Antioxidant effects of lycopene on bovine sperm survival and oxidative profile following cryopreservation
E. Tvrda, A. Mackovich, H. Greifova, F. Hashim, N. Lukachttps://doi.org/10.17221/86/2017-VETMEDCitation:Tvrda E., Mackovich A., Greifova H., Hashim F., Lukac N. (2017): Antioxidant effects of lycopene on bovine sperm survival and oxidative profile following cryopreservation. Veterinarni Medicina, 62: 429-436.
Reactive oxygen species overgeneration as a side effect of semen cryopreservation may lead to lipid peroxidation, protein degradation, DNA fragmentation and cell death, resulting in a decrease of sperm survival and fertilisation ability. Lycopene has been proposed as a potential supplement to semen extenders because of its antioxidant properties. The aim of this study was to evaluate the effects of lycopene on the structural integrity, functional activity and selected oxidative stress parameters of cryopreserved bovine sperm. Thirty bovine ejaculates were split into two aliquots and diluted with a commercial semen extender supplemented with 1.5 mmol/l lycopene or containing no supplement (control), cooled down to 4 °C, frozen and kept in liquid nitrogen. Prior to experiments, frozen straws were thawed at 37 °C for 20 s. Lycopene addition resulted in a higher sperm motility (P < 0.001), progressive motility (P < 0.001) and all secondary motion characteristics (P < 0.001 with respect to the average path velocity, linear velocity, velocity of curvilinear motion, beat cross frequency, path straightness and linearity; P < 0.01 in the case of the amplitude of lateral head displacement). Furthermore, lycopene exhibited protective effects on the sperm membrane (P < 0.05) and acrosomal (P < 0.01) integrity in comparison to control. An assay for metabolic function revealed that lycopene supplementation to the cryopreservation medium resulted in a higher preservation of the sperm mitochondrial activity (P < 0.001). Reactive oxygen species production as well as intracellular superoxide generation were decreased following lycopene addition (P < 0.01 in the case of reactive oxygen species; P < 0.001 with respect to superoxide production). Finally, the presence of lycopene led to a decrease in protein carbonyl production (P < 0.01), lipid peroxidation (P < 0.001) as well as oxidative DNA damage (P < 0.05) when compared to control. In conclusion, lycopene exhibited significant reactive oxygen species-trapping and antioxidant properties which may prevent oxidative damage to frozen-thawed sperm, and, thus, enhance the post-thaw vitality of male reproductive cells in cattle breeding.Keywords:
oxidative stress; reactive oxygen species; bulls; supplementsReferences:
Agarwal Ashok, Saleh Ramadan A., Bedaiwy Mohamed A. (2003): Role of reactive oxygen species in the pathophysiology of human reproduction. Fertility and Sterility, 79, 829-843 https://doi.org/10.1016/S0015-0282(02)04948-8Aitken R. J. (1989): Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biology of Reproduction, 41, 183-197 https://doi.org/10.1095/biolreprod41.1.183Aly Hamdy A.A., El-Beshbishy Hesham A., Banjar Zainy M. (2012): Mitochondrial dysfunction induced impairment of spermatogenesis in LPS-treated rats: Modulatory role of lycopene. European Journal of Pharmacology, 677, 31-38 https://doi.org/10.1016/j.ejphar.2011.12.027Andreea A, Stela Z (2010): Role of antioxidant additives in the protection of the cryopreserved semen against free radicals. Romanian Biotechnological Letters 15, 33–41.Atasoy Nurhayat (2012): Biochemistry of Lycopene. Journal of Animal and Veterinary Advances, 11, 2605-2610 https://doi.org/10.3923/javaa.2012.2605.2610Atessahin A, Karahan I, Turk G, Gurb S, Yilmaz S, Ceribasi AO (2006a): Protective role of lycopene on cisplatin-induced changes in sperm. Reproductive Toxicology 21, 42–47.Atessahin A, Turk G, Karahan I, Yilmaz S, Ceribasi AO, Bulmus O (2006b): Lycopene prevents adriamycin-induced testicular toxicity in rats. Fertility and Sterility 85, 1216–1222.Bailey J., Morrier A., Cormier N. (2003): Semen cryopreservation: Successes and persistent problems in farm species. Canadian Journal of Animal Science, 83, 393-401 https://doi.org/10.4141/A03-024Ball Barry A. (2008): Oxidative stress, osmotic stress and apoptosis: Impacts on sperm function and preservation in the horse. Animal Reproduction Science, 107, 257-267 https://doi.org/10.1016/j.anireprosci.2008.04.014Bucak Mustafa Numan, Ateşşahin Ahmet, Yüce Abdurrauf (2008): Effect of anti-oxidants and oxidative stress parameters on ram semen after the freeze–thawing process. Small Ruminant Research, 75, 128-134 https://doi.org/10.1016/j.smallrumres.2007.09.002Bucak Mustafa Numan, Tuncer Pürhan Barbaros, Sarıözkan Serpil, Başpınar Nuri, Taşpınar Mehmet, Çoyan Kenan, Bilgili Ali, Akalın Pınar Peker, Büyükleblebici Serhat, Aydos Sena, Ilgaz Seda, Sunguroğlu Asuman, Öztuna Derya (2010): Effects of antioxidants on post-thawed bovine sperm and oxidative stress parameters: Antioxidants protect DNA integrity against cryodamage. Cryobiology, 61, 248-253 https://doi.org/10.1016/j.cryobiol.2010.09.001Bucak M. N., Ataman M. B., Başpınar N., Uysal O., Taşpınar M., Bilgili A., Öztürk C., Güngör Ş., İnanç M. E., Akal E. (2014): Lycopene and resveratrol improve post-thaw bull sperm parameters: sperm motility, mitochondrial activity and DNA integrity. Andrologia, , n/a-n/a https://doi.org/10.1111/and.12301Choi Soo-Kyong, Seo Jung-Sook (2013): Lycopene supplementation suppresses oxidative stress induced by a high fat diet in gerbils. Nutrition Research and Practice, 7, 26- https://doi.org/10.4162/nrp.2013.7.1.26Çoyan Kenan, Başpınar Nuri, Bucak Mustafa Numan, Akalın Pınar Peker (2011): Effects of cysteine and ergothioneine on post-thawed Merino ram sperm and biochemical parameters. Cryobiology, 63, 1-6 https://doi.org/10.1016/j.cryobiol.2011.04.001de Lamirande E, Gagnon C (1992): Reactive oxygen species and human spermatozoa. I. Effects on the motility of intact spermatozoa and on sperm axonemes. Journal of Andrology 13, 368–378.Devaraj Sridevi, Mathur Surekha, Basu Arpita, Aung Hnin H., Vasu Vihas T., Meyers Stuart, Jialal Ishwarlal (2008): A Dose-Response Study on the Effects of Purified Lycopene Supplementation on Biomarkers of Oxidative Stress. Journal of the American College of Nutrition, 27, 267-273 https://doi.org/10.1080/07315724.2008.10719699Filipcikova R, Oborna I, Brezinova J, Novotny J, Wojewodka G, De Sanctis JB (2015): Lycopene improves the distorted ratio between AA/DHA in the seminal plasma of infertile males and increases the likelihood of successful pregnancy. Biomedical Papers of the Medical Faculty of the University Palacky, Olomouc, Czech Republic 159, 77–82.Goyal A., Delves G. H., Chopra M., Lwaleed B. A., Cooper A. J. (2006): Can lycopene be delivered into semen via prostasomes? In vitro incorporation and retention studies. International Journal of Andrology, 29, 528-533 https://doi.org/10.1111/j.1365-2605.2006.00690.xKashou AH, Sharma R, Agarwal A (2013): Assessment of oxidative stress in sperm and semen. Methods in Molecular Biology 927, 351–361.Mangiagalli MG, Marelli SP, Cavalchini LG (2007): Effect of lycopene on fowl sperm characteristics during in vitro storage. Archiv fur Geflugelkunde 71, 25–29.Martinez-Pastor F, Johannisson A, Gil J, Kaabi M, Anel L, Paz P, Rodriguez-Martinez H (2004): Use of chromatin stability assay, mitochondrial stain JC-1, and fluorometric assessment of plasma membrane to evaluate frozen-thawed ram semen. Animal Reproduction Science, 84, 121-133 https://doi.org/10.1016/j.anireprosci.2003.12.006Meseguer Marcos, Antonio Martinez-Conejero Jose, Muriel Lourdes, Pellicer Antonio, Remohi Jose, Garrido Nicolas (2007): The Human Sperm Glutathione System: A Key Role in Male Fertility and Successful Cryopreservation. Drug Metabolism Letters, 1, 121-126 https://doi.org/10.2174/187231207780363633Moskovtsev SI, Librach CL (2013): Methods of sperm vitality assessment. In: Carrell DT, Aston KI (eds): Spermatogenesis: Methods and Protocols, Methods in Molecular Biology. Springer Science + Business Media, New York. 13–19.Pope C.E., Zhang Y.Z., Dresser B.L. (1991): A simple staining method for quantifying the acrosomal status of cat spermatozoa. Theriogenology, 35, 257- https://doi.org/10.1016/0093-691X(91)90233-4Raj KAA, Langeswaran K, Krisnamoorthy P (2012): Attenuation of polychlorinated biphenyl induced hormonal disruption by lycopene. Journal of Pharmaceutical and Biomedical Sciences 18, 1–5.Rosato MP, Centoducati G, Santacroce MP, Iaffaldano N (2012a): Effects of lycopene on in vitro quality and lipid peroxidation in refrigerated and cryopreserved turkey spermatozoa. British Poultry Science 53, 545–552.Rosato MP, Di Iorio M, Manchisi A, Gambacorta M, Petrosino G, Centoducati G, Santacroce MP, Iaffaldano N (2012b): In vitro survival and lipid peroxidation status of rabbit spermatozoa after both chilled and frozen storage in lycopene enriched extenders. Livestock Science 146, 199–202.Sarkar PD, Gupta T, Sahu A (2012): Comparative analysis of lycopene in oxidative stress. The Journal of the Association of Physicians of India 60, 17–19.Shannon P., Vishwanath R. (1995): The effect of optimal and suboptimal concentrations of sperm on the fertility of fresh and frozen bovine semen and a theoretical model to explain the fertility differences. Animal Reproduction Science, 39, 1-10 https://doi.org/10.1016/0378-4320(95)01376-BTamiselvan P, Bharathiraja K, Vijayaprakash S, Balasubramanian MP (2013): Protective role of lycopene on bisphenol A induced changes in sperm characteristics, testicular damage and oxidative stress. International Journal of Pharma and Bio Sciences 4, 131–143.Tas M, Saruhan BG, Kurt D, Yokus B, Denli M (2010): Protective role of lycopene on aflatoxin B1 induced changes in sperm characteristics and testicular damages in rats. Kafkas Universitesi Veteriner Fakultesi Dergisi 16, 597–604.Türk Gaffari, Ateşşahin Ahmet, Sönmez Mustafa, Yüce Abdurrauf, Çeribaşi Ali Osman (2007): Lycopene protects against cyclosporine A-induced testicular toxicity in rats. Theriogenology, 67, 778-785 https://doi.org/10.1016/j.theriogenology.2006.10.013Tvrdá Eva, Kňažická Zuzana, Bárdos László, Massányi Péter, Lukáč Norbert (2011): Impact of oxidative stress on male fertility — A review. Acta Veterinaria Hungarica, 59, 465-484 https://doi.org/10.1556/AVet.2011.034Tvrda E, Kovacik A, Tusimova E, Paal D, Mackovich A, Alimov J, Lukac N (2016a): Antioxidant efficiency of lycopene on oxidative stress – induced damage in bovine spermatozoa. Journal of Animal Science and Biotechnology 7, 50–63.Tvrda E, Lukac N, Jambor T, Lukacova J, Hashim F, Massanyi P (2016b): In vitro supplementation of lycopene to bovine spermatozoa: effects on motility, viability and superoxide production. Animal Science Papers and Reports 34, 319–328.Uysal O., Bucak M. N. (): Effects of Oxidized Glutathione, Bovine Serum Albumin, Cysteine and Lycopene on the Quality of Frozen-Thawed Ram Semen. Acta Veterinaria Brno, 76, 383-390 https://doi.org/10.2754/avb200776030383Weber Daniela, Davies Michael J., Grune Tilman (2015): Determination of protein carbonyls in plasma, cell extracts, tissue homogenates, isolated proteins: Focus on sample preparation and derivatization conditions. Redox Biology, 5, 367-380 https://doi.org/10.1016/j.redox.2015.06.005Zini Armand, San Gabriel Maria, Libman Jamie (2010): Lycopene supplementation in vitro can protect human sperm deoxyribonucleic acid from oxidative damage. Fertility and Sterility, 94, 1033-1036 https://doi.org/10.1016/j.fertnstert.2009.04.004Zribi Nassira, Chakroun Nozha, Elleuch Henda, Abdallah Fatma, Ben Hamida Afifa, Gargouri Jalel, Fakhfakh Faiza, Keskes Leila (2011): Sperm DNA fragmentation and oxidation are independent of malondialdheyde. Reproductive Biology and Endocrinology, 9, 47- https://doi.org/10.1186/1477-7827-9-47