Gallic Acid Protects from Acute Multiorgan Injury Induced by Lipopolysaccharide and D-galactosamine

Author(s): Samrat Rakshit, Satendra K. Nirala, Monika Bhadauria*

Journal Name: Current Pharmaceutical Biotechnology

Volume 21 , Issue 14 , 2020


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Graphical Abstract:


Abstract:

Background: Secondary metabolites of plants, the polyphenols, play a vital role in protection from many health problems in human beings. Structurally favored phytochemicals may be studied to protect multiorgan injury. At pharmacological doses, gallic acid is nontoxic to mammals and is generally absorbed in the intestine.

Aims: In this present study, gallic acid was evaluated for its protective efficacy against Lipo Polysaccharide (LPS) and d-Galactosamine (D-GalN) induced multiorgan injury, i.e., liver, kidney and brain.

Methods: Three different doses of gallic acid (5, 10 and 20 mg/kg p.o.) were administered to the experimental animals for 6 consecutive days, followed by exposure to LPS (50 μg/kg I.P.) and D-GalN (300 mg/kg I.P.) on the 6th day.

Results: Exposure to LPS and D-GalN resulted in increased oxidative stress and proinflammatory cytokines. Altered hematology and serology due to LPS and D-GalN were restored towards control by gallic acid. Declined antioxidants such as reduced glutathione, superoxide dismutase and catalase due to injurious effects of LPS and D-GalN were rejuvenated by gallic acid.

Discussion: Exposure to LPS and D-GalN severely increased lipid peroxidation, CYP2E1 activity and tissue lipids while lowered protein content. Gallic acid restored all these parameters towards control in dose dependent manner and 20 mg/kg dose provided the best protection. Histological study showed improved histoarchitecture of liver, kidney and brain that supported biochemical endpoints.

Conclusion: Gallic acid minimized oxidative stress and provided best protection at 20 mg/kg dose against LPS and D-GalN induced multi organ acute injury.

Keywords: Gallic acid, biochemical, lipopolysaccharide, D-galactosamine, antioxidant, multiorgan injury.

[1]
Wei, L.; Ren, F.; Zhang, X.; Wen, T.; Shi, H.; Zheng, S.; Zhang, J.; Chen, Y.; Han, Y.; Duan, Z. Oxidative stress promotes D-GalN/LPS-induced acute hepatotoxicity by increasing glycogen synthase kinase 3β activity. Inflamm. Res., 2014, 63(6), 485-494.
[http://dx.doi.org/10.1007/s00011-014-0720-x] [PMID: 24531650]
[2]
Krenkel, O.; Tacke, F. Liver macrophages in tissue homeostasis and disease. Nat. Rev. Immunol., 2017, 17(5), 306-321.
[http://dx.doi.org/10.1038/nri.2017.11] [PMID: 28317925]
[3]
Hadem, J.; Tacke, F.; Bruns, T.; Langgartner, J.; Strnad, P.; Denk, G.U.; Fikatas, P.; Manns, M.P.; Hofmann, W.P.; Gerken, G. Etiologies and outcomes of acute liver failure in Germany. J. Clin. Gastroenterol. Hepatol., 2012, 10, 664-669.e662
[4]
Lee, W.M. Acute liver failure. Semin. Respir. Crit. Care Med., 2012, 33(1), 36-45.
[http://dx.doi.org/10.1055/s-0032-1301733] [PMID: 22447259]
[5]
Lee, W.M. Acute liver failure. Am. J. Med., 1994, 96(1A), 3S-9S.
[http://dx.doi.org/10.1016/0002-9343(94)90183-X] [PMID: 8109586]
[6]
Rutherford, A.; Chung, R.T. Acute liver failure: Mechanisms of hepatocyte injury and regeneration. Semin. Liver Dis., 2008, 28(2), 167-174.
[http://dx.doi.org/10.1055/s-2008-1073116] [PMID: 18452116]
[7]
Tacke, F. Targeting hepatic macrophages to treat liver diseases. J. Hepatol., 2017, 66(6), 1300-1312.
[http://dx.doi.org/10.1016/j.jhep.2017.02.026] [PMID: 28267621]
[8]
Liu, H.; Zhang, W.; Dong, S.; Song, L.; Zhao, S.; Wu, C.; Wang, X.; Liu, F.; Xie, J.; Wang, J.; Wang, Y. Protective effects of sea buckthorn polysaccharide extracts against LPS/d-GalN-induced acute liver failure in mice via suppressing TLR4-NF-κB signaling. J. Ethnopharmacol., 2015, 176, 69-78.
[http://dx.doi.org/10.1016/j.jep.2015.10.029] [PMID: 26494508]
[9]
Cheng, Z.; Yue, L.; Zhao, W.; Yang, X.; Shu, G. Protective effects of protostemonine on LPS/GalN-induced acute liver failure: Roles of increased hepatic expression of heme oxygenase-1. Int. Immunopharmacol., 2015, 29(2), 798-807.
[http://dx.doi.org/10.1016/j.intimp.2015.08.039] [PMID: 26363973]
[10]
Lekić, N.; Cerný, D.; Hořínek, A.; Provazník, Z.; Martínek, J.; Farghali, H. Differential oxidative stress responses to D-galactosamine-lipopolysaccharide hepatotoxicity based on real time PCR analysis of selected oxidant/antioxidant and apoptotic gene expressions in rat. Physiol. Res., 2011, 60(3), 549-558.
[http://dx.doi.org/10.33549/physiolres.932041] [PMID: 21401295]
[11]
Karimi-Khouzani, O.; Heidarian, E.; Amini, S.A. Anti-inflammatory and ameliorative effects of gallic acid on fluoxetine-induced oxidative stress and liver damage in rats. Pharmacol. Rep., 2017, 69(4), 830-835.
[http://dx.doi.org/10.1016/j.pharep.2017.03.011] [PMID: 28599245]
[12]
Jia, Z.; Anandh Babu, P.V.; Chen, W. Sun, X. Natural products targeting on oxidative stress and inflammation: Mechanisms, therapies, and safety assessment. Oxid. Med. Cell. Longev., 2018, 2018, 1-3.
[13]
Shruthi, S.; Vijayalaxmi, K.; Shenoy, K.B. Immunomodulatory effects of gallic acid against cyclophosphamide-and cisplatin-induced immunosuppression in Swiss albino mice. Indian J. Pharm. Sci., 2018, 80, 150-160.
[http://dx.doi.org/10.4172/pharmaceutical-sciences.1000340]
[14]
Olusoji, M.; Oyeyemi, O.; Asenuga, E.; Omobowale, T.; Ajayi, O.; Oyagbemi, A. Protective effect of gallic acid on doxorubicin‐induced testicular and epididymal toxicity. Andrologia, 2017, 49e12635
[http://dx.doi.org/10.1111/and.12635]
[15]
Shruthi, S.; Bhasker Shenoy, K. Genoprotective effects of gallic acid against cisplatin induced genotoxicity in bone marrow cells of mice. Toxicol. Res. (Camb.), 2018, 7(5), 951-958.
[http://dx.doi.org/10.1039/C8TX00058A] [PMID: 30310672]
[16]
Ahmadvand, H.; Babaeenezhad, E.; Moradi, F.H.; Venool, A.C. Effect of gallic acid on liver oxidative stress markers in renal ischemia-reperfusion injury in rats. Ann. Res. Antioxidants, 2017, 2(2)
[17]
Rasool, M.K.; Sabina, E.P.; Ramya, S.R.; Preety, P.; Patel, S.; Mandal, N.; Mishra, P.P.; Samuel, J. Hepatoprotective and antioxidant effects of gallic acid in paracetamol-induced liver damage in mice. J. Pharm. Pharmacol., 2010, 62(5), 638-643.
[http://dx.doi.org/10.1211/jpp.62.05.0012] [PMID: 20609067]
[18]
Karamac, M.; Kosiñska, A.; Pegg, R.B. Content of gallic acid in selected plant extracts. Pol. J. Food Nutr. Sci., 2006, 15, 55.
[19]
Kosuru, R.Y.; Roy, A.; Das, S.K.; Bera, S. Gallic acid and gallates in human health and disease: Do mitochondria hold the key to success? Mol. Nutr. Food Res., 2018, 62(1)1700699
[http://dx.doi.org/10.1002/mnfr.201700699] [PMID: 29178387]
[20]
Nair, G.G.; Nair, C.K.K. Radioprotective effects of gallic acid in mice. BioMed Res. Int., 2013, 2013, 953079-953079.
[http://dx.doi.org/10.1155/2013/953079] [PMID: 24069607]
[21]
Daglia, M.; Di Lorenzo, A.; Nabavi, S.F.; Talas, Z.S.; Nabavi, S.M. Polyphenols: Well beyond the antioxidant capacity: Gallic acid and related compounds as neuroprotective agents: You are what you eat! Curr. Pharm. Biotechnol., 2014, 15(4), 362-372.
[http://dx.doi.org/10.2174/138920101504140825120737] [PMID: 24938889]
[22]
Yu, Z.; Song, F.; Jin, Y-C.; Zhang, W-M.; Zhang, Y.; Liu, E-J.; Zhou, D.; Bi, L-L.; Yang, Q.; Li, H.; Zhang, B-L.; Wang, S.W. Comparative pharmacokinetics of gallic acid after oral administration of gallic acid monohydrate in normal and isoproterenol-induced myocardial infarcted rats. Front. Pharmacol., 2018, 9, 328-328.
[http://dx.doi.org/10.3389/fphar.2018.00328] [PMID: 29681855]
[23]
Moschona, A.; Kyriakidis, K.D.; Kleontas, A.D. Comparative study of natural phenolic acids and flavonols as antiplatelet and anti-Inflammatory agents. Med. Sci., 2017, 2, 057-066.
[24]
Weng, Y-P.; Hung, P-F.; Ku, W-Y.; Chang, C-Y.; Wu, B-H.; Wu, M-H.; Yao, J-Y.; Yang, J-R.; Lee, C-H. The inhibitory activity of gallic acid against DNA methylation: Application of gallic acid on epigenetic therapy of human cancers. Oncotarget, 2018, 9(1), 361-374.
[25]
Mansouri, M.T.; Farbood, Y.; Sameri, M.J.; Sarkaki, A.; Naghizadeh, B.; Rafeirad, M. Neuroprotective effects of oral gallic acid against oxidative stress induced by 6-hydroxydopamine in rats. Food Chem., 2013, 138(2-3), 1028-1033.
[http://dx.doi.org/10.1016/j.foodchem.2012.11.022] [PMID: 23411210]
[26]
Reckziegel, P.; Dias, V.T.; Benvegnú, D.M.; Boufleur, N.; Barcelos, R.C.S.; Segat, H.J.; Pase, C.S.; Dos Santos, C.M.M.; Flores, É.M.M.; Bürger, M.E. Antioxidant protection of gallic acid against toxicity induced by Pb in blood, liver and kidney of rats. Toxicol. Rep., 2016, 3, 351-356.
[http://dx.doi.org/10.1016/j.toxrep.2016.02.005] [PMID: 28959556]
[27]
Dhingra, M.S.; Dhingra, S.; Kumria, R.; Chadha, R.; Singh, T.; Kumar, A.; Karan, M. Effect of trimethylgallic acid esters against chronic stress-induced anxiety-like behavior and oxidative stress in mice. Pharmacol. Rep., 2014, 66(4), 606-612.
[http://dx.doi.org/10.1016/j.pharep.2014.01.004] [PMID: 24948061]
[28]
Chhillar, R.; Dhingra, D. Antidepressant-like activity of gallic acid in mice subjected to unpredictable chronic mild stress. Fundam. Clin. Pharmacol., 2013, 27(4), 409-418.
[http://dx.doi.org/10.1111/j.1472-8206.2012.01040.x] [PMID: 22458864]
[29]
Nayeem, N.; Asdaq, S.; Salem, H. AHEl-Alfqy, S. Gallic acid: A promising lead molecule for drug development. J. Appl. Pharm., 2016, 8, 1-4.
[http://dx.doi.org/10.4172/1920-4159.1000213]
[30]
Sen, S.; Asokkumar, K.; Umamaheswari, M.; Sivashanmugam, A. Antiulcerogenic effect of gallic acid in rats and its effect on oxidant and antioxidant parameters in stomach tissue. Indian J. Pharm. Sci., 2013, 75(2), 149-155.
[31]
Choubey, S.; Varughese, L.R.; Kumar, V.; Beniwal, V. Medicinal importance of gallic acid and its ester derivatives: A patent review. Pharm. Pat. Anal., 2015, 4(4), 305-315.
[http://dx.doi.org/10.4155/ppa.15.14] [PMID: 26174568]
[32]
Mard, S.A.; Mojadami, S.; Farbood, Y.; Gharib Naseri, M.K. The anti-inflammatory and anti-apoptotic effects of gallic acid against mucosal inflammation- and erosions-induced by gastric ischemia-reperfusion in rats. Vet. Res. Forum, 2015, 6(4), 305-311.
[PMID: 26973766]
[33]
Banerjee, D.; Maity, B.; Nag, S.K.; Bandyopadhyay, S.K.; Chattopadhyay, S. Healing potential of Picrorhiza kurroa (Scrofulariaceae) rhizomes against indomethacin-induced gastric ulceration: A mechanistic exploration. BMC Complement. Altern. Med., 2008, 8, 3-3.
[http://dx.doi.org/10.1186/1472-6882-8-3] [PMID: 18237397]
[34]
Jin, Q.; Jiang, S.; Wu, Y-L.; Bai, T.; Yang, Y.; Jin, X.; Lian, L-H.; Nan, J.X. Hepatoprotective effect of cryptotanshinone from Salvia miltiorrhiza in D-galactosamine/lipopolysaccharide-induced fulminant hepatic failure. Phytomedicine, 2014, 21(2), 141-147.
[http://dx.doi.org/10.1016/j.phymed.2013.07.016] [PMID: 24011530]
[35]
Sharma, S.K.; Krishna Murti, C.R. . Production of lipid peroxides by brain. J. Neurochem., 1968, 15(2), 147-149.
[http://dx.doi.org/10.1111/j.1471-4159.1968.tb06187.x] [PMID: 5637724]
[36]
Brehe, J.E.; Burch, H.B. Enzymatic assay for glutathione. Anal. Biochem., 1976, 74(1), 189-197.
[http://dx.doi.org/10.1016/0003-2697(76)90323-7] [PMID: 962073]
[37]
Misra, H.P.; Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem., 1972, 247(10), 3170-3175.
[PMID: 4623845]
[38]
Aebi, H. Catalase in vitro. Methods Enzymol., 1984, 105, 121-126.
[http://dx.doi.org/10.1016/S0076-6879(84)05016-3] [PMID: 6727660]
[39]
Schenkman, J.B.; Cinti, D.L. Preparation of microsomes with calcium. Methods Enzymol., 1978, 52, 83-89.
[http://dx.doi.org/10.1016/S0076-6879(78)52008-9] [PMID: 672658]
[40]
Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[PMID: 14907713]
[41]
Kato, R.; Gillette, J.R. Effect of starvation on NADPH-dependent enzymes in liver microsomes of male and female rats. J. Pharmacol. Experiment. Therapeut., 1965, 150(2), 279-284.
[42]
Neri, B.P.; Frings, C.S. Improved method for determination of triglycerides in serum. Clin. Chem., 1973, 19(10), 1201-1202.
[http://dx.doi.org/10.1093/clinchem/19.10.1201] [PMID: 4355041]
[43]
Zlatkis, A.; Zak, B.; Boyle, A.J. A new method for the direct determination of serum cholesterol. J. Lab. Clin. Med., 1953, 41(3), 486-492.
[PMID: 13035283]
[44]
Suvarna, K.S.; Layton, C.; Bancroft, J.D. Bancroft’s theory and practice of histological techniques; Elsevier Health Sciences, 2018.
[45]
Snedecor, G. Cochran statistical methods; Iowa State University Press: Ames, Iowa, 1994.
[46]
Pisoschi, A.M.; Pop, A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem., 2015, 97, 55-74.
[http://dx.doi.org/10.1016/j.ejmech.2015.04.040] [PMID: 25942353]
[47]
Galato, D.; Ckless, K.; Susin, M.F.; Giacomelli, C.; Ribeiro-do-Valle, R.M.; Spinelli, A. Antioxidant capacity of phenolic and related compounds: Correlation among electrochemical, visible spectroscopy methods and structure-antioxidant activity. Redox Rep., 2001, 6(4), 243-250.
[http://dx.doi.org/10.1179/135100001101536391] [PMID: 11642715]
[48]
Badhani, B.; Sharma, N.; Kakkar, R. Gallic acid: A versatile antioxidant with promising therapeutic and industrial applications. RSC Advances, 2015, 5, 27540-27557.
[http://dx.doi.org/10.1039/C5RA01911G]
[49]
Lu, Z.; Nie, G.; Belton, P.S.; Tang, H.; Zhao, B. Structure-activity relationship analysis of antioxidant ability and neuroprotective effect of gallic acid derivatives. Neurochem. Int., 2006, 48(4), 263-274.
[http://dx.doi.org/10.1016/j.neuint.2005.10.010] [PMID: 16343693]
[50]
De Oliveira, J.R.; Rosa, J.L.; Ambrosio, S.; Bartrons, R. Effect of galactosamine on hepatic carbohydrate metabolism: Protective role of fructose 1,6-bisphosphate. Hepatology, 1992, 15(6), 1147-1153.
[http://dx.doi.org/10.1002/hep.1840150628] [PMID: 1317340]
[51]
Stachlewitz, R.F.; Seabra, V.; Bradford, B.; Bradham, C.A.; Rusyn, I.; Germolec, D.; Thurman, R.G. Glycine and uridine prevent D-galactosamine hepatotoxicity in the rat: Role of Kupffer cells. Hepatology, 1999, 29(3), 737-745.
[http://dx.doi.org/10.1002/hep.510290335] [PMID: 10051475]
[52]
Masubuchi, Y.; Horie, T. Endotoxin-mediated disturbance of hepatic cytochrome P450 function and development of endotoxin tolerance in the rat model of dextran sulfate sodium-induced experimental colitis. Drug Metab. Dispos., 2004, 32(4), 437-441.
[http://dx.doi.org/10.1124/dmd.32.4.437] [PMID: 15039297]
[53]
Mészáros, K.; Antoni, F.; Mandl, J.; Hrabák, A.; Garzó, T. Effects of D-galactosamine on nucleotide metabolism and on microsomal membranes in mouse liver. FEBS Lett., 1974, 44(2), 141-145.
[http://dx.doi.org/10.1016/0014-5793(74)80712-X] [PMID: 4418742]
[54]
Jabaut, J.; Ckless, K. Inflammation, immunity and redox signaling. Inflammation, immunity and redox signaling. Inflammation, Chronic Diseases and Cancer-Cell and Molecular Biology, Immunology and Clinical Bases; IntechOpen, 2012.
[http://dx.doi.org/10.5772/27242]
[55]
Suliman, H.B.; Carraway, M.S.; Piantadosi, C.A. Postlipopolysaccharide oxidative damage of mitochondrial DNA. Am. J. Respir. Crit. Care Med., 2003, 167(4), 570-579.
[http://dx.doi.org/10.1164/rccm.200206-518OC] [PMID: 12480607]
[56]
Khatsenko, O.G.; Gross, S.S.; Rifkind, A.B.; Vane, J.R. Nitric oxide is a mediator of the decrease in cytochrome P450-dependent metabolism caused by immunostimulants. Proc. Natl. Acad. Sci. USA, 1993, 90(23), 11147-11151.
[http://dx.doi.org/10.1073/pnas.90.23.11147] [PMID: 7504296]
[57]
Kallapura, G.; Pumford, N.R.; Hernandez-Velasco, X.; Hargisand, B.; Tellez, G. Mechanisms involved in lipopolysaccharide derived ROS and RNS oxidative stress and septic shock. J. Microbiol. Res. Rev., 2014, 2, 6-11.
[58]
Konrad, F.M.; Knausberg, U.; Höne, R.; Ngamsri, K.C.; Reutershan, J. Tissue heme oxygenase-1 exerts anti-inflammatory effects on LPS-induced pulmonary inflammation. Mucosal Immunol., 2016, 9(1), 98-111.
[http://dx.doi.org/10.1038/mi.2015.39] [PMID: 25943274]
[59]
Ganeshpurkar, A.; Saluja, A.K. The pharmacological potential of rutin. Saudi Pharm. J., 2017, 25(2), 149-164.
[http://dx.doi.org/10.1016/j.jsps.2016.04.025] [PMID: 28344465]
[60]
Khan, R.A.; Khan, M.R.; Sahreen, S. CCl4-induced hepatotoxicity: Protective effect of rutin on p53, CYP2E1 and the antioxidative status in rat. BMC Complement. Altern. Med., 2012, 12, 178.
[http://dx.doi.org/10.1186/1472-6882-12-178] [PMID: 23043521]
[61]
Ola-Davies, O.; Azeez, O.J. Phytochemistry. Modulatory effects of gallic acid on sodium fluoride induced nephrotoxicity in the wistar rats. J. Pharmacog. Phytochem., 2018, 7, 1561-1570.
[62]
Olayinka, E.T.; Ore, A.; Ola, O.S.; Adeyemo, O.A. Ameliorative Effect of gallic acid on cyclophosphamide-induced oxidative injury and hepatic dysfunction in rats. Med. Sci. (Basel), 2015, 3(3), 78-92.
[http://dx.doi.org/10.3390/medsci3030078] [PMID: 29083393]
[63]
Shergojri, F.A.; Bhat, B.A.; Gaur, M. Amelioration of cisplatin induced hepatotoxicity in swiss albino mice by gallic acid. Int. J. Engin. Technol. Sci. Res., 2017, 4, 547-554.
[64]
Shergojri, F.A.; Bhat, B.A.; Gaur, M. Amelioration of cisplatin induced hepatotoxicity in swiss albino mice by gallic acid. Int. J. Eng. Tech. Sci. Res., 2017, 4(12), 547-554.
[65]
Vijaya Padma, V.; Sowmya, P.; Arun Felix, T.; Baskaran, R.; Poornima, P. Protective effect of gallic acid against lindane induced toxicity in experimental rats. Food Chem. Toxicol., 2011, 49(4), 991-998.
[http://dx.doi.org/10.1016/j.fct.2011.01.005] [PMID: 21219962]
[66]
Perazzoli, M.R.A.; Perondi, C.K.; Baratto, C.M.; Winter, E.; Creczynski-Pasa, T.B.; Locatelli, C. Gallic acid and dodecyl gallate prevents carbon tetrachloride-induced acute and chronic hepatotoxicity by enhancing hepatic antioxidant status and increasing p53 expression. Biol. Pharm. Bull., 2017, 40(4), 425-434.
[http://dx.doi.org/10.1248/bpb.b16-00782] [PMID: 28381798]
[67]
Sheriff, S.A.; Devaki, T. Lycopene stabilizes liver function during D-galactosamine/lipopolysaccharide induced hepatitis in rats. J. Taibah Uni. Sci., 2013, 7, 8-16.
[http://dx.doi.org/10.1016/j.jtusci.2013.01.002]
[68]
Ansar, S.; Hamed, S.; AlGhosoon, H.; AlSaedan, R.; Iqbal, M. The protective effect of rutin against renal toxicity induced by lead acetate. Toxin Rev., 2016, 35, 58-62.
[http://dx.doi.org/10.3109/15569543.2016.1155623]
[69]
Manabe, S.; Kurroda, I.; Okada, K.; Morishima, M.; Okamoto, M.; Harada, N.; Takahashi, A.; Sakai, K.; Nakaya, Y. Decreased blood levels of lactic acid and urinary excretion of 3-methylhistidine after exercise by chronic taurine treatment in rats. J. Nutr. Sci. Vitaminol. (Tokyo), 2003, 49(6), 375-380.
[http://dx.doi.org/10.3177/jnsv.49.375] [PMID: 14974726]
[70]
Hsu, C.Y.; Shih, H.Y.; Chia, Y.C.; Lee, C.H.; Ashida, H.; Lai, Y.K.; Weng, C.F. Rutin potentiates insulin receptor kinase to enhance insulin-dependent glucose transporter 4 translocation. Mol. Nutr. Food Res., 2014, 58(6), 1168-1176.
[http://dx.doi.org/10.1002/mnfr.201300691] [PMID: 24668568]
[71]
Kojima, M.; Masui, T.; Nemoto, K.; Degawa, M. Lead nitrate-induced development of hypercholesterolemia in rats: Sterol-independent gene regulation of hepatic enzymes responsible for cholesterol homeostasis. Toxicol. Lett., 2004, 154(1-2), 35-44.
[http://dx.doi.org/10.1016/j.toxlet.2004.06.010] [PMID: 15475176]
[72]
George, J.N.; Raskob, G.E.; Shah, S.R.; Rizvi, M.A.; Hamilton, S.A.; Osborne, S.; Vondracek, T. Drug-induced thrombocytopenia: a systematic review of published case reports. Ann. Intern. Med., 1998, 129(11), 886-890.
[http://dx.doi.org/10.7326/0003-4819-129-11_Part_1-199812010-00009] [PMID: 9867731]
[73]
Abbasi, M.H.; Akhtar, T.; Malik, I.A.; Fatima, S.; Khawar, B.; Mujeeb, K.A.; Mustafa, G.; Hussain, S.; Iqbal, J.; Sheikh, N. Acute and chronic toxicity of thioacteamide and alterations in blood cell indices in rats. J. Cancer Ther., 2013, 4, 251.
[http://dx.doi.org/10.4236/jct.2013.41032]
[74]
Sun, J.; Li, Y-Z.; Ding, Y-H.; Wang, J.; Geng, J.; Yang, H.; Ren, J.; Tang, J-Y. Neuroprotective effects of gallic acid against hypoxia/reoxygenation-induced mitochondrial dysfunctions in vitro and cerebral ischemia/reperfusion injury in vivo. Brain Res., 2014, 1589, 126-139.
[75]
Travlos, G.S.; Morris, R.W.; Elwell, M.R.; Duke, A.; Rosenblum, S.; Thompson, M.B. Frequency and relationships of clinical chemistry and liver and kidney histopathology findings in 13-week toxicity studies in rats. Toxicology, 1996, 107(1), 17-29.
[http://dx.doi.org/10.1016/0300-483X(95)03197-N] [PMID: 8597028]
[76]
Ola-Davies, O.; Azeez, O. Modulatory effects of gallic acid on sodium fluoride induced nephrotoxicity in the wistar rats. J. Pharmacog. Phytochem., 2018, 7, 1561-1570.
[77]
Bhadauria, M. Combined treatment of HEDTA and propolis prevents aluminum induced toxicity in rats. Food Chem. Toxicol., 2012, 50(7), 2487-2495.
[http://dx.doi.org/10.1016/j.fct.2011.12.040] [PMID: 22251571]
[78]
Severino, J.F.; Goodman, B.A.; Kay, C.W.; Stolze, K.; Tunega, D.; Reichenauer, T.G.; Pirker, K.F. Free radicals generated during oxidation of green tea polyphenols: electron paramagnetic resonance spectroscopy combined with density functional theory calculations., Free Radic. Biol. Med., 2009, 46(8), 1076-1088.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.01.004] [PMID: 19439236]
[79]
Eslami, A.C.; Pasanphan, W.; Wagner, B.A.; Buettner, G.R. Free radicals produced by the oxidation of gallic acid: An electron paramagnetic resonance study. Chem. Cent. J., 2010, 4, 15.
[http://dx.doi.org/10.1186/1752-153X-4-15] [PMID: 20687941]
[80]
Brune, M.; Rossander, L.; Hallberg, L. Iron absorption and phenolic compounds: Importance of different phenolic structures. Eur. J. Clin. Nutr., 1989, 43(8), 547-557.
[PMID: 2598894]
[81]
Glahn, D.C.; Kim, J.; Cohen, M.S.; Poutanen, V.P.; Therman, S.; Bava, S.; Van Erp, T.G.; Manninen, M.; Huttunen, M.; Lönnqvist, J.; Standertskjöld-Nordenstam, C.G.; Cannon, T.D. Maintenance and manipulation in spatial working memory: Dissociations in the prefrontal cortex. Neuroimage, 2002, 17(1), 201-213.
[http://dx.doi.org/10.1006/nimg.2002.1161] [PMID: 12482077]
[82]
Welch, R.M.; Graham, R.D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot., 2004, 55(396), 353-364.
[http://dx.doi.org/10.1093/jxb/erh064] [PMID: 14739261]
[83]
Hart, J.J.; Glahn, R. Identification of bean polyphenols that inhibit and enhance iron uptake by Caco-2 cells. J. Agric. Food Chem., 2015, 63(25), 5950-5956.
[84]
Nabavi, S.F.; Nabavi, S.M.; Habtemariam, S.; Moghaddam, A.H.; Sureda, A.; Jafari, M.; Latifi, A.M. Hepatoprotective effect of gallic acid isolated from Peltiphyllum peltatum against sodium fluoride-induced oxidative stress. Ind. Crops Prod., 2013, 44, 50-55.
[85]
Reed, J.D. Nutritional toxicology of tannins and related polyphenols in forage legumes. J. Anim. Sci., 1995, 73(5), 1516-1528.
[http://dx.doi.org/10.2527/1995.7351516x] [PMID: 7665384]
[86]
Omobowale, T.O.; Oyagbemi, A.A.; Ajufo, U.E.; Adejumobi, O.A.; Ola-Davies, O.E.; Adedapo, A.A.; Yakubu, M.A. Ameliorative effect of gallic acid in doxorubicin-induced hepatotoxicity in wistar rats through antioxidant defense system. J. Diet. Suppl., 2018, 15(2), 183-196.
[http://dx.doi.org/10.1080/19390211.2017.1335822] [PMID: 28718673]
[87]
Scalzo, R.l. Measurement of free radical scavenging activity of gallic acid and unusual antioxidants as sugars and hydroxyacids. Elect. J. Environ. Agricult. Food Chem., 2010, 9(8), 1360-1371.
[88]
Kessova, I.; Cederbaum, A.I. CYP2E1: Biochemistry, toxicology, regulation and function in ethanol-induced liver injury. Curr. Mol. Med., 2003, 3(6), 509-518.
[http://dx.doi.org/10.2174/1566524033479609] [PMID: 14527082]
[89]
Padma, V.V.; Sowmya, P.; Felix, T.A.; Baskaran, R. Protective effect of gallic acid against lindane induced toxicity in experimental rats. Food Chem. Toxicol., 2011, 49, 991-998.
[90]
Chaurasia, S.S.; Kar, A. Protective effects of vitamin E against lead-induced deterioration of membrane associated type-I iodothyronine 5′-monodeiodinase (5'D-I) activity in male mice. Toxicology, 1997, 124(3), 203-209.
[http://dx.doi.org/10.1016/S0300-483X(97)00155-8] [PMID: 9482122]
[91]
Reckziegel, P.; Dias, V.T.; Benvegnú, D.; Boufleur, N.; Silva Barcelos, R.C.; Segat, H.J.; Pase, C.S.; Dos Santos, C.M.M.; Flores, É.M.M.; Bürger, M.E. Locomotor damage and brain oxidative stress induced by lead exposure are attenuated by gallic acid treatment. Toxicol. Lett., 2011, 203(1), 74-81.
[http://dx.doi.org/10.1016/j.toxlet.2011.03.006] [PMID: 21402136]
[92]
Depboylu, B.; Giriş, M.; Olgaç, V.; Doğru-Abbasoğlu, S.; Uysal, M. Response of liver to lipopolysaccharide treatment in male and female rats. Exp. Toxicol. Pathol., 2013, 65(5), 645-650.
[http://dx.doi.org/10.1016/j.etp.2012.07.004] [PMID: 22884257]


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VOLUME: 21
ISSUE: 14
Year: 2020
Page: [1489 - 1504]
Pages: 16
DOI: 10.2174/1389201021666200615165732
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