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
Autoři:
Pei-Chih Lee aff001; Daniella M. Adams aff001; Olga Amelkina aff001; Kylie K. White aff001; Luigi A. Amoretti aff001; Marinda G. Whitaker aff001; Pierre Comizzoli aff001
Působiště autorů:
Smithsonian Conservation Biology Institute, National Zoological Park, Washington, District of Columbia, United States of America
aff001
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225440
Souhrn
Ovarian tissue contains large pools of immature oocytes enclosed in primordial follicles, making it an attractive target for fertility preservation in female cancer patients, livestock and wild species. Compared to cryopreservation, desiccation and long-term storage of samples at supra-zero temperatures (using strategies inspired from small organisms to resist extreme environments) would be more cost-effective and convenient. The objective of the study was to characterize the influence of microwave-assisted dehydration on structural and functional properties of living ovarian tissues. While this method allows preservation of single cells (cat oocytes and sperm cells so far) using trehalose as the xeroprotectant, it has not been developed for multicellular tissues yet. Ovarian cortex biopsies were reversibly permeabilized, exposed to various concentrations of trehalose, and dried for different times using a commercial microwave under thermal control. Effective dehydration of samples along with proper trehalose retention were reached within 30 min of microwave drying. Importantly, the process did not affect morphology and DNA integrity of follicles or stromal cells. Moreover, transcriptional activity and survival of follicles were partially maintained following 10 min of drying, which already was compatible with storage at non-cryogenic temperatures. Present data provide critical foundation to develop dry-preservation techniques for long-term storage of living multicellular tissues.
Klíčová slova:
DNA transcription – Specimen storage – Trehalose – Oocytes – Stromal cells – Microwave radiation – Biomaterials – Tissue dehydration
Zdroje
1. Monniaux D, Clement F, Dalbies-Tran R, Estienne A, Fabre S, Mansanet C, et al. The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biol Reprod. 2014;90(4):85. Epub 2014/03/07. doi: 10.1095/biolreprod.113.117077 24599291.
2. Pepling ME. From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis. 2006;44(12):622–32. Epub 2006/12/06. doi: 10.1002/dvg.20258 17146778.
3. Kerr JB, Myers M, Anderson RA. The dynamics of the primordial follicle reserve. Reproduction. 2013;146(6):R205–15. Epub 2013/08/10. doi: 10.1530/REP-13-0181 23929903.
4. Kristensen SG, Andersen CY. Cryopreservation of Ovarian Tissue: Opportunities Beyond Fertility Preservation and a Positive View Into the Future. Front Endocrinol (Lausanne). 2018;9:347. Epub 2018/07/14. doi: 10.3389/fendo.2018.00347 30002647; PubMed Central PMCID: PMC6031740.
5. Anderson RA, Wallace WHB, Telfer EE. Ovarian tissue cryopreservation for fertility preservation: clinical and research perspectives. Human Reproduction Open. 2017;2017(1). doi: 10.1093/hropen/hox022
6. Kim SY, Kim SK, Lee JR, Woodruff TK. Toward precision medicine for preserving fertility in cancer patients: existing and emerging fertility preservation options for women. J Gynecol Oncol. 2016;27(2):e22. Epub 2016/01/16. doi: 10.3802/jgo.2016.27.e22 26768785; PubMed Central PMCID: PMC4717227.
7. Comizzoli P. Biobanking and fertility preservation for rare and endangered species. Anim Reprod. 2017;14(1):30–3. doi: 10.21451/1984-3143-Ar889 WOS:000397098800003.
8. Hansen PJ. Current and future assisted reproductive technologies for mammalian farm animals. Advances in experimental medicine and biology. 2014;752:1–22. doi: 10.1007/978-1-4614-8887-3_1 24170352.
9. Lin TC, Yen JM, Kuo TC, Gong KB, Hsu KH, Hsu TT. Comparison of the developmental potential of 2-week-old preantral follicles derived from vitrified ovarian tissue slices, vitrified whole ovaries and vitrified/transplanted newborn mouse ovaries using the metal surface method. BMC Biotechnol. 2008;8:38. Epub 2008/04/09. doi: 10.1186/1472-6750-8-38 18394156; PubMed Central PMCID: PMC2364622.
10. Kim GA, Kim HY, Kim JW, Lee G, Lee E, Ahn JY, et al. Effectiveness of slow freezing and vitrification for long-term preservation of mouse ovarian tissue. Theriogenology. 2011;75(6):1045–51. Epub 2011/01/12. doi: 10.1016/j.theriogenology.2010.11.012 21220167.
11. Mouttham L, Comizzoli P. The preservation of vital functions in cat ovarian tissues during vitrification depends more on the temperature of the cryoprotectant exposure than on the sucrose supplementation. Cryobiology. 2016;73(2):187–95. doi: 10.1016/j.cryobiol.2016.07.013 27475292.
12. Tanpradit N, Chatdarong K, Comizzoli P. Carbonyl cyanide 4-(trifluoromethoxy)phenylhydrazone (FCCP) pre-exposure ensures follicle integrity during in vitro culture of ovarian tissue but not during cryopreservation in the domestic cat model. J Assist Reprod Genet. 2016. doi: 10.1007/s10815-016-0810-5 27639998.
13. Oskam IC, Asadi BA, Santos RR. Histologic and ultrastructural features of cryopreserved ovine ovarian tissue: deleterious effect of 1,2-propanediol applying different thawing protocols. Fertil Steril. 2010;93(8):2764–6. Epub 2010/03/20. doi: 10.1016/j.fertnstert.2010.02.003 20236634.
14. Gandolfi F, Paffoni A, Papasso Brambilla E, Bonetti S, Brevini TA, Ragni G. Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil Steril. 2006;85 Suppl 1:1150–6. doi: 10.1016/j.fertnstert.2005.08.062 16616087.
15. Mouttham L, Fortune JE, Comizzoli P. Damage to fetal bovine ovarian tissue caused by cryoprotectant exposure and vitrification is mitigated during tissue culture. J Assist Reprod Gen. 2015;32(8):1239–50. doi: 10.1007/s10815-015-0543-x WOS:000360547300013; PubMed Central PMCID: PMC4554372. 26249553
16. Kardak A, Leibo SP, Devireddy R. Membrane transport properties of equine and macaque ovarian tissues frozen in mixtures of dimethylsulfoxide and ethylene glycol. J Biomech Eng. 2007;129(5):688–94. Epub 2007/09/25. doi: 10.1115/1.2768107 17887894.
17. Isachenko V, Lapidus I, Isachenko E, Krivokharchenko A, Kreienberg R, Woriedh M, et al. Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reproduction. 2009;138(2):319–27. Epub 2009/05/15. doi: 10.1530/REP-09-0039 19439559.
18. Siebzehnrubl E, Kohl J, Dittrich R, Wildt L. Freezing of human ovarian tissue—not the oocytes but the granulosa is the problem. Mol Cell Endocrinol. 2000;169(1–2):109–11. Epub 2001/01/13. S0303-7207(00)00362-2 [pii]. doi: 10.1016/s0303-7207(00)00362-2 11155940.
19. Morano KA. Anhydrobiosis: drying out with sugar. Current biology: CB. 2014;24(23):R1121–3. Epub 2014/12/04. doi: 10.1016/j.cub.2014.10.022 25465329.
20. Weng L, Ziaei S, Elliott GD. Effects of Water on Structure and Dynamics of Trehalose Glasses at Low Water Contents and its Relationship to Preservation Outcomes. Sci Rep. 2016;6:28795. Epub 2016/07/09. doi: 10.1038/srep28795 27387435; PubMed Central PMCID: PMC4937400.
21. Oliver AE. Dry state preservation of nucleated cells: progress and challenges. Biopreserv Biobank. 2012;10(4):376–85. Epub 2012/08/01. doi: 10.1089/bio.2012.0020 24849888.
22. Arguelles JC. Why can't vertebrates synthesize trehalose? J Mol Evol. 2014;79(3–4):111–6. Epub 2014/09/19. doi: 10.1007/s00239-014-9645-9 25230776.
23. Stewart S, He X. Intracellular Delivery of Trehalose for Cell Banking. Langmuir. 2018. Epub 2018/08/07. doi: 10.1021/acs.langmuir.8b02015 30078320.
24. Loi P, Iuso D, Czernik M, Zacchini F, Ptak G. Towards storage of cells and gametes in dry form. Trends Biotechnol. 2013;31(12):688–95. Epub 2013/10/31. doi: 10.1016/j.tibtech.2013.09.004 24169600.
25. Li S, Chakraborty N, Borcar A, Menze MA, Toner M, Hand SC. Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(51):20859–64. Epub 2012/11/28. doi: 10.1073/pnas.1214893109 23185012; PubMed Central PMCID: PMC3529014.
26. Less R, Boylan KL, Skubitz AP, Aksan A. Isothermal vitrification methodology development for non-cryogenic storage of archival human sera. Cryobiology. 2013;66(2):176–85. Epub 2013/01/29. doi: 10.1016/j.cryobiol.2013.01.003 23353801; PubMed Central PMCID: PMC3601464.
27. Cellemme SL, Van Vorst M, Paramore E, Elliott GD. Advancing microwave technology for dehydration processing of biologics. Biopreserv Biobank. 2013;11(5):278–84. Epub 2014/05/20. doi: 10.1089/bio.2013.0024 24835259; PubMed Central PMCID: PMC4076997.
28. Elliott GD, Lee PC, Paramore E, Van Vorst M, Comizzoli P. Resilience of oocyte germinal vesicles to microwave-assisted drying in the domestic cat model. Biopreservation and Biobanking. 2015;13(3):164–71. doi: 10.1089/bio.2014.0078 WOS:000363940000003. 26035005
29. Patrick JL, Elliott GD, Comizzoli P. Structural integrity and developmental potential of spermatozoa following microwave-assisted drying in the domestic cat model. Theriogenology. 2017;103:36–43. Epub 2017/08/05. doi: 10.1016/j.theriogenology.2017.07.037 28772113.
30. Songsasen N, Comizzoli P, Nagashima J, Fujihara M, Wildt DE. The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro. Reprod Domest Anim. 2012;47 Suppl 6:13–8. doi: 10.1111/rda.12067 23279457; PubMed Central PMCID: PMC3579211.
31. Comizzoli P, Songsasen N, Wildt DE. Protecting and extending fertility for females of wild and endangered mammals. In: Woodruff TK, Zoloth L, Campo-Engelstein L, Rodriguez S, editors. Oncofertility, Cancer Treatment and Research. 156: Springer Science and Business Media; 2010. p. 87–100.
32. Chen T, Fowler A, Toner M. Literature review: supplemented phase diagram of the trehalose-water binary mixture. Cryobiology. 2000;40(3):277–82. Epub 2000/06/22. doi: 10.1006/cryo.2000.2244 10860627.
33. Inyang UE, Oboh IO, Etuk BR. Kinetic models for drying techniques—food materials. Advances in Chemical Engineering and Science. 2018;8:27–48. doi: 10.4236/aces.2018.82003
34. Gamli F. A review based on the relationship among drying, curve fitting and mathematical models in food system. Adv Res Agri Vet Sci. 2014;1(2):47–53.
35. Xanthopoulos G, Yanniotis S, Lambrinos G. Study of the drying behaviour in peeled and unpeeled whole figs. Journal of Food Engineering. 2010;97(3):419–24. doi: 10.1016/j.jfoodeng.2009.10.037
36. Doymaz İ, İsmail O. Drying and rehydration behaviors of green bell peppers. Food Science and Biotechnology. 2010;19(6):1449–55. doi: 10.1007/s10068-010-0207-7
37. Kingsly RP, Goyal RK, Manikantan MR, Ilyas SM. Effects of pretreatments and drying air temperature on drying behaviour of peach slice. International Journal of Food Science & Technology. 2007;42(1):65–9. doi: 10.1111/j.1365-2621.2006.01210.x
38. Nakamura Y, Obata R, Okuyama N, Aono N, Hashimoto T, Kyono K. Residual ethylene glycol and dimethyl sulphoxide concentration in human ovarian tissue during warming/thawing steps following cryopreservation. Reproductive biomedicine online. 2017;35(3):311–3. Epub 2017/06/25. doi: 10.1016/j.rbmo.2017.05.016 28645837.
39. Lynch AL, Chen R, Dominowski PJ, Shalaev EY, Yancey RJ Jr., Slater NK. Biopolymer mediated trehalose uptake for enhanced erythrocyte cryosurvival. Biomaterials. 2010;31(23):6096–103. Epub 2010/05/18. doi: 10.1016/j.biomaterials.2010.04.020 20471082.
40. Sharp DM, Picken A, Morris TJ, Hewitt CJ, Coopman K, Slater NK. Amphipathic polymer-mediated uptake of trehalose for dimethyl sulfoxide-free human cell cryopreservation. Cryobiology. 2013;67(3):305–11. Epub 2013/09/21. doi: 10.1016/j.cryobiol.2013.09.002 24045066; PubMed Central PMCID: PMC3842503.
41. Rao W, Huang H, Wang H, Zhao S, Dumbleton J, Zhao G, et al. Nanoparticle-mediated intracellular delivery enables cryopreservation of human adipose-derived stem cells using trehalose as the sole cryoprotectant. ACS Appl Mater Interfaces. 2015;7(8):5017–28. Epub 2015/02/14. doi: 10.1021/acsami.5b00655 25679454; PubMed Central PMCID: PMC4734639.
42. Zhang W, Rong J, Wang Q, He X. The encapsulation and intracellular delivery of trehalose using a thermally responsive nanocapsule. Nanotechnology. 2009;20(27):275101. Epub 2009/06/17. doi: 10.1088/0957-4484/20/27/275101 19528681.
43. Brito DCC, Domingues SFS, Rodrigues APR, Maside C, Lunardi FO, Wu X, et al. Cryopreservation of domestic cat (Felis catus) ovarian tissue: Comparison of two vitrification methods. Theriogenology. 2018;111:69–77. Epub 2018/02/13. doi: 10.1016/j.theriogenology.2018.01.015 29428847.
44. Baust JM, Fowler A, Toner M. Induction of apoptosis in response to anhydrobiotic conditions in mammalian cells. Front Clin Res. 2004;2(4):248–59.
45. Faustino LR, Santos RR, Silva CM, Pinto LC, Celestino JJ, Campello CC, et al. Goat and sheep ovarian tissue cryopreservation: Effects on the morphology and development of primordial follicles and density of stromal cell. Anim Reprod Sci. 2010;122(1–2):90–7. Epub 2010/08/31. doi: 10.1016/j.anireprosci.2010.08.001 20800393.
46. McGinnis LK, Zhu L, Lawitts JA, Bhowmick S, Toner M, Biggers JD. Mouse sperm desiccated and stored in trehalose medium without freezing. Biol Reprod. 2005;73(4):627–33. Epub 2005/06/03. doi: 10.1095/biolreprod.105.042291 15930320.
47. Di Gioacchino M, Bruni F, Ricci MA. Protection against Dehydration: a Neutron Diffraction Study on Aqueous Solutions of a Model Peptide and Trehalose. J Phys Chem B. 2018. Epub 2018/10/20. doi: 10.1021/acs.jpcb.8b08046 30339006.
48. Ragoonanan V, Aksan A. Heterogeneity in desiccated solutions: implications for biostabilization. Biophys J. 2008;94(6):2212–27. Epub 2007/12/07. doi: 10.1529/biophysj.107.110684 18055531; PubMed Central PMCID: PMC2257888.
49. Lai D, Ding J, Smith GW, Smith GD, Takayama S. Slow and steady cell shrinkage reduces osmotic stress in bovine and murine oocyte and zygote vitrification. Hum Reprod. 2015;30(1):37–45. Epub 2014/10/31. doi: 10.1093/humrep/deu284 25355589; PubMed Central PMCID: PMC4262467.
50. Zhang X, Catalano PN, Gurkan UA, Khimji I, Demirci U. Emerging technologies in medical applications of minimum volume vitrification. Nanomedicine (Lond). 2011;6(6):1115–29. Epub 2011/10/01. doi: 10.2217/nnm.11.71 21955080; PubMed Central PMCID: PMC3193162.
51. Zhang M, Oldenhof H, Sydykov B, Bigalk J, Sieme H, Wolkers WF. Freeze-drying of mammalian cells using trehalose: preservation of DNA integrity. Sci Rep. 2017;7(1):6198. Epub 2017/07/26. doi: 10.1038/s41598-017-06542-z 28740099; PubMed Central PMCID: PMC5524761.
52. Jasensky J, Swain JE. Peering beneath the surface: novel imaging techniques to noninvasively select gametes and embryos for ART. Biol Reprod. 2013;89(4):105. Epub 2013/09/27. doi: 10.1095/biolreprod.113.113076 24068105.
53. Fujihara M, Comizzoli P, Wildt DE, Songsasen N. Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium. Reprod Domest Anim. 2012;47 Suppl 6:102–8. Epub 2013/02/12. doi: 10.1111/rda.12022 23279476; PubMed Central PMCID: PMC3965327.
54. Miyamoto K, Yamashita T, Tsukiyama T, Kitamura N, Minami N, Yamada M, et al. Reversible membrane permeabilization of mammalian cells treated with digitonin and its use for inducing nuclear reprogramming by Xenopus egg extracts. Cloning Stem Cells. 2008;10(4):535–42. Epub 2008/12/04. doi: 10.1089/clo.2008.0020 19049416.
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts