Protective Effects of Gold Nanoparticles Against Malathion-Induced Cytotoxicity in Caco-2 Cells
-
Zeynab Shahmahmoodi
,
Somayeh Jafarinejad
,
Mohammad Reza Hormozi-Nezhad
,
Homanaz Ghafari
,
Mahmoud Ghazi khansari
Abstract
Malathion is an organophosphorus insecticide widely used in agriculture, residential area, and public health programs with a known mechanism of toxicity of inhibition of acetylcholinesterase and induction of oxidative stress. Gold nanoparticles (AuNPs) represent stable and easily synthesized nanoparticles with extensive use in consumer products and medicine. Due to the antioxidant property of AuNPs, it is possible that AuNPs may prevent malathion-induced oxidative damage. In this study, the cytotoxicity of malathion and AuNPs (10 and 20 nm) were measured separately in Caco-2 cells. Then the protective effects of AuNPs were evaluated by measuring the oxidative stress (lipid peroxidation level and glutathione content) and acetylcholinesterase activity. The calculated IC50s values at 48 hr were 326.8±0.32, 43.09±0.65, and 41.46±0.24 µg/ml for malathion, AuNPs 10 and 20 nm, respectively. Then, the lowest concentration of AuNPs (1 µg/ml) and IC50 concentration of malathion (326.8 µg/ml) were selected to evaluate the effects of pretreatment of Caco-2 cells with AuNPs before exposure to malathion were evaluated. Interestingly, the results showed remarkably significant protective effects of AuNPs by attenuation the different parameters of oxidative stress and cytotoxicity induced by malathion in cells (P<0.001). It is the first report showing the protective effects of AuNPs against malathion-induced cytotoxicity in the Caco-2 cell line.
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6. Chithrani, D.B., et al., Gold nanoparticles as radiation sensitizers in cancer therapy. Radiation research, 2010. 173(6): p. 719-728.
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8. Idriss, S. and J. Levitt, Malathion for head lice and scabies: treatment and safety considerations. Journal of drugs in dermatology: JDD, 2009. 8(8): p. 715-720.
9. Wilson, J.D., Toxicological profile for malathion. 2003: Agency for Toxic Substances and Disease Registry.
10. Cancer, I.A.f.R.o., Some organophosphate insecticides and herbicides: diazinon, glyphosate, malathion, parathion, and tetrachlorvinphos. Monographs on the evaluation of carcinogenic risks to humans, 2015. 112.
11. Holmstedt, B., Pharmacology of organophosphorus cholinesterase inhibitors. Pharmacological Reviews, 1959. 11(3): p. 567-688.
12. Mangas, I., et al., New insights on molecular interactions of organophosphorus pesticides with esterases. Toxicology, 2017. 376: p. 30-43.
13. Durak, D., et al., Malathion‐induced oxidative stress in human erythrocytes and the protective effect of vitamins C and E in vitro. Environmental toxicology, 2009. 24(3): p. 235-242.
14. John, S., et al., Protective effect of vitamin E in dimethoate and malathion induced oxidative stress in rat erythrocytes. The Journal of nutritional biochemistry, 2001. 12(9): p. 500-504.
15. Moore, P.D., C.G. Yedjou, and P.B. Tchounwou, Malathion‐induced oxidative stress, cytotoxicity, and genotoxicity in human liver carcinoma (HepG2) cells. Environmental toxicology, 2010. 25(3): p. 221-226.
16. Bonner, M.R., et al., Malathion exposure and the incidence of cancer in the agricultural health study. American journal of epidemiology, 2007. 166(9): p. 1023-1034.
17. Giri, S., et al., Genotoxic effects of malathion: an organophosphorus insecticide, using three mammalian bioassays in vivo. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 2002. 514(1-2): p. 223-231.
18. Khera, K., C. Whalen, and G. Trivett, Teratogenicity studies on linuron, malathion, and methoxychlor in rats. Toxicology and applied pharmacology, 1978. 45(2): p. 435-444.
19. Gioria, S., et al., A combined proteomics and metabolomics approach to assess the effects of gold nanoparticles in vitro. Nanotoxicology, 2016. 10(6): p. 736-748.
20. Chueh, P.J., et al., Differential cytotoxic effects of gold nanoparticles in different mammalian cell lines. Journal of hazardous materials, 2014. 264: p. 303-312.
21. Connor, E.E., et al., Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small, 2005. 1(3): p. 325-327.
22. Shukla, R., et al., Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir, 2005. 21(23): p. 10644-10654.
23. Mukherjee, P., et al., Antiangiogenic properties of gold nanoparticles. Clinical Cancer Research, 2005. 11(9): p. 3530-3534.
24. Rizwan, H., et al., Gold nanoparticles reduce high glucose-induced oxidative-nitrosative stress regulated inflammation and apoptosis via tuberin-mTOR/NF-κB pathways in macrophages. International journal of nanomedicine, 2017. 12: p. 5841.
25. Chen, Y.-S., et al., Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale research letters, 2009. 4(8): p. 858.
26. Suh, K.S., et al., Gold nanoparticles attenuates antimycin A-induced mitochondrial dysfunction in MC3T3-E1 osteoblastic cells. Biological trace element research, 2013. 153(1-3): p. 428-436.
27. BarathManiKanth, S., et al., Anti-oxidant effect of gold nanoparticles restrains hyperglycemic conditions in diabetic mice. Journal of nanobiotechnology, 2010. 8(1): p. 16.
28. Hidalgo, I.J., T.J. Raub, and R.T. Borchardt, Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology, 1989. 96(3): p. 736-749.
29. Yao, M., et al., Uptake of gold nanoparticles by intestinal epithelial cells: impact of particle size on their absorption, accumulation, and toxicity. Journal of agricultural and food chemistry, 2015. 63(36): p. 8044-8049.
30. Bajak, E., et al., Changes in Caco-2 cells transcriptome profiles upon exposure to gold nanoparticles. Toxicology letters, 2015. 233(2): p. 187-199.
31. Aueviriyavit, S., D. Phummiratch, and R. Maniratanachote, Mechanistic study on the biological effects of silver and gold nanoparticles in Caco-2 cells–induction of the Nrf2/HO-1 pathway by high concentrations of silver nanoparticles. Toxicology letters, 2014. 224(1): p. 73-83.
32. Bastús, N.G., J. Comenge, and V. Puntes, Kinetically controlled seeded growth synthesis of citrate-stabilized gold nanoparticles of up to 200 nm: size focusing versus Ostwald ripening. Langmuir, 2011. 27(17): p. 11098-11105.
33. Morgan, D.M., Tetrazolium (MTT) assay for cellular viability and activity, in Polyamine protocols. 1998, Springer. p. 179-184.
34. Armstrong, D. and R. Browne, The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds related to oxidative stress as applied to the clinical chemistry laboratory, in Free radicals in diagnostic medicine. 1994, Springer. p. 43-58.
35. Rahman, I., A. Kode, and S.K. Biswas, Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature protocols, 2006. 1(6): p. 3159.
36. Ellman, G.L., et al., A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical pharmacology, 1961. 7(2): p. 88-95.
37. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 1976. 72(1-2): p. 248-254.
38. Sobti, R., A. Krishan, and C. Pfaffenberger, Cytokinetic and cytogenetic effects of some agricultural chemicals on human lymphoid cells in vitro: organophosphates. Mutation Research/Genetic Toxicology, 1982. 102(1): p. 89-102.
39. Rodgers, K.E., et al., In vitro effects of malathion and O, O, S-trimethyl phosphorothioate on cytotoxic T-lymphocyte responses. Pesticide Biochemistry and Physiology, 1985. 24(2): p. 260-266.
40. Chen, X.-y., et al., Involvement of apoptosis in malathion-induced cytotoxicity in a grass carp (Ctenopharyngodon idellus) cell line. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 2006. 142(1-2): p. 36-45.
41. Malik, J. and K. Summer, Toxicity and metabolism of malathion and its impurities in isolated rat hepatocytes: role of glutathione. Toxicology and applied pharmacology, 1982. 66(1): p. 69-76.
42. Karami-Mohajeri, S. and M. Abdollahi, Toxic influence of organophosphate, carbamate, and organochlorine pesticides on cellular metabolism of lipids, proteins, and carbohydrates: a systematic review. Human & experimental toxicology, 2011. 30(9): p. 1119-1140.
43. Isoda, H., et al., Effects of organophosphorous pesticides used in China on various mammalian cells. Environmental sciences: an international journal of environmental physiology and toxicology, 2005. 12(1): p. 9-19.
44. Krstić, D.Z., et al., Inhibition of AChE by malathion and some structurally similar compounds. Journal of enzyme inhibition and medicinal chemistry, 2008. 23(4): p. 562-573.
45. Sanvicens, N. and M.P. Marco, Multifunctional nanoparticles–properties and prospects for their use in human medicine. Trends in biotechnology, 2008. 26(8): p. 425-433.
46. Pan, Y., et al., Size‐dependent cytotoxicity of gold nanoparticles. Small, 2007. 3(11): p. 1941-1949.
47. Momić, T., et al., Adsorption of organophosphate pesticide dimethoate on gold nanospheres and nanorods. Journal of Nanomaterials, 2016. 2016.
48. Nair, A.S. and T. Pradeep, Extraction of chlorpyrifos and malathion from water by metal nanoparticles. Journal of nanoscience and nanotechnology, 2007. 7(6): p. 1871-1877.
49. Li, H., et al., Visual detection of organophosphorus pesticides represented by mathamidophos using Au nanoparticles as colorimetric probe. Talanta, 2011. 87: p. 93-99.
50. Yan, X., H. Li, and X. Su, Review of Optical Sensors for Pesticides. TrAC Trends in Analytical Chemistry, 2018.
51. Xia, N., Q. Wang, and L. Liu, Nanomaterials-based optical techniques for the detection of acetylcholinesterase and pesticides. Sensors, 2014. 15(1): p. 499-514.
52. Satnami, M.L., et al., Gold nanoprobe for inhibition and reactivation of acetylcholinesterase: An application to detection of organophosphorus pesticides. Sensors and Actuators B: Chemical, 2018. 267: p. 155-164.
53. Chiang, C.-W., A. Wang, and C.-Y. Mou, CO oxidation catalyzed by gold nanoparticles confined in mesoporous aluminosilicate Al-SBA-15: Pretreatment methods. Catalysis Today, 2006. 117(1-3): p. 220-227.
54. Yakimovich, N., et al., Antioxidant properties of gold nanoparticles studied by ESR spectroscopy. Russian Chemical Bulletin, 2008. 57(3): p. 520-523.
2. Rao, C.N.R., A. Müller, and A.K. Cheetham, The chemistry of nanomaterials: synthesis, properties and applications. 2006: John Wiley & Sons.
3. Sun, H., et al., Gold Nanoparticle-Induced Cell Death and Potential Applications in Nanomedicine. International journal of molecular sciences, 2018. 19(3): p. 754.
4. Boisselier, E. and D. Astruc, Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chemical society reviews, 2009. 38(6): p. 1759-1782.
5. Ghosh, P., et al., Gold nanoparticles in delivery applications. Advanced drug delivery reviews, 2008. 60(11): p. 1307-1315.
6. Chithrani, D.B., et al., Gold nanoparticles as radiation sensitizers in cancer therapy. Radiation research, 2010. 173(6): p. 719-728.
7. Huang, X., et al., Plasmonic photothermal therapy (PPTT) using gold nanoparticles. Lasers in medical science, 2008. 23(3): p. 217.
8. Idriss, S. and J. Levitt, Malathion for head lice and scabies: treatment and safety considerations. Journal of drugs in dermatology: JDD, 2009. 8(8): p. 715-720.
9. Wilson, J.D., Toxicological profile for malathion. 2003: Agency for Toxic Substances and Disease Registry.
10. Cancer, I.A.f.R.o., Some organophosphate insecticides and herbicides: diazinon, glyphosate, malathion, parathion, and tetrachlorvinphos. Monographs on the evaluation of carcinogenic risks to humans, 2015. 112.
11. Holmstedt, B., Pharmacology of organophosphorus cholinesterase inhibitors. Pharmacological Reviews, 1959. 11(3): p. 567-688.
12. Mangas, I., et al., New insights on molecular interactions of organophosphorus pesticides with esterases. Toxicology, 2017. 376: p. 30-43.
13. Durak, D., et al., Malathion‐induced oxidative stress in human erythrocytes and the protective effect of vitamins C and E in vitro. Environmental toxicology, 2009. 24(3): p. 235-242.
14. John, S., et al., Protective effect of vitamin E in dimethoate and malathion induced oxidative stress in rat erythrocytes. The Journal of nutritional biochemistry, 2001. 12(9): p. 500-504.
15. Moore, P.D., C.G. Yedjou, and P.B. Tchounwou, Malathion‐induced oxidative stress, cytotoxicity, and genotoxicity in human liver carcinoma (HepG2) cells. Environmental toxicology, 2010. 25(3): p. 221-226.
16. Bonner, M.R., et al., Malathion exposure and the incidence of cancer in the agricultural health study. American journal of epidemiology, 2007. 166(9): p. 1023-1034.
17. Giri, S., et al., Genotoxic effects of malathion: an organophosphorus insecticide, using three mammalian bioassays in vivo. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 2002. 514(1-2): p. 223-231.
18. Khera, K., C. Whalen, and G. Trivett, Teratogenicity studies on linuron, malathion, and methoxychlor in rats. Toxicology and applied pharmacology, 1978. 45(2): p. 435-444.
19. Gioria, S., et al., A combined proteomics and metabolomics approach to assess the effects of gold nanoparticles in vitro. Nanotoxicology, 2016. 10(6): p. 736-748.
20. Chueh, P.J., et al., Differential cytotoxic effects of gold nanoparticles in different mammalian cell lines. Journal of hazardous materials, 2014. 264: p. 303-312.
21. Connor, E.E., et al., Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small, 2005. 1(3): p. 325-327.
22. Shukla, R., et al., Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir, 2005. 21(23): p. 10644-10654.
23. Mukherjee, P., et al., Antiangiogenic properties of gold nanoparticles. Clinical Cancer Research, 2005. 11(9): p. 3530-3534.
24. Rizwan, H., et al., Gold nanoparticles reduce high glucose-induced oxidative-nitrosative stress regulated inflammation and apoptosis via tuberin-mTOR/NF-κB pathways in macrophages. International journal of nanomedicine, 2017. 12: p. 5841.
25. Chen, Y.-S., et al., Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale research letters, 2009. 4(8): p. 858.
26. Suh, K.S., et al., Gold nanoparticles attenuates antimycin A-induced mitochondrial dysfunction in MC3T3-E1 osteoblastic cells. Biological trace element research, 2013. 153(1-3): p. 428-436.
27. BarathManiKanth, S., et al., Anti-oxidant effect of gold nanoparticles restrains hyperglycemic conditions in diabetic mice. Journal of nanobiotechnology, 2010. 8(1): p. 16.
28. Hidalgo, I.J., T.J. Raub, and R.T. Borchardt, Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology, 1989. 96(3): p. 736-749.
29. Yao, M., et al., Uptake of gold nanoparticles by intestinal epithelial cells: impact of particle size on their absorption, accumulation, and toxicity. Journal of agricultural and food chemistry, 2015. 63(36): p. 8044-8049.
30. Bajak, E., et al., Changes in Caco-2 cells transcriptome profiles upon exposure to gold nanoparticles. Toxicology letters, 2015. 233(2): p. 187-199.
31. Aueviriyavit, S., D. Phummiratch, and R. Maniratanachote, Mechanistic study on the biological effects of silver and gold nanoparticles in Caco-2 cells–induction of the Nrf2/HO-1 pathway by high concentrations of silver nanoparticles. Toxicology letters, 2014. 224(1): p. 73-83.
32. Bastús, N.G., J. Comenge, and V. Puntes, Kinetically controlled seeded growth synthesis of citrate-stabilized gold nanoparticles of up to 200 nm: size focusing versus Ostwald ripening. Langmuir, 2011. 27(17): p. 11098-11105.
33. Morgan, D.M., Tetrazolium (MTT) assay for cellular viability and activity, in Polyamine protocols. 1998, Springer. p. 179-184.
34. Armstrong, D. and R. Browne, The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds related to oxidative stress as applied to the clinical chemistry laboratory, in Free radicals in diagnostic medicine. 1994, Springer. p. 43-58.
35. Rahman, I., A. Kode, and S.K. Biswas, Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature protocols, 2006. 1(6): p. 3159.
36. Ellman, G.L., et al., A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical pharmacology, 1961. 7(2): p. 88-95.
37. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 1976. 72(1-2): p. 248-254.
38. Sobti, R., A. Krishan, and C. Pfaffenberger, Cytokinetic and cytogenetic effects of some agricultural chemicals on human lymphoid cells in vitro: organophosphates. Mutation Research/Genetic Toxicology, 1982. 102(1): p. 89-102.
39. Rodgers, K.E., et al., In vitro effects of malathion and O, O, S-trimethyl phosphorothioate on cytotoxic T-lymphocyte responses. Pesticide Biochemistry and Physiology, 1985. 24(2): p. 260-266.
40. Chen, X.-y., et al., Involvement of apoptosis in malathion-induced cytotoxicity in a grass carp (Ctenopharyngodon idellus) cell line. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 2006. 142(1-2): p. 36-45.
41. Malik, J. and K. Summer, Toxicity and metabolism of malathion and its impurities in isolated rat hepatocytes: role of glutathione. Toxicology and applied pharmacology, 1982. 66(1): p. 69-76.
42. Karami-Mohajeri, S. and M. Abdollahi, Toxic influence of organophosphate, carbamate, and organochlorine pesticides on cellular metabolism of lipids, proteins, and carbohydrates: a systematic review. Human & experimental toxicology, 2011. 30(9): p. 1119-1140.
43. Isoda, H., et al., Effects of organophosphorous pesticides used in China on various mammalian cells. Environmental sciences: an international journal of environmental physiology and toxicology, 2005. 12(1): p. 9-19.
44. Krstić, D.Z., et al., Inhibition of AChE by malathion and some structurally similar compounds. Journal of enzyme inhibition and medicinal chemistry, 2008. 23(4): p. 562-573.
45. Sanvicens, N. and M.P. Marco, Multifunctional nanoparticles–properties and prospects for their use in human medicine. Trends in biotechnology, 2008. 26(8): p. 425-433.
46. Pan, Y., et al., Size‐dependent cytotoxicity of gold nanoparticles. Small, 2007. 3(11): p. 1941-1949.
47. Momić, T., et al., Adsorption of organophosphate pesticide dimethoate on gold nanospheres and nanorods. Journal of Nanomaterials, 2016. 2016.
48. Nair, A.S. and T. Pradeep, Extraction of chlorpyrifos and malathion from water by metal nanoparticles. Journal of nanoscience and nanotechnology, 2007. 7(6): p. 1871-1877.
49. Li, H., et al., Visual detection of organophosphorus pesticides represented by mathamidophos using Au nanoparticles as colorimetric probe. Talanta, 2011. 87: p. 93-99.
50. Yan, X., H. Li, and X. Su, Review of Optical Sensors for Pesticides. TrAC Trends in Analytical Chemistry, 2018.
51. Xia, N., Q. Wang, and L. Liu, Nanomaterials-based optical techniques for the detection of acetylcholinesterase and pesticides. Sensors, 2014. 15(1): p. 499-514.
52. Satnami, M.L., et al., Gold nanoprobe for inhibition and reactivation of acetylcholinesterase: An application to detection of organophosphorus pesticides. Sensors and Actuators B: Chemical, 2018. 267: p. 155-164.
53. Chiang, C.-W., A. Wang, and C.-Y. Mou, CO oxidation catalyzed by gold nanoparticles confined in mesoporous aluminosilicate Al-SBA-15: Pretreatment methods. Catalysis Today, 2006. 117(1-3): p. 220-227.
54. Yakimovich, N., et al., Antioxidant properties of gold nanoparticles studied by ESR spectroscopy. Russian Chemical Bulletin, 2008. 57(3): p. 520-523.
| Files | ||
| Issue | Vol 58, No 11 (2020) | |
| Section | Articles | |
| DOI | https://doi.org/10.18502/acta.v58i11.5141 | |
| Keywords | ||
| Gold nanoparticles oxidative stress acetylcholinesterase malathion Caco-2 cells cytotoxicity | ||
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How to Cite
1.
Shahmahmoodi Z, Jafarinejad S, Hormozi-Nezhad MR, Ghafari H, Ghazi khansari M. Protective Effects of Gold Nanoparticles Against Malathion-Induced Cytotoxicity in Caco-2 Cells. Acta Med Iran. 2021;58(11):552-561.
