Evaluation of Protective Effects of Curcumin and Nanocurcumin on Aluminium Phosphide‑Induced Subacute Lung Injury in Rats: Modulation of Oxidative Stress through SIRT1/FOXO3 Signalling Pathway

Abstract

Objective Aluminum phosphide (AlP) is widely used to protect stored food products and grains from pests and rodents. The availability of AlP, especially in Asian countries it has become a desirable factor to commit suicide. The phosphine produced from ALP is a very reactive radical and a respiratory inhibitor that causes oxidative damage. There is no dedicated antidote or effective drug to manage AlP-induced lung toxicity. The present study aims to evaluate and compare the protective effects of curcumin and nanocurcumin on ALP‑induced subacute lung injury and determine the underlying mechanism.

Methods Rats were exposed to AlP (2 mg/kg/day, orally)+curcumin or nanocurcumin (100 mg/kg/day, orally) for 7 days. Then rats were anesthetized and lung tissues were collected. Oxidative stress biomarkers, genes expression of antioxidant enzymes, participated genes in the SIRT1/FOXO3 pathway, and lung histopathology were assessed by biochemical and ELISA methods, Real-Time PCR analysis, and H&E staining.

Results Curcumin and nanocurcumin produced a remarkable improvement in AlP-induced lung damage through reduction of MDA, induction of antioxidant capacity (TAC, TTG) and antioxidant enzymes (CAT, GPx), modulation of histopathological changes, and up-regulation of genes expression of SIRT1, FOXO3, FOXO1 in lung tissue.

Conclusion Nanocurcumin had a significantly more protective effect than curcumin to prevent AlP-induced lung injury via inhibition of oxidative stress. Nanocurcumin could be considered a suitable therapeutic choice for AlP poisoning.

Key words

Aluminum phosphide - curcumin - nanocurcumin - lung, oxidative stress

Publikationsverlauf

Eingereicht: 10. August 2021

Angenommen: 14. September 2021

Artikel online veröffentlicht:
06. Oktober 2021

• References

• 1 Bumbrah GS, Krishan K, Kanchan T. et al. Phosphide poisoning: a review of literature. Forensic Sci Int 2012; 214: 1-6
• 2 Shakeri S, Mehrpour O. Aluminum phosphide poisoning in animals. Int J Med Toxicol Forensic Med 2014; 5: 81-97
• 3 Hashemi-Domeneh B, Zamani N, Hassanian-Moghaddam H. et al. A review of aluminium phosphide poisoning and a flowchart to treat it. Arh Hig Rada Toksikol 2016; 67: 183-193
• 4 Shadnia S, Sasanian G, Allami P. et al. A retrospective 7-years study of aluminum phosphide poisoning in Tehran: opportunities for prevention. Hum Exp Toxicol 2009; 28: 209-213
• 5 Sciuto AM, Wong BJ, Martens ME. et al. Phosphine toxicity: a story of disrupted mitochondrial metabolism. Ann N Y Acad Sci 2016; 1374: 41-51
• 6 Hsu CH, Quistad GB, Casida JE. Phosphine-induced oxidative stress in Hepa 1c1c7 cells. Toxicol Sci 1998; 46: 204-210
• 7 Abdolghaffari AH, Baghaei A, Solgi R. et al. Molecular and biochemical evidences on the protective effects of triiodothyronine against phosphine-induced cardiac and mitochondrial toxicity. Life Sci 2015; 139: 30-39
• 8 Sharifzadeh M, Ranjbar A, Hosseini A. et al. The Effect of Green Tea Extract on Oxidative Stress and Spatial Learning in Streptozotocin-diabetic Rats. Iran J Pharm Res 2017; 16: 201-209
• 9 Alizadeh-Fanalou S, Babaei M, Hosseini A. et al. Effects of Securigera Securidaca seed extract in combination with glibenclamide on antioxidant capacity, fibroblast growth factor 21 and insulin resistance in hyperglycemic rats. J Ethnopharmacol 2020; 248: 112331
• 10 Zhang W, Huang Q, Zeng Z. et al. Sirt1 Inhibits Oxidative Stress in Vascular Endothelial Cells. Oxid Med Cell Longev 2017; 2017: 7543973
• 11 Flora G, Gupta D, Tiwari A. Nanocurcumin: a promising therapeutic advancement over native curcumin. Crit Rev Ther Drug Carrier Syst 2013; 30: 331-368
• 12 Zeng Y, Liu J, Huang Z. et al. [Effect of curcumin on antioxidant function in the mice with acute alcoholic liver injury]. Wei Sheng Yan Jiu 2014; 43: 282-285
• 13 Sevastre-Berghian AC, Făgărăsan V, Toma VA. et al. Curcumin reverses the diazepam-induced cognitive impairment by modulation of oxidative stress and ERK 1/2/NF-κB pathway in brain. Oxid Med Cell Longev. 2017 2017.
• 14 Cai J, Xu D, Bai X. et al. Curcumin mitigates cerebral vasospasm and early brain injury following subarachnoid hemorrhage via inhibiting cerebral inflammation. Brain Behav 2017; 7: e00790
• 15 Huang N, Lu S, Liu X-G. et al. PLGA nanoparticles modified with a BBB-penetrating peptide co-delivering Aβ generation inhibitor and curcumin attenuate memory deficits and neuropathology in Alzheimer’s disease mice. Oncotarget 2017; 8: 81001
• 16 Wang Y, Hu PC, Gao FF. et al. The protective effect of curcumin on hepatotoxicity and ultrastructural damage induced by cisplatin. Ultrastruct Pathol 2014; 38: 358-362
• 17 Lee JC, Kinniry PA, Arguiri E. et al. Dietary curcumin increases antioxidant defenses in lung, ameliorates radiation-induced pulmonary fibrosis, and improves survival in mice. Radiat Res 2010; 173: 590-601
• 18 Xiao X, Yang M, Sun D. et al. Curcumin protects against sepsis-induced acute lung injury in rats. J Surg Res 2012; 176: e31-e39
• 19 Tyagi N, Kumari A, Dash D. et al. Protective effects of intranasal curcumin on paraquot induced acute lung injury (ALI) in mice. Environ Toxicol Pharmacol 2014; 38: 913-921
• 20 Xu F, Diao R, Liu J. et al. Curcumin attenuates staphylococcus aureus-induced acute lung injury. Clin Respir J 2015; 9: 87-97
• 21 Hosseini A, Rasaie D, Soleymani Asl S. et al. Evaluation of the protective effects of curcumin and nanocurcumin against lung injury induced by sub-acute exposure to paraquat in rats. Toxin Reviews 2019; 1-9
• 22 Hussain Z, Thu HE, Amjad MW. et al. Exploring recent developments to improve antioxidant, anti-inflammatory and antimicrobial efficacy of curcumin: A review of new trends and future perspectives. Mater Sci Eng C Mater Biol Appl 2017; 77: 1316-1326
• 23 Karthikeyan A, Senthil N, Min T. Nanocurcumin: A Promising Candidate for Therapeutic Applications. Front Pharmacol 2020; 11: 487
• 24 Khosropanah MH, Dinarvand A, Nezhadhosseini A. et al. Analysis of the antiproliferative effects of curcumin and nanocurcumin in MDA-MB231 as a breast cancer cell line. Iranian journal of pharmaceutical research: IJPR 2016; 15: 231
• 25 Dende C, Meena J, Nagarajan P. et al. Nanocurcumin is superior to native curcumin in preventing degenerative changes in Experimental Cerebral Malaria. Scientific reports 2017; 7: 1-12
• 26 Benzie IF, Strain J. [2] Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods in Enzymology. Vol. 299. Elsevier; 1999. p 15-27
• 27 Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-358
• 28 Rao B, Simpson C, Lin H. et al. Determination of thiol functional groups on bacteria and natural organic matter in environmental systems. Talanta 2014; 119: 240-247
• 29 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. methods 2001; 25: 402-408.
• 30 Kariman H, Heydari K, Fakhri M. et al. Aluminium phosphide poisoning and oxidative stress: serum biomarker assessment. J Med Toxicol 2012; 8: 281-284
• 31 Anand R, Sharma DR, Verma D. et al. Mitochondrial electron transport chain complexes, catalase and markers of oxidative stress in platelets of patients with severe aluminum phosphide poisoning. Hum Exp Toxicol 2013; 32: 807-816
• 32 Maleki A, Hosseini MJ, Rahimi N. et al. Adjuvant potential of selegiline in treating acute toxicity of aluminium phosphide in rats. Basic Clin Pharmacol Toxicol 2019; 125: 62-74
• 33 Ibrahim RM, Abd Elaal FEZA, Zaki S. Effect of Curcumin and Nano-curcumin on Reduce Aluminum Toxicity in Rats. Int J Food Sci Bioechnol 2019; 4: 64
• 34 Naksuriya O, Okonogi S, Schiffelers RM. et al. Curcumin nanoformulations: a review of pharmaceutical properties and preclinical studies and clinical data related to cancer treatment. Biomaterials 2014; 35: 3365-3383
• 35 Zhang Z-y, Jiang M, Fang J. et al. Enhanced therapeutic potential of nano-curcumin against subarachnoid hemorrhage-induced blood–brain barrier disruption through inhibition of inflammatory response and oxidative stress. Molecular neurobiology 2017; 54: 1-14
• 36 Zhang F, Li ZL, Xu XM. et al. Protective effects of icariin-mediated SIRT1/FOXO3 signaling pathway on intestinal ischemia/reperfusion-induced acute lung injury. Mol Med Rep 2015; 11: 269-276
• 37 Li Z, Zhang L, Wang H. Curcumin inhibits lung cancer progression and metastasis through induction of FOXO1 (Retraction of Vol 35, Pg 111, 2014). Sage Publications LTD 1 Olivers Yard; 55 City Road, London EC1Y 1SP, England: 2017
• 38 Yang Y, Duan W, Lin Y. et al. SIRT1 activation by curcumin pretreatment attenuates mitochondrial oxidative damage induced by myocardial ischemia reperfusion injury. Free Radic Biol Med 2013; 65: 667-679
• 39 Sun Q, Jia N, Wang W. et al. Activation of SIRT1 by curcumin blocks the neurotoxicity of amyloid-β25–35 in rat cortical neurons. Biochemical and Biophysical Research Communications 2014; 448: 89-94
• 40 Sun Y, Hu X, Hu G. et al. Curcumin Attenuates Hydrogen Peroxide-Induced Premature Senescence via the Activation of SIRT1 in Human Umbilical Vein Endothelial Cells. Biol Pharm Bull 2015; 38: 1134-1141
• 41 Iside C, Scafuro M, Nebbioso A. et al. SIRT1 Activation by Natural Phytochemicals: An Overview. Front Pharmacol 2020; 11: 1225
• 42 Wang M, Jiang S, Zhou L. et al. Potential Mechanisms of Action of Curcumin for Cancer Prevention: Focus on Cellular Signaling Pathways and miRNAs. Int J Biol Sci 2019; 15: 1200-1214
• 43 Tyagi N, Dash D, Singh R. Curcumin inhibits paraquat induced lung inflammation and fibrosis by extracellular matrix modifications in mouse model. Inflammopharmacology 2016; 24: 335-345
• 44 Saghir SA, Alharbi SA, Al-Garadi MA. et al. Curcumin Prevents Cyclophosphamide-Induced Lung Injury in Rats by Suppressing Oxidative Stress and Apoptosis. Processes 2020; 8: 127
• 45 Punithavathi D, Venkatesan N, Babu M. Curcumin inhibition of bleomycin-induced pulmonary fibrosis in rats. Br J Pharmacol 2000; 131: 169-172
• 46 Smith MR, Gangireddy SR, Narala VR. et al. Curcumin inhibits fibrosis-related effects in IPF fibroblasts and in mice following bleomycin-induced lung injury. Am J Physiol Lung Cell Mol Physiol 2010; 298: L616-L625
• 47 Zhang D, Huang C, Yang C. et al. Antifibrotic effects of curcumin are associated with overexpression of cathepsins K and L in bleomycin treated mice and human fibroblasts. Respir Res 2011; 12: 154
• 48 Ranjbar A, Gholami L, Ghasemi H. et al. EEffects of nano-curcumin and curcumin on the oxidant and antioxidant system of the liver mitochondria in aluminum phosphide-induced experimental toxicity. Nanomedicine Journal 2020; 7: 58-64