Use of anti-freezing proteins in seminal fish cryopreservation
Keywords:
Reproduction, Sperm, Teleost, AFPAbstract
Seminal cryopreservation is one of the most promising reproductive biotechniques for aquaculture, as it allows the transport of gametes, ensures genetic improvements in desired species and minimizes asynchrony between breeding males and females. Despite the benefits, cell damage can be caused during the freezing process, causing decreased quality of sperm. Therefore, studies that seek alternatives that minimize such damage are of great importance. Antifreeze proteins (AFPs) are important compounds originated from evolutionary processes in organisms that live in polar environments. AFPs can be used as possible cryoprotective agents, as they are able to decrease ice crystals and protect the plasma membrane of cells during the freezing process. Thus, this review aims to gather information about the use of antifreeze proteins in the conservation of fish semen and present the main results found in the literature. It was observed that the use of these substances in seminal cryopreservation in fish promoted improvements in the rates of sperm motility, velocities and integrity of the plasma membrane. Such improvements were observed in an interspecific manner. Therefore, further studies are needed in order to verify the effect of AFPs on fertilization capacity, seeking the best option for supplementing the medium.
References
ABED-ELMDOUST, A.; FARAHMAND, H.; AMIRI, B.M.; RAFIEE, G.; RAHIMI, R. Novel droplet vitrification combined with fish antifreeze protein type III enhances cryoprotection of semen in wild endangered Persian sturgeon Acipenser persicus (Borodin, 1897). Aquaculture Research, v.46, n.10 p.2392-2397, 2015.
BAKHACH, J. The cryopreservation of composite tissues: principles and recent advancement on cryopreservation of diferente type of tissues. Organogenesis, v.5, n.3, p.119–126, 2009.
BATISTA, M.; ALAMO, D.; GONZALEZ, F.; CRUZ, M.G.; GRACIA, A. Influence of the freezing technique (nitrogen liquid vs ultra-freezer of -152 degrees and male-to-male variation over the semen quality in Canarian Mastiff breed dogs. Reproduction in Domestic Animals, v.41, n.5, p.423-428, 2006.
BEIRÃO, J.; ZILLI, L.; VILELLA, S.; CABRITA, E.; SCHIAVONE, R.; HERRÁEZ, M.P. Improving sperm cryopreservation with antifreeze proteins: effect on gilthead seabream (Sparus aurata) plasma membrane lipids Biology of Reproduction, v.86, n.2, p.1–9, 2012.
BORYSHPOLETS, S.; SOCHOROVA, D.; RODINA, M.; LINHART, O.; DZYUBA, B. Cryopreservation of carp (Cyprinus carpio L.) sperm: impact of seeding and freezing rates on post–thaw outputs. Biopreservation and Biobanking, v.15, n.3, p.234–240, 2017.
CABRITA, E.; SARASQUETE, C.; MÁRTINEZ-PARAMO, S.; ROBLES, V.; BEIRÃO, J.; PEREZ-CEREZALES, S.; HERRAEZ, M.P. Cryopreservation of fish sperm: applications and perspectives. Journal of Applied Ichthyology, v.26, n.5, p.623-635, 2010.
CAPICCIOTTI, C.J.; DOSHI, M.; BEN, R.N. Ice recrystallization inhibitors: From biological antifreezes to small molecules. In: WILSON, P. Recent Developments in the study of recrystallization. 1a ed., Ottawa: Intech, p.177-224, 2013.
CARNEIRO, P.C.F. Tecnologias de produção e armazenamento de sêmen de peixes. Revista Brasileira de Reprodução Animal, v.31, n.3, p.361-366, 2007.
CARNEIRO, P.C.F.; AZEVEDO, H.C.; SANTOS, J.P.; MARIA, A.N. Cryopreservation of tambaqui (Colossoma macropomum) semen: Extenders, cryoprotectants, dilution ratios and freezing methods. Cryoletters, v.33, n.5, p.285- 393, 2012.
CUEVAS-URIBE, R.; TIERSCH, T.R. Non-Equilibrium vitrification: an introduction and review of studies done in fish. In: TIERSCH, T.R.; GREEN, C.C. Cryopreservation in Aquatic Species, 2a ed., World Aquaculture Society, Baton Rouge, Louisiana, p.309–324, 2011.
CAROLSFELD, J.; GODINHO, H.P.; ZANIBONI, F.E.; HARVEY, B.J. Cryopreservation of sperm in Brazilian migratory fish conservation. Journal of Fish Biology, v.63, p.472-489, 2003.
DEVRIES, A.L.; WOHLSCHLAG, D.E. Freezing resistance in some Antarctic fishes, Science (New York, N.Y.), v.163, n.3871, p.1073–1075, 1969.
DOLEV, M.B.; BRASLAVSKY, I.; DAVIES, P.L. Ice-binding proteins and their function, Annual review of biochemistry. v.85, n.1, p.515–542, 2016.
EWART, K.V.; LIN, Q.; HEW, C.L. Structure, function and evolution of antifreeze proteins. Cellular and Molecular Life Sciences, v.55, n.2, p.271-283, 1999.
FELIZARDO, V.O.; MURGAS, L.D.S.; NAVARRO, R.D.; GONÇALVES, A.C.S.; PAULINO, M. S. Osmolaridade e taxa de diluição na ativação do sêmen criopreservado de curimba (Prochilodus lineatus). Archivos de zootecnia, Córdoba, v.60, n.232, p.1255-1262, 2011.
FIGUEROA, E.; FARIAS. J.G.; LEE-ESTEVEZ, M.; VALDEBENITO, I.; RISOPATRÓN, J.; MAGNOTTI, C.; ROMERO, J.; WATANABE, I.; OLIVEIRA, R.P. 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, v.493, n.1, p.1–8, 2018.
FIGUEROA, E.; VALDEBENITO, I.; FARIAS, J.G. Technologies used in the study of sperm function in cryopreserved fish spermatozoa. Aquaculture research, v.47, n.6, p.1691–1705, 2016.
FIGUEROA, E.; VALDEBENITO, I.; ZEPEDA, A.B.; FIGUEROA, C.A.; DUMORNE, K.; CASTILLO, R.L.; FARIAS, J.G. Effects of cryopreservation on mitochondria of fish spermatozoa. Reviews in Aquaculture, v.9, n.1, p.76-87, 2017.
GRAETHER, S.P.; KUIPER, M.J.; GAGNE, S.M.; WALKER, V.K.; JIA, Z.; SYKES, B.D.; DAVIES, P.L. Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature, v.406, n.6793, p.325-328, 2000.
GUPTA, R.; DESWAL, R. Antifreeze proteins enable plants to survive in freezing conditions. Journal of Biosciences, v.39, n.5, p.931-944, 2014.
GWO, J.C.; ARNOLD, C.R. Cryopreservation of Atlantic croaker spermatozoa: evaluation of morphological changes. Journal of Experimental Zoology, v.264, n.4, p.444–453, 1992.
HE, S.; WOODS, I.L.C. Effects of dimethyl sulfoxide and glycine on cryopreservation induced damage of plasma membranes and mitochondria to striped bass Morone saxatilis) sperm. Cryobiology, v.48, n.3, p.254–262, 2004.
KANDASWAMY, K.K.; CHOU, K.C.; MARTINETZ, T.; MOLLER, S.; SUGANTHAN, P.N.; SRIDHARAN, S.; PUGALENTHI, G. AFP-Pred: A random forest approach for predicting antifreeze proteins from sequence-derived properties. Journal of Theoretical Biology, v.270, n.1, p.56-62, 2011.
KIM, H.J.; LEE, J.H.; HUR, Y.B.; LEE, C.W.; PARK, S.H.; KOO, B.W. Marine antifreeze proteins: structure, function, and application to cryopreservation as a potential cryoprotectant. Mar Drugs, v.15, n.2, p.27, 2017.
KNIGHT, C.A. Adding to the antifreeze agenda. Nature, v.406, n.6793, p.249-251, 2000.
LAHNSTEINER, F.; BERGER, B.; WEISMANN, T.; PATZNER, R. Changes in morphology, physiology, metabolism, and fertilization capacity of rainbow trout semen following cryopreservation. The progressive Fish-Culturist, v.58, n.3, p.149–159, 1996.
LAHNSTEINER, F. Semen cryopreservation in the salmonidae and in the northern pike. Aquaculture Research, v.31, n.3, p.245-258, 2000.
LEGENDRE, M.; BILLARD, R. Cryopreservation of rainbow trout sperm by deep-freezing. Reproduction Nutrition Development, v.20, n.6, p.1859-1868, 1980.
LEITE, L.V. Dose inseminante, embriogênese e criopreservação de sêmen de tambaqui (Colossoma macropomum). 2011. 72p. (Mestrado em Reprodução Animal). Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, Fortaleza, 2011.
LINHART, O.; RODINA, M.; COSSON, J. Cryopreservation of sperm in common carp Cyprinus carpio: sperm motility and hatching success of embryos. Cryobiology, v.41, n.3, p.241–250, 2000.
MAGNOTTI, C.; CERQUEIRA, V.; LEE-ESTEVEZ, M.; FARIAS, J.G.; VALDEBENITO, I.; FIGUEROA, E. Cryopreservation and vitrification of fish semen: a review with special emphasis on marine species. Reviews in Aquaculture, v.10, n.1, p.15–25, 2018.
MARIA, N.A.; AZEVEDO, H.C.; CARNEIRO, P.C.F. Criopreservação de sêmen de peixes no contexto do agronegócio da piscicultura. In: TAVARES-DIAS, M. (Org.). Manejo e sanidade de peixes em cultivo. Amapá: Embrapa Amapá, v.1, p.47-63, 2009.
MERINO, O.; SÁNCHEZ, R.; RISOPATRÓN, J.; ISACHENKO, E.; KATKOV, I.I.; FIGUEROA, E.; VALDEBENITO, I.; MALLMANNP, K.; ISACHENKO, V. Cryoprotectant-free vitrification of fish (Oncorhynchus mykiss) spermatozoa: first report. Andrologia. v.44, n.1, p.390–395, 2012.
MIMS, S.D.; TSVETKOVA, L.I.; BROWN, G.G.; GOMELSKY, B.I. Cryopreservation of sperm of sturgeon and pad- dlefish. Cryopreservation in Aquatic Species (ed. by R.T. TIERSCH; P.M. MAZIK). World AquacultureSociety, Baton Rouge, pv.7, n.1, p.123-129, 2000.
NASCIMENTO, A.F.; MARIA, N.A.; PESSOA, N.O.; CARVALHO, M.A.M.; VIVEIROS, A.T.M. Out-of-season sperm cryopreserved in different media of the Amazonian freshwater fish pirapitinga (Piaractus brachypomus). Animal Reproduction Science, v.118, n.2-4, p.324-329, 2010.
PAYNE, S.R.; OLIVER, J.E.; UPRETI, G.C. Effect of antifreeze proteins on the motility of ram spermatozoa. Cryobiology, v.31, n.2, p.180–184, 1994.
PRATHALINGAM, N.S.; HOLT, W.V.; REVELL, S.G.; MIRCZUK, S.; FLECK, R.A.; WATSON, P.F. Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology, v.66, n.8, p.1894–1900, 2006.
ROBLES, V.; CABRITA, E.; ANEL, L.; HERRÁEZ, M.P. Microinjection of the antifreeze protein type III (AFPIII) in turbot (Scophthalmus maximus) embryos: toxicity and protein dis- tribution. Aquaculture, v.261, n.4, p.1299–1306, 2006.
SALMITO-VANDERLEY, C.S.B.; VIEIRA, M.J.A.F.; LEITE, L.V.; OLIVEIRA, F.C.E.; LINHARES, F.R.A.; SALGUEIRO, C.C.M.; NUNES, J.F. Meios de congelação para conservação de sêmen de peixes da família Characidae. Ciência animal, v.22, n.1, p.255-268, 2012.
SHALIUTINA-KOLEŠOVÁ, A.; GAZO, I.; COSSON, J.; LINHART, O. Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czech journal of Animal sScience, v.58, n.7, p.313-320, 2013.
SULIS, D.B. Sequências nucleotídicas potencialmente capazes de conferir tolerância ao frio e/ou ao congelamento em plantas. 2015. 69p. (Trabalho de conclusão de curso - Biotecnologia). Universidade Federal do Rio Grande do Sul, Porto Alegre, 2015.
TOMCZAK, M.M.; HINCHA, D.K.; ESTRADA, S.D.; WOLKERS, W.F.; CROWE, L.M. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophysical Journal, v.82, n.2, p.874–881, 2002.
VERSTEGEN, J.; IGUER-OUADA, M.; ONCLIN, K. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology, v.57, n.1, p.149-179, 2002.
VIVEIROS, A.T.D.M.; GODINHO, H.P. Sperm quality and cryopreservation of Brazilian freshwater fish species: a review. Fish Physiology and Biochemistry, v.35, n.1, p.137-150, 2009.
VIVEIROS, A.T.D.M.; NASCIMENTO, A.F.; ORFÃO, L.H.; ISAÚ, Z.A. Motility and fertility of the subtropical freshwater fish streaked prochilodus (Prochilodus lineatus) sperm cryopreserved in powdered coconut water. Theriogenology, v.74, n.4, p.551-556, 2010.
WATSON, P.F. Recent developments and concepts in the cryopreservation of spermatozoa and assessment of their post-thawing function. Reproduction Fertility and Development, v.7, n.4, p.871-891, 1995.
XIANG, H.; YANG, X.; KE, L.; HU, Y. The properties, biotechnologies, and applications of antifreeze proteins. International journal of biological macromolecules, v.153, n.1, p.661-675, 2020.
XIN, M.; TUČKOVÁ, V.; RODINA, M.; KHOLODNYY, V.; DADRAS, H.; BORYSHPOLETS, S.; LINHART, O. Effects of antifreeze proteins on cryopreserved sterlet (Acipenser ruthenus) sperm motility variables and fertilization capacity. Animal reproduction science, v.196, p.143-149, 2018.
ZILLI, L.; SCHIAVONE, R.; ZONNO, V.; STORELLI, C.; VILELLA, S. Evaluation of DNA damage in Dicentrarchuslabrax sperm following cryopreservation. Cryobiology v.47, n.3, p.227–235, 2003.
ZILLI, L.; BEIRÃO, J.; SCHIAVONE, R.; HERRAEZ, M.P.; GNONI, A.; VILELLA, S. Comparative proteome analysis of cryopreserved flagella and head plasma membrane proteins from sea bream spermatozoa: effect of antifreeze proteins. PLoS One, v.9, n.6, p.1-10, 2014.
