Abstract
Cryopreservation of male gametes is one of the most important methods of assisted reproductive technologies, which allows preserving gametes for research or further use. However, the fertilizing ability of spermatozoa after cryopreservation decreases by 30–70%, which makes it urgent to search for new substances with cryoprotective properties. The review considers the main causes of cell damage during cryopreservation. The relevance of methods for assessing the formation of crystals and the physicochemical properties of cryoprotective media depending on various compositions is discussed. The problem of stabilization of the spermatozoa membrane during cryopreservation is considered. A possible solution to the problem of membrane integrity may consist in modification of the basic cryoprotective media with yolk emulsion or development of methods for saturation of the membrane phospholipid layer with cholesterol.
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Aitken RJ, Baker MA (2006) Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol 250:66–69. https://doi.org/10.1016/j.mce.2005.12.026
Als-Nielsen J, McMorrow D (2011) Elements of modern X-ray physics, 2nd edn. Wiley
Amirata L, Tainturier D, Jeanneau L, Thorin C, Gerard O, Courtens JL, Anton M (2004) Bull semen in vitro fertility after cryopreservation using egg yolk LDL: a comparison with Optidyl, commercial egg yolk extender. Theriogenology 61:895–907. https://doi.org/10.1016/s0093-691x(03)00259-0
Anger JT, Gilbert BR, Goldstein M (2003) Cryopreservation of sperm: indications, methods and results. J Urol 170(4):1079–1084. https://doi.org/10.1097/01.ju.0000084820.98430.b8
Bachler J, Fuentes-Landete V, Jahn DA, Wong J, Giovambattista N, Loerting T (2016) Glass polymorphism in glycerol-water mixtures: II. Experimental Studies Phys Chem Chem Phys 18(16):11058–11068. https://doi.org/10.1039/C5CP08069J
Bank H, Mazur P (1973) Visualization of freezing damage. J of Cell Biology 57(729). https://doi.org/10.1083/jcb.57.3.729
Barry J. (2004) Life in the frozen state.
Belous AM, Grishenko VI (1986) Cryopreservation of reproductive cells, V.4, Kiev
Best B (2006) Vitrification in cryonics. https://www.benbest.com/cryonics/vitrify.html
Best B (2008) Scientific justification of cryonics practice. Rejuvenation Res 11(2):493–503. https://doi.org/10.1089/rej.2008.0661
Bezugly N, Medvedovsky A (1997) Osmotic response of mammalian oocytes and embryos in cryoprotactive solutions. A method of complex evaluation of potential damaging action of penetrating cryoprotectants. J Problemi Kryobiologii 3:22–26
Bohon RL, Conway WT (1972). DTA Studies on the Glycerol-Water System. https://doi.org/10.1016/0040-6031(72)87016-3
Bourton P, Kaufmann A (1978) Stability of the amorphous state in the system water-glycerol-dimethylsulfoxude. Cryobiology 15:93–108. https://doi.org/10.1016/0011-2240(78)90012-3
Cesar A. Lo ́pez, Alex H. de Vries, Siewert J. Marrink (2013) Computational microscopy of cyclodextrin mediated cholesterol extraction from lipid model membranes. Scientific reports 2071. doi: https://doi.org/10.1038/srep02071
Christian AE, Haynes MP, Phillips MC, Rothblat GH (1997) Use of Cyclodextrins for Manipulating Cellular Cholesterol Content. J Lipid Res 38(11):2264–2272
Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103. https://doi.org/10.1146/annurev.physiol.60.1.73
Darin-Bennett A, White IG (1977) Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold-shock. Cryobiology 14:466–470. https://doi.org/10.1016/0011-2240(77)90008-6
De las Mercedes Carro M. (2020) Cholesterol and desmosterol incorporation into ram sperm membrane before cryopreservation: Effects on membrane biophysical properties and sperm quality. BBA–Biomembranes 1862(3). doi: https://doi.org/10.1016/j.bbamem.2020.183357
Deka BC, Rao AR (1985) Effect of extenders on freezability of buck semen. Ind J Anim Sci 55(12):1038–1040
Deka BC, Rao AR (1986) Effect of egg yolk levels on quality of frozen buck semen. Ind Vet J 63(12):909–912
Di Santo M, Tarozzi N, Nadalini M, Borini A (2012) Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Advances in Urology 2012:1–12. https://doi.org/10.1155/2012/854837
Dunayevskaya AV, Chub NN, Kramar MI, Rodionova VL (2003) Acrosin Activity in Cryopreserved Human Spermatozoa. Problems of Cryobiology and Cryomedicine, (1):65–70. http://cryo.org.ua/journal/index.php/probl-cryobiol-cryomed/article/view/1012
Eroglu A, Toner M, Toth TL (2002) Beneficial effect of microinjected trehalose on the cryosurvival of human oocytes. Fertil Steril 77(1):152–158. https://doi.org/10.1016/s0015-0282(01)02959-4
Fujikawa S. (1981) The effect of various cooling rates on the membrane ultrastructure of frozen human erythrocytes and its relation to the extent of haemolysis after thawing. J. of Cell Science 49(369). doi: https://doi.org/10.1242/jcs.49.1.369
Gao DY (1992) Glycerol permeability of human spermatozoa and its activation energy. Cryobiology 29(6):657–667. https://doi.org/10.1016/0011-2240(92)90068-d
García BM, Ferrusola CO, Aparicio IM, Miró-Morán A, Rodriguez AM, Bolaños JG, Fernandez LG, da Silva CB, Martínez HR, Tapia JA, Peña FJ (2012) Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential. Theriogenology 77(7):1280–1289. https://doi.org/10.1016/j.theriogenology.2011.10.033
Garde JJ, Olmo A, Soler AJ, Espeso G, Roldan ERS, Gomendio M (2008) Effect of egg yolk, cryoprotectant, and various sugars on semen cryopreservation in endangered Cuvier’s gazelle (Gazella cuvieri). Anim Reprod Sci 108:384–401. https://doi.org/10.1016/j.anireprosci.2007.09.010
Grigorieva A, Simonenko E, Garmaeva S, Mironova A, Yakovenko S (2019) Human gametes cryopreservation with cryoprotectant modified by egg yolk. CryoLetters 40(3):187–192. PMID: 31095668
Heimburg T (1998) Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochim Biophys Acta 1415:147–162. https://doi.org/10.1016/S0005-2736(98)00189-8
Hunt CJ (2017) Cryopreservation: vitrification and controlled rate. Cooling Stem Cell Banking 1590:41–77. https://doi.org/10.1007/978-1-4939-6921-0_5
Iaffaldano N, Di Iorio M, Rosato MP, Manchisi A (2014) Cryopreservation of rabbit semen using non-permeable cryoprotectants: effectiveness of different concentrations of low-density lipoproteins (LDL) from egg yolk versus egg yolk or sucrose. Anim Reprod Sci 151:220–228. https://doi.org/10.1016/j.anireprosci.2014.10.020
Ivanova AA, Pryadun VV, Yefanov AN, Yakovenko SA, Simonenko EU (2020) Termodynamic and structural features of water-glycerol solutions as the main component of cryoprotective media for cryopreservation of cells. Rus J Biol Phys Chem 5(3):434–437
Kakar SS, Anand SR (1984) Acrosomal damage and enzyme leakage during freezing preservation of buffalo spermatozoa. Ind J Exp Biol 22(1):5–10
Kalyan S (2011) High-resolution calorimetry on thermal behavior of glycerol (I): Glass transition, crystallization and melting, and discovery of a solid–solid transition. Chem Phys Lett 506:4–6. https://doi.org/10.1016/j.cplett.2011.03.043
Khodko A (2012) Critical phenomena, phase transitions and physical states of water-glycerol solutions during cooling-warming. Chemical Series of Kharkov University Bulletin 21(44):177–184. https://doi.org/10.26565/2220-637X-2012-21-15
Kiryanov KV (2007) Calorimetric research methods. Lobachevskiy State University, Nighniy Novgorod, N.I
Knight CA (1967) The freezing of supercooled liquids. D. Van Nostrand Company Inc, Princeton, NJ
Lone SA (2018) Possible mechanisms of cholesterol-loaded cyclodextrin action on sperm during cryopreservation. Anim Reprod Sci 192:1–5. https://doi.org/10.1016/j.anireprosci.2018.03.009
Lundheim R (2002) Physiological and ecological significance of biological ice nucleators. Philos Trans R Soc Lond B Biol Sci 357(1423):937–943. https://doi.org/10.1098/rstb.2002.1082
Luyet B, Rasmussen D (1968) Study by differential thermal analysis of the temperatures of instability of rapidly cooled solutions of glycerol, ethylene glycol, sucrose and glucose. Biodynamica 10:167–191
MacFarlane DR, Forsyth M (1987) Devitrification and recrystallization of glass forming aqueous solutions. The Biophysics of Organ Cryopreservation 147:237–263
Mazur P (1984) Freezing of living cells: mechanisms and implications. J Physiol 247:C125–C142. https://doi.org/10.1152/ajpcell.1984.247.3.C125
Meyer F, Smit B (2009) Effect of cholesterol on the structure of a phospholipid bilayer. PNAS 106(10):3654–3658. https://doi.org/10.1073/pnas.0809959106
Mocé E (2010) Use of cholesterol in sperm cryopreservation: present moment and perspectives to future. Reprod Domest Anim 45:57–66. https://doi.org/10.1111/j.1439-0531.2010.01635.x
Muldrew K, McGann LE (1994) The osmotic rupture hypothesis of intracellular freezing injury. Biophys J 66(2):532–541. https://doi.org/10.1016/s0006-3495(94)80806-9
Murata K-I, Tanaka H (2012) Liquid–liquid transition without macroscopic phase separation in a water–glycerol mixture. Nat Mater 11(5):436–443. https://doi.org/10.1038/nmat3271
Murata K-I, Tanaka H (2013) General nature of liquid-liquid transition in aqueous organic solutions. Nat Commun 4:2844. https://doi.org/10.1038/ncomms3844(2013)
Nauk VA (1985) Structural and biochemical cryodamages of gamete biomembranes in male farm animals. Cryobiology 2:47–50
Ohvo H, Peter Slotte J (1996)- Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol - structure and phospholipids on desorption rate. Biochemistry 35(24). doi: https://doi.org/10.1021/bi9528816
Petrunkina A (2007) Fundamental aspects of gamete cryobiology. J Reproductionsmed Endokrinol 4(2):78–91
Pillet E et al (2011) Egg yolk plasma can replace egg yolk in stallion freezing extenders. Theriogenology 75(1):105–114. https://doi.org/10.1016/j.theriogenology.2010.07.015p.105-114
Popov I, Greenbaum GA, Sokolov AP, Feldman Y (2015) The puzzling first-order phase transition in water–glycerol mixtures. Phys Chem Chem Phys J 17(27):18063–18071. https://doi.org/10.1039/C5CP02851E
Purdy P, Graham J (2004) Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility. Biol Reprod 71:522–527. https://doi.org/10.1095/biolreprod.103.025577
Quinn PJ (1985) A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology 22(2):128–146. https://doi.org/10.1016/0011-2240(85)90167-1
Ri-Cheng C (2010) Cryobiology: an overview Chapter 1, in Fertility Cryopreservation, Cambridge, pp 1-9. https://doi.org/10.1017/CBO9780511730207.002
Roffay C. (2021) Passive coupling of membrane tension and cell volume during active response of cells to osmosis. PNAS: Biophysics and computational biology, 118(47).doi: https://doi.org/10.1073/pnas.2103228118
Salmon VM et al (2016) Cholesterol-Loaded Cyclodextrin Increases the Cholesterol Content of Goat Sperm to Improve Cold and Osmotic Resistance and Maintain Sperm Function after Cryopreservation. Biol Reprod 94(4):85. https://doi.org/10.1095/biolreprod.115.128553
Sheriff DS (2010) Perspective on plasma membrane cholesterol efflux and spermatozoal function. J Hum Reprod Sci 3(2):68–75. https://doi.org/10.4103/0974-1208.69337
Simonenko EU, Pryadun VV, Ivanova AA, Burmistrova EV, Vasiliev AN, Yakovenko SA (2019) An adiabatic calorimetry method to determine the thermodynamic characteristics of cryoprotectants. Biophysics 64(1):1–6. https://doi.org/10.1134/S0006350919010172
Simpson AM, White JG (1986) Effect of cold shock and cooling rate on calcium uptake of ram spermatozoa. Anim Reprod Sci 12(2):131–143. https://doi.org/10.1016/0378-4320(86)90053-9
Thomas P, Meizel S (1988) An influx of extracelluar calcium is required for initiation of the human sperm acrosome reaction induced by human follicular fluid. Gamete Res 20(4):397–411. https://doi.org/10.1002/mrd.1120200402
Torska J, Swidowicz K, Strezek J (1985) Biochemiczne I morfologiczne zmiany w plemenikach zdyskwalifikowanego nasienia buhajow. Med Weter 41(1):48–50
Vali G (1995) Principles of ice nucleation. APS Press, Wyoming
Watson PF, Martin IC (1975) The influence of some fractions of egg yolk on the survival of ram spermatozoa at 5 degrees C. Aust J Biol Sci 28:145–152. https://doi.org/10.1071/bi9750145
Yildiz C, Bozkurt Y, Yavas I (2013) An evaluation of soybean lecithin as an alternative to avian egg yolk in the cryopreservation of fish sperm. Cryobiology 67:91–94. https://doi.org/10.1016/j.cryobiol.2013.05.008
Zhmakin A (2008) Physical aspects of cryobiology. J Phys Usp 51:231–252. https://doi.org/10.3367/UFNr.0178.200803b.0243
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A.I. and E.S. conceptualized, outlined, and wrote the first draft of the manuscript. All authors finalized the manuscript.
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Ivanova, A., Simonenko, E., Yakovenko, S. et al. Problems of human spermatozoa cryopreservation: research methods, solutions. Biophys Rev 15, 1223–1232 (2023). https://doi.org/10.1007/s12551-023-01133-x
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DOI: https://doi.org/10.1007/s12551-023-01133-x