. Eur J Pharmacol 2021;903:174112.
27. Garza Lombo C, Pappa A, Panayiotidis MI, Franco R. Redox homeostasis, oxidative stress and mitophagy. Mitochondrion 2020;51:105-17.
28. Chang WC, Wu JS, Chen CW, Kuo PL, Chien MM, Wang TY, et al. Protective effect of vanillic acid against hyperinsulinemia, hyperglycemia and hyperlipidemia via alleviating hepatic insulin resistance and inflammation in high-fat diet (HFD-) fed rats. Nutrients 2015;7:9946-59.
29. Itoh A, Isoda K, Kondah M, Kawase M, Kobayashi M, Tamesada M, et al. Hepatoprotectie effect of gallic acid and vanillic acid on concanavalin-a induced liver injury. Biol Pharm Bull 2009;32:1215-9.
30. Rasheeda K, Bharathi H, Fathima NN. Vanillic acid and syringic acid: exceptionally robust aromatic moieties for inhibiting in vitro self-assembly of type I collagen. Int J Biol Macromol 2018;113:952-60.
31. Vinoth A, Kowsalya R. Chemopreventive potential of vanillic acid against 7,12-dimethylbenz(a)anthrazene-induced hamster buccal pouch carcinogenesis. J Cancer Res Ther 2018;14:1285-90.
32. Velli S, Sundaram J, Murugan M, Balaraman G, Thiruvengadam D. Protective effect of vanillic acid against benzo(a)pyrene induced lung cancer in swiss albino mice. J Biochem Mol Toxicol 2019;33:e22382.
33. Coll Tane M, Krebbers A, Castells Nobau A, Zweier C, Schencka A. Intellectual disability and autism spectrum disorders ‘on the fly’: insights from Drosophila. Dis Models Mech 2019;12:dmm039180. DOI:10.1242/dmm.039180.
34. Pendergrass JC, Targum SD, Harrison JE. Cognitive impairment associated with cancer: a brief review. Innovations Clin Neurosci 2018;15:36-44.
35. Haddadi M, Jahromi SR, Sagar BK, Patil RK, Shivanandappa T, Ramesh SR. Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster. Behav Brain Res 2012;259:60-9.
36. Aleanizy FS, Alqahtani FH, Eltayb EK, Alrumikan N, Almebki R, Alhossan A, et al. Evaluating the effect of antibiotics sub-inhibitory dose on Pseudomonas aeruginosa quorum sensing dependent virulence and its phenotypes. Saudi J Biol Sci 2021;28:550-9.
37. Burrell Saward H, Harris AJ, LaFlor R, Sallam H, Alavijeh MS, Ward TH, et al. Dose-dependent effect and pharmacokinetics of fexinidabole and its metabolites in a mouse model of human African trypanosomiasis. Int J Antimic Agents 2017;50:203-9.
38. Subramanian P, Jayapalan JJ, Abdul Rahman PS, Manjula A, Hashim OH. Temporal regulation of proteome profile in the fruit fly, Drosophila melanogaster. Peer J 2016;4:2080.
39. Macmillan HA, Hughson BN. A high-throughput method of hemolymph collection from adult Drosophila without anesthesia. J Insect Physiol 2014;63:27-31.
40. Neckameyer WS, Bhatt P. Protocols to study behavior in Drosophila. In: Dahmann C. Ed. Drosophila: methods and protocols, Springer: New York; 2016. p. 303-20.
41. Feany MB, Bender WW. A Drosophila model of Parkinson’s disease. Nature 2000;404:394-8.
42. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Meth Enzymol 1990;186:464-78.
43. Niehaus WG, Samuelsson B. Formation of malondialdehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 1968;6:126-30.
44. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82:70-7.
45. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8.
46. Habig WH, Palst MJ, Jakpoly WB. Glutathione transferase: A first enzymatic step in mercapturic acid and formation. J Biol Chem 1974;249:7130-9.
47. Kakkar P, Das B, Viswanathan PN. A modified spectrophotometric assay of superoxide dismutase (SOD). Ind J Biochem Biophys 1984;21:130-2.
48. Sinha KA. Colorimetric assay of catalase. Anal Biochem 1972;7:389-94.
49. Rotruck JT, Pope A, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG. Selenium: biochemical roles as components of glutathione peroxidase. Science 1973;179:588–90.
50. Takahashi E, Marczylo TH, Watanabe T, Nagai S, Hayatsu H, Negishi T. Preventive effects of anthraquinone food pigments on the DNA damage induced by carcinogens in Drosophila. Mut Res 2001;1:139-45.
51. Hosamani R, Muralidhara. Neuroprotective efficacy of Bacopa monnieri against rotenone induced oxidative stress and neurotoxicity in Drosophila melanogaster. Neurotoxicology 2009;30:977-85.
52. Hill VM, O'Connor RM, Sissoko GB, Irobunda IS, Leong S, Canman JC, et al. A bidirectional relationship between sleep and oxidative stress in Drosophila. PLoS Biol 2018;16:e2005206.
53. Silveira TFF, Souza TC, Carvalho AV, Ribeiro AB, Kuhnle GCC, Godoy HT. White acai juice (Euterpe oleracea): phenolic composition by LC-ESI-MS/MS, antioxidant capacity and inhibition effect on the formation of colorectal cancer related compounds. J Func Foods 2017;36:215-23.
54. Huang X, Xi Y, Mao Z, Chu X, Ma RZ, Cheng H, et al. Vanillic acid attenuates cartilage degeneration by regulating the MAPK and PI3K/AKT/NF-?B pathways. Eur J Pharmacol 2019;859:172481.
55. Taqvi S, Bhat EA, Sajjad N, Sabir JSM, Quershi A, Rather IA, et al. Protective effect of vanillic acid in hydrogen-peroxide induced oxidative stress in D. mel-2 cell line. Saudi J Biol Sci 2021;28:1795-800.
56. Yang Y, Zhang G, Guo F, Li Q, Luo H, Shu Y, et al. Mitochondrial UQCC3 modulates hypoxia adaptation by orchestrating OXPHOS and glycolysis in hepatocellular carcinoma. Cell Rep 2020;33:108340.
57. Weinberg F, Ramnath N, Nagrath D. Reactive oxygen species in the tumor microenvironment: an overview. Cancers 2019;11:1191.
58. Kasapoglu M, Ozben T. Alterations of antioxidant enzymes and oxidative stress markers in aging. Exp Gerontol 2001;36:209-20.
59. Aguiar LM, Figueira FH, Gottschalk MS, Rosa CE. Glyphosphate-based herbicide exposure causes antioxidant defense responses in the fruit fly Drosophila melanogaster. Comp Biochem Physiol C: Toxicol Pharmacol 2016;185-186:94-101.
60. Kuo CL, Chou HY, Chiu YC, Cheng AN, Fan CC, Chang YN, et al. Mitochondrial oxidative stress by Lon-PYCR1 maintains an immunosuppressive tumor microenvironment that promotes cancer progression and metastasis. Cancer Lett 2020;474:138-50.
61. Gaya Bover A, Hernandez Lopez R, Alorda Clara M, Rosa JM, Fernandez T, Company MM, et al. Antioxidant enzymes change in different non-metastatic changes in tumoral and peritumoral tissues of colorectal cancer. Int J Biochem Cell Biol 2020;120:105698.
62. Ishii N, Homma T, Guo X, Yamada KI, Yamada S, Fujii J. Ascorbic acid prevents N-nitrosodiethylamine induced hepatic injury and hepatocarcinogenesis in Akr1a-knockout mice. Toxicol Lett 2020;333:192-201.
Published
15-07-2021
How to Cite
KANI, A., and P. SUBRAMANIAN. “DOSE-DEPENDENT INFLUENCES OF VANILLIC ACID ON COGNITIVE FUNCTION AND REDOX HOMEOSTASIS STATUS IN N-NITROSODIETHYLAMINE TREATED DROSOPHILA MELANOGASTER”. International Journal of Current Pharmaceutical Research, vol. 13, no. 4, July 2021, pp. 85-92, doi:10.22159/ijcpr.2021v13i4.42750.
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