Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-04T20:11:05.411Z Has data issue: false hasContentIssue false
  • English
  • Français

Resveratrol reduces oxidative damage and inflammation in mice infected with Trichinella spiralis

Published online by Cambridge University Press:  02 April 2020

D.I. Elgendy Open the ORCID record for D.I. Elgendy [Opens in a new window] ,
A.A. Othman ,
M.A. Hasby Saad ,
N.A. Soliman  and
S.E. Mwafy
D.I. Elgendy*
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Tanta University, Egypt
A.A. Othman
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Tanta University, Egypt
M.A. Hasby Saad
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Tanta University, Egypt
N.A. Soliman
Affiliation:
Medical Biochemistry Department, Faculty of Medicine, Tanta University, Egypt
S.E. Mwafy
Affiliation:
Pathology Department, Faculty of Medicine, Tanta University, Egypt
*
Author for correspondence: D.I. Elgendy, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Trichinellosis is a serious food-borne zoonotic infection of cosmopolitan distribution. Currently, treatment for trichinellosis is far from ideal. Given the important role of oxidative stress and immune-mediated inflammation in the pathogenesis of trichinellosis, this study was designed to evaluate the possible protective effects of resveratrol (RSV) during the intestinal and muscular phases of Trichinella spiralis infection in mice. The oral administration of RSV at a dose of 20 mg/kg once daily for two weeks resulted in significant reductions in both adult and larval counts; significant improvements in the redox status of the small intestine and muscles; a significant reduction in interleukin 4, pentraxin 3 and vascular endothelial growth factor expression; and the mitigation of intestinal and muscular inflammation. In conclusion, this study identifies RSV as a promising agent for the treatment of experimental trichinellosis, and more studies in experimental animals and humans are worth consideration.

Keywords

Trichinella spiralisintestinal phasemuscular phaseresveratroloxidative stressIL-4PTX3VEGF
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e140
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arizmendi, N, Yepez-Mulia, L and Cedillo-Rivera, R (2001) Interleukin mRNA changes in mast cells stimulated by TSL-1 antigens. Parasite 8, 114–116.CrossRefGoogle ScholarPubMed
Badri, W, Miladi, K, Nazari, QA, Greige-Gerges, H, Fessi, H and Elaissari, A (2016) Encapsulation of NSAIDs for inflammation management: overview, progress, challenges and prospects. International Journal of Pharmaceutics 515, 757–773.CrossRefGoogle ScholarPubMed
Barnes, PJ (2014) Glucocorticoids. Chemical Immunology and Allergy 100, 311–316.CrossRefGoogle ScholarPubMed
Blum, LK, Mohanan, S, Fabre, MV, Yafawi, RE and Appleton, JA (2013) Intestinal infection with T. spiralis induces distinct, regional immune responses. Veterinary Parasitology 194, 101–105.CrossRefGoogle Scholar
Bradamante, S, Barenghi, L and Villa, A (2004) Cardiovascular protective effects of resveratrol. Cardiovascular Drug Reviews 22, 169–188.CrossRefGoogle ScholarPubMed
Bruschi, F and Chiumiento, L (2011) Trichinella inflammatory myopathy: host or parasite strategy? Parasites & Vectors 4, 42.CrossRefGoogle ScholarPubMed
Bruschi, F, Saviozzi, M, Piaggi, S, Malvaldi, G and Casini, A (2003) Up-regulation of the 31 kDa dehydroascorbate reductase in the modified skeletal muscle cell (nurse cell) during Trichinella spp. infection. International Journal for Parasitology 33, 1035–1042.CrossRefGoogle ScholarPubMed
Capó, VA, Despommier, DD and Polvere, RI (1998) T. spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. Journal of Parasitology 84, 209–214.CrossRefGoogle Scholar
Chabert, P, Fougerousse, A and Brouillard, R (2006) Anti-mitotic properties of resveratrol analog (Z)-3,5,4'-trimethoxystilbene. Biofactors 27, 37–46.CrossRefGoogle Scholar
Chan, MM (2002) Antimicrobial effect of resveratrol on dermatophytes and bacterial pathogens of the skin. Biochemical Pharmacology 63(2), 99–104.CrossRefGoogle ScholarPubMed
Chedea, VS, Vicas, SI, Sticozzi, C, Pessina, F, Frosini, M, Maioli, E and Valacchi, G (2017) Resveratrol: from diet to topical usage. Food & Function 8, 3879–3892.CrossRefGoogle ScholarPubMed
Chiumiento, L and Bruschi, F (2009) Enzymatic antioxidant systems in helminth parasites. Parasitology Research 105, 593–603.CrossRefGoogle ScholarPubMed
Cong, X, Li, Y, Lu, N, Dai, Y, Zhang, H, Zhao, X and Liu, Y (2014) Resveratrol attenuates the inflammatory reaction induced by ischemia/reperfusion in the rat heart. Molecular Medicine Reports 9, 2528–2532.CrossRefGoogle ScholarPubMed
Coutinho, DS, Pacheco, MT, Frozza, RL and Bernardi, A (2018) Anti-inflammatory effects of resveratrol: mechanistic insights. International Journal of Molecular Sciences 19, e1812.CrossRefGoogle Scholar
Das, SK, Mukherjee, S, Gupta, G, Rao, DN and Vasudevan, DM (2010) Protective effect of resveratrol and vitamin E against ethanol-induced oxidative damage in mice: biochemical and immunological basis. Indian Journal of Biochemistry and Biophysics 47(1), 32–37.Google ScholarPubMed
Ding, J, Bai, X, Wang, X, Shi, H, Cai, X, Luo, X, Liu, M and Liu, X (2017) Immune cell responses and cytokine profile in intestines of mice infected with T. spiralis. Frontiers in Microbiology 8, e2069.CrossRefGoogle Scholar
Docherty, JJ, Fu, MM, Stiffler, BS, Limperos, RJ, Pokabla, CM and DeLucia, AL (1999) Resveratrol inhibition of herpes simplex virus replication. Antiviral Research 43(3), 145–155.CrossRefGoogle ScholarPubMed
Donnelly, LE, Newton, R, Kennedy, GE, Fenwick, PS, Leung, RH, Ito, K, Russell, RE and Barnes, PJ (2004) Anti-inflammatory effects of resveratrol in lung epithelial cells: molecular mechanisms. American Journal of Physiology-Lung Cellular and Molecular Physiology 287, 774–783.CrossRefGoogle ScholarPubMed
Dunn, IJ and Wright, KA (1985) Cell injury caused by T. spiralis in the mucosal epithelium of B10A mice. Journal of Parasitology 71(6), 757–766.CrossRefGoogle Scholar
Erbas, O, Pala, HG, Pala, EE, Oltulu, F, Aktug, H, Yavasoglu, A and Taskiran, D (2014) Ovarian failure in diabetic rat model: nuclear factor-kappaB, oxidative stress, and pentraxin-3. Taiwanese Journal of Obstetrics and Gynecology 53(4), 498–503.CrossRefGoogle ScholarPubMed
Fazzini, F, Peri, G, Doni, A, et al. (2001) PTX3 in small-vessel vasculitides: an independent indicator of disease activity produced at sites of inflammation. Arthritis & Rheumatology 44, 2841–2850.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Finkleman, FD, Shea-Donohue, T, Goldhill, J, Sullivan, CA, Morris, SC, Madden, KB, Gause, WC and Urban, JF (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505–533.CrossRefGoogle Scholar
Garlanda, C, Bottazzi, B, Bastone, A and Mantovani, A (2005) Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annual Review of Immunology 23, 337–366.CrossRefGoogle ScholarPubMed
Gou, HF, Chen, XC, Zhu, J, Jiang, M, Yang, Y, Cao, D and Hou, M (2011) Expressions of COX-2 and VEGF-C in gastric cancer: correlations with lymphangiogenesis and prognostic implications. Journal of Experimental & Clinical Cancer Research 30(1), 14.CrossRefGoogle ScholarPubMed
Hamza, RZ and El-Shenawy, NS (2017) Anti-inflammatory and antioxidant role of resveratrol on nicotine-induced lung changes in male rats. Toxicology Reports 4, 399–407.CrossRefGoogle ScholarPubMed
Hori, YS, Kuno, A, Hosoda, R, Tanno, M, Miura, T, Shimamoto, K and Horio, Y (2011) Resveratrol ameliorates muscular pathology in the dystrophic mdx mouse, a model for Duchenne muscular dystrophy. Journal of Pharmacology and Experimental Therapeutics 338, 784–794.CrossRefGoogle Scholar
Jaillon, S, Peri, G, Delneste, Y, et al. (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. Journal of Experimental Medicine 204, 793–804.CrossRefGoogle ScholarPubMed
Jiang, YG, Peng, T, Luo, Y, Li, MC and Lin, YH (2008) Resveratrol reestablishes spermatogenesis after testicular injury in rats caused by 2,5-hexanedione. Chinese Medical Journal 121, 1204–1209.CrossRefGoogle ScholarPubMed
Jung, HJ, Hwang, IA, Sung, WS, Kang, H, Kang, BS, Seu, YB and Lee, DG (2005) Fungicidal effect of resveratrol on human infectious fungi. Archives of Pharmacal Research 28, 557–560.CrossRefGoogle ScholarPubMed
Kazemzadeh, H, Mohammad, F and Mohammad, F (2014) Evaluating expression of oxidative stress genes in response to Trichinells spiralis infection. Indian Journal of Scientific Research 5(1), 305–309.Google Scholar
Kedzierski, L, Curtis, JM, Kaminska, M, Jodynis-Liebert, J and Murias, M (2007) In vitro antileishmanial activity of resveratrol and its hydroxylated analogues against Leishmania major promastigotes and amastigotes. Parasitology Research 102, 91–97.CrossRefGoogle ScholarPubMed
Khan, WI (2008) Physiological changes in the gastrointestinal tract and host protective immunity: learning from the mouse-T. spiralis model. Parasitology 135, 671–682.CrossRefGoogle ScholarPubMed
Khan, WI, Blennerhasset, P, Ma, C, Matthaei, KI and Collins, SM (2001) Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunology 23, 39–42.CrossRefGoogle ScholarPubMed
Koracevic, D, Koracevic, G, Djordjevic, V, Andrejevic, S and Cosic, V (2001) Method for the measurement of antioxidant activity in human fluids. Journal of Clinical Pathology 54(5), 356–361.CrossRefGoogle ScholarPubMed
Kunnumakkara, AB, Sailo, BL, Banik, K, Harsha, C, Prasad, S, Gupta, SC, Bharti, AC and Aggarwal, BB (2018) Chronic diseases, inflammation, and spices: how are they linked? Journal of Translational Medicine 16, 14.CrossRefGoogle ScholarPubMed
Lai, PK and Roy, J (2004) Antimicrobial and chemopreventive properties of herbs and spices. Current Medicinal Chemistry 11, 1451–1460.CrossRefGoogle ScholarPubMed
Lamas, J, Morais, P, Arranz, JA, Sanmartín, ML, Orallo, F and Leiro, J (2009) Resveratrol promotes an inhibitory effect on the turbot scuticociliate parasite Philasterides dicentrarchi by mechanisms related to cellular detoxification. Veterinary Parasitology 161, 307–315.CrossRefGoogle ScholarPubMed
Lawrence, CE, Paterson, JCM, Higgins, LM, MacDonald, TT, Kennedy, MW and Garside, P (1998) IL-4-regulated enteropathy in an intestinal nematode infection. European Journal of Immunology 28, 2672–2684.3.0.CO;2-F>CrossRefGoogle Scholar
Lee, M, Kim, S, Kwon, OK, Oh, SR, Lee, HK and Ahn, K (2009) Anti-inflammatory and anti-asthmatic effects of resveratrol, a polyphenolic stilbene, in a mouse model of allergic asthma. International Immunopharmacology 9, 418–424.CrossRefGoogle Scholar
Leiro, J, Cano, E, Ubeira, FM, Orallo, F and Sanmartín, ML (2004) In vitro effects of resveratrol on the viability and infectivity of the microsporidian Encephalitozoon cuniculi. Antimicrobial Agents and Chemotherapy 48, 2497–2501.CrossRefGoogle ScholarPubMed
Leonard, SS, Xia, C, Jiang, BH, Stinefelt, B, Klandorf, H, Harris, GK and Shi, X (2003) Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochemical and Biophysical Research Communications 309, 1017–1026.CrossRefGoogle ScholarPubMed
Li, J, Xie, C, Zhuang, J, Li, H, Yao, Y, Shao, C and Wang, H (2015) Resveratrol attenuates inflammation in the rat heart subjected to ischemia-reperfusion: role of the TLR4/ NF-κB signaling pathway. Molecular Medicine Reports 11, 1120–1126.Google ScholarPubMed
Litwack, G, Bothwell, JW, Williams, JN and Elvehjem, CA (1952) A colorimetric assay for xanthine oxidase in rat liver homogenates. Journal of Biological Chemistry 200(1), 303–310.Google Scholar
Liu, Z, Li, Y and Yang, R (2012) Effects of resveratrol on vascular endothelial growth factor expression in osteosarcoma cells and cell proliferation. Oncology Letters 4, 837–839.CrossRefGoogle ScholarPubMed
Liu, XJ, Bao, HR, Zeng, XL and Wei, JM (2016) Effects of resveratrol and genistein on NF-κB, TNFα and matrix metalloproteinase-9 in patients with chronic obstructive pulmonary disease. Molecular Medicine Reports 13, 4266–4272.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL and Randall, RJ (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193(1), 265–275.Google ScholarPubMed
Mido, S, Fath, EM, Farid, AS, Nonaka, N, Oku, Y and Horii, Y (2012) T. spiralis: infection changes serum paraoxonase-1 levels, lipid profile, and oxidative status in rats. Experimental Parasitology 131(2), 190–204.CrossRefGoogle Scholar
Moridi, H, Karimi, J, Sheikh, N, et al. (2015) Resveratrol-dependent down-regulation of receptor for advanced glycation end-products and oxidative stress in kidney of rats with diabetes. International Journal of Endocrinology and Metabolism 13(2), e23542.CrossRefGoogle ScholarPubMed
Murrell, KD and Pozio, E (2011) Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases 17, 2194–2202.CrossRefGoogle ScholarPubMed
Norata, GD, Garlanda, C and Catapano, AL (2010) The long pentraxin PTX3: a modulator of the immunoinflammatory response in atherosclerosis and cardiovascular diseases. Trends in Cardiovascular Medicine 20, 35–40.CrossRefGoogle Scholar
Ock, MS, Cha, HJ and Choi, YH (2013) Verifiable hypotheses for thymosin β4-dependent and independent angiogenic induction of T. spiralis-triggered nurse cell formation. International Journal of Molecular Sciences 14, 23492–23498.CrossRefGoogle Scholar
Oray, M, Abu Samra, K, Ebrahimiadib, N, Meese, H and Foster, CS (2016) Long-term side effects of glucocorticoids. Expert Opinion on Drug Safety 15, 457–465.CrossRefGoogle ScholarPubMed
Othman, AA, Abou Rayia, DM, Ashour, DS, Saied, EM, Zineldeen, DH and El-Ebiary, AA (2016) Atorvastatin and metformin administration modulates experimental Trichinella spiralis infection. Parasitology International 65, 105–112.CrossRefGoogle ScholarPubMed
Ozkoc, S, Tuncay, S, Delibas, SB and Akisu, C (2009) In vitro effects of resveratrol on T. spiralis. Parasitology Research 105, 1139–1143.CrossRefGoogle Scholar
Palsamy, P and Subramanian, S (2008) Resveratrol a natural phytoalexin, normalizes hyperglycemia in streptozotocin-nicotinamide induced experimental diabetic rats. Biomedicine & Pharmacotherapy 62, 598–605.CrossRefGoogle ScholarPubMed
Pozio, E (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary parasitology 149(1-2), 3–21.CrossRefGoogle ScholarPubMed
Robb, EL, Page, MM, Wiens, BE and Stuart, JA (2008) Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochemical and Biophysical Research Communications 367, 406–412.CrossRefGoogle ScholarPubMed
Sang, N, Fang, J, Srinivas, V, Leshchinsky, I and Caro, J (2002) Carboxyl-terminal transactivation activity of hypoxia-inducible factor 1 α is governed by a von Hippel–Lindau protein independent, hydroxylation-regulated association with p300/CBP. Molecular and Cellular Biology 22, 2984–2992.CrossRefGoogle ScholarPubMed
Savchenko, AS, Inoue, A, Ohashi, R, et al. (2011) Long pentraxin 3 (PTX3) expression and release by neutrophils in vitro and in ulcerative colitis. Pathology International 61, 290–297.CrossRefGoogle ScholarPubMed
Scales, HE, Ierna, MX and Lawrence, CE (2007) The role of IL-4, IL-13 and IL-4Ralpha in the development of protective and pathological responses to T. spiralis. Parasite Immunology 29(2), 81–91.CrossRefGoogle Scholar
Schneider, Y, Chabert, P, Stutzmann, J, Coelho, D, Fougerousse, A, Gossé, F, Launay, JF, Brouillard, R and Raul, F (2003) Resveratrol analog (Z)-3,5,4'-trimethoxystilbene is a potent anti-mitotic drug inhibiting tubulin polymerization. International Journal of Cancer 107, 189–196.CrossRefGoogle Scholar
Serna, H, Porras, M and Vergara, P (2006) Mast cell stabilizer ketotifen [4-(1-methyl-4-piperidylidene)-4h-benzo[4,5]cyclohepta[1,2-b]thiophen-10(9H)-one fumarate] prevents mucosal mast cell hyperplasia and intestinal dysmotility in experimental T. spiralis inflammation in the rat. Journal of Pharmacology and Experimental Therapeutics 319(3), 1104–1111.CrossRefGoogle Scholar
Shimoni, Z, Klein, Z, Weiner, P, Assous, MV and Froom, P (2007) The use of prednisone in the treatment of trichinellosis. Israel Medical Association Journal 9, 537–539.Google ScholarPubMed
Sofronic-Milosavljevic, LJ, Radovic, I, Ilic, N, Majstorovic, I, Cvetkovic, J and Gruden-Movsesijan, A (2013) Application of dendritic cells stimulated with T. spiralis excretory-secretory antigens alleviates experimental autoimmune encephalomyelitis. Medical Microbiology and Immunology 202, 239–249.CrossRefGoogle Scholar
Soliman, RH, Ismail, AO, Badr, MS and Nasr, SM (2017) Resveratrol ameliorates oxidative stress and organ dysfunction in Schistosoma mansoni infected mice. Experimental Parasitology 174, 52–58.CrossRefGoogle ScholarPubMed
Stadler, M, Dagne, E and Anke, H (1994) Nematicidal activities of two phytoalexins from Taverniera abyssinica. Planta Medica 60, 550–552.CrossRefGoogle ScholarPubMed
Su, HC, Hung, LM and Chen, JK (2006) Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. American Journal of Physiology-Endocrinology and Metabolism 290, 1339–1346.CrossRefGoogle ScholarPubMed
Sun, HY, Xiao, CF, Cai, YC, Chen, Y, Wei, W, Liu, XK, Lv, ZL and Zou, Y (2010) Efficient synthesis of natural polyphenolic stilbenes: resveratrol, piceatannol and oxyresveratrol. Chemical and Pharmaceutical Bulletin 58(11), 1492–1496.CrossRefGoogle ScholarPubMed
Szkudelska, K and Szkudelski, T (2010) Resveratrol, obesity and diabetes. European Journal of Pharmacology 635(3), 1–8.CrossRefGoogle Scholar
Taguri, T, Tanaka, T and Kouno, I (2004) Antimicrobial activity of 10 different plant polyphenols against bacteria causing food-borne disease. Biological & Pharmaceutical Bulletin 27, 1965–1969.CrossRefGoogle ScholarPubMed
Tanno, M, Kuno, A, Yano, T, Miura, T, Hisahara, S, Ishikawa, S, Shimamoto, K and Horio, Y (2010) Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. Journal of Biological Chemistry 285, 8375–8382.CrossRefGoogle ScholarPubMed
Toklu, HZ, Sehirli, O, Ers-ahin, M, Sü leymanoğ lu, S, Yiğiner, O, Emekli-Alturfan, E, Yarat, A, Yeğen, BC and Sener, G (2010) Resveratrol improves cardiovascular function and reduces oxidative organ damage in the renal, cardiovascular and cerebral tissues of two-kidney, one clip hypertensive rats. Journal of Pharmacy and Pharmacology 62, 1784–1793.CrossRefGoogle ScholarPubMed
Turkmen, R, Birdane, YO, Demirel, HH, Kabu, M and Ince, S (2019) Protective effects of resveratrol on biomarkers of oxidative stress, biochemical and histopathological changes induced by sub-chronic oral glyphosate-based herbicide in rats. Toxicological Research 8(2), 238–245.CrossRefGoogle ScholarPubMed
Urban, JF, Maliszewski, CR, Madden, KB, Katona, IM and Finkelman, FD (1995) IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. Journal of Immunology 154, 4675–4684.Google ScholarPubMed
Vidavalur, R, Otani, H, Singal, PK and Maulik, N (2006) Significance of wine and resveratrol in cardiovascular diseases: Frensh paradox revisited. Clinical and Experimental Cardiology 11, 217–225.Google Scholar
Wakelin, D and Lloyd, M (1976) Immunity to primary and challenge infection of T. spiralis in mice a re-examination of conventional parameters. Parasitology 71, 173–182.CrossRefGoogle Scholar
Wang, WB, Lai, HC, Hsueh, PR, Chiou, RYY, Lin, SB and Liaw, SJ (2006) Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol. Journal of Medical Microbiology 55, 1313–1321.CrossRefGoogle ScholarPubMed
Wang, XL, Li, T, Li, JH, Miao, SY and Xiao, XZ (2017) The effects of resveratrol on inflammation and oxidative stress in a rat model of chronic obstructive pulmonary disease. Molecules 22, e1529.CrossRefGoogle Scholar
Wojtkowiak-Giera, A, Wandurska-Nowak, E, Michalak, M, Derda, M and Łopaciuch, J (2012) Trichinellosis in mice: effect of albendazole on the glutathione transferase in the intestines. Folia Parasitologica 59(4), 311–324.CrossRefGoogle ScholarPubMed
Wu, JM and Hsieh, TC (2011) Resveratrol: a cardioprotective substance. Annals of the New York Academy of Sciences 1215, 16–21.CrossRefGoogle ScholarPubMed
Wu, Z, Sofronic-Milosavljevic, L, Nagano, I and Takahashi, Y (2008) Trichinella spiralis: nurse cell formation with emphasis on analogy to muscle cell repair. Parasites & vectors 1(1), 27.CrossRefGoogle ScholarPubMed
Yan, F, Sun, X and Xu, C (2018) Protective effects of resveratrol improve cardiovascular function in rats with diabetes. Experimental and Therapeutic Medicine 15, 1728–1734.Google ScholarPubMed
Yar, AS, Menevse, S and Alp, E (2011) The effects of resveratrol on cyclooxygenase-1 and -2, nuclear factor kappa beta, matrix metalloproteinase-9, and sirtuin 1 mRNA expression in hearts of streptozotocin-induced diabetic rats. Genetics and Molecular Research 10(4), 2962–7295.CrossRefGoogle ScholarPubMed