Bio-Antioxidants Protect the Buffalo Bone Marrow Derived Mesenchymal Stem Cells against Oxidative Stress Induced During Freeze-Thaw Cycle


Affiliations

  • College of Veterinary Science, Guru Angad Dev Veterinary and Animal Sciences University, Department of Veterinary Physiology and Biochemistry, Ludhiana, Punjab, 141001, India
  • Guru Angad Dev Veterinary and Animal Sciences University, Department of Veterinary Pharmacology and Toxicology, Ludhiana, Punjab, 141001, India
  • Guru Angad Dev Veterinary and Animal Sciences University, Department of Veterinary Surgery and Radiology, Ludhiana, Punjab, 141001, India

Abstract

The present investigation was planned to evaluate the effect of curcumin (CUR) and resveratrol (RES) on oxidative stress indicators (LPO, O2- radical, ROS and TPC), antioxidant status (GSH, GPx, SOD, CAT and GST) and cytotoxicity markers (ALP, LDH, GGT and CK-MB) in mesenchymal stem cells (MSCs) derived from buffalo bone marrow during the freeze-thaw cycle of one month. MSCs were isolated and cultured in high glucose DMEM supplemented with 15% FBS. MSCs were found to be positive for alkaline phosphatase (AP) activity and stem cell markers (CD73 and OCT4). Results revealed a significant reduction in (p≤0.05) in oxidative stress parameters and cytotoxicity markers, while, the levels of cellular antioxidants were found to be significantly increased (p≤0.05) in CUR/RES alone and in combination groups as compared to the control group. In conclusion, the addition of bioantioxidants in the cryopreservation medium has improved the post-thaw cell recovery through suppression of oxidative stress-induced during the freeze-thaw cycle.

Keywords

Antioxidants, Buffalo, Curcumin, Mesenchymal Stem Cells, Oxidative Stress, Resveratrol

Subject Discipline

Physiology

Full Text:

References

Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol. 2016. https://doi.org/10.1155/2016/6940283 PMid:27516776 PMCid:PMC4969512

Markoski MM. Advances in the use of stem cells in veterinary medicine: From basic research to clinical practice. Scientifica (Cairo). 2016. https://doi.org/10.1155/2016/4516920 PMid:27379197 PMCid:PM C4917716

Das J, Nath I, Das RK, Poutary P, Behra SS. Autologous stem cell therapy to treat chronic ulcer in heifer - A case study. Vet World. 2012; 12:771-4. https://doi.org/10.5455/vetworld.2012.771-774

Doan CC, Truong NH, Vu NB, Nguyen TT, Nguyen HM, Nguyen KG, Do S, Phan NK, Pham PV. Isolation, culture and cryopreservation of human bone marrow derived mesenchymal stem cells. Int J Plant, Anim Environ Sci. 2012; 2(2):358-67.

Mitchell A, Rivas KA, Smith R, Watts AE. Cryopreservation of equine mesenchymal stem cells in 95% autologous serum and 5% DMSO does not alter post-thaw growth or morphology in vitro compared to fetal bovine serum or allogeneic serum at 20 or 95% and DMSO at 10 or 5%. Stem Cell Res Ther. 2015; 6(1):231-43. https://doi.org/10.1186/s13287-015-0230-y PMid:26611913 PMCid:PMC4661990

Shivakumar SB, Bharti D, Jang S, Hwang S, Park J, Shin J, Byun J, Park B, Rho G. Cryopreservation of human wharton’s jelly-derived mesenchymal stem cells following controlled rate freezing protocol using different cryoprotectants: A comparative study. Int J Stem Cells. 2015; 8(2):155-69. https://doi.org/10.15283/ijsc.2015.8.2.155 PMid:26634064 PMCid:PMC4651280

Yong KW, Murphy BP, Xu F, Bakar WA, Abas W, Choi JR, Omar SZ, Azmi AD N, Chua KH, Safwan WKZW. Phenotypic and functional characterization of longterm cryopreserved human adipose-derived stem cells. Sci Rep. 2015; 5. https://doi.org/10.1038/srep09596 PMid:25872464 PMCid:PMC4397835

Lopez M, Bollag RJ, Jack CY, Isales CM, Eroglu A. Chemically defined and xeno-free cryopreservation of human adipose-derived stem cells. PloS One. 2016; (3). https://doi.org/10.1371/journal.pone.0152161 PMid:27010403 PMCid:PMC4806986

Makashovo OE, Babijchuk LO, Zubova OL, Zubov PM. Optimization of cryopreservation technique for human cord blood nucleated cells using combination of cryoprotectant DMSO and antioxidant N-acetyl-Lcysteine. Probl Cryobiol Cryomed. 2016; 26(4):295-307. https://doi.org/10.15407/cryo26.04.295

Devi P, Sharma M, Singh D, Lonare MK, Udehiya R. Viability and expression pattern of cryopreserved mesenchymal stem cells derived from buffalo bone marrow. Rumin Sci. 2017; 6(1):7-12.

Aliakbari F, Gilani MAS, Amidi F, Baazm M, Korouji M, Izadyar F, Abbasi M. Improving the efficacy of cryopreservation of spermatogonia stem cells by antioxidant supplements. Cell Reprogram. 2016; 18(2):87-95. https://doi.org/10.1089/cell.2015.0067 PM id:27055629

Ha SJ, Kim BG, Lee YA, Kim YH, Kim BJ, Jung SE, Ryu BY. Effect of antioxidants and apoptosis inhibitors on cryopreservation of murine germ cells enriched for spermatogonial stem cells. PloS One. 2016; 11(8). https://doi.org/10.1371/journal.pone.0161372 PMid:27548381 PMCid:PMC4993461

Singh AK, Jha A, Bit A, Kiassov AP, Rizvanov A, Ojha A, Bhoi P, Patra PK, Kumar A, Bissoyi A. Selaginella bryopteris aqueous extract improves stability and function of cryopreserved human mesenchymal stem cells. Oxid Med Cell Longev. 2017. https://doi.org/10.1155/2017/8530656 PMid:28811868 PMCid:PMC5546 052

Tian Y, Li X, Xie H, Wang X, Xie Y, Chen C, Chen D. Protective mechanism of the antioxidant baicalein toward hydroxyl radical-treated bone marrow-derived mesenchymal stem cells. Molecules. 2018; 23(1). https://doi.org/10.3390/molecules23010223 PMid:29361712 P MCid:PMC6017293

Amidi F, Rashidi Z, KhosravizadehZ, Khodamoradi K, Talebi A, Navid S, Abbasi M. Antioxidant effects of quercetin in freeze-thawing process of mouse spermatogonial stem cells. Asian Pac J Reprod. 2019; 8(1):7-12. https://doi.org/10.4103/2305-0500.250417

Gade NE, Pratheesh MD, Nath A, Dubey PK, Amarpal, Sharma B, Saikumar G, Sharma GT. Molecular and cellular characterization of buffalo bone marrow-derived mesenchymal stem cells. Reprod Domest Anim. 2012; 48(3):10-15. https://doi.org/10.1111/j.1439-0531.2012.02156.x PMid:23679988

Peltz L, Gomez J, Marquez M, Alencastro F, Atashpanjeh N, Quang T, Zhao Y. Resveratrol exerts dosage and duration dependent effect on human mesenchymal stem cell development. PLoS One. 2012; 7(5). https://doi.org/10.1371/journal.pone.0037162 PMid:22615926 PMCid:PMC3353901

Wang N, Wang F, Gao Y, Yin P, Pan C, Liu W, Wang J. Curcumin protects human adipose-derived mesenchymal stem cells against oxidative stress-induced inhibition of osteogenesis. J Pharmacol Sci. 2016; 132(3):192-200. https://doi.org/10.1016/j.jphs.2016.10.005 PMid:27840063

Stocks J, Dormandy TL. The autoxidation of human red cell lipids induced by hydrogen peroxide. Br J Haematol. 1971; 20:95-111. https://doi.org/10.1111/j.1365-2141.19 71.tb00790.x PMid:5540044

Choi HS, Kim JW, Cha YN, Kim C. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoassay Immunochem. 2006; 27(1):31-44. https://doi.org/10.1080/15321810500403722 PMid:16450867

Aranda A, Sequedo L, Tolosa L, Quintas G, Burello E, Castell JV, Gombau L. Dichloro-dihydro-fluoroscein diacetate (DCFH-DA) assay: A quantitative method for oxidative stress assessment of nanoparticles-treated cells. Toxicol In Vitro. 2013; 27(2):954-63. https://doi.org/10.1016/j.tiv.2013.01.016 PMid:23357416

Lowry H, Rosebrough NJ, Farr A, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chemis. 1951; 1:265-75. https://doi.org/10.1016/S0021- 9258(19)52451-6

Madesh M, Balasubramanian KA. Microtiter plate assay for superoxide dismutase using MTT reduction by superoxide. Indian J Biochem Biophys. 1998; 35:184-8.

Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chemis. 1974; 249(22):7130-9. https://doi.org/10.1016/S0021-9258(19)42083-8

Hafeman DG, Sunde RA, Hoekstra WG. Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J Nutr. 1974; 104:580-7. https://doi.org/10.1093/jn/104.5.580 PMid:4823943

Aebi H. Catalase in vitro, Methods Enzymol. 1984; 105:121-6. https://doi.org/10.1016/S0076-6879(84)05016-3

Beutler E, Kelly BM. The effect of sodium nitrite on red cell GSH. Experientia. 1963; 19:96-7. https://doi.org/10.1007/BF02148042 PMid:13967892

Marnett LJ. Oxy radicals, lipid peroxidation and DNA damage. Toxicology. 2002; 27:181-2. https://doi.org/10.1016/S0300-483X(02)00448-1

Ortega Ferrusola C, Gonzalez FL, Morrell JM, Salazar SC, Macas GB, Rodrıguez MH. Tapia JA, Pena FJ. Lipid peroxidation, assessed with BODIPY-C11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes. Reproduction. 2009; 138:55-63. https://doi.org/10.1530/REP-08-0484 PMid:19380427

Martin M, Ortega Ferrusola P, Vizuete C, Plaza Da’vila GM, Rodriguez Martinez H, Pena FJ. Depletion of intracellular thiols and increased production of 4-hydroxynonenal that occur during cryopreservation of stallion spermatozoa lead to caspase activation, loss of motility, and cell death. Biol Reprod. 2015; 93(6):143, 1-11. https://doi.org/10.1095/biolreprod.115.132878 PMid:26536905

Puts CF, Berendsen TA, Bruinsma BG, Ozer S, Luitje M, Usta OB. Polyethylene glycol protects primary hepatocytes during supercooling preservation. Cryobiology. 2015; 71:125-9. https://doi.org/10.1016/j. cryobiol.2015.04.010 PMid:25936340 PMCid:PMC450 6890

Del BC, Fracassetti D, Lanti C, Porrini M, Riso P. Comparison of DNA damage by the comet assay in fresh versus cryopreserved peripheral blood mononuclear cells obtained following dietary intervention. Mutagenesis. 2015; 30:29-35. https://doi.org/10.1093/mutage/geu058 PMid:25527725

Alotaibi NAS, Slater NKH, Rahmoune H. Salidroside as a novel protective agent to improve red blood cell cryopreservation. PLoS One. 2016; 11. https://doi.org/10.1371/journal.pone.0162748 PMid:27631782 PMCid:PMC5025239

Limaye LS. Bone marrow cryopreservation: Improved recovery due to bioantioxidant additives in the freezing solution. Stem Cells. 1997; 15:353-8. https://doi.org/10.1002/stem.150353 PMid:9323797

Silva ECB, Cajueiro JFP, Silva SV, Soares PC, Guerra MMP. Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology 2012; 77:1722-6. https://doi.org/10.1016/j.theriogenology.2011.11.023 PMid:22289215

Swami DS, Kumar P, Malik RK, Saini M, Kumar D, Jan MH. The cryoprotective effect of iodixanol in buffalo semen cryopreservation. Anim Reprod Sci. 2017; 179:20-6. https://doi.org/10.1016/j.anireprosci.2017.01. 012 PMid:28189350

Okada K, Wangpoengtrakul C, Tanaka T, Toyokuni S, Uchida K, Osawa T. Curcumin and especially tetrahydrocurcumin ameliorate oxidative stressinduced renal injury in mice. J Nutr. 2001; 131:2090-5. https://doi.org/10.1093/jn/131.8.2090 PMid:11481399

Rukkumani R, Aruna K, Varma PS, Rajasekaran KN, Menon VP. Comparative effects of curcumin and an analog of curcumin on alcohol and PUFA induced oxidative stress. J Pharmacol Sci. 2004; 7:274-83.

Waly MI, Al Moundhri MS, Ali BH. Effect of curcumin on cisplatin-and oxaliplatin-induced oxidative stress in human embryonic kidney (HEK) 293 cells. Ren Fail. 2011; 33(5):518-23. https://doi.org/10.3109/0886022X. 2011.577546 PMid:21574897

Zhang BY, Shi YQ, Chen X, Dai J, Jiang ZF, Li N, Zhang ZB. Protective effect of curcumin against formaldehyde induced genotoxicity in A549 cell lines. J Appl Toxicol. 2013; 33(12):1468-73. https://doi.org/10.1002/jat.2814 PMid:23059809

Linnik O, Gonchar O, Nosar V, Drevytska T, Kovalyov O, Mankovska I. Effect of curcumin on mitochondrial function of cardiomyocytes with doxorubicin-induced oxidative stress. Fiziol Zh. 2017; 63(1):10-16. https://doi.org/10.15407/fz63.01.010 PMid:29975823

Pathan A, Nariya A, Shah N, Shaikh I, Vyas J, Jhala D. In Vitroamelioration by curcumin on genotoxicity in workers with elevated blood cadmium level. J Nat Remed 2017; 17(1):20-7. https://doi.org/10.18311/ jnr/2017/15752

Branco CS, Garcez ME, Pasqualotto FF, Erdtman B, Salvador M. Resveratrol and ascorbic acid prevent DNA damage induced by cryopreservation in human semen. Cryobiology. 2010; 60:235-7. https://doi.org/10.1016/j. cryobiol.2009.10.012 PMid:19895799

Shen C, Cheng W, Yu P, Wang L, Zhou L, Zeng L, Yang Q. Resveratrol pretreatment attenuates injury and promotes proliferation of neural stem cells following oxygen-glucose deprivation/reoxygenation by upregula ting the expression of Nrf2, HO-1 and NQO1 in vitro. Mol Med Rep. 2016; 14(4):3646-54. https://doi.org/10.3892/mmr.2016.5670 PMid:27573874 PMCid:PMC5 042764

Goel A, Aggarwal BB. Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr Cancer. 2010; 62(7):919-30. https://doi.org/10.1080/01635581.2010.509835 PMid:20924967

Kelkel M, Jacob C, Dicato M, Diederich M. Potential of the dietary antioxidants resveratrol and curcumin in prevention and treatment of hematologic malignancies. Molecule. 2010; 15(10):7035-74. https://doi.org/10.3390/molecules15107035 PMid:20944521 P MCid:PMC6259231

Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell. 2002; 9:387-99. https://doi.org/10.1016/ S1097-2765(02)00445-8

Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014; 24:R453-62. https://doi.org/10.1016/j.cub.2014.03.034 PMid:24845678 PMCid:PMC4055301

Bortolin RC, Gasparotto J, Vargas AR, da Silva Morrone M, Kunzler A, Henkin BS, Chaves PR, Roncato S, Gelain DP, Moreira JCF. Effects of freeze-thaw and storage on enzymatic activities, protein oxidative damage, and immunocontent of the blood, liver, and brain of rats, Biopreserv Biobank. 2017; 15:182-90. https://doi.org/10.1089/bio.2016.0023 PMid:27662116

Mostek A, Dietrich MA, Slowin Ska M, Ciereszko A. Cryopreservation of bull semen is associated with carbonylation of sperm proteins. Theriogenology. 2017; 92:95-102. https://doi.org/10.1016/j.theriogenology.2017.01.011 PMid:28237350

Grune T, Davies KJ. The proteasomal system and HNEmodified proteins. Mol Aspects Med. 2003; 24(4-5):195- 204. https://doi.org/10.1016/S0098-2997(03)00014-1

Li J, Wu N, Chen X, Chen H, Yang X, Liu C. Curcumin protects islet cells from glucolipo toxicity by inhibiting oxidative stress and NADPH oxidase activity both in vitro and in vivo. Islets. 2019; 1(5):152-64. https://doi.org/10.1080/19382014.2019.1690944 PMid:31750757 P MCid:PMC6930025

Len JS, Darius KWS, Shi-Xiong T. The roles of reactive oxygen species and antioxidants in cryopreservation. Biosci Rep. 2019; 39(8). https://doi.org/10.1042/BSR20 191601 PMid:31371631 PMCid:PMC6712439

Aliakbari F, Gilani MAS, Amidi F, Baazm M, Korouji M, Izadyar F, Abbasi M. Improving the efficacy of cryopreservation of spermatogonia stem cells by antioxidant supplements. Cell Reprogram. 2016; 18(2):87-95. https://doi.org/10.1089/cell.2015.0067 PM id:27055629

Dudylina AL, Ivanova MV, Shumaev KB, Ruugev EK. Superoxide formation in cardiac mitochondria and effect of phenolic antioxidants. Cell Biochem Biophys. 2019; 77(1):99-107. https://doi.org/10.1007/s12013-018 -0857-2 PMid:30218405

Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell Signal. 2007; 19(9):1807- 19. https://doi.org/10.1016/j.cellsig.2007.04.009 PMid: 17570640

Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007; 39(1):44-84. https://doi.org/10.1016/j.biocel.2006.07.001 PMid:16978905

Rajendran P, Nandakumar N, Rengarajan T. Antioxidants and human diseases. Clin Chim Acta. 2014; 436:332-47. https://doi.org/10.1016/j.cca.2014.06.004 PMid:24933428

Pizzino G, Irrera N, Cucinotta M. Oxidative stress: Harms and benefits for human health, Oxid Med Cell Longev. 2017; 2017. https://doi.org/10.1155/2017/8416 763 PMid:28819546 PMCid:PMC5551541

Therond P. Oxidative stress and damages to biomolecules (lipids, proteins, DNA), Ann Pharm Fr. 2006; 64(6):383- 9. https://doi.org/10.1016/S0003-4509(06)75333-0

Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012; 5:9-19. https://doi.org/10.1097/WOX.0b013e3182439613 PMid:23268465 PMCid:PMC3488923

Hardikar AA, Risbud MV, Remacle C, Reusens B, Hoet JJ, Bhonde RR. Islet cryopreservation: Improved recovery following taurine pretreatment. Cell Transplant. 2001; 10(3):247-53. https://doi.org/10.3727/000000001783986756 PMid:11437070

Sasnoor LM, Kale VP, Limaye LS. Prevention of apoptosis as a possible mechanism behind improved cryoprotection of hematopoietic cells by catalase and trehalose. Transplantation. 2005; 80(9):1251-60. https://doi.org/10.1097/01.tp.0000169028.01327.90 PMid:16314793

Katenz E, Vondran FWR, Schwartlander R, Pless G, Gong X, Cheng X. Cryopreservation of primary human hepatocytes: The benefit of trehalose as an additional cryoprotective agent. Liver Transpl. 2007; 13(1):38-45. https://doi.org/10.1002/lt.20921 PMid:17154395

Lee YA, Kim YH, Kim BJ, Kim BG, Kim KJ, Auh JH. Cryopreservation in trehalose preserves functional capacity of murine spermatogonial stem cells. PLoS One. 2013; 8. https://doi.org/10.1371/journal.pone.0054 889 PMid:23349986 PMCid:PMC3551902

Shinde P, Khan N, Melinkeri S, Kale V, Limaye L. Freezing of dendritic cells with trehalose as an additive in the conventional freezing medium results in improved recovery after cryopreservation. Transfusion. 2019; 59(2):686-96. https://doi.org/10.1111/trf.15028 PM id:30456902

Tecklenburg SL, Mickleborough TD, Fly AD, Bai Y, Stager J M. Ascorbic acid supplementation attenuates exercise-induced bronchoconstriction in patients with asthma. Respir Med. 2007; 101(8):1770-8. https://doi org/10.1016/j.rmed.2007.02.014 PMid:17412579

Kalthur G, Raj S, Thiyagarajan A, Kumar S, Kumar P, Adiga SK. Vitamin E supplementation in semenfreezing medium improves the motility and protects sperm from freeze-thaw induced DNA damage, Fertil Steril. 2011; 95(3):1149-51. https://doi.org/10.1016/j.fertnstert.2010.10.005 PMid:21067726

Xue WJ, Luo XH, Li Y, Liu HB, Tian XH, Feng XS. Effects of astragalosides on cultured islets after cryopreservation in rats. Transplant Proc. 2011; 43(10):3908-12. https://doi.org/10.1016/j.transproceed.2011.10.039 PMid:22172871

Matsumura K, Hayashi F, Nagashima T, Hyon SH. Long-term cryopreservation of human mesenchymal stem cells using carboxylated poly-l-lysine without the addition of proteins or dimethyl sulfoxide. J Biomater Sci Polym Ed. 2013; 24(12):1484-97. https://doi.org/10.1080/09205063.2013.771318 PMid:23829460

Zeng W, Xiao J, Zheng G, Xing F, Tipoe GL, Wang X, He C, Chen ZY, Liu Y. Antioxidant treatment enhances human mesenchymal stem cell anti- stress ability and therapeutic efficacy in acute liver failure model. Sci Rep. 2015; 5. https://doi.org/10.1038/srep11100 PMid:26057 841 PMCid:PMC4460871

Aliakbari F, Gilani MAS, Yazdekhasti H, Koruji M, Asgari HR, Baazm M. Izadyar F, Kharrazi NE, Khanezad M, Abbasi M. Effects of antioxidants, catalase and α-tocopherol on cellviability and oxidative stress variables in frozen-thawed mice spermatogonial stem cells. Artif Cells Nanomed Biotechnol. 2017; 45:63-8. https://doi.org/10.3109/21691401.2016.1138491 PMid: 27123904

Shabani H, Zandi M, Ofogi H, Sanjabi MR, Pajooh KH. The effect of combining vitamin E and C on the viability improvement of transfected ovine spermatogonial stem cells after cryopreservation and thawing. Turkish J Vet Anim Sci. 2017; 41(5):648-55. https://doi.org/10.3906/vet-1701-38

Abdillah DA, Setyawan EMN, Oh HJ, Ra K, Lee SH, Kim MJ, Lee BC. Iodixanol supplementation during sperm cryopreservation improves protamine level and reduces reactive oxygen species of canine sperm. J Vet Sci. 2019; 20:79-86. https://doi.org/10.4142/jvs.2019.20.1.79 PMid:30481988 PMCid:PMC6351762

Hirzel E, Lindinger PW, Maseneni S, Giese M, Rhein VV, Eckert A, Eberle AN. Differential modulation of ROS signals and other mitochondrial parameters by the antioxidants MitoQ, resveratrol and curcumin in human adipocyte. J Recept Signal Transduct Res. 2013; 33(5):304-12. https://doi.org/10.3109/10799893.2013.822887 PMid:23914782

Gerets HHJ, Hanon E, Cornet M, Dhalluin S, Depelchin O, Canning M, Atienzar FA. Selection of cytotoxicity markers for the screening of new chemical entities in a pharmaceutical context: A preliminary study using a multiplexing approach. Toxicol in Vitro. 2009; 23(2):319-32. https://doi.org/10.1016/j.tiv.2008.11.012 PMid:19110050

Lonare MK, Vemu B, Singh AK, Dumka VK, Singla S, Sharma SK. Cytotoxicity and oxidative stress alterations induced by aldrinin balb/c 3T3 fibroblast cells. Proc Natl Acad Sci India, B: Biol Sci. 2017; 87(4):1209-16. https://doi.org/10.1007/s40011-015-0694-7

Arun P, Oguntayo S, Alamneh Y, Honnold C, Wang Y, Valiyaveettil M, Long JB, Nambiar MP. Rapid release of tissue enzymes into blood after blast exposure: Potential use as biological dosimeters. PLoS One. 2012; 7(4). https://doi.org/10.1371/journal.pone.0033798 PMid:22493674 PMCid:PMC3320892

Waghe P, Saini SPS, Rampal S, Prakash N. Sub-chronic exposure to carbendazim induces biochemical and hematological alterations in male goats. Toxicol Environ Chem. 2013; 95(2):330-6. https://doi.org/10.1080/02772 248.2013.770859

Alam J, Md. Mujahid B, Jahan Y, Bagga P, Md. Azizur R. Hepatoprotective potential of ethanolic extract of Aquilaria agallocha leaves against paracetamol induced hepatotoxicity in SD rats. J Tradit Complement Med. 2017; 7(1):9-13. https://doi.org/10.1016/j.jtcme.2015.12.006 PMid:28053882 PMCid:PMC5198823

Chakroun S, Intissar G, Lobna E, Oumaima A, Fadoua N, Emna K, Najjar MF, Zohra H, Hassen BC. Imidacloprid enhances liver damage in wistar rats: Biochemical, oxidative damage and histological Assessment. J Coast Life Med. 2017; 5(12):540-6. https://doi.org/10.12980/jclm.5.2017J7-149

Gelen V, Sengul E, Gedikli S, Atila G, Uslu H , Makav M. The protective effect of rutin and quercetin on 5-FU-induced hepatotoxicity in rats. Asian Pac J Trop Biomed. 2017; 7(7):647-53. https://doi.org/10.1016/j.apjtb.2017.06.013

Mahmoodzadeh Y, Mohammad M, Rezagholizadeh L. Hepatoprotective effect of methanolic Tanacetum parthenium extract on CCl4-induced liver damage in rats. Toxicol Rep. 2017; 4:455-62. https://doi.org/10.1016/j.toxrep.2017.08.003 PMid:28959674 PMCid:PMC56 15166

Abou Seif HS. Physiological changes due to hepatotoxicity and the protective role of some medicinal plants. Beni-Suef Univ J Basic Appl Sci. 2016; 5:134-46. https://doi.org/10.1016/j.bjbas.2016.03.004

Boz I, Belviranli M, Okudan N. Curcumin modulates muscle damage but not oxidative stress and antioxidant defense following eccentric exercise in rats. Int J Vitam Nutr Res. 2014; 84(4):163-72. https://doi.org/10.1024/0300-9831/a000203 PMid:26098480

McFarlin BK, Venable AS, Henning AL, Sampson JNB, Pennel K, Vingren JL, Hill DW. Reduced inflammatory and muscle damage biomarkers following oral supplementation with bioavailable curcumin. BBA Clin. 2016:72-8. https://doi.org/10.1016/j.bbacli.2016.02.003 PMid:27051592 PMCid:PMC4802396

Ighodaro OM, Akinloye OA. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J Med. 2018; 54(4):287-93. https://doi.org/10.1016/j.ajme.2017.09.001

Odani M, Komatsu Y, Oka S, Iwahashi H. Screening of genes that respond to cryopreservation stress using yeast DNA microarray. Cryobiology. 2003; 47(2):155- 64. https://doi.org/10.1016/j.cryobiol.2003.09.001 PM id:14580849

Takahashi S, Ando A, Takagi H, Shima J. Insufficiency of copper ion homeostasis causes freeze-thaw injury of yeast cells as revealed by indirect gene expression analysis. Appl Environ Microbiol. 2009; 75(21):6706- 11. https://doi.org/10.1128/AEM.00905-09 PMid:19749 072 PMCid:PMC2772427

Park JI, Grant CM, Davies MJ, Dawes IW. The cytoplasmic Cu, Zn superoxide dismutase of Saccha romyces cerevisiae is required for resistance to freezethaw stress. Generation of free radicals during freezing and thawing. J Biol Chem. 1998; 273(36):22921-8. https://doi.org/10.1074/jbc.273.36.22921 PMid:9722512

Iqbal M, Sharma SD, Okazaki Y, Fujisawa M, Okada S. Dietary supplementation of curcumin enhances antioxidant and phase II metabolizing enzymes in ddY male mice: Possible role in protection against chemical carcinogenesis and toxicity. Pharmacol Toxicol. 2003; 92(1):33-8. https://doi.org/10.1034/j.1600-0773.2003.92 0106.x PMid:12710595

Li Y, Cao Z, Zhu H. Upregulation of endogenous antioxidants and phase 2 enzymes by the red wine polyphenol, resveratrol in cultured aortic smooth muscle cells leads to cytoprotection against oxidative and electrophilic stress. Pharmacol Res. 2006; 53(1):6-15. https://doi.org/10.1016/j.phrs.2005.08.002 PMid:16169 743

Eddine BI, Hakima T, Abdelkrim T. Combined effect of quercetin and resveratrol induces anxiolytic-like behavior and improves brain antioxidant capacity in male wistar rat. Asian J Anim Sci. 2015; 91:157-61. https://doi.org/10.3923/ajas.2015.157.161

Watanabe S, Fukui T. Suppressive effect of curcumin on trichloroethylene-induced oxidative stress. J Nutr Sci Vitaminol (Tokyo). 2000; 46(5):230-4. https://doi.org/10.3177/jnsv.46.230 PMid:11234915

Singh R, Sharma P. Hepatoprotective effect of curcumin on lindane-induced oxidative stress in male wistar rats. Toxicol Int. 2011; 18(2):124-9. https://doi.org/10.4103/0971-6580.84264 PMid:21976817 PMCid: PMC3183619

Sankar P, Telang AG, Manimaran A. Protective effect of curcumin on cypermethrin-induced oxidative stress in wistar rats. Exp Toxicol Pathol. 2012; 64(5):487-93. https://doi.org/10.1016/j.etp.2010.11.003 PMid:21130633

Samarghandian S, Azimi-Nezhad M, Farkhondeh T, Samini F. Anti-oxidative effects of curcumin on immobilization-induced oxidative stress in rat brain, liver and kidney. Biomed Pharmacother. 2017; 87:223-9. https://doi.org/10.1016/j.biopha.2016.12.105 PMid:280 61405

Rubio-Ruiz ME, Guarner-Lans V, Cano-Martinez A, Diaz-Diaz E, Manzano-Pech L, Gamas-Magana A, Castrejon-Tellez V, Tapia-Cortina C, Perez-Torres I. Resveratrol and quercetin administration improves antioxidant defenses and reduces fatty liver in metabolic syndrome rats. Molecules. 2019; 24(7). https://doi.org/10.3390/molecules24071297 PMid:30987086 PMC id:PMC6479544


Refbacks

  • There are currently no refbacks.