Hostname: page-component-669899f699-7xsfk Total loading time: 0 Render date: 2025-04-26T02:44:51.497Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological evaluation of adult domestic cat testicular biopsy after vitrification

Published online by Cambridge University Press:  13 May 2024

Julyne Vivian Guimarães de Carvalho Open the ORCID record for Julyne Vivian Guimarães de Carvalho [Opens in a new window] ,
Airton Renan Bastos Soares Open the ORCID record for Airton Renan Bastos Soares [Opens in a new window] ,
Inara Tayná Alves Evangelista Open the ORCID record for Inara Tayná Alves Evangelista [Opens in a new window] ,
Danuza Leite Leão Open the ORCID record for Danuza Leite Leão [Opens in a new window] ,
Regiane Rodrigues dos Santos Open the ORCID record for Regiane Rodrigues dos Santos [Opens in a new window]  and
Sheyla Farhayldes Souza Domingues Open the ORCID record for Sheyla Farhayldes Souza Domingues [Opens in a new window]
Julyne Vivian Guimarães de Carvalho
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil Postgraduate Programme in Animal Health and Production in the Amazon, Federal Rural University of Amazonia, Belém, Pará, Brazil
Airton Renan Bastos Soares
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil
Inara Tayná Alves Evangelista
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil
Danuza Leite Leão
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil
Regiane Rodrigues dos Santos
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil
Sheyla Farhayldes Souza Domingues*
Affiliation:
Laboratory of Wild Animal Biotechnology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil Postgraduate Programme in Animal Health and Production in the Amazon, Federal Rural University of Amazonia, Belém, Pará, Brazil
*
Corresponding author: Sheyla Farhayldes Souza Domingues; Email: shfarha@ufpa.br
Get access Rights & Permissions [Opens in a new window]

Summary

Testicular biopsies (9 mm3) from domestic cats (n = 10) submitted to orchiectomy were submitted to equilibrium vitrification in the presence of ethylene glycol (EG) alone or combined with dimethylsulfoxide (DMSO) as intracellular cryoprotectants, and sucrose or trehalose as extracellular cryoprotectants. The samples were vitrified with 40% EG or 20% EG + 20% DMSO, plus 0.1 M or 0.5 M of sucrose or trehalose. The study was divided into Step 1 and Step 2. In Step 1, intratubular cells (spermatogonia, spermatids, spermatocytes, and Sertoli cells) were quantified and classified as intact or degenerated (pyknotic and/or vacuolated cells). Cryodamage of seminiferous cords was determined by spermatogonia and Sertoli cell scoring of nuclei alterations, tubular basement membrane detachment, epithelium shrinkage, and tubular measures (total area, epithelium area, larger and smaller diameter, and height of the epithelium). In Step 2, Hoechst 33342 stain and propidium iodide (PI) fluorescent stain were used to assess the cell viability of the four best experimental groups in Step 1. The effect of treatments on all analyses was accessed using analysis of variance (ANOVA), and Fisher’s post hoc test at P < 0.05 significance was considered. In Step 1, the mean percentage of spermatogonia and Sertoli cells morphological integrity did not show a difference when using both sugars at different concentrations, but their morphology was more affected when DMSO was used. EG use associated with 0.1 M of sucrose or trehalose positively affected spermatocyte and spermatid morphology, respectively. The larger diameter and epithelium height of seminiferous tubules were increased using DMSO plus 0.5 M sucrose and DMSO plus 0.1 M trehalose. The changes in spermatogonial/Sertoli nucleoli visualization were best scored in the EG groups, while the nuclei condensation was lower with sucrose. The basement membrane was satisfactorily preserved with 0.1 M sucrose. In Step 2, the percentage of cell viability was higher when EG plus 0.1 M sucrose was used. Therefore, DMSO’s negative effect on the vitrification of testicular biopsies of adult domestic cats was evident. The EG plus 0.1 M of sucrose or trehalose associations are the most suitable CPAs to preserve the testicular histology structure of adult domestic cats in vitrification.

Keywords

CryopreservationCryoprotectantsDomestic catTesticular tissueVitrification
Type
Research Article
Information
Zygote , Volume 32 , Issue 3 , June 2024 , pp. 207 - 214
Check for updates
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abrishami, M., Anzar, M., Yang, Y. and Honaramooz, A. (2010). Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology, 73(1), 86–96. doi: 10.1016/j.theriogenology.2009.08.004 CrossRefGoogle ScholarPubMed
Amorim, C. A., Curaba, M., Van Langendonckt, A., Dolmans, M.-M. and Donnez, J. (2011). Vitrification as an alternative means of cryopreserving ovarian tissue. Reproductive Biomedicine Online, 23(2), 160–186. doi: 10.1016/j.rbmo.2011.04.005 CrossRefGoogle Scholar
Baert, Y., Goossens, E., van Saen, D., Ning, L., in’t Veld, P. and Tournaye, H. (2012). Orthotopic grafting of cryopreserved prepubertal testicular tissue: In search of a simple yet effective cryopreservation protocol. Fertility and Sterility, 97(5), 1152–7.e1. doi: 10.1016/j.fertnstert.2012.02.010 CrossRefGoogle ScholarPubMed
Brito, D. C., Domingues, S. F. S., Silva, J. K., Wu, X., Santos, R. R. and Pieczarka, J. C. (2016). Detrimental effect of phenol red on the vitrification of cat (Felis catus) ovarian tissue. Biopreservation and Biobanking, 14(1), 17–22. doi: 10.1089/bio.2015.0025 CrossRefGoogle ScholarPubMed
Comizzoli, P. (2015). Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian Journal of Andrology, 17(4), 640–645. doi: 10.4103/1008-682X.153849 CrossRefGoogle ScholarPubMed
Comizzoli, P. and Wildt, D. E. (2013). 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. doi: 10.1071/RD13259 CrossRefGoogle Scholar
Crowe, J. H., Crowe, L. M., Carpenter, J. F., Rudolph, A. S., Wistrom, C. A., Spargo, B. J. and Anchordoguy, T. J. (1988). Interactions of sugars with membranes. Biochimica et Biophysica Acta, 947(2), 367–384. doi: 10.1016/0304-4157(88)90015-9 CrossRefGoogle Scholar
Curaba, M., Verleysen, M., Amorim, C. A., Dolmans, M.-M., Van Langendonckt, A., Hovatta, O., Wyns, C. and Donnez, J. (2011). Cryopreservation of prepubertal mouse testicular tissue by vitrification. Fertility and Sterility, 95(4), 1229–34.e1. doi: 10.1016/j.fertnstert.2010.04.062 CrossRefGoogle ScholarPubMed
da Silva, A. M., Bezerra, L. G. P., Praxedes, E. C. G., Moreira, S. S. J., de Souza, C. M. P., de Oliveira, M. F., Pereira, A. F., Comizzoli, P. and Silva, A. R. (2019). Combination of intracellular cryoprotectants preserves the structure and the cells proliferative capacity potential of adult collared peccary testicular tissue subjected to solid surface vitrification. Cryobiology, 91, 53–60. doi: 10.1016/j.cryobiol.2019.10.199 CrossRefGoogle ScholarPubMed
Diagone, K. V., Feliciano, M. A. R., Pacheco, M. R. and Vicente, W. R. R. (2012). Histology and morphometry of the testes of adult domestic cats (Felis catus). Journal of Feline Medicine and Surgery, 14(2), 124–130. doi: 10.1177/1098612X11431531 CrossRefGoogle Scholar
Dumont, L., Oblette, A., Rondanino, C., Jumeau, F., Bironneau, A., Liot, D., Duchesne, V., Wils, J. and Rives, N. (2016). Vitamin A prevents round spermatid nuclear damage and promotes the production of motile sperm during in vitro maturation of vitrified pre-pubertal mouse testicular tissue. Molecular Human Reproduction, 22(12), 819–832. doi: 10.1093/molehr/gaw063 Google Scholar
França, L. R. and Godinho, C. L. (2003). Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biology of Reproduction, 68(5), 1554–1561. doi: 10.1095/biolreprod.102.010652 CrossRefGoogle Scholar
Gouk, S. S., Loh, Y. F. J., Kumar, S. D., Watson, P. F. and Kuleshova, L. L. (2011). Cryopreservation of mouse testicular tissue: Prospect for harvesting spermatogonial stem cells for fertility preservation. Fertility and Sterility, 95(7), 2399–2403. doi: 10.1016/j.fertnstert.2011.03.035 CrossRefGoogle Scholar
Gurtovenko, A. A. and Anwar, J. (2007). Modulating the structure and properties of cell membranes: The molecular mechanism of action of dimethyl sulfoxide. The Journal of Physical Chemistry. B, 111(35), 10453–10460. doi: 10.1021/jp073113e CrossRefGoogle Scholar
Hajiaghalou, S., Ebrahimi, B., Shahverdi, A., Sharbatoghli, M. and Beigi Boroujeni, N. (2016). Comparison of apoptosis pathway following the use of two protocols for vitrification of immature mouse testicular tissue. Theriogenology, 86(8), 2073–2082. doi: 10.1016/j.theriogenology.2016.06.027 CrossRefGoogle Scholar
Higaki, S., Kuwata, N., Tanaka, K., Tooyama, I., Fujioka, Y., Sakai, N. and Takada, T. (2017). Successful vitrification of whole juvenile testis in the critically endangered cyprinid honmoroko (Gnathopogon caerulescens). Zygote, 25(5), 652–661. doi: 10.1017/S0967199417000430 CrossRefGoogle Scholar
Hoshino, P., Nakaghi, L. S. O., Pacheco, M. R., Lui, J. F. and Malheiros, E. B. (2002). Morfometria dos túbulos seminíferos e ductos epididimários de cães e gatos provenientes de cirurgia de castração. Biotemas, 15(1), 97–110. https://periodicos.ufsc.br/index.php/biotemas/article/view/21647/19640 Google Scholar
International Union for Conservation of Nature and Natural Resources. (2020). The IUCN Red List of Threatened Species. Version 2020–2. https://www.iucnredlist.org. Retrieved July 09, 2023Google Scholar
Iwatani, M., Ikegami, K., Kremenska, Y., Hattori, N., Tanaka, S., Yagi, S. and Shiota, K. (2006). Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cells, 24(11), 2549–2556. doi: 10.1634/stemcells.2005-0427 CrossRefGoogle Scholar
Lima, A. C., Jung, M., Rusch, J., Usmani, A., Lopes, A. M. and Conrad, D. F. (2017a). A Standardized approach for multispecies purification of mammalian male germ cells by mechanical tissue dissociation and flow cytometry. Journal of Visualized Experiments: JoVE, (125), 1–11. doi: 10.3791/55913 Google ScholarPubMed
Lima, D., Silva, T., Morais, G. B., Aquino-Cortez, A., Evangelista, J., Xavier Júnior, F., Viana, D. A. and Silva, L. (2017b). Different associations of cryoprotectants for testicular tissue of prepubertal cats submitted to vitrification. Reproduction in Domestic Animals, 52(2) Suppl. 2, 235–241. doi: 10.1111/rda.12833 CrossRefGoogle Scholar
Lima, D. B. C., Silva, T. F. P. D., Aquino-Cortez, A., Leiva-Revilla, J. and Silva, L. D. M. D. (2018). Vitrification of testicular tissue from prepubertal cats in cryotubes using different cryoprotectant associations. Theriogenology, 110, 110–115. doi: 10.1016/j.theriogenology.2017.12.037 CrossRefGoogle Scholar
Lima, S. L. G., Soares, A. R. B., Stalker, L., Santos, R. R. and Domingues, S. F. S. (2021). Epididymal tail solid-surface vitrification as an effective method for domestic cat sperm cryobanking. Zygote, 29(6), 452–458. doi: 10.1017/S096719942100006X CrossRefGoogle ScholarPubMed
Sowińska, N. (2021). The domestic cat as a research model in the assisted reproduction procedures of wild felids. Postepy Biochemii, 67(4), 362–369. doi: 10.18388/pb.2021_416 Google Scholar
Neubauer, K., Jewgenow, K., Blottner, S., Wildt, D. E. and Pukazhenthi, B. S. (2004). Quantity rather than quality in teratospermic males: A histomorphometric and flow cytometric evaluation of spermatogenesis in the domestic cat (Felis catus). Biology of Reproduction, 71(5), 1517–1524. doi: 10.1095/biolreprod.104.031062 CrossRefGoogle Scholar
Ning, L., Goossens, E., Geens, M., Van Saen, D. V. and Tournaye, H. (2012). Spermatogonial stem cells as a source for regenerative medicine. Middle East Fertility Society Journal, 17(1), 1–7. doi: 10.1016/J.MEFS.2011.06.002 CrossRefGoogle Scholar
Pan, C. Y., Yu, S., Zhang, P. F., Wang, B., Zhu, Z. D., Liu, Y. Y. and Zeng, W. X. (2017). Effect of sucrose on cryopreservation of pig spermatogonial stem cells. Journal of Integrative Agriculture, 16(5), 1120–1129. doi: 10.1016/S2095-3119(16)61489-2 CrossRefGoogle Scholar
Poels, J., Van Langendonckt, A., Dehoux, J. P., Donnez, J. and Wyns, C. (2012). Vitrification of non-human primate immature testicular tissue allows maintenance of proliferating spermatogonial cells after xenografting to recipient mice. Theriogenology, 77(5), 1008–1013. doi: 10.1016/j.theriogenology.2011.10.015 CrossRefGoogle Scholar
Prentice, J. R. and Anzar, M. (2010). Cryopreservation of mammalian oocyte for conservation of animal genetics. Veterinary Medicine International, 2011, 1–11. doi: 10.4061/2011/146405 CrossRefGoogle Scholar
Pukazhenthi, B. S., Nagashima, J., Travis, A. J., Costa, G. M., Escobar, E. N., França, L. R. and Wildt, D. E. (2015). Slow freezing, but not vitrification supports complete spermatogenesis in cryopreserved, neonatal sheep testicular xenografts. PLOS ONE, 10(4), e0123957. doi: 10.1371/journal.pone.0123957 CrossRefGoogle Scholar
Radaelli, M. R. M., Almodin, C. G., Minguetti-Câmara, V. C., Cerialli, P. M. A., Nassif, A. E. and Gonçalves, A. J. (2017). A comparison between a new vitrification protocol and the slow freezing method in the cryopreservation of prepubertal testicular tissue. JBRA Assisted Reproduction, 21(3), 188–195. doi: 10.5935/1518-0557.20170037 CrossRefGoogle Scholar
Santos, R. R., Tharasanit, T., Van Haeften, T., Figueiredo, J. R., Silva, J. R. and Van den Hurk, R. (2007). Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods. Cell and Tissue Research, 327(1), 167–176. doi: 10.1007/s00441-006-0240-2 CrossRefGoogle Scholar
Sum, A. K., Faller, R. and de Pablo, J. J. (2003). Molecular simulation study of phospholipid bilayers and insights of the interactions with disaccharides. Biophysical Journal, 85(5), 2830–2844. doi: 10.1016/s0006-3495(03)74706-7 CrossRefGoogle Scholar
Tian, T., Zhao, G., Han, D., Zhu, K., Chen, D., Zhang, Z., Wei, Z., Cao, Y. and Zhou, P. (2015). Effects of vitrification cryopreservation on follicular morphology and stress relaxation behaviors of human ovarian tissues: Sucrose versus trehalose as the non-permeable protective agent. Human Reproduction, 30(4), 877–883. doi: 10.1093/humrep/dev012 CrossRefGoogle Scholar
Unni, S., Kasiviswanathan, S., D’Souza, S., Khavale, S., Mukherjee, S., Patwardhan, S. and Bhartiya, D. (2012). Efficient cryopreservation of testicular tissue: Effect of age, sample state, and concentration of cryoprotectant. Fertility and Sterility, 97(1), 200–8.e1. doi: 10.1016/j.fertnstert.2011.10.018 CrossRefGoogle Scholar
Xu, X.-R., Tan, F.-Q., Zhu, J.-Q., Ye, T., Wang, C.-L., Zhu, Y.-F., Dahms, H.-U., Jin, F. and Yang, W.-X. (2014). Detection of DNA damage caused by cryopreservation using a modified SCGE in large yellow croaker, Pseudosciaena crocea . Acta Biologica Hungarica, 65(4), 405–413. doi: 10.1556/ABiol.65.2014.4.5 CrossRefGoogle Scholar
Zhang, X.-G., Wang, Y.-H., Han, C., Hu, S., Wang, L.-Q. and Hu, J.-H. (2015). Effects of trehalose supplementation on cell viability and oxidative stress variables in frozen–thawed bovine calf testicular tissue. Cryobiology, 70(3), 246–252. doi: 10.1016/j.cryobiol.2015.03.004 CrossRefGoogle Scholar