Vitrification of Ovarian Tissue from Non-Human Primates
DOI:
https://doi.org/10.22456/1679-9216.80757Keywords:
non-human primates, ovarian tissue, cryopreservation.Abstract
Background: One of the strategies to preserve genetic material from nonhuman primates (NHP) consists in the implementation of germplasm banks, for future application in reproductive biotechniques, as well as for biomedical research. Based on the success rates achieved in human, there is a prominent possibility to succeed also with NHP. However, studies with NHP are still scarce, especially regarding the cryopreservation of ovarian tissue.
Review: Neotropical non-human primates, especially males, have been used in research related to reproductive biotechniques in Brazil. Regarding research on female reproduction and ovarian tissue preservation, most studies were performed using domestic animals as models. Current concepts and controversies in the restoration of gametes in adult females does not exclude the needs to preserve ovarian tissue. Importantly, ovarian tissue can be collected and preserved even after the death of the donors, being applied when finding dead females. Furthermore, collection of ovarian biopsies is also feasible and will not affect reproductive function. Among the cryopreservation methods, the vitrification has been indicated due to practical logistic, as well as because it will avoid the formation of large intracellular ice crystals, and it is claimed that ovarian stromal damage will be decreased under vitrification. Considering the number of threatened primate species and the needs to preserve their habitat, but also their gametes, development of preservation protocols are needed. Among the procedures, vitrification appears as a practical method to be applied in the near future. Although a low number of studies is reported, most of them were performed in the recent years. In this context, this article reviews recent information on the vitrification of ovarian tissue of non-human primates. Due to the limited number of studies in these species, observed data are compared with the literature in domestic and human mammals.
Conclusion: Despite the advances summarized here, it is possible to conclude that there is still a need to improve procedures for the preservation of genetic material, including in post-mortem situations. The technique of vitrification, therefore, consists of a feasible and promising option. However, it is needed to study properly the methods of vitrification, as well as the introduction of new systems and supplements to minimize or avoid the cell damage caused by the cryopreservation procedure (physical and chemical).
Downloads
References
Almeida D.V., Santos R.R., Scalercio S.R., Leão D.L., Haritova A., Oskam I.C. & Domingues S.F. 2012. Morphological and morphometrical characterization, and estimation of population of preantral ovarian follicles from senile common squirrel monkey (Saimiri sciureus). Animal Reproduction Science. 134(3-4): 210-215.
Amorim C.A., Curaba M., Van Langendonckt A., Dolmans M.M. & Donnez J. 2011. Vitrification as an alternative means of cryopreserving ovarian tissue. Reproductive Biomedicine Online. 23(2): 160-186.
Amorim C.A., Dolmans M.M., David A., Jaeger J., Vanacker J., Camboni A., Donnez J. & Van Langendonckt A. 2012. Vitrification and xenografting of human ovarian tissue. Fertility and Sterility. 98(5): 1291-1298.
Amorim C.A., Jacobs S., Devireddy R.V., Van Langendonckt A., Vanacker J., Jaeger J., Luyckx V., Donnez J. & Dolmans M.M. 2013. Successful vitrification and autografting of baboon (Papio anubis) ovarian tissue. Human Reproduction. 28(8): 2146-2156.
Brito A.B., Santos R.R., Van den Hurk, R., Lima J.S., Miranda M.S., Ohashi OM & Domingues S.F. 2013. Short-term culture of ovarian cortical strips from capuchin monkeys (Sapajus apella): a morphological, viability, and molecular study of preantral follicular development in vitro. Reproductive Sciences. 20(8): 990-997.
Brito D.C., Brito A.B., Scalercio S.R., Percario S. Miranda M.S., Rocha R.M., Diniz J.A., Oskam I.C., Van den Hurk R., Paris M.C., Domingues S.F. & Santos R.R. 2014. Vitamin E-analog Trolox prevents endoplasmic reticulum stress in frozen-thawed ovarian tissue of capuchin monkey (Sapajus apella). Cell and Tissue Research. 355(2): 471-480.
Brito D.C., Domingues S.F., Silva J.K., Wu X., Santos R.R. & 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.
Carvalho A.A., Faustino L.R., Silva C.M., Castro S.V., Lobo C.H., Santos F.W., Santos R.R., Campello C.C., Bourdignon V., Figueiredo J.R. & Rodrigues A.P. 2014. Catalase addition to vitrification solutions maintain goat ovarian preantral follicles stability. Research in Veterinary Science. 97(1): 140-147.
Carvalho A.A., Faustino L.R., Silva C.M., Castro S.V., Lopes C.A., Santos R.R., Bao S.N., Figueiredo J.R. & Rodrigues A.P. 2013. Novel wide-capacity model for vitrification of caprine ovaries: ovarian tissue cryosystem (OTC). Animal Reproduction Science. 138(3-4): 220-227.
Celestino J.J., Santos R.R., Melo M.A., Rodrigues A.P. & Figueiredo J.R. 2010. Vitrification of bovine ovarian tissue by the solid-surface vitrification method. Biopreservation and Biobanking. 8(4): 219-221.
Dolmans M.M., Binda M.M., Jacobs S., Dehoux J.P., Squifflet J.L., Ambroises J., Donnez J. & Amorim C.A. 2015. Impact of the cryopreservation technique and vascular bed on ovarian tissue transplantation in cynomolgus monkeys. Journal of Assisted Reproduction and Genetics. 32(1): 1251-1262.
Domingues S.F., Almeida D.V., Scalercio S.R., Kastelic J.P. & Santos R.R. 2011. Unilateral ovarian absence in two capuchin monkeys. Journal of Medical Primatology. 40(1): 37-40.
Domingues S.F., Caldas-Bussiere M.C., Petretski M.D., Ohashi O.M., Lima J.S., Santos R.R., Cordeiro M.S. & Gomes de Castro P.H. 2010. Effects of follicular phase and oocyte-cumulus complexes quality on the protein profile and in vitro oocyte meiosis competence in Cebus apella. Fertility and Sterility. 93(5): 1662-1667. F.I.=4.373.
Domingues S.F.S., Lima J.S., Oliveira K.G. & Santos R.R. 2011. Biotecnologias de reprodução como uma estratégia complementar à conservação in situ de primatas neotropicais ameaçados de extinção: perspectivas e desafios. Revista Brasileira de Reprodução Animal. 35(2): 124-129.
Faustino L.R., Santos R.R., Silva C.M., Pinto L.C., Celestino J.J., Campello C.C., Figueiredo J.R. & Rodrigues A.P. 2010. Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell. Animal Reproduction Science. 122(1-2): 90-97.
Fereydouni B., Salinas-Riester G., Heistermann M., Dressel R., Lewerich L., Drummer C. & Behr R. 2016. Long-term oocyte-like cell develoment in cultures derived from neonatal marmoset monkey ovary. Stem Cell. 2016: 2480-2498.
Figueiredo J.R., Rodrigues A.P., Silva J.R. & Santos R.R. 2011. Cryopreservation and in vitro culture of caprine Preantral follicles. Reproduction, Fertility and Development. 23(1): 40-47.
Friedman O., Orvieto R., Fisch B., Felz C., Freud E., Ben-Haroush A. & Abir R. 2012. Possible improvements in human ovarian grafting by various host and graft treatments. Human Reproduction. 27(2): 474-482.
Ganji R., Nabiuni M. & Faraji R. 2015. Development of mouse preantral follicle after in vitro culture in a medium containing melatonin. Cell Journal. 16(4): 546-553.
Hashimoto S., Suzuki N., Yamanaka M., Hosoi Y., Ishizuka B. & Morimoto Y. 2010. Effects of vitrification solutions and equilibration times on the morphology of cynomologus ovarian tissues. Reproductive Biomedicine Online. 21(4): 501-509.
Jimenez C.R., Penitente-Filho J.M., Torres C.A.A., Medeiros A.M. & Silva L.S. 2016. Vitrification of bovine preantral follicles with dimethylsulfoxide and sucrose plus α-tocopherol. Pesquisa Veterinária Brasileira. 36(3): 209-215.
Kawamura K., Cheng Y., Suzuki N., Deguchi M., Sato Y., Takae S., Ho C.H., Kawamura N., Tamura M., Hashimoto S., Sugishita Y., Morimoto Y., Hosoi Y., Yoshioka N., Ishizuka B. & Hsueh A.J. 2013. Hippo signalling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proceedings of National Academy of Science. 110(43): 17474-17479.
Keros V., Xella S., Hultenby K., Pettersson K., Sheikhi M., Volpe A., Hreinsson J. & Hovatta O. 2009. Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Human Reproduction. 24(7): 1670-1683.
Kim E.J., Lee H.J., Lee J., Youm H.W., Lee J.R., Suh C.S. & Kim S.H. 2015. The benefitial effects of polyethylene glycol-superoxide dismutase on ovarian tissue culture and transplantation. Journal of Assisted Reproduction and Genetics. 32(10): 1561-1569.
Leão D.L., Brito A.B., Miranda S.A., Oliveira K.G., Almeida D.V.C., Santos R.R. & Domingues S.F. 2017. Extender supplementation with catalase maintains the integrity of sperm plasma membrane after freezing-thawing of semen from capuchin monkey. Zygote. 25(2): 231-234.
Leão D.L., Miranda S.A., Brito A.B., Lima J.S., Santos R.R. & Domingues S.F. 2015. Efficacious long-term cooling and freezing of Sapajus apella semen in ACP-118®. Animal Reproduction Science159(1): 118-123.
Lima J.S., Leão D.L., Sampaio R.V., Brito A.B., Santos R.R., Miranda M.S., Ohashi O.M. & Domingues S.F. 2013. Embryo production by parthenogenetic activation and fertilization of in vitro matured oocytes from Cebus apella. Zygote. 21(2): 162-166.
Lima-Verde I.B., Matos M.H.T., Bruno J.B., Martins F.S., Santos R.R., Bao S.N., Luque M.C.A., Vieira G.A.B., Silveira E.R., Rodrigues A.P.R., Figueiredo J.R., Oliveria M.A.L. & Lima P.F. 2009. Effects of α-tocopherol and ternatin antioxidants on morphology and activation of goat preantral follicles in vitro cultured. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 61(1): 57-65.
Lopes G.P., Brito A.B., Paim F.P., Santos R.R., Queiroz H.L. & Domingues S.F. 2017. Comparative characterization of the external genitalia and reproductive tubular organs of three species of the genus Saimiri Voigt, 1831 (Primates: Cebidae). Anatomia, Histologia Embryologia. 46(2): 143-161.
Lopes G.P., Brito A.B., Santos R.R., Domingues S.F., Paim F.P. & Queiroz H.L. 2017. Unilateral ovarian absence in a Black-headed squirrel monkey (Saimiri vanzolinii Ayres, 1985), a threatened neotropical primate species. Journal of Medical Primatology. 46(3): 87-89.
Lopes G.P., Santos R.R., Almeida D.V., Brito A.B., Queiroz H.L. & Domingues S.F. 2017. Population estimate and morphometry of ovarian preantral follicles from three recently recognized squirrel monkey species: a comparative study. Zygote. 25(3): 279-287.
Lu X.L., Yu J., Zhang G., Wei Z.T., Li J.T. & Zhang J.M. 2014. Effects of varying tissue sizes on the efficiency of baboon ovarian tissue vitrification. Cryobiology. 69(1): 79-83.
Lunardi F.O., Bass C.S., Bernuci M.P., Chaves R.N., Lima L.F., Silva R.F., Figueiredo J.R. & Rodrigues A.P. 2015. Ewe ovarian tissue vitrification: a model for the study of fertility preservation in women. JBRA Assisted Reproduction. 19(4): 241-251.
Lunardi F.O., de Aguiar F.L., Apolloni L.B., Duarte A.B., de Sá N.A.R., Leal E.S.S., Sales A.D., Lobo C.H., Campello C.C., Smitz J., Apgar G.A., Figueiredo J.R. & Rodrigues A.P. 2017. Sheep isolated secondary follicles are able to produce metaphase II oocytes after vitrification and long-term in vitro growth. Biopreservation and Biobanking. 15(4): 321-331.
Lunardi F.O., de Aguiar F.L., Duarte A.B., Araujo V.R., de Lima L.F., Ribeiro de Sa N.A., Vieira Correia H.H., Domingues S.F., Campello C.C., Smitz J. Figueiredo J.R. & Rodrigues A.P. 2016. Ovine secondary follicles vitrified out the ovarian tissue grow and develop in vitro better than those vitrified into the ovarian fragments. Theriogenology. 85(7): 1203-1210.
Luz H.K., Santos R.R., Wanderley L.S., Faustino L.R., Silva C.M., Carvalho A.A., Campello C.C., Santos F.W., Figueiredo J.R. & Rodrigues A.P. 2012. Catalase prevents lipid peroxidation and enhances survival of caprine preantral follicles cryopreserved in a 1,2-propanediol-freezing medium. Biopreservation and Biobanking. 10(4): 338-342.
Luz V.B., Santos R.R., Pinto L.C., Soares A.A., Celestino J.J., Mafezoli J., Campelo C.C., Figueiredo J.R. & Rodrigues A.P. 2009. Dimethyl sulfoxide perfusion in caprine ovarian tissue and its relationship with follicular viability after cryopreservation. Fertility and Sterility. 91(4 Suppl): 1513-1515.
Melo M.A., Oskam I.C., Celestino J.J., Carvalho A.A., Castro S.V., Figueiredo J.R., Rodrigues A.P. & Santos R.R. 2011. Adding ascorbic acid to vitrification and IVC medium influences preantral follicle mophology, but not viability. Reproduction in Domestic Animals. 46(4): 742-745.
Motohashi H.H. & Ishibachi H. 2016. Cryopreservation of ovaries from neonatal marmoset monkeys. Experimental Animals. 65(3): 189-196.
Nyachieo A., Spiessens C., Chai D.C., Kiulia N.M., Willemen D., Mwenda J.M., Bourgain C. & D’Hooghe T.M. 2013. Ovarian tissue cryopreservation by vitrification in olive baboons (Papio Anubis): A pilot study. Gynecologic and Obstetric Investigation. 75(1): 157-162.
Oliveira K.G., Leão D.L., Almeida D.V., Santos R.R. & Domingues S.F. 2015. Seminal characteristics and cryopreservation of sperm from the squirrel monkey, Saimiri collinsi. Theriogenology. 84(5): 743-749.
Oliveira K.G., Santos R.R., Leão D.L., Brito A.B., Lima J.S., Sampaio W.V. & Domingues S.F. 2016. Cooling and freezing of sperm from captive, free-living and endangered squirrel monkey species. Cryobiology. 72(3): 283-289.
Oskam I.C., Asadi B.A. & Santos R.R. 2010. Histologic and ultrastructural features of cryopreserved ovine ovarian tissue: deleterious effect of 1,2-propanediol applying different thawing protocols. Fertility and Sterility. 93(8): 27642766.
Oskam I.C., Lund T. & Santos R.R. 2011. Irreversible damage in ovine ovarian tissue after cryopreservation in propanediol: analyses after in vitro culture and xenotransplantation. Reproduction in Domestic Animals. 46(5): 793-799.
Pinto L.C., Santos R.R., Faustino L.R., Silva C.G.M., Luz V.B., Maia Junior J.E., Soares A.A.X., Celestino J.J.H., Mafezoli J., Campello C.C., Figueiredo J.R. & Rodrigues A.P. 2008. Quantification of dimethyl sulfoxide perfusion in sheep ovarian tissue: A predictive parameter for follicular survival to cryopreservation. Biopreservation and Biobanking. 6(1): 269-276.
Prasath E.B. 2008. Ovarian tissue cryopreservation: an update. Journal of Human Reproductive Science. 1(2): 50-55.
Rodrigues J.K., Navarro P.A.A.S., Zelinski M.B., Stouffer R.L. & Xu J. 2015. Local role of androgens in the development of preantral follicles from nonhuman primates cultured individually a in three dimensional matrix. Reprodução & Climatério. 29(3): 93-104.
Rodrigues J.K., Navarro P.A.A.S., Zelinski M.B., Stouffer R.L. & Xu J. 2015. Direct actions of androgens on the survival, growth and secretion of steroids and anti-Müllerian hormone by individual macaque follicles during threedimensional culture. Human Reproduction. 30(3): 664-674.
Sales A.D., Duarte A.B., Santos R.R., Alves K.A., Lima L.F., Rodrigues G.Q., Brito I.R., Lobo C.H., Bruno J.B., Locatelli Y., Figueiredo J.R. & Rodrigues A.P. 2016. Modulation of aquaporins 3 and 9 after exposure of ovine ovarian tissue to cryoprotectants followed by in vitro culture. Cell and Tissue Research. 365(2): 415-424.
Sanfilippo S., Canis M., Smitz J., Sion B., Darcha C., Janny L. & Brugnon F. 2015. Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reproductive Biology and Endocrinology. 13(1): 67.
Santana L.N., Brito A.B., Brito D.C., Lima J.S., Domingues S.F. & Santos R.R. 2013. Adaptation of a trap door technique for the recovery of cortical biopsies from Cebus apella (capuchin monkeys). Zygote. 21(2): 158-161.
Santana L.N., Van den Hurk R., Oskam I.C., Brito A.B., Brito D.C., Domingues S.F. & Santos R.R. 2012. Vitrification of ovarian tissue from primates and domestic ruminants: an overview. Biopreservation and Biobanking. 10(3): 288-294.
Santos R.R., Amorim C., Cecconi S., Fassbender M., Imhof M., Lornage J., Paris M., Schoenfeldt V. & MartinezMadrid B. 2010. Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds. Animal Reproduction Science. 122(3-4): 151-163.
Santos R.R., Knijn H.M., Vos P.L., Oei C.H., van Loon T., Colenbrander B., Gadella B.M., van den Hurk R. & Roelen B.A. 2009. Complete follicular development and recovery of ovarian function of frozen-thawed, autotransplanted caprine ovarian cortex. Fertility and Sterility. 91(4 Suppl.): 1455-1458.
Santos R.R., Tharasanit T., Van Haeften T., Figueiredo J.R., Silva J.R. & 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.
Santos R.R., Van Haeften T., Roelen B.A., Knijn H.M., Colenbrander B., Gadella B.M. & Van den Hurk. 2008. Osmotic tolerance and freezability of isolated caprine early-staged follicles. Cell and Tissue Research. 333(2): 323-331.
Scalercio S.R., Amorim C.A., Brito D.C., Percário S., Oskam I.C., Domingues S.F.S. & Santos R.R. 2015. Trolox enhances follicular survival after ovarian tissue autograft in squirrel monkey (Saimiri collinsi). Reproduction, Fertility and Development. 28(11): 1854-1864.
Scalercio S.R., Brito A.B., Domingues S.F., Santos R.R. & Amorim C.A. 2015. Immunolocalization of growth, inhibitory, and proliferative factors involved in initial ovarian folliculogenesis from adult common squirrel monkey (Saimiri collinsi). Reproductive Sciences. 22(1): 68-74.
Tian T., Zhao G., Han D., Zhu K., Chen D., Zhang Z., Wei Z., Cao Y. & Zhou P. 2015. Effects of vitrification cryopreservation on follicular morphology and stress relaxation behaviours of human ovarian tissues: sucrose versus trehalose as the non-permeable protective agent. Human Reproduction. 30(4): 877-883.
Ting A.Y., Yeoman R.R., Campos J.R., Lawson M.S., Mullen S.F., Fahy G.M. & Zelinski M.B. 2013. Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Human Reproduction. 28(5): 1267-1279.
Ting A.Y., Yeoman R.R., Lawson M.S., Zelinski M.B. 2011. In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Human Reproduction. 26(9): 2461-2472.
Ting A.Y., Yeoman R.R., Lawson M.S. & Zelinski M.B. 2012. Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles. Cryobiology. 65(1): 1-11.
Yeoman R.R., Wolf D.P. & Lee D.M. 2005. Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing. Fertility and Sterility. 83(Suppl 1): 1248-1254.
Published
How to Cite
Issue
Section
License
This journal provides open access to all of its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. Such access is associated with increased readership and increased citation of an author's work. For more information on this approach, see the Public Knowledge Project and Directory of Open Access Journals.
We define open access journals as journals that use a funding model that does not charge readers or their institutions for access. From the BOAI definition of "open access" we take the right of users to "read, download, copy, distribute, print, search, or link to the full texts of these articles" as mandatory for a journal to be included in the directory.
La Red y Portal Iberoamericano de Revistas Científicas de Veterinaria de Libre Acceso reúne a las principales publicaciones científicas editadas en España, Portugal, Latino América y otros países del ámbito latino
