Cryopreservation of farm animal gametes and embryos: recent updates and progress

Abstract

Cryopreservation has undergone tremendous advances and is widely used in animal production based on decades of study of cellular permeability, freezability and empirical generalization. Several improvement are particularly important: the cryopreservation protocol has been continuously refined over the years to achieve greater reproductive performance; cryoprotective agents are more effective and less toxic than previously; there has been significant innovation in advanced cryopreservation systems and carriers. Despite this, there are still problems that urgently require practical solutions, such as remedies for cryodamage and encouraging the use of frozen–thawed porcine sperm in pig production.

Keywords

vitrification / gametes / embryo / animal production / cryoprotective agent / freezability

References

[1] Saragusty J, Arav A. Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction, 2011, 141(1): 1–19

[2] Roca J, Parrilla I, Gil M A, Cuello C, Martinez E A, Rodriguez-Martinez H. Non-viable sperm in the ejaculate: lethal escorts for contemporary viable sperm. Animal Reproduction Science, 2016, 169: 24–31

[3] Gordon I. Reproductive technologies in farm Animals. In: Gordon I. In vitro embryo production. 2nd ed. Cambridge: CABI Pub, 2017, 100–101

[4] George P. 2015 statistics of embryo collection and transfer in domestic farm animals. IETS Data Retrieval Committee, 2015

[5] Thompson M, Nemits M, Ehrhardt R. Rate-controlled cryopreservation and thawing of mammalian cells. Protocol Exchange2011. doi: 10.1038/protex.2011.224

[6] Day J G, Stacey G N, Gefriertrocknen. Cryopreservation and freeze-drying protocols. FEBS Letters, 2007, 377(2): 281–282

[7] Arav A. Cryopreservation of oocytes and embryos. Theriogenology, 2014, 81(1): 96–102

[8] Brambillasca F, Guglielmo M C, Coticchio G, Mignini Renzini M, Dal Canto M, Fadini R. The current challenges to efficient immature oocyte cryopreservation. Journal of Assisted Reproduction and Genetics, 2013, 30(12): 1531–1539

[9] Moussa M, Shu J, Zhang X, Zeng F. Cryopreservation of mammalian oocytes and embryos: current problems and future perspectives. Science China Life Sciences, 2014, 57(9): 903–914

[10] Shepherd V A. The cytomatrix as a cooperative system of macromolecular and water networks. Current Topics in Developmental Biology, 2006, 75: 171–223

[11] Pessarakli M. Handbook of plant and crop stress. 3rd ed. Boca Raton: CRC Press, 2011, 1215

[12] Yavin S, Arav A. Measurement of essential physical properties of vitrification solutions. Theriogenology, 2007, 67(1): 81–89

[13] Vajta G, Holm P, Kuwayama M, Booth P J, Jacobsen H, Greve T, Callesen H. Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Molecular Reproduction and Development, 1998, 51(1): 53–58

[14] Rall W F. Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology, 1987, 24(5): 387–402

[15] Varghese A C, Nagy Z P, Agarwal A. Current trends, biological foundations and future prospects of oocyte and embryo cryopreservation. Reproductive Biomedicine Online, 2009, 19(1): 126–140

[16] Leibo S P. A one-step method for direct nonsurgical transfer of frozen-thawed bovine embryos. Theriogenology, 1984, 21(5): 767–790

[17] Rexer-Huber K M J, Bishop P J, Wharton D A. Skin ice nucleators and glycerol in the freezing-tolerant frog Litoria ewingii. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 2011, 181(6): 781–792

[18] Saha S, Otoi T, Takagi M, Boediono A, Sumantri C, Suzuki T. Normal calves obtained after direct transfer of vitrified bovine embryos using ethylene glycol, trehalose, and polyvinylpyrrolidone. Cryobiology, 1996, 33(3): 291–299

[19] Kasai M, Niwa K, Iritani A. Effects of various cryoprotective agents on the survival of unfrozen and frozen mouse embryos. Journal of Reproduction and Fertility, 1981, 63(1): 175–180

[20] Whittingham D G, Leibo S P, Mazur P. Survival of mouse embryos frozen to –196 degrees and –269 degrees C. Science, 1972, 178(4059): 411–414

[21] Arav A, Saragusty J. Directional freezing of spermatozoa and embryos. Reproduction, Fertility, and Development, 2013, 26(1): 83–90

[22] Chen S U, Lien Y R, Cheng Y Y, Chen H F, Ho H N, Yang Y S. Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids. Human Reproduction, 2001, 16(11): 2350–2356

[23] Puhlev I, Guo N, Brown D R, Levine F. Desiccation tolerance in human cells. Cryobiology, 2001, 42(3): 207–217

[24] Guo N, Puhlev I, Brown D R, Mansbridge J, Levine F. Trehalose expression confers desiccation tolerance on human cells. Nature Biotechnology, 2000, 18(2): 168–171

[25] Arav A, Yavin S, Zeron Y, Natan D, Dekel I, Gacitua H. New trends in gamete’s cryopreservation. Molecular and Cellular Endocrinology, 2002, 187(1–2): 77–81

[26] Arav A, Zeron Y. Vitrification of bovine oocytes using modified minimum drop size technique (MDS) is effected by the composition and the concentration of the vitrification solution and by the cooling conditions. Theriogenology, 1997, 47(1): 341

[27] Yavin S, Aroyo A, Roth Z, Arav A. Embryo cryopreservation in the presence of low concentration of vitrification solution with sealed pulled straws in liquid nitrogen slush. Human Reproduction, 2009, 24(4): 797–804

[28] Wilmut I, Rowson L E. Experiments on the low-temperature preservation of cow embryos. Veterinary Record, 1973, 92(26): 686–690

[29] Wilmut I, Rowson L E. The successful low-temperature preservation of mouse and cow embryos. Journal of Reproduction and Fertility, 1973, 33(2): 352–353

[30] Rall W F, Fahy G M. Ice-free cryopreservation of mouse embryos at -196 degrees C by vitrification. Nature, 1985, 313(6003): 573–575

[31] Massip A, Zwalmen P V D, Scheffen B, Ectors F. Pregnancies following transfer of cattle embryos preserved by vitrification. Cryo Letters, 1986, 7: 270–273

[32] Yuswiati E, Holtz W. Work in progress: successful transfer of vitrified goat embryos. Theriogenology, 1990, 34(4): 629–632

[33] Széll A, Zhang J, Hudson R. Rapid cryopreservation of sheep embryos by direct transfer into liquid nitrogen vapour at -180 degrees C. Reproduction, Fertility, and Development, 1990, 2(6): 613–618

[34] Dobrinsky J R. Cellular approach to cryopreservation of embryos. Theriogenology, 1996, 45(45): 17–26

[35] Pedro P B, Yokoyama E, Zhu S E, Yoshida N, Valdez D M Jr, Tanaka M, Edashige K, Kasai M. Permeability of mouse oocytes and embryos at various developmental stages to five cryoprotectants. Journal of Reproduction and Development, 2005, 51(2): 235–246

[36] Lonergan P, Rizos D, Gutiérrez-Adán A, Fair T, Boland M P. Effect of culture environment on embryo quality and gene expression- experience from animal studies. Reproductive Biomedicine Online, 2003, 7(6): 657–663

[37] McEvoy T G, Robinson J J, Sinclair K D. Developmental consequences of embryo and cell manipulation in mice and farm animals. Reproduction, 2001, 122(4): 507–518

[38] Abdalla H, Shimoda M, Hara H, Morita H, Kuwayama M, Hirabayashi M, Hochi S. Vitrification of ICSI- and IVF-derived bovine blastocysts by minimum volume cooling procedure: effect of developmental stage and age. Theriogenology, 2010, 74(6): 1028–1035

[39] Dos Santos Neto P C, Vilariño M, Barrera N, Cuadro F, Crispo M, Menchaca A. Cryotolerance of Day 2 or Day 6 in vitro produced ovine embryos after vitrification by Cryotop or Spatula methods. Cryobiology, 2015, 70(1): 17–22

[40] Shirazi A, Shams-Esfandabadi N, Ahmadi E, Heidari B. Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development. Reproduction in Domestic Animals, 2010, 45(3): 530–536

[41] Pereira R M, Baptista M C, Vasques M I, Horta A E, Portugal P V, Bessa R J, Silva J C, Pereira M S, Marques C C. Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Animal Reproduction Science, 2007, 98(3–4): 293–301

[42] Barceló-Fimbres M, Seidel G E Jr. Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro. Molecular Reproduction and Development, 2007, 74(11): 1406–1418

[43] Sudano M J, Paschoal D M, Rascado T S, Magalhães L C, Crocomo L F, de Lima-Neto J F, Landim-Alvarenga F C. Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology, 2011, 75(7): 1211–1220

[44] Pryor J H, Looney C R, Romo S, Kraemer D C, Long C R. Cryopreservation of in vitro produced bovine embryos: effects of lipid segregation and post-thaw laser assisted hatching. Theriogenology, 2011, 75(1): 24–33

[45] Pero M E, Zullo G, Esposito L, Iannuzzi A, Lombardi P, De Canditiis C, Neglia G, Gasparrini B. Inhibition of apoptosis by caspase inhibitor Z-VAD-FMK improves cryotolerance of in vitro derived bovine embryos. Theriogenology, 2018, 108: 127–135

[46] Yacoub A N A, Gauly M, Holtz W. Open pulled straw vitrification of goat embryos at various stages of development. Theriogenology, 2010, 73(8): 1018–1023

[47] Varago F C, Moutacas V S, Carvalho B C, Serapião R V, Vieira F, Chiarini-Garcia H, Brandão F Z, Camargo L S, Henry M, Lagares M A. Comparison of conventional freezing and vitrification with dimethylformamide and ethylene glycol for cryopreservation of ovine embryos. Reproduction in Domestic Animals, 2014, 49(5): 839–844

[48] Mara L, Sanna D, Dattena M, Mayorga Muñoz I M. Different in vitro culture systems affect the birth weight of lambs from vitrified ovine embryos. Zygote, 2015, 23(1): 53–57

[49] Succu S, Pasciu V, Manca M E, Chelucci S, Torres-Rovira L, Leoni G G, Zinellu A, Carru C, Naitana S, Berlinguer F. Dose-dependent effect of melatonin on postwarming development of vitrified ovine embryos. Theriogenology, 2014, 81(8): 1058–1066

[50] Romão R, Marques C C, Baptista M C, Barbas J P, Horta A E M, Carolino N, Bettencourt E, Pereira R M. Cryopreservation of in vitro-produced sheep embryos: effects of different protocols of lipid reduction. Theriogenology, 2015, 84(1): 118–126

[51] Pezhman M, Hosseini S M, Ostadhosseini S, Rouhollahi Varnosfaderani S, Sefid F, Nasr-Esfahani M H. Cathepsin B inhibitor improves developmental competency and cryo-tolerance of in vitro ovine embryos. BMC Developmental Biology, 2017, 17(1): 10

[52] Sefid F, Ostadhosseini S, Hosseini S M, Ghazvini Zadegan F, Pezhman M, Nasr Esfahani M H. Vitamin K2 improves developmental competency and cryo-tolerance of in vitro derived ovine blastocyst. Cryobiology, 2017, 77: 34–40

[53] Polge C, Willadsen S M. Freezing eggs and embryos of farm animals. Cryobiology, 1978, 15(3): 370–373

[54] Dobrinsky J R, Nagashima H, Pursel V G, Long C R, Johnson L A. Cryopreservation of swine embryos with reduced lipid content. Theriogenology, 1999, 51(1): 164–164

[55] Nagashima H, Kashiwazaki N, Ashman R, Grupen C, Seamark R F, Nottle M. Recent advances in cryopreservation of porcine embryos. Theriogenology, 1994, 41(1): 113–118

[56] Men H, Agca Y, Riley L K, Critser J K. Improved survival of vitrified porcine embryos after partial delipation through chemically stimulated lipolysis and inhibition of apoptosis. Theriogenology, 2006, 66(8): 2008–2016

[57] Mullen S F, Fahy G M. A chronologic review of mature oocyte vitrification research in cattle, pigs, and sheep. Theriogenology, 2012, 78(8): 1709–1719

[58] Men H, Zhao C, Si W, Murphy C N, Spate L, Liu Y, Walters E M, Samuel M S, Prather R S, Critser J K. Birth of piglets from in vitro-produced, zona-intact porcine embryos vitrified in a closed system. Theriogenology, 2011, 76(2): 280–289

[59] Kamoshita M, Kato T, Fujiwara K, Namiki T, Matsumura K, Hyon S H, Ito J, Kashiwazaki N. Successful vitrification of pronuclear-stage pig embryos with a novel cryoprotective agent, carboxylated ε-poly-L-lysine. PLoS One, 2017, 12(4): e0176711

[60] Mito T, Yoshioka K, Noguchi M, Yamashita S, Misumi K, Hoshi T, Hoshi H. Birth of piglets from in vitro-produced porcine blastocysts vitrified and warmed in a chemically defined medium. Theriogenology, 2015, 84(8): 1314–1320

[61] Toner M, Cravalho E G, Karel M. Thermodynamics and kinetics of intracellular ice formation during freezing of biological cells. Journal of Applied Physics, 1990, 67(3): 1582–1593

[62] Gook D A, Osborn S M, Johnston W I H. Cryopreservation of mouse and human oocytes using 1,2-propanediol and the configuration of the meiotic spindle. Human Reproduction, 1993, 8(7): 1101–1109

[63] Larman M G, Sheehan C B, Gardner D K. Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction, 2006, 131(1): 53–61

[64] Ruffing N A, Steponkus P L, Pitt R E, Parks J E. Osmometric behavior, hydraulic conductivity, and incidence of intracellular ice formation in bovine oocytes at different developmental stages. Cryobiology, 1993, 30(6): 562–580

[65] Genicot G, Leroy J L, Soom A V, Donnay I. The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian oocytes. Theriogenology, 2005, 63(4): 1181–1194

[66] Wu G, Jia B, Mo X, Liu C, Fu X, Zhu S, Hou Y. Nuclear maturation and embryo development of porcine oocytes vitrified by cryotop: effect of different stages of in vitro maturation. Cryobiology, 2013, 67(1): 95–101

[67] Khosravi-Farsani S, Sobhani A, Amidi F, Mahmoudi R. Mouse oocyte vitrification: the effects of two methods on maturing germinal vesicle breakdown oocytes. Journal of Assisted Reproduction and Genetics, 2010, 27(5): 233–238

[68] Isachenko E F, Ostashko F I, Isachenko V V. Culture of bull semen in heat-inactivated and non-inactivated bovine estrual serum. Theriogenology, 1992, 37(1): 226–226

[69] Fuku E, Kojima T, Shioya Y, Marcus G J, Downey B R. In vitro fertilization and development of frozen-thawed bovine oocytes. Cryobiology, 1992, 29(4): 485–492

[71] Hou Y P, Dai Y P, Zhu S E, Zhu H B, Wu T Y, Gong G C, Wang H P, Wang L L, Liu Y, Li R, Wan R, Li N. Bovine oocytes vitrified by the open pulled straw method and used for somatic cell cloning supported development to term. Theriogenology, 2005, 64(6): 1381–1391

[72] Checura C M, Seidel G E Jr. Effect of macromolecules in solutions for vitrification of mature bovine oocytes. Theriogenology, 2007, 67(5): 919–930

[73] Prentice J R, Singh J, Dochi O, Anzar M. Factors affecting nuclear maturation, cleavage and embryo development of vitrified bovine cumulus-oocyte complexes. Theriogenology, 2011, 75(4): 602–609

[74] Boonkusol D, Faisaikarm T, Dinnyes A, Kitiyanant Y. Effects of vitrification procedures on subsequent development and ultrastructure of in vitro-matured swamp buffalo (Bubalus bubalis) oocytes. Reproduction, Fertility, and Development, 2007, 19(2): 383–391

[75] Chasombat J, Nagai T, Parnpai R, Vongpralub T. Pretreatment of in vitro matured bovine oocytes with docetaxel before vitrification: effects on cytoskeleton integrity and developmental ability after warming. Cryobiology, 2015, 71(2): 216–223

[76] Matos J E, Marques C C, Moura T F, Baptista M C, Horta A E, Soveral G, Pereira R M. Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate. Reproductive Biology and Endocrinology, 2015, 13(1): 60

[77] Chankitisakul V, Somfai T, Inaba Y, Techakumphu M, Nagai T. Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology, 2013, 79(4): 590–598

[78] Hara H, Yamane I, Noto I, Kagawa N, Kuwayama M, Hirabayashi M, Hochi S. Microtubule assembly and in vitro development of bovine oocytes with increased intracellular glutathione level prior to vitrification and in vitro fertilization. Zygote, 2014, 22(4): 476–482

[79] Ezoe K, Yabuuchi A, Tani T, Mori C, Miki T, Takayama Y, Beyhan Z, Kato Y, Okuno T, Kobayashi T, Kato K. Developmental competence of vitrified-warmed bovine oocytes at the germinal-vesicle stage is improved by cyclic adenosine monophosphate modulators during in vitro maturation. PLoS One, 2015, 10(5): e0126801

[80] Arcarons N, Morató R, Vendrell M, Yeste M, López-Bejar M, Rajapaksha K, Anzar M, Mogas T. Cholesterol added prior to vitrification on the cryotolerance of immature and in vitro matured bovine oocytes. PLoS One, 2017, 12(9): e0184714

[81] Ruiz-Conca M, Vendrell M, Sabés-Alsina M, Mogas T, Lopez-Bejar M. Coenzyme Q₁₀ supplementation during in vitro maturation of bovine oocytes (Bos taurus) helps to preserve oocyte integrity after vitrification. Reproduction in Domestic Animals, 2017, 52(S4): 52–54

[82] Wang N, Hao H S, Li C Y, Zhao Y H, Wang H Y, Yan C L, Du W H, Wang D, Liu Y, Pang Y W, Zhu H B, Zhao X M. Calcium ion regulation by BAPTA-AM and ruthenium red improved the fertilisation capacity and developmental ability of vitrified bovine oocytes. Scientific Reports, 2017, 7(1): 10652

[83] Guo X F, Yu X L, Zhang F, Wu H, Pei X Z, Li X X, Li Y H. Effect of liquid helium vitrification on cytoskeleton of immature cattle oocytes. Animal Reproduction Science, 2017, 187: 91–99

[84] Moawad A R, Zhu J, Choi I, Amarnath D, Chen W, Campbell K H. Production of good-quality blastocyst embryos following IVF of ovine oocytes vitrified at the germinal vesicle stage using a cryoloop. Reproduction, Fertility, and Development, 2013, 25(8): 1204–1215

[85] Rao B S, Mahesh Y U, Charan K V, Suman K, Sekhar N, Shivaji S. Effect of vitrification on meiotic maturation and expression of genes in immature goat cumulus oocyte complexes. Cryobiology, 2012, 64(3): 176–184

[86] Begin I, Bhatia B, Baldassarre H, Dinnyes A, Keefer C L. Cryopreservation of goat oocytes and in vivo derived 2- to 4-cell embryos using the cryoloop (CLV) and solid-surface vitrification (SSV) methods. Theriogenology, 2003, 59(8): 1839–1850

[87] Succu S, Leoni G G, Bebbere D, Berlinguer F, Mossa F, Bogliolo L, Madeddu M, Ledda S, Naitana S. Vitrification devices affect structural and molecular status of in vitro matured ovine oocytes. Molecular Reproduction and Development, 2007, 74(10): 1337–1344

[88] Ebrahimi B, Valojerdi M R, Eftekhari-Yazdi P, Baharvand H. In vitro maturation, apoptotic gene expression and incidence of numerical chromosomal abnormalities following cryotop vitrification of sheep cumulus-oocyte complexes. Journal of Assisted Reproduction and Genetics, 2010, 27(5): 239–246

[89] Quan G B, Wu G Q, Wang Y J, Ma Y, Lv C R, Hong Q H. Meiotic maturation and developmental capability of ovine oocytes at germinal vesicle stage following vitrification using different cryodevices. Cryobiology, 2016, 72(1): 33–40

[90] Naderi M M, Borjian Boroujeni S, Sarvari A, Heidari B, Akhondi M M, Zarnani A H, Shirazi A. The effect of media supplementation with angiotensin on developmental competence of ovine embryos derived from vitrified-warmed oocytes. Avicenna Journal of Medical Biotechnology, 2016, 8(3): 139–144

[91] Zhang X, Trokoudes K M, Pavlides C. Vitrification of biopsied embryos at cleavage, morula and blastocyst stage. Reproductive Biomedicine Online, 2009, 19(4): 526–531

[92] Silvestre M A, Yániz J, Salvador I, Santolaria P, López-Gatius F. Vitrification of pre-pubertal ovine cumulus-oocyte complexes: effect of cytochalasin B pre-treatment. Animal Reproduction Science, 2006, 93(1–2): 176–182

[93] Asgari V, Hosseini S M, Ostadhosseini S, Hajian M, Azhdari Z T, Mosaie M, Nasr-Esfahani M H. Specific activation requirements of in vitro-matured sheep oocytes following vitrification-warming. Molecular Reproduction and Development, 2012, 79(7): 434–444

[94] Somfai T, Yoshioka K, Tanihara F, Kaneko H, Noguchi J, Kashiwazaki N, Nagai T, Kikuchi K. Generation of live piglets from cryopreserved oocytes for the first time using a defined system for in vitro embryo production. PLoS One, 2014, 9(5): e97731

[95] Gajda B, Skrzypczak-Zielińska M, Gawrońska B, Słomski R, Smorąg Z. Successful production of piglets derived from mature oocytes vitrified using OPS method. Cryo Letters, 2015, 36(1): 8–18

[96] Fujihira T, Nagai H, Fukui Y. Relationship between equilibration times and the presence of cumulus cells, and effect of taxol treatment for vitrification of in vitro matured porcine oocytes. Cryobiology, 2005, 51(3): 339–343

[97] Liu Y, Du Y, Lin L, Li J, Kragh P M, Kuwayama M, Bolund L, Yang H, Vajta G. Comparison of efficiency of open pulled straw (OPS) and Cryotop vitrification for cryopreservation of in vitro matured pig oocytes. Cryo Letters, 2008, 29(4): 315–320

[98] Somfai T, Nakai M, Tanihara F, Noguchi J, Kaneko H, Kashiwazaki N, Egerszegi I, Nagai T, Kikuchi K. Comparison of ethylene glycol and propylene glycol for the vitrification of immature porcine oocytes. Journal of Reproduction and Development, 2013, 59(4): 378–384

[99] Nohalez A, Martinez C A, Gil M A, Almiñana C, Roca J, Martinez E A, Cuello C. Effects of two combinations of cryoprotectants on the in vitro developmental capacity of vitrified immature porcine oocytes. Theriogenology, 2015, 84(4): 545–552

[100] Huang J, Li Q, Zhao R, Li W, Han Z, Chen X, Xiao B, Wu S, Jiang Z, Hu J, Liu L. Effect of sugars on maturation rate of vitrified-thawed immature porcine oocytes. Animal Reproduction Science, 2008, 106(1–2): 25–35

[101] Shi W Q, Zhu S E, Zhang D, Wang W H, Tang G L, Hou Y P, Tian S J. Improved development by Taxol pretreatment after vitrification of in vitro matured porcine oocytes. Reproduction, 2006, 131(4): 795–804

[102] Fu X W, Shi W Q, Zhang Q J, Zhao X M, Yan C L, Hou Y P, Zhou G B, Fan Z Q, Suo L, Wusiman A, Wang Y P, Zhu S E. Positive effects of Taxol pretreatment on morphology, distribution and ultrastructure of mitochondria and lipid droplets in vitrification of in vitro matured porcine oocytes. Animal Reproduction Science, 2009, 115(1–4): 158–168

[103] Ogawa B, Ueno S, Nakayama N, Matsunari H, Nakano K, Fujiwara T, Ikezawa Y, Nagashima H. Developmental ability of porcine in vitro matured oocytes at the meiosis II stage after vitrification. Journal of Reproduction and Development, 2010, 56(3): 356–361

[104] Fu X W, Wu G Q, Li J J, Hou Y P, Zhou G B, Lun-Suo , Wang Y P, Zhu S E. Positive effects of Forskolin (stimulator of lipolysis) treatment on cryosurvival of in vitro matured porcine oocytes. Theriogenology, 2011, 75(2): 268–275

[105] de Matos D G, Gasparrini B, Pasqualini S R, Thompson J G. Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology, 2002, 57(5): 1443–1451

[106] Reis A, Rooke J A, McCallum G J, Staines M E, Ewen M, Lomax M A, McEvoy T G. Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro. Reproduction, Fertility, and Development, 2003, 15(5): 275–284

[107] Feugang J M, de Roover R, Moens A, Léonard S, Dessy F, Donnay I. Addition of beta-mercaptoethanol or Trolox at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents. Theriogenology, 2004, 61(1): 71–90

[108] Giaretta E, Spinaci M, Bucci D, Tamanini C, Galeati G. Effects of resveratrol on vitrified porcine oocytes. Oxidative Medicine and Cellular Longevity, 2013, 2013(7): 920257

[109] Santos E, Appeltant R, Dang-Nguyen T Q, Noguchi J, Kaneko H, Kikuchi K, Somfai T. The effect of resveratrol on the developmental competence of porcine oocytes vitrified at germinal vesicle stage. Reproduction in Domestic Animals, 2018,53(2): 304–312

[110] Gupta M K, Uhm S J, Lee H T. Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertility and Sterility, 2010, 93(8): 2602–2607

[111] Nakagawa S, Yoneda A, Hayakawa K, Watanabe T. Improvement in the in vitro maturation rate of porcine oocytes vitrified at the germinal vesicle stage by treatment with a mitochondrial permeability transition inhibitor. Cryobiology, 2008, 57(3): 269–275

[112] Kopeika J, Thornhill A, Khalaf Y. The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence. Human Reproduction Update, 2015, 21(2): 209–227

[113] Ishijima S, Iwamoto T, Nozawa S, Matsushita K. Motor apparatus in human spermatozoa that lack central pair microtubules. Molecular Reproduction and Development, 2002, 63(4): 459–463

[114] Johnson L A, Weitze K F, Fiser P, Maxwell W M. Storage of boar semen. Animal Reproduction Science, 2000, 62(1–3): 143–172

[115] Bailey J L, Bilodeau J F, Cormier N. Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. Journal of Andrology, 2000, 21(1): 1–7

[116] Huang S Y, Kuo Y H, Lee W C, Tsou H L, Lee Y P, Chang H L, Wu J J, Yang P C. Substantial decrease of heat-shock protein 90 precedes the decline of sperm motility during cooling of boar spermatozoa. Theriogenology, 1999, 51(5): 1007–1016

[117] Zeng W X, Terada T. Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin. Theriogenology, 2001, 55(2): 615–627

[118] Mazur P, Leibo S P, Seidel G E Jr. Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions. Biology of Reproduction, 2008, 78(1): 2–12

[119] Salisbury G W, Fuller H K, Willett E L. Preservation of bovine spermatozoa in yolk-citrate diluent and field results from its use. Journal of Dairy Science, 1941, 24(11): 905–910

[120] Davis I S, Bratton R W, Foote R H. Livability of bovine spermatozoa at 5 C in tris-buffered and citrate-buffered yolk-glycerol extenders. Journal of Dairy Science, 1963, 46(1): 57–60

[121] Steinbach J, Foote R H. Effect of catalase and anaerobic conditions upon the post-thawing survival of bovine spermatozoa frozen in citrate- and tris-buffered yolk extenders 1. Journal of Dairy Science, 1964, 47(7): 812–815

[122] Polge C, Smith A U, Parkes A S. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature, 1949, 164(4172): 666

[123] Zeng C, Tang K, He L, Peng W, Ding L, Fang D, Zhang Y. Effects of glycerol on apoptotic signaling pathways during boar spermatozoa cryopreservation. Cryobiology, 2014, 68(3): 395–404

[124] De Leeuw F E, De Leeuw A M, Den Daas J H, Colenbrander B, Verkleij A J. Effects of various cryoprotective agents and membrane-stabilizing compounds on bull sperm membrane integrity after cooling and freezing. Cryobiology, 1993, 30(1): 32–44

[125] Woelders H. Fundamentals and recent development in cryopreservation of bull and boar semen. Veterinary Quarterly, 1997, 19(3): 135–138

[126] Moussa M, Marinet V, Trimeche A, Tainturier D, Anton M. Low density lipoproteins extracted from hen egg yolk by an easy method: cryoprotective effect on frozen-thawed bull semen. Theriogenology, 2002, 57(6): 1695–1706

[127] Amirat L, Tainturier D, Jeanneau L, Thorin C, Gérard O, Courtens J L, Anton M. Bull semen in vitro fertility after cryopreservation using egg yolk LDL: a comparison with Optidyl, a commercial egg yolk extender. Theriogenology, 2004, 61(5): 895–907

[128] Zhao X L, Li Y K, Cao S J, Hu J H, Wang W H, Hao R J, Gui L S, Zan L S. Protective effects of ascorbic acid and vitamin E on antioxidant enzyme activity of freeze-thawed semen of Qinchuan bulls. Genetics & Molecular Research, 2015, 14(1): 2572–2581

[129] Ashrafi I, Kohram H, Ardabili F F. Antioxidative effects of melatonin on kinetics, microscopic and oxidative parameters of cryopreserved bull spermatozoa. Animal Reproduction Science, 2013, 139(1–4): 25–30

[130] Martín-Hidalgo D, Barón F J, Bragado M J, Carmona P, Robina A, García-Marín L J, Gil M C. The effect of melatonin on the quality of extended boar semen after long-term storage at 17 °C. Theriogenology, 2011, 75(8): 1550–1560

[131] Bernstein A D, Petropavlovsky V V. Effect of non-electrolytes on viability of spermatozoa. Biulleten’ Eksperimental’Noi Biologii i Meditsiny, 2013, 3: 41–43 (in Russian)

[132] Smirnov I V. Preservation of domestic animals’ semen by deep cooling. Sov Zootech, 1949, 4: 63–65

[133] Smirnov I V. Deep freezing of semen of farm animals. Journal Obtsej Biologii, 1950, 11(3): 185

[134] Youngquist R S, Threlfall W R. Current therapy in large animal theriogenology. 2nd ed. St. Louis, Mo.: Saunders Elsevier, 2007, 1061

[135] Purdy P H. The post-thaw quality of ram sperm held for 0 to 48 h at 5 degrees C prior to cryopreservation. Animal Reproduction Science, 2006, 93(1–2): 114–123

[136] Mackepladze I B, Gugusvili K F, Bregadze M A, Haratisvili G. Storage and use of frozen bull and ram semen. Zhivotnovodstvo, 1960: 77–78

[137] Feredean T, Bragaru F L. Studies on conservation of ram semen by freezing to -79 °C. Lucr Stiint Inst Cercet Zooteh, 1964, 21: 357–368 (in Rumanian)

[138] Aboagla E M, Terada T. Trehalose-enhanced fluidity of the goat sperm membrane and its protection during freezing. Biology of Reproduction, 2003, 69(4): 1245–1250

[139] Arando A, Gonzalez A, Delgado J V, Arrebola F A, Perez-Marín C C. Storage temperature and sucrose concentrations affect ram sperm quality after vitrification. Animal Reproduction Science, 2017, 181: 175–185

[140] John Morris G, Acton E, Murray B J, Fonseca F. Freezing injury: the special case of the sperm cell. Cryobiology, 2012, 64(2): 71–80

[141] Ritar A J, Salamon S. Effects of seminal plasma and of its removal and of egg yolk in the diluent on the survival of fresh and frozen-thawed spermatozoa of the Angora goat. Australian Journal of Biological Sciences, 1982, 35(3): 305–312

[142] Yang J. The research to protecting effect of frozen semen in sheep semen diluent with supplement of PUFA. Dissertation for the Doctoral Degree. Hohhot: Inner Mongolia Agricultural University, 2006 (in Chinese)

[143] Pursel V G, Johnson L A. Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. Journal of Animal Science, 1975, 40(1): 99–102

[144] Westendorf P, Richter L, Treu H. Zur Tiefgefrierung von Ebersperma. Labor- und Besamungsergebnisse mit dem Hulsenberger Pailletten-Verfahren. Dtw Dtsch Tierarztl Wochenschr, 1975, 82(7): 261–267 (in German)

[145] Didion B A, Braun G D, Duggan M V. Field fertility of frozen boar semen: a retrospective report comprising over 2600 AI services spanning a four year period. Animal Reproduction Science, 2013, 137(3-4): 189–196

[146] Baishya S K, Biswas R K, Kadirvel G, Deka B C, Kumar S, Sinha S, Dutta D J, Saikia G K. Effect of conventional and controlled freezing method on the post thaw characteristics of boar spermatozoa. Animal Reproduction Science, 2014, 149(3-4): 231–237

[147] Polge C, Salamon S, Wilmut I. Fertilizing capacity of frozen boar semen following surgical insemination. Veterinary Record, 1970, 87(15): 424–429

[148] Milovanov V K, Baranov F A, Qhil’Tsova L S, Oivadis R N. Developing methods for freezing boar semen. Zhivotnovodstvo, 1974

[149] Richter L, Romeny E, Weitze K F, Zimmermann F. Zur Tiefgefrierung von Ebersperma. VII. Weitere Labor- und Besamungsversuche mit dem Verdunner Hulsenberg VIII. Dtw Dtsch Tierarztl Wochenschr, 1975, 82(4): 155–162 (in German)

[150] Shapiev I S, Moroz L G, Korban N V. Problem of technology of freezing boar semen. Zhivotnovodstvo, 1976

[151] Park H K, Kim S H, Kim K J, Choi K M. Studies on the frozen boar semen. I. Studies on the development of diluents for freezing of boar semen. Han'guk Ch'uksan Hakhoe chi (Korean journal of animal sciences), 1977

[152] Wang P, Wang Y F, Wang C W, Bu S H, Hu J H, Li Q W, Pang W J, Yang G S. Effects of low-density lipoproteins extracted from different avian yolks on boar spermatozoa quality following freezing-thawing. Zygote, 2014, 22(2): 175–181

[153] Pinho R O, Lima D M, Shiomi H H, Siqueira J B, Silva H T, Lopes P S, Guimarães S E, Guimarães J D. Effect of different cryo-protectants on the viability of frozen/thawed semen from boars of the Piau breed. Animal Reproduction Science, 2014, 146(3–4): 187–192

[154] Peña F J, Johannisson A, Wallgren M, Rodriguez-Martinez H. Effect of hyaluronan supplementation on boar sperm motility and membrane lipid architecture status after cryopreservation. Theriogenology, 2004, 61(1): 63–70

[155] Lee Y S, Lee S, Lee S H, Yang B K, Park C K. Effect of cholesterol-loaded-cyclodextrin on sperm viability and acrosome reaction in boar semen cryopreservation. Animal Reproduction Science, 2015, 159: 124–130

[156] Trzcińska M, Bryła M, Gajda B, Gogol P. Fertility of boar semen cryopreserved in extender supplemented with butylated hydroxytoluene. Theriogenology, 2015, 83(3): 307–313

[157] Tomas C, Gómez-Fernandez J, Gómez-Izquierdo E, Gómez-Fidalgo E, Sánchez-Sánchez R, González-Bulnes A, de Mecado E. Effect of the pH pre-adjustment in the freezing extender on post-thaw boar sperm quality. Cryo Letters, 2015, 36(2): 97–103

[160] Tian S J, Yan C L, Yang H X, Zhou G B, Yang Z Q, Zhu S E. Vitrification solution containing DMSO and EG can induce parthenogenetic activation of in vitro matured ovine oocytes and decrease sperm penetration. Animal Reproduction Science, 2007, 101(3–4): 365–371

[161] Succu S, Bebbere D, Bogliolo L, Ariu F, Fois S, Leoni G G, Berlinguer F, Naitana S, Ledda S. Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Molecular Reproduction and Development, 2008, 75(3): 538–546

[163] Grossfeld R, Sieg B, Struckmann C, Frenzel A, Maxwell W M, Rath D. New aspects of boar semen freezing strategies. Theriogenology, 2008, 70(8): 1225–1233

[164] Yeste M. Sperm cryopreservation update: cryodamage, markers, and factors affecting the sperm freezability in pigs. Theriogenology, 2016, 85(1): 47–64

Acknowledgements

This study was supported by National Natural Science Foundation of China (31101714) and National Transgenic Creature Breeding Grand Project (2016ZX08008-003) .

Compliance with ethics guidelines

Zhengyuan Huang, Lei Gao, Yunpeng Hou, Shien Zhu, and Xiangwei Fu declare that they have no conflicts of interest or financial conflicts to disclose.

This article is a review and does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2018. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)