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http://dx.doi.org/10.14405/kjvr.2021.61.e29

Supplementation of cryoprotective extender with resveratrol decreases apoptosis index and reactive oxygen species levels in post-thaw dog sperm  

Bang, Seonggyu (College of Veterinary Medicine, Chungnam National University)
Tanga, Bereket Molla (College of Veterinary Medicine, Chungnam National University)
Qamar, Ahmad Yar (College of Veterinary Medicine, Chungnam National University)
Fang, Xun (College of Veterinary Medicine, Chungnam National University)
Seong, Gyeonghwan (College of Veterinary Medicine, Chungnam National University)
Nabeel, Abdelbagi Hamad Talha (Laboratory of Theriogenology and Reproductive Biotechnology, College of Veterinary Medicine and Bio-safety Research Institute, Jeonbuk National University)
Yu, Iljeoung (Laboratory of Theriogenology and Reproductive Biotechnology, College of Veterinary Medicine and Bio-safety Research Institute, Jeonbuk National University)
Cho, Jongki (College of Veterinary Medicine, Chungnam National University)
Publication Information
Korean Journal of Veterinary Research / v.61, no.4, 2021 , pp. 29.1-29.7 More about this Journal
Abstract
Resveratrol (RSV, 3,5,4'-trihydroxytrans-stilbene) protects sperm from cryo-induced damage in various animal and human species. In this study, we aimed to assess the effect of dog sperm cryoprotective extender containing RSV on the quality of post-thaw dog sperm. Sperm were collected from 4 Beagles and supplemented with different concentrations of RSV (0, 100, 200, and 400 µM). After thawing, apoptosis index, and reactive oxygen species (ROS) levels were assessed to determine post-thaw sperm quality. Dog sperm cryopreserved with 400 µM RSV showed significant improvement in post-thaw sperm quality with lower apoptosis index and ROS levels (p < 0.05). Our results showed that the supplementation of dog sperm cryoprotective extender with RSV at a concentration of 400 µM improved the post-thaw dog sperm quality in the term of sperm ROS production and apoptosis. In addition, we emphasize the necessity of testing the ROS levels and apoptosis index using flow cytometry to determine the quality of post-thaw semen.
Keywords
apoptosis; cryopreservation; dog; resveratrol; reactive oxygen species;
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1 Stojanovic S, Sprinz H, Brede O. Efficiency and mechanism of the antioxidant action of trans-resveratrol and its analogues in the radical liposome oxidation. Arch Biochem Biophys 2001;391:79-89.   DOI
2 Collodel G, Federico MG, Geminiani M, Martini S, Bonechi C, Rossi C, Figura N, Moretti E. Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod Toxicol 2011;31:239-246.   DOI
3 Hossain MS, Johannisson A, Wallgren M, Nagy S, Siqueira AP, Rodriguez-Martinez H. Flow cytometry for the assessment of animal sperm integrity and functionality: state of the art. Asian J Androl 2011;13:406-419.   DOI
4 Moustafa MH, Sharma RK, Thornton J, Mascha E, Abdel-Hafez MA, Thomas AJ Jr, Agarwal A. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod 2004;19:129-138.   DOI
5 Chatterjee S, Gagnon C. Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Mol Reprod Dev 2001;59:451-458.   DOI
6 Wang AW, Zhang H, Ikemoto I, Anderson DJ, Loughlin KR. Reactive oxygen species generation by seminal cells during cryopreservation. Urology 1997;49:921-925.   DOI
7 Aitken RJ, Buckingham DW, Brindle J, Gomez E, Baker HW, Irvine DS. Analysis of sperm movement in relation to the oxidative stress created by leukocytes in washed sperm preparations and seminal plasma. Hum Reprod 1995;10:2061-2071.   DOI
8 Bomfim MM, Andrade GM, Del Collado M, Sangalli JR, Fontes PK, Nogueira MF, Meirelles FV, da Silveira JC, Perecin F. Antioxidant responses and deregulation of epigenetic writers and erasers link oxidative stress and DNA methylation in bovine blastocysts. Mol Reprod Dev 2017;84:1296-1305.   DOI
9 Zhang T, Chi Y, Ren Y, Du C, Shi Y, Li Y. Resveratrol reduces oxidative stress and apoptosis in podocytes via Sir2-related enzymes, sirtuins1 (SIRT1)/peroxisome proliferator-activated receptor γ co-activator 1α (PGC-1α) axis. Med Sci Monit 2019;25:1220-1231.   DOI
10 Kim EJ, Talha NA, Jeon YB, Yu IJ. Effect of κ-carrageenan on sperm quality in cryopreservation of canine semen. J Anim Reprod Biotechnol 2019;34:57-63.   DOI
11 Zorn B, Golob B, Ihan A, Kopitar A, Kolbezen M. Apoptotic sperm biomarkers and their correlation with conventional sperm parameters and male fertility potential. J Assist Reprod Genet 2012;29:357-364.   DOI
12 Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006;5:14.   DOI
13 Tanga BM, Qamar AY, Raza S, Bang S, Fang X, Yoon K, Cho J. Semen evaluation: methodological advancements in sperm quality-specific fertility assessment: a review. Anim Biosci 2021;34:1253-1270.   DOI
14 Najafi A, Daghigh Kia H, Hamishehkar H, Moghaddam G, Alijani S. Effect of resveratrol-loaded nanostructured lipid carriers supplementation in cryopreservation medium on post-thawed sperm quality and fertility of roosters. Anim Reprod Sci 2019;201:32-40.   DOI
15 Cheng L, Yan B, Chen K, Jiang Z, Zhou C, Cao J, Qian W, Li J, Sun L, Ma J, Ma Q, Sha H. Resveratrol-induced downregulation of NAF-1 enhances the sensitivity of pancreatic cancer cells to gemcitabine via the ROS/Nrf2 signaling pathways. Oxid Med Cell Longev 2018;2018:9482018.
16 Chen TT, Peng S, Wang Y, Hu Y, Shen Y, Xu Y, Yin J, Liu C, Cao J. Improvement of mitochondrial activity and fibrosis by resveratrol treatment in mice with Schistosoma japonicum infection. Biomolecules 2019;9:658.   DOI
17 Guzick DS, Overstreet JW, Factor-Litvak P, Brazil CK, Nakajima ST, Coutifaris C, Carson SA, Cisneros P, Steinkampf MP, Hill JA, Xu D, Vogel DL; National Cooperative Reproductive Medicine Network. Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 2001;345:1388-1393.   DOI
18 Baumber J, Ball BA, Linfor JJ, Meyers SA. Reactive oxygen species and cryopreservation promote DNA fragmentation in equine spermatozoa. J Androl 2003;24:621-628.   DOI
19 Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Gips H, Schill WB, Kruger TF. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004;81:965-972.   DOI
20 Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516.   DOI
21 Kim DS, Hwangbo Y, Cheong HT, Park CK. Effects of discontinuous Percoll gradient containing alpha-linolenic acid on characteristics of frozen-thawed boar spermatozoa. J Anim Reprod Biotechnol 2020;35:58-64.   DOI
22 Kang SS, Kim UH, Lee MS, Lee SD, Cho SR. Spermatozoa motility, viability, acrosome integrity, mitochondrial membrane potential and plasma membrane integrity in 0.25 mL and 0.5 mL straw after frozen-thawing in Hanwoo bull. J Anim Reprod Biotechnol 2020;35:307-314.   DOI
23 Thomassen R, Farstad W. Artificial insemination in canids: a useful tool in breeding and conservation. Theriogenology 2009;71:190-199.   DOI
24 Mahiddine FY, Qamar AY, Kim MJ. Canine amniotic membrane derived mesenchymal stem cells exosomes addition in canine sperm freezing medium. J Anim Reprod Biotechnol 2020;35:268-272.   DOI
25 Bailey JL, Lessard C, Jacques J, Breque C, Dobrinski I, Zeng W, Galantino-Homer HL. Cryopreservation of boar semen and its future importance to the industry. Theriogenology 2008; 70:1251-1259.   DOI
26 Ugur MR, Saber Abdelrahman A, Evans HC, Gilmore AA, Hitit M, Arifiantini RI, Purwantara B, Kaya A, Memili E. Advances in cryopreservation of bull sperm. Front Vet Sci 2019;6:268.   DOI
27 Said TM, Gaglani A, Agarwal A. Implication of apoptosis in sperm cryoinjury. Reprod Biomed Online 2010;21:456-462.   DOI
28 Qamar AY, Fang X, Kim MJ, Cho J. Improved viability and fertility of frozen-thawed dog sperm using adipose-derived mesenchymal stem cells. Sci Rep 2020;10:7034.   DOI
29 Aprioku JS. Pharmacology of free radicals and the impact of reactive oxygen species on the testis. J Reprod Infertil 2013;14:158-172.
30 Banday MN, Lone FA, Rasool F, Rashid M, Shikari A. Use of antioxidants reduce lipid peroxidation and improve quality of crossbred ram sperm during its cryopreservation. Cryobiology 2017;74:25-30.   DOI
31 Lucio CF, Regazzi FM, Silva LC, Angrimani DS, Nichi M, Vannucchi CI. Oxidative stress at different stages of two-step semen cryopreservation procedures in dogs. Theriogenology 2016;85:1568-1575.   DOI
32 Qamar AY, Fang X, Bang S, Kim MJ, Cho J. Effects of kinetin supplementation on the post-thaw motility, viability, and structural integrity of dog sperm. Cryobiology 2020;95:90-96.   DOI
33 Silva EC, Cajueiro JF, Silva SV, Soares PC, Guerra MM. Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology 2012;77:1722-1726.   DOI
34 Mehdipour M, Daghigh Kia H, Nazari M, Najafi A. Effect of lecithin nanoliposome or soybean lecithin supplemented by pomegranate extract on post-thaw flow cytometric, microscopic and oxidative parameters in ram semen. Cryobiology 2017;78:34-40.   DOI
35 Cheng CK, Luo JY, Lau CW, Chen ZY, Tian XY, Huang Y. Pharmacological basis and new insights of resveratrol action in the cardiovascular system. Br J Pharmacol 2020;177:1258-1277.   DOI
36 Guthrie HD, Welch GR. Use of fluorescence-activated flow cytometry to determine membrane lipid peroxidation during hypothermic liquid storage and freeze-thawing of viable boar sperm loaded with 4, 4-difluoro-5-(4-phenyl-1,3-butadienyl)-4-bora-3a,4a-diaza-s-indacene-3-undecanoic acid. J Anim Sci 2007;85:1402-1411.   DOI
37 Waberski D, Riesenbeck A, Schulze M, Weitze KF, Johnson L. Application of preserved boar semen for artificial insemination: past, present and future challenges. Theriogenology 2019;137:2-7.   DOI
38 Jha PK, Sapkota S, Gorkhali NA, Pokharel BR, Jha AK, Bhandari S, Shrestha BS. Seminal attributes and semen cryo-banking of Nepalese Indigenous Achhami (Bos indicus) bull under ex-situ conservation. J Anim Reprod Biotechnol 2019;34:272-279.   DOI
39 Bilodeau JF, Chatterjee S, Sirard MA, Gagnon C. Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing. Mol Reprod Dev 2000;55:282-288.   DOI
40 Qamar AY, Fang X, Bang S, Shin ST, Cho J. The effect of astaxanthin supplementation on the post-thaw quality of dog semen. Reprod Domest Anim 2020;55:1163-1171.   DOI