Cryopreservation of Reproductive Cells and Embryos of Laboratory, Agricultural and Wild Animals
DOI:
https://doi.org/10.15407/cryo29.01.003Keywords:
cryopreservation, spermatozoa, oocytes, embryos, vitrificationAbstract
This review describes the state of the art in cryopreservation of spermatozoa, oocytes and animal embryos. We have analyzed methodical approaches for the effective low-temperature preservation of the genetic resources of animal world and speciï¬ed the procedures of cryopreservation of animal gametes and embryos. The history of efficient cryopreservation for animal reproductive cells and embryos was described. To date the germ cells and embryos of many laboratory, agricultural and wild animals have been successfully cryopreserved, nevertheless there is still pending the issue with the oocytes and embryos of some species of birds, ï¬ shes and mammals. The paper discusses the ways for developing the methods to preserve the genetic material of those species that have not been successfully cryopreserved yet.
Â
Probl Cryobiol Cryomed 2019; 29(1): 003–018
References
Am-in N, Kirkwood RN, Techakumphu M, Tantasuparuk W. Lipid profiles of sperm and seminal plasma from boars having normal or low sperm motility. Theriogenology. 2011; 15;75(5):897-903.
Baust JG, Gao D, Baust JM. Cryopreservation an emerging paradigm change. Organogenesis. 2009; 5(3): 90–6.
Benjamin P Cryoprotectant Toxicity: Facts, Issues, and Questions. Rejuvenation Res. 2015 Oct 1; 18(5): 422–36. CrossRef
Billard R, Cosson J, Noveiric SB, Pourkazemi M. Cryopreservation and short-term storage of sturgeon sperm, a review. Aquaculture. 2004;236(1–4):1–9. CrossRef
Blaxter IHS. Herring rearing 1. The storage of herring gametes. Mar Res Scot. 1955;(3):1–12.
Bromfield JJ. A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction. 2016;152(6):R223–R232.
Buderatska NO, Petrushko MP. Oocytes as Alternative to Embryos in Cryopreservation Applied in Assisted Reproductive Technologies. Probl Cryobiol Cryomed. 2016; 26(4):375–82. CrossRef
Carroll J, Depypere H, Matthews CD. Freeze–thaw-induced changes of the ZP explains decreased rates of fertilization in frozen–thawed mouse oocytes. J Reprod Fertil. 1990;90(2):547–53. CrossRef
Chen SL, Tian YS. Cryopreservation of flounder (Paralichthys olivaceus) embryos by vitrification. Theriogenology. 2005; 63(4):1207-19. CrossRef
Ciereszko A. Chemical composition of seminal plasma and its physiological relationship with sperm motility, fertilizing capacity and cryopreservation in fish. In: Alavi SHM, Cosson J, Coward K, Rafiee G, editors. Fish spermatology. Oxford: Alpha Science International Ltd; 2007. p. 215–40.
Clark NA, Swain JE. Oocyte cryopreservation: searching for novel improvement strategies. J Assist Reprod Genet. 2013;30(7):865–75. CrossRef
Clulow J, Clulow S. Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reprod Fertil Dev. 2016; 28(8): 1116-32. CrossRef
Comizzoli P, Songsasen N, Hagedorn M, Wildt DE. Comparative cryobiological traits and requirements for gametes and gonadal tissues collected from wildlife species. Theriogenology. 2012;78(8):1666–81. CrossRef
D’Alessandro AG, Martemucci G. Evaluation of seasonal variations of semen freezability in Leccese ram. Anim Reprod Sci. 2003; 79(1–2):93–102. CrossRef
Dalimata AM, Graham JK. Cryopreservation of rabbit spermatozoa using acetamide in combination with trehalose and methyl cellulose. Theriogenology. 1997; 48(5): 831–41. CrossRef
Deng A, Wang WH. Assessment of aneuploidy formation in human blastocysts resulting from cryopreserved donor eggs. Mol Cytogenet [Internet]. 2015 Feb 15 [cited 17.01.2019]; 8:12-9. Available from: https://molecularcytogenetics.biomedcentral.com/articles/10.1186/s13039-015-0117-8
Di Santo M, Tarozzi N, Nadalini M, Borini A. Human Sperm Cryopreservation: Update on Techniques, Effect on DNA Integrity, and Implications for ART. Adv Urol [Internet]. 2012 [cited 17.01.2019]; 2012: 854837 Available from: https://www.hindawi.com/journals/au/2012/854837/
Didukh YaP, ed. [Green Book of Ukraine: endangered rare plants and plants, and typical natural flora groups, which are subject to protection]. Kyiv: AlterPress, 2009. 448 p. Ukrainian.
Dzyuba B, Cosson J, Yamaner G, et al. Hypotonic treatment prior to freezing improves cryoresistance of common carp (Cyprinus carpio L) spermatozoa. Cryobiology. 2013;66(2): 192-4. CrossRef
Erdahl DH, Graham EF. Preservation of gametes of freshwater. In: Proceedings of the 9th International Congress on Animal Reproduction and Artificial Insemination. 1980 16-20 June, Madrid, Spain. Madrid; 1980. Vol. 2. p. 317–26.
Esaki R, Ueda H, Kurome M, et al. Cryopreservation of porcine embryos derived from in vitro-matured oocytes. Biol Reprod. 2004;71(2):432-7. CrossRef
Farstad W. Assisted reproductive technology in canid species Theriogenology. 2000; 53(1):175–86. CrossRef
Gajda B, Skrzypczak-Zielińska M, Gawrońska B, et al. Suc-cessful production of piglets derived from mature oocytes vitrified using OPS method. CryoLetters. 2015;36(1):8–18.
Garrels W, Mates L, Holler S, et al. Germline transgenic pigs by Sleeping Beauty transposition in porcine ygotes and targeted integration in the pig genome. PLoS One [Internet]. 2011 [Cited 17.01.2019]; 6(8):e23573. Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0023573
Gomis J, Cuello C, Sanchez-Osorio J, et al. Forskolin improves the cryosurvival of in vivo-derived porcine embryos at veryearly stages using two vitrification methods. Cryobiology. 2013; 66(2):144–50. CrossRef
Gould KG. Techniques and significance of gamete collection and storage in the great apes. J Med Primatol. 1990;19(6): 537–51. PubMed
Grishchenko VI, Kopeyka EF, Petrushko MP. [Problems of Cryobiology and Conservation of Genetic Resources]. Tsytologia. 2004;46(9):784–5. Russian.
Guan MI, Rawson DM, Zhang T. Cryopreservation of zebrafish (Danio rerio) oocytes by vitrification. CryoLetters. 2010; 31(3): 230–8.
Hagedorn M, Peterson A, Mazur P, Kleinhans FW. High ice nucleation temperature of zebrafish embryos: slow freezing is not an option. Cryobiology. 2004;49(2):181–9. CrossRef
Hamano S, Koikeda A, Kuwayama M, Nagai T. Full-term development of in vitro-matured, vitriï¬ed and ferfilized bovine oocytes. Theriogenology. 1992;38(6):1085–90. CrossRef
Horváth Ã, Miskolczi E, Urbányi B. Cryopreservation of common carp sperm. Aquat Living Resour. 2003; 16(5):457–60. CrossRef
Hwang IS, Kwon DJ, Im GS, et al. Ðigh incidence of polyspermic fertilization in bovine oocytes matured in vitro after cryotop vitrification. CryoLetters. 2016;37(1):27–33.
Jamieson BGM, Barrie GM. Live preservation of fish gametes. In: Fish evolution and systematics: evidence from spermatozoa. Cambridge, UK. Cambridge: Cambridge University Press; 1991. p. 245–69.
Kadam PD, Chuan HH. Rectocutaneous fistula with trans-migration of the suture: a rare delayed complication of vault fixation with the sacrospinous ligament. Int Urogynecol J. 2016; 27(1):155-7. CrossRef
Katanbafzadeh H, Barati F, Tabandeh M. Cryoprotectant-free freezing of the goat epididymal sperm. CryoLetters. 2014; 35(4): 293-8.
Katkov II, Bolyukh VF, Chernetsov OA, et al. Kinetic vitrification of spermatozoa of vertebrates: what can we learn from nature? In: Katkov II, editor. Current Frontiers in Cryobiology. InTech Open Access Books, 2012; Chapter. 1; p. 3-40 [Cited 25.07.2018] Available from: http://cdn.intechopen.com/pdfs/31227/InTech-Kinetic_vitrification_of_spermatozoa_of_vertebrates_what_can_we_learn_from_nature_.pdf CrossRef
Khosla K, Wang Y, Hagedorn M, et al. Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano 2017; 11(8): 7869-78. CrossRef
Kopeika E, Kopeika J, Zhang T. Cryopreservation of fish cryopreservation and freeze-drying protocols. In: Day JG, Stacey GN, editors. Cryopreservation and Freeze-Drying Protocols. Totowa, New Jersey: Humana Press; 2007. p. 203–17. CrossRef
Kopeika EF, Drokin SI, Cherepanov VV, et al. [Cryopreserved sperm quality carp after 25 years of storage]. In: [‘Modern problems of theoretical ichthyology’]. Proceedings of the IV International Ichthyological Scientific-Practical. Conference. 2011 7-11 Sept, Odessa, Ukraine. Odessa: Feniks; 2011. p. 136–8. Russian.
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): 209–27. CrossRef
Li MW, Vallelunga JM, Kinchen KL, et al. IVF recovery of mutant mouse lines using sperm cryopreserved with mtg in cryovials. CryoLetters. 2014; 35(2):145-53.
Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14(3):141–52. CrossRef
Liang YY, Srirattana K, Phermthai T. Effects of vitrification cryoprotectant treatment and cooling method on the viability and development of buffalo oocytes after intracytoplasmic sperm injection. Cryobiology. 2012; 65(2):151–6. CrossRef
Linhart O, Rodina M, Cosson J. Cryopreservation of sperm in common carp cyprinus carpio: sperm motility and hatching success of embryos. Cryobiology. 2000;41(3):241-50.CrossRef
Linnik TP, Martynyuk IN. Approaches to creation of cryoprotective media for cryopreservation of avian sperm. Problems of Cryobiology. 2010;20(2):109–22.
Liu KC, Chou TC, Lin HD. Cryosurvival of goldfish embryo after subzero freezing. Aquat Living Resour. 1993;6(1):63–6. CrossRef
Long JA, Purdy PH, Zuidberg K, et al. Cryopreservation of turkey semen: effect of breeding line and freezing method on post-thaw sperm quality, fertilization, and hatching. Cryobiology. 2014;68(3):371-8. CrossRef
Mandawala AA, Harvey SC, Roy TK, Fowler KE. Cryopreservation of animal oocytes and embryos: Current progress and future prospects. Theriogenology. 2016 15;86(7):1637–44.
Mara L, Casu S, Carta A, Dattena M. Cryobanking of farm animal gametes and embryos as a means of conserving livestock genetics. Anim Reprod Sci. 2013;138(1–2):25–38. CrossRef
Marco-Jiménez F, Casares-Crespo L, Vicente JS. Porcine oocyte vitrification in optimized low toxicity solution with open pulled straws. Zygote. 2014; 22(2): 204-12. CrossRef
MartÃnez-Páramo S, Horváth Ã, Labbé C, et al. Cryobanking of aquatic species. Aquaculture. 2017 Apr 1;472:156-77. CrossRef
Mavrides A, Morroll D. Bypassing the effect of ZP changes on embryo formation following cryopreservation of bovine oocytes. Eur J Obstet Gynecol Reprod Biol. 2005;118(1):66–70. CrossRef
McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK: Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact ZP. J Reprod Fertil. 2000; 118(1):163–70. CrossRef
Mikson KB, Kopeika EF, Linnik TP. conditions for loach (Mis-gurnus fossilis) embryo vitrification in cryoprotective media. Problems of Cryobiology. 2009; 19(2):154–62.
Mikson KB, Zinchenko AB, Bobrova EM. [Cryoconservation of loach’s embryos by vitrification]. In: Proceedings of the international conference ‘Cryoconservation of genetic resources, current status, problems and prospects’; 2014 October 28–30, Pushchino. Pushchino; 2014. p. 123–5. Russian.
Miller RR Jr, Cornett CL, Waterhouse KE, Farstad W. Comparative aspects of sperm membrane fatty acid composition in silver (Vulpes vulpes) and blue (Alopex lagopus) foxes, and their relationship to cell cryopreservation. Cryobiology. 2005;51(1):66–75. CrossRef
Moore DT, Purdy PH, Blackburn HD. A method for cryopreserving chicken primordial germ cells. Poult Sci. 2006;85(10):1784-90. CrossRef
Nagashima H, Kashiwazaki N, Ashman RJ, et al. Removal of cytoplasmic lipid enhances the tolerance of porcine embryos to chilling. Biol Reprod. 1994;51(4):618–22. CrossRef
Nakagata N. High survival rate of unfertilized mouse oocytes after vitrification. J Reprod Fertil. 1989;87(2):479–83. CrossRef
Okutsu T, Yano A, Nagasawa K, et al. Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J Reprod Dev. 2006;52(6):685-93. CrossRef
[On approval of the concept of the national program for the conservation of biodiversity for 2005-2025] Order of the Cabinet of Ministers of Ukraine from 22.09.04 â„– 675-p. [Cited 04.11.2017] Available from: https://zakon.rada.gov.ua/laws/show/675-2004-%D1%80 Ukrainian.
Pace MM, Graham EF. Components in egg yolk which protect bovine spermatozoa during freezing. J Anim Sci. 1974;39(6):1144–9. CrossRef
Parkening TA, Tsunoda Y, Chang MC. Effects of various low temperatures, cryoprotective agents and cooling rates on the survival, fertilizability and development of frozen-thawed mouse eggs. J Exp Zool. 1976;197(3):369–74. CrossRef
Parks JE, Lynch DV. Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology. 1992;29(2):255-66. CrossRef
Pavlovych O, Revenko O, Gapon G. Optimization of Thawing Regimen for Cryopreserved Human Sperm at Normo- and Pathospermia. Probl Cryobiol Cryomed. 2016; 26(1):45-52. CrossRef
Petrushko MP. [The use of cryopreserved human embryos in assisted reproductive technologies]. Problems of Cryobiology. 2000;(1):171. Russian.
Petrushko MP. [Current state of the problem of cryopreservation of reproductive cells and human embryos]. Visnyk Nac Acad Nauk Ukr. 2017; (7): 44‒52. Ukrainian.
Polge C, Smith AU, Parkes AS. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature. 1949;164(4172):666. CrossRef
Poulos A, Darin Bennett A, White IG. The phospholipid bound fatty acids and aldehydes of mammalian spermatozoa. Comparative Biochemistry and Physiology. 1973; 468:541-9.
Pushkar NS, Shrago MI, Belous AM, et al. [Cryoprotectors]. Kyiv: Naukova Dumka. 1978. 406 p. Russian.
Ruane J, Sonnino A. The role of biotechnology in exploring and protecting agricultural genetic resources. Food and Agriculture Organization of the United Nations. Rome: FAO. 2006. 188 p.
Ruffing NA, Steponcks PL, Pitt RE, et al. Osmometric behavior, hydraulic conductivity, and incidence of intracellular ice formation in bovine oocytes at different developmental stages. Cryobiology. 1993;30(6):562–80. CrossRef
Salamon SI, Maxwell WM. Storage of ram semen. Anim Reprod Sci. 2000; 62(1–3):77–111. CrossRef
Salmani H, Towhidi A, Zhandi M, et al. In vitro assessment of soybean lecithin and egg yolk based diluents for cryopreservation of goat semen. Cryobiology. 2014;68(2):276–80. CrossRef
Saragusty J, Arav A. Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction. 2011;141(1):1-19. CrossRef
Seidel GE Jr. Modifying oocytes and embryos to improve their cryopreservation. Theriogenology. 2006; 65(1):228–35. CrossRef
Shahverdi A, Rastegarnia A, Topraggaleh TR. Effect of extender and equilibration time on post thaw motility and chromatin structure of buffalo bull (Bubalus bubalis) spermatozoa. Cell J. 2014; 16(3): 279–88. PubMed
Shimazaki M, Sambuu R, Sato Y, et al. Effects of orvus es paste on the motility and viability of yak (bos grunniens) epididymal and ejaculated spermatozoa after freezing and thawing. CryoLetters. 2015; 36(4): 264–9.
Sieme H, Oldenhof H, Wolkers WF. Mode of action of cryoprotectants for sperm preservation. Anim Reprod Sci. 2016; 169: 2–5. CrossRef
Sieme H, Oldenhof H. Cryopreservation of semen from domestic livestock Methods. Mol Biol. 2015;1257:277-87. CrossRef
SprÃcigo JF, Morais K, Ferreira AR, et al. Vitrification of bovine oocytes at different meiotic stages using the Cryotop method: assessment of morphological, molecular and functional patterns. Cryobiology. 201; 69(2): 256–65.
Takeuchi Y, Yoshizaki G, Kobayashi T, Takeuchi T. Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol Reprod. 2002;67(4):1087-92. CrossRef
Tonus C, Cloquette K, Ectors F, et al. Long term-cultured and cryopreserved primordial germ cells from various chicken breeds retain high proliferative potential and gonadal colonisation competency. Reprod Fertil Dev. 2016;28(5):628–39. CrossRef
Walther TC, Farese RV Jr. The life of lipid droplets. Biochim Biophys Acta. 2009;1791(6):459–66. CrossRef
Wassall SR, Stillwell W. Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. Biochim Biophys Acta. 2009;1788(1):24-32. CrossRef
Waterhouse KE, Hofmo PO, Tverdal A, Miller Jr. RR Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction. 2006; 131(5): 887–94. CrossRef
Whittingham D, Leibo S, Mazur P. Survival of mouse embryos frozen to –196° and –269°C. Science. 1972 Oct 27; 178(4059):411–4. CrossRef
Whittingham DG. Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at −196 degrees C. J Reprod Fertil. 1977;49(1):89–94. CrossRef
Wirtu G, McGill J, Crawford L, et al Targeting lipid metabolism to improve oocyte cryopreservation (OCP) in domestic animals. Trans Clin Bio. 2013; 1(1):15–20. CrossRef
Woelders H, Zuidberg CA, Hiemstra SJ. Animal genetic resources conservation in the Netherlands and Europe: poultry perspective. Send to Poult Sci. 2006;85(2):216-22. CrossRef
Yang CH, Wu TW, Cheng FP, et al. Effects of different cryoprotectants and freezing methods on post-thaw boar semen quality. Reprod Biol. 2016;16(1):41–6. CrossRef
Yasui GS, Arias-Rodriguez L, Fujimoto T, Arai K. Simple and inexpensive method for cryopreservation of fish sperm combining straw and powdered dry ice. CryoLetters. 2008;29(5):383-90.
Downloads
Published
How to Cite
Issue
Section
License
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
