Use of glycosaminoglycans from Oreochromis niloticus skin as an antioxidant supplement for milt cryopreservation of Brazilian bocachico
DOI:
https://doi.org/10.5433/1679-0359.2021v42n5p2959Keywords:
Cryopreservation, Oxidative stress, Rheophilic fish, Spermatozoa kinetics, Sulfated glycans.Abstract
The study aimed to evaluate the in vitro antioxidant action of glycosaminoglycans (GAGs) from the skin of Oreochromis niloticus, and to determine their ideal concentration to supplement the sperm freezing medium of Prochilodus brevis. In experiment 1, the in vitro antioxidant properties of GAGs were verified through the analysis of DPPH, chelating ferrous ability, and total antioxidant capacity. In experiment 2, milt pools were formed, which were frozen in solution supplemented or not with different GAGs concentrations: 0 (control), 0.5, 1.0, 1.5, 2.0, 2.5, 3.0, 3.5, 4.0, 4.5, or 5.0 mg mL-1 (total of 10 treatments). The samples were evaluated for membrane integrity, DNA integrity, sperm morphology, and sperm kinetics. The results of experiment 1 showed that the GAGs exhibited, with the increase of the concentration, significant antioxidant action, for all the evaluated tests, mainly in the chelating ferrous ability. In experiment 2, it was observed that the increase of GAGs concentration decreased kinetic parameters (P < 0.05), however, the control and 0.5 mg mL-1 GAGs concentration showed similar results. For the other parameters (membrane integrity, DNA integrity, and sperm morphology), there was no decrease in results with the increase of GAGs concentration. In conclusion, GAGs extracted from O. niloticus skin have antioxidant action, and the concentration of 0.5 mg mL-1 was the most adequate to supplement the P. brevis sperm-freezing medium.Downloads
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References
Alencar, P. O. C., Lima, G. C., Barros, F. C. N., Costa, L. E. C., Ribeiro, C. V. P. E., Sousa, W. M.,... Freitas, A. L. P. (2019). A novel antioxidant sulfated polysaccharide from the algae Gracilaria caudata: In vitro and in vivo activities. Food Hydrocolloids, 90, 28-34. doi: 10.1016/j.foodhyd.2018.12.007
Almeida-Monteiro, P. S., Oliveira-Araújo, M. S., Pinheiro, R. R. R., Lopes, J. T., Ferreira, Y. M., Montenegro, A. R.,... Salmito-Vanderley, C. S. B. (2017). Influence of vitamins C and E on the quality of cryopreserved semen Prochilodus brevis (Prochilodontidae, Teleostei). Semina: Ciências Agrárias, 38(4), 2669-2679. doi: 10.5433/1679-0359.2017v38n4Supl1p2669
Almeida‐Monteiro, P. S., Pinheiro, R. R. R., Oliveira-Araújo, M. S., Sales, Y. S., Nascimento, R. V., Nunes, L. T.,... Salmito-Vanderley, C. S. B. (2020). Sperm vitrification of Prochilodus brevis using Powder Coconut Water (ACP-104) in association with different cryoprotectant concentrations. Aquaculture Research, 51(11), 4565-4574. doi: 10.1111/are.14802
Bai, M., Han, W., Zhao, X., Wang, Q., Gao, Y., & Deng, S. (2018). Glycosaminoglycans from a sea snake (Lapemis curtus): extraction, structural characterization and antioxidant activity. Marine Drugs, 16(5), 170. doi: 10.3390/md16050170
Blois, M. S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181(4617), 1199-1200. doi: 10.1038/1811199a0
Blom, E. (1950). A one-minute live-dead sperm stain by means of eosin-nigrosin. Fertility and Sterility, 1(2), 176-177. doi: 10.1016/s0015-0282(16)30125-x
Bomfim, A. C., Peretti, D., Camillo, C. S., Costa, S. A. G. L., & Nascimento, R. S. S. (2015). Reproductive biology and variations in the gonadal development of the fish Curimatã (Prochilodus brevis Steindachner, 1875) in captivity. Biota Amazônia, 5(2), 65-70. doi: 10.18561/2179-5746/biotaamazonia. v5n2p65-70
Browne, R. K., Kaurova, S. A., Uteshev, V. K., Shishova, N. V., McGinnity, D., Figiel, C. R.,… Cosson J. (2015). Sperm motility of externally fertilizing fish and amphibians. Theriogenology, 83(1), 1-13. doi: 10.1016/j.theriogenology.2014.09.018
Cabrita, E., Ma, S., Diogo, P., Martínez-Páramo, S., Sarasquete, C., & Dinis, M. T. (2011). The influence of certain aminoacids and vitamins on post-thaw fish sperm motility, viability and DNA fragmentation. Animal Reproduction Science, 125(1-4), 189-195. doi: 10.1016/j.anireprosci.2011.03.003
Chen, Y. K., Liu, Q. H., Li, J., Xiao, Z. Z., Xu, S. H., Shi, X. H., & Ma, D. Y. (2010). Effect of long-term cryopreservation on physiological characteristics, antioxidant activities and lipid peroxidation of red seabream (Pagrus major) sperm. Cryobiology, 61(2), 189-193. doi: 10.1016/j.cryobiol.2010.07.003
Chew, Y. L., Lim, Y. Y., Omar, M., & Khoo, K. S. (2008). Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT-Food Science and Technology, 41(6), 1067-1072. doi: 10.1016 /j.lwt.2007.06.013
Costa, B. B., Marques, L. S., Lassen, P. G., Rodrigues, R. B., & Streit, D. P. (2019). Cryopreservation‐induced morphological changes in the sperm of South American silver catfish (Rhamdia quelen). Journal of Applied Ichthyology, 35(4), 987-993. doi: 10.1111/jai.13928
Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. D. A., Câmara, R. B. G.,... Rocha, H. A. O. (2010). Biological activities of sulfated polysaccharides from tropical seaweeds. Biomedicine & Pharmacotherapy, 64(1), 21-28. doi: 10.1016/j.biopha.2009.03.005
Costa, R. B., Carvalho, M. A. M., Abreu, K. L., Vidal, D. L., Sales, R. O., Maggioni, R.,... Farias, J. O. (2015). Criação da curimatã comum, Prochilodus cearaensis Steindachner, 1911, em tanque rede. Revista Brasileira de Higiene e Sanidade Animal, 9(3), 482-492. doi: 10.5935/1981-2965.20150044
Donnelly, E. T., McClure, N., & Lewis, S. E. M. (1999). Antioxidant supplementation in vitro does not improve human sperm motility. Fertility and Sterility, 72(3), 484-495. doi: 10.1016/s0015-0282(99)002 67-8
Farias, W. R., Valente, A. P., Pereira, M. S., & Mourão, P. A. (2000). Structure and anticoagulant activity of sulfated galactans isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. Journal of Biological Chemistry, 275(38), 29299-29307. doi: 10.1074/jbc.M002422200
Fernandez, J. L., Muriel, L., Goyanes, V., Segrelles, E., Gosálvez, J., Enciso, M.,... Jonge, C. (2005). Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertility and Sterility, 84(4), 833-842. doi: 10.1016/j.fertnstert.2004.11.089
Fernández-Díez, C., González-Rojo, S., Lombó, M., & Herraez, M. P. (2016). Impact of sperm DNA damage and oocyte-repairing capacity on trout development. Reproduction, 152(1), 57-67. doi: 10.1530/ rep-16-0077
Fernández-Díez, C., González-Rojo, S., Montfort, J., Cam, A. L., Bobe, J., Robles, V.,… Herráez, M. P. (2015). Inhibition of zygotic DNA repair: transcriptome analysis of the offspring in trout (Oncorhynchus mykiss). Reproduction, 149(1), 101-111. doi: 10.1530/REP-14-0382
Ferreira, Y. M. (2019). Efeito da osmolalidade de diferentes soluções ativadoras sobre a cinética espermática do sêmen fresco, resfriado e descongelado de Prochilodus brevis (Actinopterygii:Prochilodontidae). Dissertação de mestrado, Universidade Estadual do Ceará, Fortaleza, CE, Brasil. Recuperado de http://www.uece.br/ppgcv/wp-content/uploads/sites/6/2020/01/Yasmim Maia_Dissertação.pdf
Figueroa, E., Farias, J. G., Lee-Estevez, M., Valdebenito, I., Risopatrón, J., Magnotti, C.,... Oliveira, R. P. S. (2018). Sperm cryopreservation with supplementation of α-tocopherol and ascorbic acid in freezing media increase sperm function and fertility rate in Atlantic salmon (Salmo salar). Aquaculture, 493, 1-8. doi: 10.1016/j.aquaculture.2018.04.046
Figueroa, E., Valdebenito, I., Merino, O., Ubilla, A., Risopatrón, J., & Farias, J. G. (2016). Cryopreservation of Atlantic salmon Salmo salar sperm: effects on sperm physiology. Journal of Fish Biology, 89(3), 1537-1550. doi: 10.1111/jfb.13052
Food and Agriculture Organization of the United Nations (2018). The State Of World Fisheries And Aquaculture. Retrieved from http://www.fao.org/3/i9540en/i9540en.pdf
Gurgel, L. D. L., Verani, J. R., & Chellappa, S. (2012). Reproductive ecology of Prochilodus brevis an endemic fish from the semiarid region of Brazil. The Scientific World Journal, 2012, 1-7. doi: 10.1100/ 2012/810532
Jridi, M., Nasri, R., Marzougui, Z., Abdelhedi, O., Hamdi, M., & Nasri, M. (2019). Characterization and assessment of antioxidant and antibacterial activities of sulfated polysaccharides extracted from cuttlefish skin and muscle. International Journal of Biological Macromolecules, 123, 1221-1228. doi: 10.1016/j.ijbiomac.2018.11.170
Kershaw-Young, C. M., Stuart, C., Evans, G., & Maxwell, W. M. C. (2013). The effect of glycosaminoglycan enzymes and proteases on the viscosity of alpaca seminal plasma and sperm function. Animal Reproduction Science, 138(3-4), 261-267. doi: 10.1016/j.anireprosci.2013.02.005
Lahnsteiner, F., Mansour, N., & Kunz, F. A. (2011). The effect of antioxidants on the quality of cryopreserved semen in two salmonid fish, the brook trout (Salvelinus fontinalis) and the rainbow trout (Oncorhynchus mykiss). Theriogenology, 76(5), 882-890. doi: 10.1016/j.theriogenology.2011.04.019
Leite, L. V., Melo, M. A. P., Oliveira, F. C. E., Pinheiro, J. P. S., Campello, C. C., Nunes, J. F., & Salmito-Vanderley, C. S. B. (2013). Determinação da dose inseminante e embriogênese na fertilização artificial de tambaqui (Colossoma macropomum). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 65(2), 421-429. doi: 10.1590/S0102-09352013000200018
Lopes, J. T., Pinheiro, J. P. S., Nunes, L. T., Pinheiro, R. R. R., Souza, M. E. M., Almeida, P. S.,... Salmito-Vanderley, C. S. B. (2014). Avaliação de diferentes crioprotetores e taxas de diluição na criopreservação seminal de Prochilodus brevis. Revista Brasileira de Reprodução Animal, 38(3), 170-175.
Martínez-Páramo, S., Diogo, P., Dinis, M. T., Herráez, M. P., Sarasquete, C., & Cabrita, E. (2012). Incorporation of ascorbic acid and a-tocopherol to the extender media to enhance antioxidant system of cryopreserved seabass sperm. Theriogenology, 77(6), 1129-1136. doi: 10.1016/j.theriogenology.2011. 10.017
Mendoza, G., Prieto, J., Real, R., Perez, M., Merino, G., & Alvarez, A. (2009). Antioxidant profile of hyaluronan: physico-chemical features and its role in pathologies. Mini Reviews in Medicinal Chemistry, 9(13), 1479-1488. doi: 10.2174/138955709790361494
Miliorini, A. B., Murgas, L. D. S., Rosa, P. V., Oberlender, G., Pereira, G. J. M., & Costa, D. V. (2011). A morphological classification proposal for curimba (Prochilodus lineatus) sperm damages after cryopreservation. Aquaculture Research, 42(2), 177-187. doi: 10.1111/j.1365-2109.2010.02575.x
Najafi, A., Najafi, M., Zanganeh, Z., Sharafi, M., Martinez-Pastor, F., & Adeldust, H. (2014). Cryopreservation of ram semen in extenders containing soybean lecithin as cryoprotectant and hyaluronic acid as antioxidant. Reproduction in Domestic Animals, 49(6), 934-940. doi: 10.1111/rda.1 2405
Nascimento, R. V., Leite-Castro, L. V., Montenegro, A. R., Oliveira-Araújo, M. S., Lopes, J. T., Almeida-Monteiro, P. S.,... Salmito-Vanderley, C. S. B. (2017). Influence of cooling time and diluents on the freezability of Prochilodus brevis semen. Acta Scientiae Veterinariae, 45(1), 1-9. doi: 10.22456/1679-9216.80488
Nunes, L. T., Oliveira, M. S., Lopes, J. T., Souza, M. E. M., Pinheiro, R. R. R., Campello, C. C., & Salmito-Vanderley, C. S. B. (2016). Cryopreservation of Prochilodus brevis semen: freezing media and thawing rates. Semina: Ciências Agrárias, 37(3), 1643-1654. doi: 10.5433/1679-0359.2016v37n3p1643
Nunes, L. T., Oliveira-Araújo, M. S., Lopes, J. T., Almeida-Monteiro, P. S., Nascimento, R. V., Pereira, V. A.,... Salmito-Vanderley, C. S. B. (2019). Fertilizing capacity of the cryopreserved sperm of Prochilodus brevis. Acta Scientiae Veterinariae, 47(1), 1-6. doi: 10.22456/1679-9216.92791
Öğretmen, F., İnanan, B. E., Kutluyer, F., & Kayim, M. (2015). Effect of semen extender supplementation with cysteine on postthaw sperm quality, DNA damage, and fertilizing ability in the common carp (Cyprinus carpio). Theriogenology, 83(9), 1548-1552. doi: 10.1016/j.theriogenology.2015.02.001
Pereira, V. A., Alencar, D. B., Araújo, I. W. F., Rodrigues, J. A. G., Lopes, J. T., Nunes, L. T.,... Salmito-Vanderley, C. S. B. (2020). Supplementation of cryodiluent media with seaweed or Nile tilapia skin sulfated polysaccharides for freezing of Colossoma macropomum (Characiformes: Serrasalmidae) semen. Aquaculture, 528, 1-6. doi: 10.1016/j.aquaculture.2020.735553
Pérez-Cerezales, S., Martínez-Paramo, S., Beirão J., & Herraez, M. P. (2010). Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant. Theriogenology, 74(2), 282-289. doi: 10.1016/j.theriogenology.2010.02.012
Pinheiro, J. P. S., Melo-Maciel, M. A. P., Linhares, F. R. A., Lopes, J. T., Almeida-Monteiro, P. S., Pinheiro, R. R. R., & Salmito-Vanderley, C. S. B. (2016). Use of glucose or BTS™ combined with DMSO or methylglycol under two different freezing protocols for the cryopreservation of sperm from the common curimatã (Prochilodus brevis). Animal Reproduction, 13(4), 779-786. doi: 10.21451/1984-3143-AR782
Pisoschi, A. M., & Pop, A. (2015). The role of antioxidants in the chemistry of oxidative stress: a review. European Journal of Medicinal Chemistry, 97, 55-74. doi: 10.1016/j.ejmech.2015.04.040
Prieto, P., Pineda, M., & Aguilar, M. (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry, 269(2), 337-341. doi: 10.1006/abio.1999.4019
Qian, L., Yu, S., & Zhou, Y. (2016). Protective effect of hyaluronic acid on cryopreserved boar sperm. International Journal of Biological Macromolecules, 87, 287-289. doi: 10.1016/j.ijbiomac.2016.02.075
Salles, T. C., Rodrigues, J. A. G., Barcellos, P. G., Amaral, G. F., Araújo, I. W. F., & Mourão, P. A. S. (2017). Inhibition of thrombin generation by dermatan sulfate isolated from the skin of Oreochromis niloticus. Revista Brasileira de Ciências Agrárias, 12(1), 98-104. doi: 10.5039/agraria.v12i1a5412
Shaliutina-Kolešová, A., Gazo, I., Cosson, J., & Linhart, O. (2013). Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czech Journal of Animal Science, 58(7), 313-320. doi: 10.17221/6861-cjas
Statistical Analysis System Institute (2202). SAS Institute. Statistical Analysis System user’sguide. Version 9.0 ed. Cary: SAS Institute, USA.
Suzuki, K., Eriksson, B., Shimizu, H., Nagai, T., & Rodriguez-Martinez, H. (2000). Effect of hyaluronan on monospermic penetration of porcine oocytes fertilized in vitro. International Journal of Andrology, 23(1), 13-21. doi: 10.1046/j.1365-2605.2000.t01-1-00198.x
Valcarcel, J., Novoa-Carballal, R., Pérez-Martín, R. I., Reis, R. L., & Vázquez, J. A. (2017). Glycosaminoglycans from marine sources as therapeutic agents. Biotechnology Advances, 35(6), 711-725. doi: 10.1016/j.biotechadv.2017.07.008
Zhang, Y. Z., Zhang, S. C., Liu, X. Z., Xu, Y. Y., Wang, C. L., Sawant, M. S.,... Chen, S. L. (2003). Cryopreservation of flounder (Paralichthys olivaceus) sperm with a practical methodology. Theriogenology, 60(5), 989-996. doi: 10.1016/S0093-691X(03)00097-9
Zhang, Y., Duan, X., & Zhuang, Y. (2012). Purification and characterization of novel antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) skin gelatin. Peptides, 38(1), 13-21. doi: 10.1016/j.peptides.2012.08.014
Almeida-Monteiro, P. S., Oliveira-Araújo, M. S., Pinheiro, R. R. R., Lopes, J. T., Ferreira, Y. M., Montenegro, A. R.,... Salmito-Vanderley, C. S. B. (2017). Influence of vitamins C and E on the quality of cryopreserved semen Prochilodus brevis (Prochilodontidae, Teleostei). Semina: Ciências Agrárias, 38(4), 2669-2679. doi: 10.5433/1679-0359.2017v38n4Supl1p2669
Almeida‐Monteiro, P. S., Pinheiro, R. R. R., Oliveira-Araújo, M. S., Sales, Y. S., Nascimento, R. V., Nunes, L. T.,... Salmito-Vanderley, C. S. B. (2020). Sperm vitrification of Prochilodus brevis using Powder Coconut Water (ACP-104) in association with different cryoprotectant concentrations. Aquaculture Research, 51(11), 4565-4574. doi: 10.1111/are.14802
Bai, M., Han, W., Zhao, X., Wang, Q., Gao, Y., & Deng, S. (2018). Glycosaminoglycans from a sea snake (Lapemis curtus): extraction, structural characterization and antioxidant activity. Marine Drugs, 16(5), 170. doi: 10.3390/md16050170
Blois, M. S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181(4617), 1199-1200. doi: 10.1038/1811199a0
Blom, E. (1950). A one-minute live-dead sperm stain by means of eosin-nigrosin. Fertility and Sterility, 1(2), 176-177. doi: 10.1016/s0015-0282(16)30125-x
Bomfim, A. C., Peretti, D., Camillo, C. S., Costa, S. A. G. L., & Nascimento, R. S. S. (2015). Reproductive biology and variations in the gonadal development of the fish Curimatã (Prochilodus brevis Steindachner, 1875) in captivity. Biota Amazônia, 5(2), 65-70. doi: 10.18561/2179-5746/biotaamazonia. v5n2p65-70
Browne, R. K., Kaurova, S. A., Uteshev, V. K., Shishova, N. V., McGinnity, D., Figiel, C. R.,… Cosson J. (2015). Sperm motility of externally fertilizing fish and amphibians. Theriogenology, 83(1), 1-13. doi: 10.1016/j.theriogenology.2014.09.018
Cabrita, E., Ma, S., Diogo, P., Martínez-Páramo, S., Sarasquete, C., & Dinis, M. T. (2011). The influence of certain aminoacids and vitamins on post-thaw fish sperm motility, viability and DNA fragmentation. Animal Reproduction Science, 125(1-4), 189-195. doi: 10.1016/j.anireprosci.2011.03.003
Chen, Y. K., Liu, Q. H., Li, J., Xiao, Z. Z., Xu, S. H., Shi, X. H., & Ma, D. Y. (2010). Effect of long-term cryopreservation on physiological characteristics, antioxidant activities and lipid peroxidation of red seabream (Pagrus major) sperm. Cryobiology, 61(2), 189-193. doi: 10.1016/j.cryobiol.2010.07.003
Chew, Y. L., Lim, Y. Y., Omar, M., & Khoo, K. S. (2008). Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT-Food Science and Technology, 41(6), 1067-1072. doi: 10.1016 /j.lwt.2007.06.013
Costa, B. B., Marques, L. S., Lassen, P. G., Rodrigues, R. B., & Streit, D. P. (2019). Cryopreservation‐induced morphological changes in the sperm of South American silver catfish (Rhamdia quelen). Journal of Applied Ichthyology, 35(4), 987-993. doi: 10.1111/jai.13928
Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. D. A., Câmara, R. B. G.,... Rocha, H. A. O. (2010). Biological activities of sulfated polysaccharides from tropical seaweeds. Biomedicine & Pharmacotherapy, 64(1), 21-28. doi: 10.1016/j.biopha.2009.03.005
Costa, R. B., Carvalho, M. A. M., Abreu, K. L., Vidal, D. L., Sales, R. O., Maggioni, R.,... Farias, J. O. (2015). Criação da curimatã comum, Prochilodus cearaensis Steindachner, 1911, em tanque rede. Revista Brasileira de Higiene e Sanidade Animal, 9(3), 482-492. doi: 10.5935/1981-2965.20150044
Donnelly, E. T., McClure, N., & Lewis, S. E. M. (1999). Antioxidant supplementation in vitro does not improve human sperm motility. Fertility and Sterility, 72(3), 484-495. doi: 10.1016/s0015-0282(99)002 67-8
Farias, W. R., Valente, A. P., Pereira, M. S., & Mourão, P. A. (2000). Structure and anticoagulant activity of sulfated galactans isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. Journal of Biological Chemistry, 275(38), 29299-29307. doi: 10.1074/jbc.M002422200
Fernandez, J. L., Muriel, L., Goyanes, V., Segrelles, E., Gosálvez, J., Enciso, M.,... Jonge, C. (2005). Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertility and Sterility, 84(4), 833-842. doi: 10.1016/j.fertnstert.2004.11.089
Fernández-Díez, C., González-Rojo, S., Lombó, M., & Herraez, M. P. (2016). Impact of sperm DNA damage and oocyte-repairing capacity on trout development. Reproduction, 152(1), 57-67. doi: 10.1530/ rep-16-0077
Fernández-Díez, C., González-Rojo, S., Montfort, J., Cam, A. L., Bobe, J., Robles, V.,… Herráez, M. P. (2015). Inhibition of zygotic DNA repair: transcriptome analysis of the offspring in trout (Oncorhynchus mykiss). Reproduction, 149(1), 101-111. doi: 10.1530/REP-14-0382
Ferreira, Y. M. (2019). Efeito da osmolalidade de diferentes soluções ativadoras sobre a cinética espermática do sêmen fresco, resfriado e descongelado de Prochilodus brevis (Actinopterygii:Prochilodontidae). Dissertação de mestrado, Universidade Estadual do Ceará, Fortaleza, CE, Brasil. Recuperado de http://www.uece.br/ppgcv/wp-content/uploads/sites/6/2020/01/Yasmim Maia_Dissertação.pdf
Figueroa, E., Farias, J. G., Lee-Estevez, M., Valdebenito, I., Risopatrón, J., Magnotti, C.,... Oliveira, R. P. S. (2018). Sperm cryopreservation with supplementation of α-tocopherol and ascorbic acid in freezing media increase sperm function and fertility rate in Atlantic salmon (Salmo salar). Aquaculture, 493, 1-8. doi: 10.1016/j.aquaculture.2018.04.046
Figueroa, E., Valdebenito, I., Merino, O., Ubilla, A., Risopatrón, J., & Farias, J. G. (2016). Cryopreservation of Atlantic salmon Salmo salar sperm: effects on sperm physiology. Journal of Fish Biology, 89(3), 1537-1550. doi: 10.1111/jfb.13052
Food and Agriculture Organization of the United Nations (2018). The State Of World Fisheries And Aquaculture. Retrieved from http://www.fao.org/3/i9540en/i9540en.pdf
Gurgel, L. D. L., Verani, J. R., & Chellappa, S. (2012). Reproductive ecology of Prochilodus brevis an endemic fish from the semiarid region of Brazil. The Scientific World Journal, 2012, 1-7. doi: 10.1100/ 2012/810532
Jridi, M., Nasri, R., Marzougui, Z., Abdelhedi, O., Hamdi, M., & Nasri, M. (2019). Characterization and assessment of antioxidant and antibacterial activities of sulfated polysaccharides extracted from cuttlefish skin and muscle. International Journal of Biological Macromolecules, 123, 1221-1228. doi: 10.1016/j.ijbiomac.2018.11.170
Kershaw-Young, C. M., Stuart, C., Evans, G., & Maxwell, W. M. C. (2013). The effect of glycosaminoglycan enzymes and proteases on the viscosity of alpaca seminal plasma and sperm function. Animal Reproduction Science, 138(3-4), 261-267. doi: 10.1016/j.anireprosci.2013.02.005
Lahnsteiner, F., Mansour, N., & Kunz, F. A. (2011). The effect of antioxidants on the quality of cryopreserved semen in two salmonid fish, the brook trout (Salvelinus fontinalis) and the rainbow trout (Oncorhynchus mykiss). Theriogenology, 76(5), 882-890. doi: 10.1016/j.theriogenology.2011.04.019
Leite, L. V., Melo, M. A. P., Oliveira, F. C. E., Pinheiro, J. P. S., Campello, C. C., Nunes, J. F., & Salmito-Vanderley, C. S. B. (2013). Determinação da dose inseminante e embriogênese na fertilização artificial de tambaqui (Colossoma macropomum). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 65(2), 421-429. doi: 10.1590/S0102-09352013000200018
Lopes, J. T., Pinheiro, J. P. S., Nunes, L. T., Pinheiro, R. R. R., Souza, M. E. M., Almeida, P. S.,... Salmito-Vanderley, C. S. B. (2014). Avaliação de diferentes crioprotetores e taxas de diluição na criopreservação seminal de Prochilodus brevis. Revista Brasileira de Reprodução Animal, 38(3), 170-175.
Martínez-Páramo, S., Diogo, P., Dinis, M. T., Herráez, M. P., Sarasquete, C., & Cabrita, E. (2012). Incorporation of ascorbic acid and a-tocopherol to the extender media to enhance antioxidant system of cryopreserved seabass sperm. Theriogenology, 77(6), 1129-1136. doi: 10.1016/j.theriogenology.2011. 10.017
Mendoza, G., Prieto, J., Real, R., Perez, M., Merino, G., & Alvarez, A. (2009). Antioxidant profile of hyaluronan: physico-chemical features and its role in pathologies. Mini Reviews in Medicinal Chemistry, 9(13), 1479-1488. doi: 10.2174/138955709790361494
Miliorini, A. B., Murgas, L. D. S., Rosa, P. V., Oberlender, G., Pereira, G. J. M., & Costa, D. V. (2011). A morphological classification proposal for curimba (Prochilodus lineatus) sperm damages after cryopreservation. Aquaculture Research, 42(2), 177-187. doi: 10.1111/j.1365-2109.2010.02575.x
Najafi, A., Najafi, M., Zanganeh, Z., Sharafi, M., Martinez-Pastor, F., & Adeldust, H. (2014). Cryopreservation of ram semen in extenders containing soybean lecithin as cryoprotectant and hyaluronic acid as antioxidant. Reproduction in Domestic Animals, 49(6), 934-940. doi: 10.1111/rda.1 2405
Nascimento, R. V., Leite-Castro, L. V., Montenegro, A. R., Oliveira-Araújo, M. S., Lopes, J. T., Almeida-Monteiro, P. S.,... Salmito-Vanderley, C. S. B. (2017). Influence of cooling time and diluents on the freezability of Prochilodus brevis semen. Acta Scientiae Veterinariae, 45(1), 1-9. doi: 10.22456/1679-9216.80488
Nunes, L. T., Oliveira, M. S., Lopes, J. T., Souza, M. E. M., Pinheiro, R. R. R., Campello, C. C., & Salmito-Vanderley, C. S. B. (2016). Cryopreservation of Prochilodus brevis semen: freezing media and thawing rates. Semina: Ciências Agrárias, 37(3), 1643-1654. doi: 10.5433/1679-0359.2016v37n3p1643
Nunes, L. T., Oliveira-Araújo, M. S., Lopes, J. T., Almeida-Monteiro, P. S., Nascimento, R. V., Pereira, V. A.,... Salmito-Vanderley, C. S. B. (2019). Fertilizing capacity of the cryopreserved sperm of Prochilodus brevis. Acta Scientiae Veterinariae, 47(1), 1-6. doi: 10.22456/1679-9216.92791
Öğretmen, F., İnanan, B. E., Kutluyer, F., & Kayim, M. (2015). Effect of semen extender supplementation with cysteine on postthaw sperm quality, DNA damage, and fertilizing ability in the common carp (Cyprinus carpio). Theriogenology, 83(9), 1548-1552. doi: 10.1016/j.theriogenology.2015.02.001
Pereira, V. A., Alencar, D. B., Araújo, I. W. F., Rodrigues, J. A. G., Lopes, J. T., Nunes, L. T.,... Salmito-Vanderley, C. S. B. (2020). Supplementation of cryodiluent media with seaweed or Nile tilapia skin sulfated polysaccharides for freezing of Colossoma macropomum (Characiformes: Serrasalmidae) semen. Aquaculture, 528, 1-6. doi: 10.1016/j.aquaculture.2020.735553
Pérez-Cerezales, S., Martínez-Paramo, S., Beirão J., & Herraez, M. P. (2010). Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant. Theriogenology, 74(2), 282-289. doi: 10.1016/j.theriogenology.2010.02.012
Pinheiro, J. P. S., Melo-Maciel, M. A. P., Linhares, F. R. A., Lopes, J. T., Almeida-Monteiro, P. S., Pinheiro, R. R. R., & Salmito-Vanderley, C. S. B. (2016). Use of glucose or BTS™ combined with DMSO or methylglycol under two different freezing protocols for the cryopreservation of sperm from the common curimatã (Prochilodus brevis). Animal Reproduction, 13(4), 779-786. doi: 10.21451/1984-3143-AR782
Pisoschi, A. M., & Pop, A. (2015). The role of antioxidants in the chemistry of oxidative stress: a review. European Journal of Medicinal Chemistry, 97, 55-74. doi: 10.1016/j.ejmech.2015.04.040
Prieto, P., Pineda, M., & Aguilar, M. (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry, 269(2), 337-341. doi: 10.1006/abio.1999.4019
Qian, L., Yu, S., & Zhou, Y. (2016). Protective effect of hyaluronic acid on cryopreserved boar sperm. International Journal of Biological Macromolecules, 87, 287-289. doi: 10.1016/j.ijbiomac.2016.02.075
Salles, T. C., Rodrigues, J. A. G., Barcellos, P. G., Amaral, G. F., Araújo, I. W. F., & Mourão, P. A. S. (2017). Inhibition of thrombin generation by dermatan sulfate isolated from the skin of Oreochromis niloticus. Revista Brasileira de Ciências Agrárias, 12(1), 98-104. doi: 10.5039/agraria.v12i1a5412
Shaliutina-Kolešová, A., Gazo, I., Cosson, J., & Linhart, O. (2013). Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czech Journal of Animal Science, 58(7), 313-320. doi: 10.17221/6861-cjas
Statistical Analysis System Institute (2202). SAS Institute. Statistical Analysis System user’sguide. Version 9.0 ed. Cary: SAS Institute, USA.
Suzuki, K., Eriksson, B., Shimizu, H., Nagai, T., & Rodriguez-Martinez, H. (2000). Effect of hyaluronan on monospermic penetration of porcine oocytes fertilized in vitro. International Journal of Andrology, 23(1), 13-21. doi: 10.1046/j.1365-2605.2000.t01-1-00198.x
Valcarcel, J., Novoa-Carballal, R., Pérez-Martín, R. I., Reis, R. L., & Vázquez, J. A. (2017). Glycosaminoglycans from marine sources as therapeutic agents. Biotechnology Advances, 35(6), 711-725. doi: 10.1016/j.biotechadv.2017.07.008
Zhang, Y. Z., Zhang, S. C., Liu, X. Z., Xu, Y. Y., Wang, C. L., Sawant, M. S.,... Chen, S. L. (2003). Cryopreservation of flounder (Paralichthys olivaceus) sperm with a practical methodology. Theriogenology, 60(5), 989-996. doi: 10.1016/S0093-691X(03)00097-9
Zhang, Y., Duan, X., & Zhuang, Y. (2012). Purification and characterization of novel antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) skin gelatin. Peptides, 38(1), 13-21. doi: 10.1016/j.peptides.2012.08.014
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2021-07-02
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Nascimento, R. V. do, Pereira, V. A., Almeida-Monteiro, P. S., Sales, Y. S., Araújo, I. W. F. de, Rodrigues, J. A. G., … Salmito-Vanderley, C. S. B. (2021). Use of glycosaminoglycans from Oreochromis niloticus skin as an antioxidant supplement for milt cryopreservation of Brazilian bocachico. Semina: Ciências Agrárias, 42(5), 2959–2978. https://doi.org/10.5433/1679-0359.2021v42n5p2959
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