Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

New strategies for germ cell cryopreservation: Cryoinjury modulation

  • Sang-Eun Jung (Department of Animal Science & Technology, Chung-Ang University) ;
  • Buom-Yong Ryu (Department of Animal Science & Technology, Chung-Ang University)
  • Received : 2023.03.19
  • Accepted : 2023.07.17
  • Published : 2023.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cryopreservation is an option for the preservation of pre- or post-pubertal female or male fertility. This technique not only is beneficial for human clinical applications, but also plays a crucial role in the breeding of livestock and endangered species. Unfortunately, frozen germ cells, including oocytes, sperm, embryos, and spermatogonial stem cells, are subject to cryoinjury. As a result, various cryoprotective agents and freezing techniques have been developed to mitigate this damage. Despite extensive research aimed at reducing apoptotic cell death during freezing, a low survival rate and impaired cell function are still observed after freeze-thawing. In recent decades, several cell death pathways other than apoptosis have been identified. However, the relationship between these pathways and cryoinjury is not yet fully understood, although necroptosis and autophagy appear to be linked to cryoinjury. Therefore, gaining a deeper understanding of the molecular mechanisms of cryoinjury could aid in the development of new strategies to enhance the effectiveness of the freezing of reproductive tissues. In this review, we focus on the pathways through which cryoinjury leads to cell death and propose novel approaches to enhance freezing efficacy based on signaling molecules.

Keywords

Acknowledgement

This work was supported by the Basic Science Research Program, which is facilitated through the National Research Foundation of Korea (NRF), under the grant number NRF-2018R1A6A1A03025159, in the Republic of Korea and the Chung-Ang University research grant in 2023.

References

  1. Rezazadeh Valojerdi M, Eftekhari-Yazdi P, Karimian L, Hassani F, Movaghar B. Vitrification versus slow freezing gives excellent survival, post warming embryo morphology and pregnancy outcomes for human cleaved embryos. J Assist Reprod Genet 2009;26:347-54. https://doi.org/10.1007/s10815-009-9318-6
  2. Whaley D, Damyar K, Witek RP, Mendoza A, Alexander M, Lakey JR. Cryopreservation: an overview of principles and cell-specific considerations. Cell Transplant 2021;30:963689721999617.
  3. Fowler A, Toner M. Cryo-injury and biopreservation. Ann N Y Acad Sci 2005;1066:119-35. https://doi.org/10.1196/annals.1363.010
  4. Gao D, Critser JK. Mechanisms of cryoinjury in living cells. ILAR J 2000;41:187-96. https://doi.org/10.1093/ilar.41.4.187
  5. Len JS, Koh WSD, Tan SX. The roles of reactive oxygen species and antioxidants in cryopreservation. Biosci Rep 2019;39:BSR20191601.
  6. Litvan GG. Mechanism of cryoinjury in biological systems. Cryobiology 1972;9:182-91. https://doi.org/10.1016/0011-2240(72)90030-2
  7. Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, et al. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ 2018;25:486-541. https://doi.org/10.1038/s41418-017-0012-4
  8. Gallardo Bolanos JM, Miro Moran A, Balao da Silva CM, Morillo Rodriguez A, Plaza Davila M, Aparicio IM, et al. Autophagy and apoptosis have a role in the survival or death of stallion spermatozoa during conservation in refrigeration. PLoS One 2012;7:e30688.
  9. Jung SE, Ahn JS, Kim YH, Oh HJ, Kim BJ, Kim SU, et al. Autophagy modulation alleviates cryoinjury in murine spermatogonial stem cell cryopreservation. Andrology 2022;10:340-53. https://doi.org/10.1111/andr.13105
  10. Jung SE, Ahn JS, Kim YH, Oh HJ, Kim BJ, Ryu BY. Necrostatin-1 improves the cryopreservation efficiency of murine spermatogonial stem cells via suppression of necroptosis and apoptosis. Theriogenology 2020;158:445-53. https://doi.org/10.1016/j.theriogenology.2020.10.004
  11. Lee JR, Youm HW, Kim SK, Jee BC, Suh CS, Kim SH. Effect of necrostatin on mouse ovarian cryopreservation and transplantation. Eur J Obstet Gynecol Reprod Biol 2014;178:16-20. https://doi.org/10.1016/j.ejogrb.2014.04.040
  12. Bissoyi A, Pramanik K. Role of the apoptosis pathway in cryopreservation-induced cell death in mesenchymal stem cells derived from umbilical cord blood. Biopreserv Biobank 2014;12:246-54. https://doi.org/10.1089/bio.2014.0005
  13. Girka E, Gatenby L, Gutierrez EJ, Bondioli KR. The effects of microtubule stabilizing and recovery agents on vitrified bovine oocytes. Theriogenology 2022;182:9-16. https://doi.org/10.1016/j.theriogenology.2022.01.031
  14. Hwang IS, Hochi S. Recent progress in cryopreservation of bovine oocytes. Biomed Res Int 2014;2014:570647.
  15. Jung SE, Oh HJ, Ahn JS, Kim YH, Kim BJ, Ryu BY. Antioxidant or apoptosis inhibitor supplementation in culture media improves post-thaw recovery of murine spermatogonial stem cells. Antioxidants (Basel) 2021;10:754.
  16. Pagano N, Longobardi V, De Canditiis C, Zuchegna C, Romano A, Michal Andrzej K, et al. Effect of caspase inhibitor Z-VAD-FMK on bovine sperm cryotolerance. Reprod Domest Anim 2020;55:530-6. https://doi.org/10.1111/rda.13648
  17. Shukla KK, Mahdi AA, Rajender S. Apoptosis, spermatogenesis and male infertility. Front Biosci (Elite Ed) 2012;4:746-54. https://doi.org/10.2741/e415
  18. Kist M, Vucic D. Cell death pathways: intricate connections and disease implications. EMBO J 2021;40:e106700.
  19. Hacker G. The morphology of apoptosis. Cell Tissue Res 2000;301:5-17. https://doi.org/10.1007/s004410000193
  20. Nossing C, Ryan KM. 50 Years on and still very much alive: 'apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics'. Br J Cancer 2023;128:426-31. https://doi.org/10.1038/s41416-022-02020-0
  21. Lossi L. The concept of intrinsic versus extrinsic apoptosis. Biochem J 2022;479:357-84. https://doi.org/10.1042/BCJ20210854
  22. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 2014;15:135-47.
  23. Newton K, Manning G. Necroptosis and inflammation. Annu Rev Biochem 2016;85:743-63. https://doi.org/10.1146/annurev-biochem-060815-014830
  24. Seo J, Nam YW, Kim S, Oh DB, Song J. Necroptosis molecular mechanisms: recent findings regarding novel necroptosis regulators. Exp Mol Med 2021;53:1007-17. https://doi.org/10.1038/s12276-021-00634-7
  25. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008;133:693-703. https://doi.org/10.1016/j.cell.2008.03.036
  26. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009;137:1112-23. https://doi.org/10.1016/j.cell.2009.05.037
  27. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 2012;150:339-50. https://doi.org/10.1016/j.cell.2012.06.019
  28. Bertheloot D, Latz E, Franklin BS. Necroptosis, pyroptosis and apoptosis: an intricate game of cell death. Cell Mol Immunol 2021;18:1106-21. https://doi.org/10.1038/s41423-020-00630-3
  29. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 2010;221:3-12. https://doi.org/10.1002/path.2697
  30. Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol 2018;19:349-64. https://doi.org/10.1038/s41580-018-0003-4
  31. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 2008;9:1004-10. https://doi.org/10.1038/nrm2529
  32. Bialik S, Dasari SK, Kimchi A. Autophagy-dependent cell death: where, how and why a cell eats itself to death. J Cell Sci 2018;131:jcs215152.
  33. Jung S, Jeong H, Yu SW. Autophagy as a decisive process for cell death. Exp Mol Med 2020;52:921-30. https://doi.org/10.1038/s12276-020-0455-4
  34. Liu Y, Levine B. Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 2015;22:367-76. https://doi.org/10.1038/cdd.2014.143
  35. Dasari SK, Bialik S, Levin-Zaidman S, Levin-Salomon V, Merrill AH Jr, Futerman AH, et al. Signalome-wide RNAi screen identifies GBA1 as a positive mediator of autophagic cell death. Cell Death Differ 2017;24:1288-302. https://doi.org/10.1038/cdd.2017.80
  36. Fahy GM. The relevance of cryoprotectant "toxicity" to cryobiology. Cryobiology 1986;23:1-13. https://doi.org/10.1016/0011-2240(86)90013-1
  37. Men H, Monson RL, Parrish JJ, Rutledge JJ. Degeneration of cryopreserved bovine oocytes via apoptosis during subsequent culture. Cryobiology 2003;47:73-81. https://doi.org/10.1016/S0011-2240(03)00070-1
  38. Vallorani C, Spinaci M, Bucci D, Porcu E, Tamanini C, Galeati G. Pig oocyte vitrification by Cryotop method and the activation of the apoptotic cascade. Anim Reprod Sci 2012;135:68-74. https://doi.org/10.1016/j.anireprosci.2012.08.020
  39. Rajaei F, Abedpour N, Salehnia M, Jahanihashemi H. The effect of vitrification on mouse oocyte apoptosis by Cryotop method. Iran Biomed J 2013;17:200-5.
  40. Dai J, Wu C, Muneri CW, Niu Y, Zhang S, Rui R, et al. Changes in mitochondrial function in porcine vitrified MII-stage oocytes and their impacts on apoptosis and developmental ability. Cryobiology 2015;71:291-8. https://doi.org/10.1016/j.cryobiol.2015.08.002
  41. Martin G, Sabido O, Durand P, Levy R. Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 2004;71:28-37. https://doi.org/10.1095/biolreprod.103.024281
  42. Grunewald S, Paasch U, Wuendrich K, Glander HJ. Sperm caspases become more activated in infertility patients than in healthy donors during cryopreservation. Arch Androl 2005;51:449-60. https://doi.org/10.1080/014850190947813
  43. Said TM, Gaglani A, Agarwal A. Implication of apoptosis in sperm cryoinjury. Reprod Biomed Online 2010;21:456-62. https://doi.org/10.1016/j.rbmo.2010.05.011
  44. Karabulut S, Demiroglu-Zergeroglu A, Yilmaz E, Kutlu P, Keskin I. Effects of human sperm cryopreservation on apoptotic markers in normozoospermic and non-normozoospermic patients. Zygote 2018;26:308-13. https://doi.org/10.1017/S0967199418000254
  45. Mehdipour M, Daghigh Kia H, Najafi A, Mohammadi H, Alvarez-Rodriguez M. Effect of crocin and naringenin supplementation in cryopreservation medium on post-thaw rooster sperm quality and expression of apoptosis associated genes. PLoS One 2020;15:e0241105.
  46. Curaba M, Verleysen M, Amorim CA, Dolmans MM, Van Langendonckt A, Hovatta O, et al. Cryopreservation of prepubertal mouse testicular tissue by vitrification. Fertil Steril 2011;95:1229-34. https://doi.org/10.1016/j.fertnstert.2010.04.062
  47. Lee YA, Kim YH, Ha SJ, Kim KJ, Kim BJ, Kim BG, et al. Cryopreservation of porcine spermatogonial stem cells by slow-freezing testis tissue in trehalose. J Anim Sci 2014;92:984-95. https://doi.org/10.2527/jas.2013-6843
  48. Lee YA, Kim YH, Kim BJ, Kim BG, Kim KJ, Auh JH, et al. Cryopreservation in trehalose preserves functional capacity of murine spermatogonial stem cells. PLoS One 2013;8:e54889.
  49. Kim KJ, Lee YA, Kim BJ, Kim YH, Kim BG, Kang HG, et al. Cryopreservation of putative pre-pubertal bovine spermatogonial stem cells by slow freezing. Cryobiology 2015;70:175-83. https://doi.org/10.1016/j.cryobiol.2015.02.007
  50. Jung SE, Kim M, Ahn JS, Kim YH, Kim BJ, Yun MH, et al. Effect of equilibration time and temperature on murine spermatogonial stem cell cryopreservation. Biopreserv Biobank 2020;18:213-21. https://doi.org/10.1089/bio.2019.0116
  51. Bissoyi A, Nayak B, Pramanik K, Sarangi SK. Targeting cryopreservation-induced cell death: a review. Biopreserv Biobank 2014;12:23-34. https://doi.org/10.1089/bio.2013.0032
  52. Yang Y, Cheung HH, Law WN, Zhang C, Chan WY, Pei X, et al. New insights into the role of autophagy in ovarian cryopreservation by vitrification. Biol Reprod 2016;94:137.
  53. Xie Y, Chen H, Luo D, Yang X, Yao J, Zhang C, et al. Inhibiting necroptosis of spermatogonial stem cell as a novel strategy for male fertility preservation. Stem Cells Dev 2020;29:475-87. https://doi.org/10.1089/scd.2019.0220
  54. Um DE, Shin H, Park D, Ahn JM, Kim J, Song H, et al. Molecular analysis of lipid uptake- and necroptosis-associated factor expression in vitrified-warmed mouse oocytes. Reprod Biol Endocrinol 2020;18:37.
  55. Gao HH, Li JT, Liu JJ, Yang QA, Zhang JM. Autophagy inhibition of immature oocytes during vitrification-warming and in vitro mature activates apoptosis via caspase-9 and -12 pathway. Eur J Obstet Gynecol Reprod Biol 2017;217:89-93. https://doi.org/10.1016/j.ejogrb.2017.08.029
  56. Bang S, Shin H, Song H, Suh CS, Lim HJ. Autophagic activation in vitrified-warmed mouse oocytes. Reproduction 2014;148:11-9. https://doi.org/10.1530/REP-14-0036
  57. Ha SJ, Kim BG, Lee YA, Kim YH, Kim BJ, Jung SE, et al. Effect of antioxidants and apoptosis inhibitors on cryopreservation of murine germ cells enriched for spermatogonial stem cells. PLoS One 2016;11:e0161372.
  58. Niu Y, Dai J, Wu C, Chen Y, Zhang S, Zhang D. The application of apoptotic inhibitor in apoptotic pathways of MII stage porcine oocytes after vitrification. Reprod Domest Anim 2016;51:953-9. https://doi.org/10.1111/rda.12772
  59. Colombo M, Zahmel J, Jansch S, Jewgenow K, Luvoni GC. Inhibition of apoptotic pathways improves DNA integrity but not developmental competence of domestic cat immature vitrified oocytes. Front Vet Sci 2020;7:588334.
  60. Jung SE, Ahn JS, Kim YH, Kim SM, Um TG, Kim BJ, et al. Inhibition of caspase-8 activity improves freezing efficiency of male germline stem cells in mice. Biopreserv Biobank 2021;19:493-502. https://doi.org/10.1089/bio.2021.0017
  61. Ortega Ferrusola C, Gonzalez Fernandez L, Salazar Sandoval C, Macias Garcia B, Rodriguez Martinez H, Tapia JA, et al. Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa. Theriogenology 2010;74:458-65. https://doi.org/10.1016/j.theriogenology.2010.02.029
  62. Ruiz-Conca M, Vendrell M, Sabes-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. Reprod Domest Anim 2017;52 Suppl 4:52-4.
  63. Kazemzadeh S, Mohammadpour S, Madadi S, Babakhani A, Shabani M, Khanehzad M. Melatonin in cryopreservation media improves transplantation efficiency of frozen-thawed spermatogonial stem cells into testes of azoospermic mice. Stem Cell Res Ther 2022;13:346.
  64. Trzcinska M, Bryla M, Gajda B, Gogol P. Fertility of boar semen cryopreserved in extender supplemented with butylated hydroxytoluene. Theriogenology 2015;83:307-13. https://doi.org/10.1016/j.theriogenology.2014.07.045
  65. Dominguez-Rebolledo AE, Fernandez-Santos MR, Bisbal A, Ros-Santaella JL, Ramon M, Carmona M, et al. Improving the effect of incubation and oxidative stress on thawed spermatozoa from red deer by using different antioxidant treatments. Reprod Fertil Dev 2010;22:856-70. https://doi.org/10.1071/RD09197
  66. Maia Mda S, Bicudo SD, Sicherle CC, Rodello L, Gallego IC. Lipid peroxidation and generation of hydrogen peroxide in frozen-thawed ram semen cryopreserved in extenders with antioxidants. Anim Reprod Sci 2010;122:118-23. https://doi.org/10.1016/j.anireprosci.2010.08.004
  67. Nekoonam S, Nashtaei MS, Naji M, Zangi BM, Amidi F. Effect of Trolox on sperm quality in normozospermia and oligozospermia during cryopreservation. Cryobiology 2016;72:106-11. https://doi.org/10.1016/j.cryobiol.2016.02.008
  68. Bang S, Qamar AY, Tanga BM, Fang X, Cho J. Resveratrol supplementation into extender protects against cryodamage in dog post-thaw sperm. J Vet Med Sci 2021;83:973-80. https://doi.org/10.1292/jvms.21-0125
  69. Delmas D, Jannin B, Latruffe N. Resveratrol: preventing properties against vascular alterations and ageing. Mol Nutr Food Res 2005;49:377-95. https://doi.org/10.1002/mnfr.200400098
  70. Stojanovic S, Sprinz H, Brede O. Efficiency and mechanism of the antioxidant action of trans-resveratrol and its analogues in the radical liposome oxidation. Arch Biochem Biophys 2001;391:79-89. https://doi.org/10.1006/abbi.2001.2388
  71. Zhao H, Jaffer T, Eguchi S, Wang Z, Linkermann A, Ma D. Role of necroptosis in the pathogenesis of solid organ injury. Cell Death Dis 2015;6:e1975.
  72. Feng TY, Li Q, Ren F, Xi HM, Lv DL, Li Y, et al. Melatonin protects goat spermatogonial stem cells against oxidative damage during cryopreservation by improving antioxidant capacity and inhibiting mitochondrial apoptosis pathway. Oxid Med Cell Longev 2020;2020:5954635.
  73. Lee GK, Shin H, Lim HJ. Rapamycin influences the efficiency of in vitro fertilization and development in the mouse: a role for autophagic activation. Asian-Australas J Anim Sci 2016;29:1102-10.
  74. Pero ME, Zullo G, Esposito L, Iannuzzi A, Lombardi P, De Canditiis C, et al. Inhibition of apoptosis by caspase inhibitor Z-VAD-FMK improves cryotolerance of in vitro derived bovine embryos. Theriogenology 2018;108:127-35. https://doi.org/10.1016/j.theriogenology.2017.11.031
  75. Trapphoff T, Heiligentag M, Simon J, Staubach N, Seidel T, Otte K, et al. Improved cryotolerance and developmental potential of in vitro and in vivo matured mouse oocytes by supplementing with a glutathione donor prior to vitrification. Mol Hum Reprod 2016;22:867-81.
  76. Wang Y, Zhang M, Chen ZJ, Du Y. Resveratrol promotes the embryonic development of vitrified mouse oocytes after in vitro fertilization. In Vitro Cell Dev Biol Anim 2018;54:430-8. https://doi.org/10.1007/s11626-018-0262-6
  77. Ahmadi E, Shirazi A, Shams-Esfandabadi N, Nazari H. Antioxidants and glycine can improve the developmental competence of vitrified/warmed ovine immature oocytes. Reprod Domest Anim 2019;54:595-603. https://doi.org/10.1111/rda.13402
  78. Kafi M, Ashrafi M, Azari M, Jandarroodi B, Abouhamzeh B, Asl AR. Niacin improves maturation and cryo-tolerance of bovine in vitro matured oocytes: an experimental study. Int J Reprod Biomed 2019;17:621-8.
  79. Gavella M, Lipovac V. Pentoxifylline-mediated reduction of superoxide anion production by human spermatozoa. Andrologia 1992;24:37-9. https://doi.org/10.1111/j.1439-0272.1992.tb02606.x
  80. Oeda T, Henkel R, Ohmori H, Schill WB. Scavenging effect of N-acetyl-L-cysteine against reactive oxygen species in human semen: a possible therapeutic modality for male factor infertility? Andrologia 1997;29:125-31.
  81. Boroujeni MB, Peidayesh F, Pirnia A, Boroujeni NB, Ahmadi SAY, Gholami M. Effect of selenium on freezing-thawing damage of mice spermatogonial stem cell: a model to preserve fertility in childhood cancers. Stem Cell Investig 2019;6:36.
  82. Fontoura P, Mello MD, Gallo-Sa P, Erthal-Martins MC, Cardoso MC, Ramos C. Leptin improves sperm cryopreservation via antioxidant defense. J Reprod Infertil 2017;18:172-8.
  83. Treulen F, Aguila L, Arias ME, Jofre I, Felmer R. Impact of post-thaw supplementation of semen extender with antioxidants on the quality and function variables of stallion spermatozoa. Anim Reprod Sci 2019;201:71-83. https://doi.org/10.1016/j.anireprosci.2018.12.011
  84. Pomar FJ, Teerds KJ, Kidson A, Colenbrander B, Tharasanit T, Aguilar B, et al. Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology 2005;63:2254-68. https://doi.org/10.1016/j.theriogenology.2004.10.015
  85. Bisht S, Dada R. Oxidative stress: major executioner in disease pathology, role in sperm DNA damage and preventive strategies. Front Biosci (Schol Ed) 2017;9:420-47. https://doi.org/10.2741/s495
  86. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, et al. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 1998;12:1304-14. https://doi.org/10.1101/gad.12.9.1304