Damages and stress responses in sperm cells and other germplasms during dehydration and storage at nonfreezing temperatures for fertility preservation.
ambient temperatures
cellular damages
dehydration
fertility preservation
germplasms
long-term preservation
stress response
Journal
Molecular reproduction and development
ISSN: 1098-2795
Titre abrégé: Mol Reprod Dev
Pays: United States
ID NLM: 8903333
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
revised:
26
10
2022
received:
28
08
2022
accepted:
02
11
2022
pubmed:
13
11
2022
medline:
3
1
2023
entrez:
12
11
2022
Statut:
ppublish
Résumé
Long-term preservation of sperm, oocytes, and gonadal tissues at ambient temperatures has the potential to lower the costs and simplify biobanking in human reproductive medicine, as well as for the management of animal populations. Over the past decades, different dehydration protocols and long-term storage solutions at nonfreezing temperatures have been explored, mainly for mammalian sperm cells. Oocytes and gonadal tissues are more challenging to dehydrate so little to no progress have been made. Currently, the detrimental effects of the drying process itself are better characterized than the impact of long-term storage at nonfreezing temperatures. While structural and functional properties of germ cells can be preserved after dehydration, a long list of damages and stresses in nuclei, organelles, and cytoplasmic membranes have been reported and sometimes mitigated. Characterizing those damages and better understanding the response of germ cells and tissues to the stress of dehydration is fundamental. It will contribute to the development of optimal protocols while proving the safety of alternative storage options for fertility preservation. The objective of this review is to (1) document the types of damages and stress responses, as well as their mitigation in cells dried with different techniques, and (2) propose new research directions.
Types de publication
Journal Article
Review
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
565-578Subventions
Organisme : NIH HHS
ID : R01 OD023139
Pays : United States
Informations de copyright
© 2022 Wiley Periodicals LLC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
Références
Abazari, A., Meimetis, L. G., Budin, G., Bale, S. S., Weissleder, R., & Toner, M. (2015). Engineered trehalose permeable to mammalian cells. PLoS One, 10(6), e0130323. https://doi.org/10.1371/JOURNAL.PONE.0130323
Abdalla, H., Hirabayashi, M., & Hochi, S. (2009a). Demethylation dynamics of the paternal genome in pronuclear-stage bovine zygotes produced by in vitro fertilization and ooplasmic injection of freeze-thawed or freeze-dried spermatozoa. The Journal of Reproduction and Development, 55(4), 433-439. https://doi.org/10.1262/JRD.20229
Abdalla, H., Hirabayashi, M., & Hochi, S. (2009b). The ability of freeze-dried bull spermatozoa to induce calcium oscillations and resumption of meiosis. Theriogenology, 71(3), 543-552. https://doi.org/10.1016/J.THERIOGENOLOGY.2008.08.021
Alonso, A., Baca Castex, C., Ferrante, A., Pinto, M., Castañeira, C., Trasorras, V., Gambarotta, M. C., Losinno, L., & Miragaya, M. (2015). In vitro equine embryo production using air-dried spermatozoa, with different activation protocols and culture systems. Andrologia, 47(4), 387-394. https://doi.org/10.1111/AND.12273
Amelkina, O., & Comizzoli, P. (2020). Initial response of ovarian tissue transcriptome to vitrification or microwave-assisted dehydration in the domestic cat model. BMC Genomics, 21(1), 828. https://doi.org/10.1186/S12864-020-07236-Z
Arav, A. (2020). From cryo-preservation to dry-preservation of reproductive cells. Theriogenology, 150, 263-267. https://doi.org/10.1016/J.THERIOGENOLOGY.2020.01.060
Arav, A., & Saragusty, J. (2016). Directional freezing of sperm and associated derived technologies. Animal Reproduction Science, 169, 6-13. https://doi.org/10.1016/j.anireprosci.2016.02.007
Arayatham, S., Buntasana, S., Padungros, P., & Tharasanit, T. (2022). Membrane-permeable trehalose improves the freezing ability and developmental competence of in-vitro matured feline oocytes. Theriogenology, 181, 16-23. https://doi.org/10.1016/J.THERIOGENOLOGY.2022.01.003
Balsa, E., Soustek, M. S., Thomas, A., Cogliati, S., García-Poyatos, C., Martín-García, E., Jedrychowski, M., Gygi, S. P., Enriquez, J. A., & Puigserver, P. (2019). ER and nutrient stress promote assembly of respiratory chain supercomplexes through the PERK-eIF2α axis. Molecular Cell, 74(5), 877-890. https://doi.org/10.1016/j.molcel.2019.03.031
Bebbere, D., Arav, A., Nieddu, S. M., Burrai, G. P., Succu, S., Patrizio, P., & Ledda, S. (2021). Molecular and histological evaluation of sheep ovarian tissue subjected to lyophilization. Animals: An Open Access Journal from MDPI, 11(12), 3407. https://doi.org/10.3390/ANI11123407
Bhowmick, S., Zhu, L., McGinnis, L., Lawitts, J., Nath, B. D., Toner, M., & Biggers, J. (2003, December). Desiccation tolerance of spermatozoa dried at ambient temperature: Production of fetal mice. Biology of Reproduction, 68(2002), 1779-1786. https://doi.org/10.1095/biolreprod.102.009407
Bossi, R., Cabral, M., Oliveira, M., Lopes, S., Hurtado, R., Sampaio, M., & Geber, S. (2021). Ultrastructural analysis of lyophilized human spermatozoa. JBRA Assisted Reproduction, 25(3), 473. https://doi.org/10.5935/1518-0557.20210028
Brogna, R., Fan, J., Sieme, H., Wolkers, W. F., & Oldenhof, H. (2021). Drying and temperature induced conformational changes of nucleic acids and stallion sperm chromatin in trehalose preservation formulations. Scientific Reports, 11(1), 14076. https://doi.org/10.1038/S41598-021-93569-Y
Carretero, M. I., Chaves, M. G., Arraztoa, C. C., Fumuso, F. G., Gambarotta, M. C., & Neild, D. M. (2020). Air-drying llama sperm affects DNA integrity. Frontiers in Veterinary Science, 7, 597952. https://doi.org/10.3389/FVETS.2020.597952
Chakrabortee, S., Boschetti, C., Walton, L. J., Sarkar, S., Rubinsztein, D. C., & Tunnacliffe, A. (2007). Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proceedings of the National Academy of Sciences United States of America, 104(46), 18073-18078. https://doi.org/10.1073/PNAS.0706964104
Chakraborty, N., Biswas, D., Parker, W., Moyer, P., & Elliott, G. D. (2008). A role for microwave processing in the dry preservation of mammalian cells. Biotechnology and Bioengineering, 100(4), 782-796. https://doi.org/10.1002/bit.21801
Chen, T., Fowler, A., & Toner, M. (2000). Literature review: Supplemented phase diagram of the trehalose-water binary mixture. Cryobiology, 40(3), 277-282. https://doi.org/10.1006/cryo.2000.2244
Choi, Y. H., Varner, D. D., Love, C. C., Hartman, D. L., & Hinrichs, K. (2011). Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. Reproduction, 142(4), 529-538. https://doi.org/10.1530/REP-11-0145
Comizzoli, P., He, X., & Lee, P.-C. (2022). Long-term preservation of germ cells and gonadal tissues at ambient temperatures. Reproduction & Fertility, 3(2), 42. https://doi.org/10.1530/RAF-22-0008
Comizzoli, P., Loi, P., Patrizio, P., & Hubel, A. (2022). Long-term storage of gametes and gonadal tissues at room temperatures: The end of the ice age. Journal of Assisted Reproduction and Genetics, 39(2), 321-325. https://doi.org/10.1007/s10815-021-02392-x
Comizzoli, P., & Wildt, D. E. (2014). Mammalian fertility preservation through cryobiology: Value of classical comparative studies and the need for new preservation options. Reproduction, Fertility, and Development, 26(1), 91-98. https://doi.org/10.1071/RD13259
Comizzoli, P., & Wildt, D. E. (2017). Cryobanking biomaterials from wild animal species to conserve genes and biodiversity: Relevance to human biobanking and biomedical research. In P. Hainaut, J. Vaught, & K. Zatloukal (Eds.), Biobanking of human biospecimens: Principles and practice (1st ed., pp. 217-235). Springer. https://doi.org/10.1007/978-3-319-55120-3_13
Crowe, J. H. (2012). Introduction: Stabilization of dry biological materials. Biopreservation and Biobanking, 10(4), 375. https://doi.org/10.1089/bio.2012.1043
Crowe, J. H., Carpenter, J. F., & Crowe, L. M. (2003). The role of vitrification in anhydrobiosis. Annual Review of Physiology, 60, 73-103. https://doi.org/10.1146/ANNUREV.PHYSIOL.60.1.73
Czarny, N. A., Harris, M. S., de Iuliis, G. N., & Rodger, J. C. (2009). Acrosomal integrity, viability, and DNA damage of sperm from dasyurid marsupials after freezing or freeze drying. Theriogenology, 72(6), 817-825. https://doi.org/10.1016/J.THERIOGENOLOGY.2009.05.018
Czernik, M., Fidanza, A., Luongo, F. P., Valbonetti, L., Scapolo, P. A., Patrizio, P., & Loi, P. (2020). Late embryogenesis abundant (LEA) proteins confer water stress tolerance to mammalian somatic cells. Cryobiology, 92, 189-196. https://doi.org/10.1016/J.CRYOBIOL.2020.01.009
Dang-Nguyen, T. Q., Nguyen, H. T., Nguyen, M. T., Somfai, T., Noguchi, J., Kaneko, H., & Kikuchi, K. (2018). Maturation ability after transfer of freeze-dried germinal vesicles from porcine oocytes. Animal Science Journal, 89(9), 1253-1260. https://doi.org/10.1111/asj.13067
Elliott, G. D., Lee, P.-C., Paramore, E., van Vorst, M., & Comizzoli, P. (2015). Resilience of oocyte germinal vesicles to microwave-assisted drying in the domestic cat model. Biopreservation and Biobanking, 13(3), 164-171. https://doi.org/10.1089/bio.2014.0078
Elmoazzen, H. Y., Lee, G. Y., Li, M. W., McGinnis, L. K., Kent Lloyd, K. C., Toner, M., & Biggers, J. D. (2009). Further optimization of mouse spermatozoa evaporative drying techniques. Cryobiology, 59(1), 113-115. https://doi.org/10.1016/J.CRYOBIOL.2009.03.005
Garcia, A., Gil, L., Malo, C., Martinez, F., Kershaw-Young, C., & de Blas, I. (2014). Effect of different disaccharides on the integrity and fertilising ability of freeze-dried boar spermatozoa: A preliminary study. Cryo Letters, 35(4), 277-285. https://europepmc.org/article/med/25282494
Gianaroli, L., Magli, M. C., Stanghellini, I., Crippa, A., Crivello, A. M., Pescatori, E. S., & Ferraretti, A. P. (2012). DNA integrity is maintained after freeze-drying of human spermatozoa. Fertility and Sterility, 97(5), 1067-1073. https://doi.org/10.1016/J.FERTNSTERT.2012.02.014
Golovina, E. A., Golovin, A., Hoekstra, F. A., & Faller, R. (2010). Water replacement hypothesis in atomic details: Effect of trehalose on the structure of single dehydrated POPC bilayers. Langmuir, 26(13), 11118-11126. https://doi.org/10.1021/LA100891X
Graves-Herring, J. E., Wildt, D. E., & Comizzoli, P. (2013). Retention of structure and function of the cat germinal vesicle after air-drying and storage at suprazero temperature. Biology of Reproduction, 88(6), 139. https://doi.org/10.1095/biolreprod.113.108472
Hara, H., Abdalla, H., Morita, H., Kuwayama, M., Hirabayashi, M., & Hochi, S. (2011). Procedure for bovine ICSI, not sperm freeze-drying, impairs the function of the microtubule-organizing center. Journal of Reproduction and Development, 57(3), 428-432. http://www.ncbi.nlm.nih.gov/pubmed/21325738
Hibshman, J. D., Clegg, J. S., & Goldstein, B. (2020). Mechanisms of desiccation tolerance: Themes and variations in brine shrimp, roundworms, and tardigrades. Frontiers in Physiology, 11, 1326. https://doi.org/10.3389/FPHYS.2020.592016/XML/NLM
Hirabayashi, M., Kato, M., Ito, J., & Hochi, S. (2005). Viable rat offspring derived from oocytes intracytoplasmically injected with freeze-dried sperm heads. Zygote, 13(1), 79-85. https://doi.org/10.1017/S096719940500300X
Hochi, S., Watanabe, K., Kato, M., & Hirabayashi, M. (2008). Live rats resulting from injection of oocytes with spermatozoa freeze-dried and stored for one year. Molecular Reproduction and Development, 75(5), 890-894. https://doi.org/10.1002/MRD.20825
Holt, W. v., & Comizzoli, P. (2021). Genome resource banking for wildlife conservation: Promises and caveats. CryoLetters, 42(6), 309-320.
Huang, Z., & Tunnacliffe, A. (2004). Response of human cells to desiccation: Comparison with hyperosmotic stress response. The Journal of Physiology, 558(1), 181-191. https://doi.org/10.1113/JPHYSIOL.2004.065540
Huang, Z., & Tunnacliffe, A. (2005). Gene induction by desiccation stress in human cell cultures. FEBS Letters, 579(22), 4973-4977. https://doi.org/10.1016/J.FEBSLET.2005.07.084
Hubel, A., Spindler, R., & Skubitz, A. P. N. (2014). Storage of human biospecimens: Selection of the optimal storage temperature. Biopreservation and Biobanking, 12(3), 165-175. https://doi.org/10.1089/BIO.2013.0084
Ito, D., Wakayama, S., Emura, R., Ooga, M., & Wakayama, T. (2021). Mailing viable mouse freeze-dried spermatozoa on postcards. IScience, 24(8), 102815. https://doi.org/10.1016/J.ISCI.2021.102815
Ito, D., Wakayama, S., Kamada, Y., Shibasaki, I., Kamimura, S., Ooga, M., & Wakayama, T. (2019). Effect of trehalose on the preservation of freeze-dried mice spermatozoa at room temperature. Journal of Reproduction and Development, 65(4), 353-359. https://doi.org/10.1262/JRD.2019-058
Iuso, D., Czernik, M., di Egidio, F., Sampino, S., Zacchini, F., Bochenek, M., Smorag, Z., Modlinski, J. A., Ptak, G., & Loi, P. (2013). Genomic stability of lyophilized sheep somatic cells before and after nuclear transfer. PLoS One, 8(1), e51317. https://doi.org/10.1371/JOURNAL.PONE.0051317
Jain, N. K., & Roy, I. (2008). Effect of trehalose on protein structure. Protein Science, 18(1), 24-36. https://doi.org/10.1002/PRO.3
Kamada, Y., Wakayama, S., Shibasaki, I., Ito, D., Kamimura, S., Ooga, M., & Wakayama, T. (2018). Assessing the tolerance to room temperature and viability of freeze-dried mice spermatozoa over long-term storage at room temperature under vacuum. Scientific Reports, 8(1), 10602. https://doi.org/10.1038/s41598-018-28896-8
Kaneko, T., Ito, H., Sakamoto, H., Onuma, M., & Inoue-Murayama, M. (2014). Sperm preservation by freeze-drying for the conservation of wild animals. PLoS One, 9(11), e113381. https://doi.org/10.1371/journal.pone.0113381
Kaneko, T., Kimura, S., & Nakagata, N. (2009). Importance of primary culture conditions for the development of rat ICSI embryos and long-term preservation of freeze-dried sperm. Cryobiology, 58(3), 293-297. https://doi.org/10.1016/J.CRYOBIOL.2009.02.004
Kaneko, T., & Nakagata, N. (2005). Relation between storage temperature and fertilizing ability of freeze-dried mouse spermatozoa. Comparative Medicine, 55(2), 140-144. https://pubmed.ncbi.nlm.nih.gov/15884775/
Kaneko, T., & Nakagata, N. (2006). Improvement in the long-term stability of freeze-dried mouse spermatozoa by adding of a chelating agent. Cryobiology, 53(2), 279-282. https://doi.org/10.1016/J.CRYOBIOL.2006.06.004
Kaneko, T., & Serikawa, T. (2012a). Successful long-term preservation of rat sperm by freeze-drying. PLoS One, 7(4), e35043. https://doi.org/10.1371/JOURNAL.PONE.0035043
Kaneko, T., & Serikawa, T. (2012b). Long-term preservation of freeze-dried mouse spermatozoa. Cryobiology, 64(3), 211-214. https://doi.org/10.1016/J.CRYOBIOL.2012.01.010
Kaneko, T., Whittingham, D. G., & Yanagimachi, R. (2003). Effect of pH value of freeze-drying solution on the chromosome integrity and developmental ability of mouse spermatozoa. Biology of Reproduction, 68(1), 136-139. https://doi.org/10.1095/BIOLREPROD.102.008706
Kawase, Y., Araya, H., Kamada, N., Jishage, K., & Suzuki, H. (2005). Possibility of long-term preservation of freeze-dried mouse spermatozoa. Biology of Reproduction, 72(3), 568-573. https://doi.org/10.1095/biolreprod.104.035279
Kawase, Y., Hani, T., Kamada, N., Jishage, K., & Suzuki, H. (2007). Effect of pressure at primary drying of freeze-drying mouse sperm reproduction ability and preservation potential. Reproduction, 133(4), 841-846. https://doi.org/10.1530/REP-06-0170
Kawase, Y., Wada, N. A., & Jishage, K. (2009). Evaluation of DNA fragmentation of freeze-dried mouse sperm using a modified sperm chromatin structure assay. Theriogenology, 72(8), 1047-1053. https://doi.org/10.1016/J.THERIOGENOLOGY.2009.06.021
Keskintepe, L., Pacholczyk, G., Machnicka, A., Norris, K., Curuk, M. A., Khan, I., & Brackett, B. G. (2002). Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biology of Reproduction, 67(2), 409-415. http://www.ncbi.nlm.nih.gov/pubmed/12135874
Klooster, K. L., Burruel, V. R., & Meyers, S. A. (2011). Loss of fertilization potential of desiccated rhesus macaque spermatozoa following prolonged storage. Cryobiology, 62(62), 161-166. https://doi.org/10.1016/J.CRYOBIOL.2011.02.002
Kusakabe, H., & Kamiguchi, Y. (2004). Chromosomal integrity of freeze-dried mouse spermatozoa after 137Cs γ-ray irradiation. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 556(1-2), 163-168. https://doi.org/10.1016/J.MRFMMM.2004.08.001
Kusakabe, H., Szczygiel, M. A., Whittingham, D. G., & Yanagimachi, R. (2001). Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proceedings of the National Academy of Sciences United States of America, 98(24), 13501-13506. https://doi.org/10.1073/PNAS.241517598
Kusakabe, H., & Tateno, H. (2011). Characterization of chromosomal damage accumulated in freeze-dried mouse spermatozoa preserved under ambient and heat stress conditions. Mutagenesis, 26(3), 447-453. https://doi.org/10.1093/MUTAGE/GER003
Kusakabe, H., & Tateno, H. (2017). Prevention of high-temperature-induced chromosome damage in mouse spermatozoa freeze-dried using Ca2+ chelator-containing buffer alkalinized with NaOH or KOH. Cryobiology, 79, 71-77. https://doi.org/10.1016/J.CRYOBIOL.2017.08.007
Kusakabe, H., Yanagimachi, R., & Kamiguchi, Y. (2007). Mouse and human spermatozoa can be freeze-dried without damaging their chromosomes. Human Reproduction, 23(2), 233-239. https://doi.org/10.1093/HUMREP/DEM252
Kwon, I. K., Park, K. E., & Niwa, K. (2004). Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biology of Reproduction, 71(5), 1430-1436. https://doi.org/10.1095/BIOLREPROD.104.031260
Lee, K. B., & Niwa, K. (2006). Fertilization and development in vitro of bovine oocytes following intracytoplasmic injection of heat-dried sperm heads. Biology of Reproduction, 74(1), 146-152. https://doi.org/10.1095/BIOLREPROD.105.044743
Lee, K. B., Park, K. E., Kwon, I. K., Tripurani, S. K., Kim, K. J., Lee, J. H., Niwa, K., & Kim, M. K. (2013). Develop to term rat oocytes injected with heat-dried sperm heads. PLoS One, 8(11), e78260. https://doi.org/10.1371/JOURNAL.PONE.0078260
Lee, P.-C., Adams, D. M., Amelkina, O., White, K. K., Amoretti, L. A., Whitaker, M. G., & Comizzoli, P. (2019). Influence of microwave-assisted dehydration on morphological integrity and viability of cat ovarian tissues: First steps toward long-term preservation of complex biomaterials at supra-zero temperatures. PLoS One, 14(12), e0225440. https://doi.org/10.1371/journal.pone.0225440
Lee, P. C., & Comizzoli, P. (2019). Desiccation and supra-zero temperature storage of cat germinal vesicles lead to less structural damage and similar epigenetic alterations compared to cryopreservation. Molecular Reproduction and Development, 86(12), 1822-1831. https://doi.org/10.1002/mrd.23276
Lee, P. C., Zahmel, J., Jewgenow, K., & Comizzoli, P. (2022). Desiccated cat spermatozoa retain DNA integrity and developmental potential after prolonged storage and shipping at non-cryogenic temperatures. Journal Of Assisted Reproduction And Genetics, 39(1), 141-151. https://doi.org/10.1007/s10815-021-02337-4
Letterie, G., & Fox, D. (2020). Lawsuit frequency and claims basis over lost, damaged, and destroyed frozen embryos over a 10-year period. F&S Reports, 1(2), 78-82. https://doi.org/10.1016/J.XFRE.2020.06.007
Li, M. W., Baridon, B., Trainor, A., Djan, E., Koehne, A., Griffey, S. M., Biggers, J. D., Toner, M., & Lloyd, K. C. K. (2012). Mutant mice derived by ICSI of evaporatively dried spermatozoa exhibit expected phenotype. Reproduction, 143(4), 449-453. https://doi.org/10.1530/REP-12-0005
Li, M. W., Biggers, J. D., Elmoazzen, H. Y., Toner, M., McGinnis, L., & Lloyd, K. C. K. (2007). Long-term storage of mouse spermatozoa after evaporative drying. Reproduction, 133(5), 919-929. https://doi.org/10.1530/REP-06-0096
Li, M. W., Willis, B. J., Griffey, S. M., Spearow, J. L., & Lloyd, K. C. K. (2009). Assessment of three generations of mice derived by ICSI using freeze-dried sperm. Zygote, 17(3), 239-251. https://doi.org/10.1017/S0967199409005292
Li, S., Chakraborty, N., Borcar, A., Menze, M. A., Toner, M., & Hand, S. C. (2012). Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation. Proceedings of the National Academy of Sciences United States of America, 109(51), 20859-20864. https://doi.org/10.1073/PNAS.1214893109
Li, X. X., Diao, Y. F., Wei, H. J., Wang, S. Y., Cao, X. Y., Zhang, Y. F., Chang, T., Li, D. L., Kim, M. K., & Xu, B. (2017). Tauroursodeoxycholic acid enhances the development of porcine embryos derived from in vitro-matured oocytes and evaporatively dried spermatozoa. Scientific Reports, 7(1), 6773. https://doi.org/10.1038/s41598-017-07185-w
Liu, J., Lee, G. Y., Lawitts, J. A., Toner, M., & Biggers, J. D. (2012). Preservation of mouse sperm by convective drying and storing in 3-O-methyl-d-glucose. PLoS One, 7(1), e29924. https://doi.org/10.1371/JOURNAL.PONE.0029924
Liu, J., Lee, G. Y., Lawitts, J. A., Toner, M., & Biggers, J. D. (2014). Live pups from evaporatively dried mouse sperm stored at ambient temperature for up to 2 years. PLoS One, 9(6), e99809.
Liu, J. L., Kusakabe, H., Chang, C. C., Suzuki, H., Schmidt, D. W., Julian, M., Pfeffer, R., Bormann, C. L., Tian, X. C., Yanagimachi, R., & Yang, X. (2004). Freeze-dried sperm fertilization leads to full-term development in rabbits. Biology of Reproduction, 70(6), 1776-1781. https://doi.org/10.1095/BIOLREPROD.103.025957
Liu, Q. C., Chen, T., Huang, X. Y., & Sun, F. Z. (2005). Mammalian freeze-dried sperm can maintain their calcium oscillation-inducing ability when microinjected into mouse eggs. Biochemical and Biophysical Research Communications, 328(4), 824-830. https://doi.org/10.1016/J.BBRC.2005.01.034
Loi, P., Anzalone, D. A., Palazzese, L., Dinnyés, A., Saragusty, J., & Czernik, M. (2021). Dry storage of mammalian spermatozoa and cells: State-of-the-art and possible future directions. Reproduction, Fertility, and Development, 33(2), 82-90. https://doi.org/10.1071/RD20264
Loi, P., Matsukawa, K., Ptak, G., Clinton, M., Fulka, J., Nathan, Y., & Arav, A. (2008). Freeze-dried somatic cells direct embryonic development after nuclear transfer. PLoS One, 3(8), e2978. https://doi.org/10.1371/journal.pone.0002978
Ma, X., Jamil, K., MacRae, T. H., Clegg, J. S., Russell, J. M., Villeneuve, T. S., Euloth, M., Sun, Y., Crowe, J. H., Tablin, F., & Oliver, A. E. (2005). A small stress protein acts synergistically with trehalose to confer desiccation tolerance on mammalian cells. Cryobiology, 51(1), 15-28. https://doi.org/10.1016/J.CRYOBIOL.2005.04.007
Martins, C. F., Báo, S. N., Dode, M. N., Correa, G. a, & Rumpf, R. (2007). Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm. Theriogenology, 67(8), 1307-1315. https://doi.org/10.1016/j.theriogenology.2007.01.015
McGinnis, L. K., Zhu, L., Lawitts, J. A., Bhowmick, S., Toner, M., & Biggers, J. D. (2005). Mouse sperm desiccated and stored in trehalose medium without freezing. Biology of Reproduction, 73(4), 627-633. https://doi.org/10.1095/biolreprod.105.042291
Men, N. T., Kikuchi, K., Nakai, M., Fukuda, A., Tanihara, F., Noguchi, J., Kaneko, H., Linh, N. V., Nguyen, B. X., Nagai, T., & Tajima, A. (2013). Effect of trehalose on DNA integrity of freeze-dried boar sperm, fertilization, and embryo development after intracytoplasmic sperm injection. Theriogenology, 80(9), 1033-1044. https://doi.org/10.1016/J.THERIOGENOLOGY.2013.08.001
Mercati, F., Domingo, P., Pasquariello, R., Dall'Aglio, C., di Michele, A., Forti, K., Cocci, P., Boiti, C., Gil, L., Zerani, M., & Maranesi, M. (2020). Effect of chelating and antioxidant agents on morphology and DNA methylation in freeze-drying rabbit (Oryctolagus cuniculus) spermatozoa. Reproduction in Domestic Animals, 55(1), 29-37. https://doi.org/10.1111/RDA.13577
Muneto, T., & Horiuchi, T. (2011). Full-term development of hamster embryos produced by injecting freeze-dried spermatozoa into oocytes. Journal of Mammalian Ova Research, 28(1), 32-39. https://doi.org/10.1274/JMOR.28.32
Nakai, M., Kashiwazaki, N., Takizawa, A., Maedomari, N., Ozawa, M., Noguchi, J., Kaneko, H., Shino, M., & Kikuchi, K. (2007). Effects of chelating agents during freeze-drying of boar spermatozoa on DNA fragmentation and on developmental ability in vitro and in vivo after intracytoplasmic sperm head injection. Zygote, 15(1), 15-24. https://doi.org/10.1017/S0967199406003935
Olaciregui, M., Luño, V., Domingo, P., González, N., & Gil, L. (2017). In vitro developmental ability of ovine oocytes following intracytoplasmic injection with freeze-dried spermatozoa. Scientific Reports, 7(1), 1096. https://doi.org/10.1038/s41598-017-00583-0
Olaciregui, M., Luño, V., Gonzalez, N., de Blas, I., & Gil, L. (2015). Freeze-dried dog sperm: Dynamics of DNA integrity. Cryobiology, 71(2), 286-290. https://doi.org/10.1016/J.CRYOBIOL.2015.08.001
Olaciregui, M., Luño, V., González, N., Domingo, P., de Blas, I., & Gil, L. (2017). Chelating agents in combination with rosmarinic acid for boar sperm freeze-drying. Reproductive biology, 17(3), 193-198. https://doi.org/10.1016/J.REPBIO.2017.05.001
Oldenhof, H., Zhang, M., Narten, K., Bigalk, J., Sydykov, B., Wolkers, W. F., & Sieme, H. (2017). Freezing-induced uptake of disaccharides for preservation of chromatin in freeze-dried stallion sperm during accelerated aging. Biology of Reproduction, 97(6), 892-901. https://doi.org/10.1093/BIOLRE/IOX142
Olsson, C., Genheden, S., García Sakai, V., & Swenson, J. (2019). Mechanism of Trehalose-Induced protein stabilization from neutron scattering and modeling. The Journal of Physical Chemistry B, 123(17), 3679-3687. https://doi.org/10.1021/ACS.JPCB.9B01856
Palazzese, L., Anzalone, D. A., Turri, F., Faieta, M., Donnadio, A., Pizzi, F., Pittia, P., Matsukawa, K., & Loi, P. (2020). Whole genome integrity and enhanced developmental potential in ram freeze-dried spermatozoa at mild sub-zero temperature. Scientific Reports, 10(1), 18873. https://doi.org/10.1038/S41598-020-76061-X
Palazzese, L., Gosálvez, J., Anzalone, D. A., Loi, P., & Saragusty, J. (2018). DNA fragmentation in epididymal freeze-dried ram spermatozoa impairs embryo development. Journal of Reproduction and Development, 64(5), 393-400. https://doi.org/10.1262/JRD.2018-033
Patrick, J. L., Elliott, G. D., & Comizzoli, P. (2017). Structural integrity and developmental potential of spermatozoa following microwave-assisted drying in the domestic cat model. Theriogenology, 103, 36-43. https://doi.org/10.1016/j.theriogenology.2017.07.037
Polge, C., Smith, A. U., & Parkes, A. S. (1949). Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature, 164(4172), 666. https://doi.org/10.1038/164666A0
Pomeroy, K. O., Reed, M. L., LoManto, B., Harris, S. G., Hazelrigg, W. B., & Kelk, D. A. (2019). Cryostorage tank failures: Temperature and volume loss over time after induced failure by removal of insulative vacuum. Journal of Assisted Reproduction And Genetics, 36(11), 2271-2278. https://doi.org/10.1007/S10815-019-01597-5
Restrepo, G., Varela, E., Duque, J. E., Gómez, J. E., & Rojas, M. (2019). Freezing, vitrification, and freeze-drying of equine spermatozoa: impact on mitochondrial membrane potential, lipid peroxidation, and DNA integrity. Journal of Equine Veterinary Science, 72, 8-15. https://doi.org/10.1016/J.JEVS.2018.10.006
Ringleb, J., Waurich, R., Wibbelt, G., Streich, W. J., & Jewgenow, K. (2011). Prolonged storage of epididymal spermatozoa does not affect their capacity to fertilise in vitro-matured domestic cat (Felis catus) oocytes when using ICSI. Reproduction, Fertility, and Development, 23(6), 818-825. https://doi.org/10.1071/RD10192
Sánchez-Partida, L. G., Simerly, C. R., & Ramalho-Santos, J. (2008). Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection. Fertility and Sterility, 89(3), 742-745. https://doi.org/10.1016/j.fertnstert.2007.02.066
Saragusty, J., Anzalone, D. A., Palazzese, L., Arav, A., Patrizio, P., Gosálvez, J., & Loi, P. (2020). Dry biobanking as a conservation tool in the Anthropocene. Theriogenology, 150, 130-138. https://doi.org/10.1016/J.THERIOGENOLOGY.2020.01.022
Shahba, M. I., El-Sheshtawy, R. I., El-Azab, A. S. I., Abdel-Ghaffar, A. E., Ziada, M. S., & Zaky, A. A. (2016). The effect of freeze-drying media and storage temperature on ultrastructure and DNA of freeze-dried buffalo bull spermatozoa. Asian Pacific Journal of Reproduction, 5(6), 524-535. https://doi.org/10.1016/J.APJR.2016.11.002
Shahmoradi, E., Baheiraei, N., & Halvaei, I. (2022). Trehalose attenuates detrimental effects of freeze-drying on human sperm parameters. Biopreservation and Biobanking, 20(1), 31-37. https://doi.org/10.1089/BIO.2020.0167/ASSET/IMAGES/LARGE/BIO.2020.0167_FIGURE_1.JPEG
Silva, H. V. R., da Silva, A. M., Lee, P. C., Brito, B. F., Silva, A. R., da Silva, L. D. M., & Comizzoli, P. (2020). Influence of microwave-assisted drying on structural integrity and viability of testicular tissues from adult and prepubertal domestic cats. Biopreservation and Biobanking, 18(5), 415-424. https://doi.org/10.1089/BIO.2020.0048
Sitaula, R., Elmoazzen, H., Toner, M., & Bhowmick, S. (2009). Desiccation tolerance in bovine sperm: A study of the effect of intracellular sugars and the supplemental roles of an antioxidant and a chelator. Cryobiology, 58(3), 322-330. https://doi.org/10.1016/J.CRYOBIOL.2009.03.002
Stanishevskaya, O., Silyukova, Y., Pleshanov, N., Kurochkin, A., Fedorova, E., & Radaev, A. A. (2022). A successful protocol for achieving anhydrobiosis of Gallus Gallus domesticus spermatozoa while maintaining their fertility IN VIVO. Cryobiology, 104, 102-106. https://doi.org/10.1016/J.CRYOBIOL.2021.11.002
Stewart, S., Arminan, A., & He, X. (2020). Nanoparticle-mediated delivery of cryoprotectants for cryopreservation. Cryo Letters, 41(6), 308-316.
Thorat, L., Oulkar, D., Banerjee, K., Gaikwad, S. M., & Nath, B. B. (2017). High-throughput mass spectrometry analysis revealed a role for glucosamine in potentiating recovery following desiccation stress in Chironomus. Scientific Reports, 7(1), 3659. https://doi.org/10.1038/S41598-017-03572-5
Tsujimoto, Y., Kaneko, T., Yoshida, T., Kimura, K., Inaba, T., Sugiura, K., & Hatoya, S. (2020). Development of feline embryos produced using freeze-dried sperm. Theriogenology, 147, 71-76. https://doi.org/10.1016/J.THERIOGENOLOGY.2020.02.021
Ujaoney, A. K., Padwal, M. K., & Basu, B. (2017). Proteome dynamics during post-desiccation recovery reveal convergence of desiccation and gamma radiation stress response pathways in Deinococcus radiodurans. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1865(9), 1215-1226. https://doi.org/10.1016/J.BBAPAP.2017.06.014
Ushigome, N., Wakayama, S., Yamaji, K., Ito, D., Ooga, M., & Wakayama, T. (2022). Production of offspring from vacuum-dried mouse spermatozoa and assessing the effect of drying conditions on sperm DNA and embryo development. Journal of Reproduction and Development, 68(4), 262-270. https://doi.org/10.1262/JRD.2022-048
Wakayama, S., Ito, D., Hayashi, E., Ishiuchi, T., & Wakayama, T. (2022). Healthy cloned offspring derived from freeze-dried somatic cells. Nature Communications, 13(1), 3666. https://doi.org/10.1038/S41467-022-31216-4
Wakayama, S., Ito, D., Kamada, Y., Yonemura, S., Ooga, M., Kishigami, S., & Wakayama, T. (2019). Tolerance of the freeze-dried mouse sperm nucleus to temperatures ranging from −196 °C to 150 °C. Scientific Reports, 9(1), 5719. https://doi.org/10.1038/s41598-019-42062-8
Wakayama, S., Kamada, Y., Yamanaka, K., Kohda, T., Suzuki, H., Shimazu, T., Tada, M. N., Osada, I., Nagamatsu, A., Kamimura, S., Nagatomo, H., Mizutani, E., Ishino, F., Yano, S., & Wakayama, T. (2017). Healthy offspring from freeze-dried mouse spermatozoa held on the International Space Station for 9 months. Proceedings of the National Academy of Sciences United States of America, 114(23), 5988-5993. https://doi.org/10.1073/pnas.1701425114
Wakayama, T., & Yanagimachi, R. (1998). Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nature Biotechnology, 16(7), 639-641. https://doi.org/10.1038/NBT0798-639
Wang, S., Lee, P. C., Elsayed, A., Zhang, F., Zhang, Y., Comizzoli, P., & Elliott, G. D. (2021). Preserving the female genome in trehalose glass at supra-zero temperatures: The relationship between moisture content and DNA damage in feline germinal vesicles. Cellular and Molecular Bioengineering, 14(1), 101-112. https://doi.org/10.1007/s12195-020-00635-y
Ward, M. A., Kaneko, T., Kusakabe, H., Biggers, J. D., Whittingham, D. G., & Yanagimachi, R. (2003). Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection. Biology of Reproduction, 69(6), 2100-2108. https://doi.org/10.1095/BIOLREPROD.103.020529
Watanabe, H., Asano, T., Abe, Y., Fukui, Y., & Suzuki, H. (2009). Pronuclear formation of freeze-dried canine spermatozoa microinjected into mouse oocytes. Journal of Assisted Reproduction And Genetics, 26(9-10), 531-536. https://doi.org/10.1007/S10815-009-9358-Y
Weng, L. (2021). Technologies and applications toward preservation of cells in a dry state for therapies. Biopreservation and Biobanking, 19(4), 332-341. https://doi.org/10.1089/BIO.2020.0130
Whelan, D. R., Bambery, K. R., Heraud, P., Tobin, M. J., Diem, M., McNaughton, D., & Wood, B. R. (2011). Monitoring the reversible B to A-Like transition of DNA in eukaryotic cells using Fourier transform infrared spectroscopy. Nucleic Acids Research, 39(13), 5439-5448. https://doi.org/10.1093/NAR/GKR175
Wolkers, W. F., & Oldenhof, H. (2021). Principles underlying cryopreservation and freeze-drying of cells and tissues. Methods in Molecular Biology (Clifton, N.J.), 2180, 3-25. https://doi.org/10.1007/978-1-0716-0783-1_1
Wolkers, W. F., Oldenhof, H., & Glasmacher, B. (2010). Dehydrating phospholipid vesicles measured in real-time using ATR Fourier transform infrared spectroscopy. Cryobiology, 61(1), 108-114. https://doi.org/10.1016/J.CRYOBIOL.2010.06.001
Yamada, T. G., Suetsugu, Y., Deviatiiarov, R., Gusev, O., Cornette, R., Nesmelov, A., Hiroi, N., Kikawada, T., & Funahashi, A. (2018). Transcriptome analysis of the anhydrobiotic cell line Pv11 infers the mechanism of desiccation tolerance and recovery. Scientific Reports, 8(1), 17941. https://doi.org/10.1038/s41598-018-36124-6
Zhang, M., Oldenhof, H., Sieme, H., & Wolkers, W. F. (2016). Freezing-induced uptake of trehalose into mammalian cells facilitates cryopreservation. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1858(6), 1400-1409. https://doi.org/10.1016/j.bbamem.2016.03.020
Zhang, Y., Wang, H., Stewart, S., Jiang, B., Ou, W., Zhao, G., & He, X. (2019). Cold-responsive nanoparticle enables intracellular delivery and rapid release of trehalose for organic-solvent-free cryopreservation. Nano Letters, 19(12), 9051-9061. https://doi.org/10.1021/acs.nanolett.9b04109
Zhu, W. J., Li, J., & Xiao, L. J. (2016). Changes on membrane integrity and ultrastructure of human sperm after freeze-drying. Journal of Reproduction and Contraception, 2(27), 76-81. https://doi.org/10.7669/J.ISSN.1001-7844.2016.02.0076