Skip to main content

Cryopreservation of Testicular Stem Cells and Its Application in Veterinary Science

  • Chapter
  • First Online:
Stem Cells in Veterinary Science

Abstract

Testis-derived spermatogonial stem cells (SSCs) and its in vitro counterpart, male germline stem (GS) cells, can repopulate the empty seminiferous tubules of infertile males and, therefore, are rapidly emerging as newer biotechnological tools for the treatment of male infertility, posthumous reproduction, preservation of elite germplasm and animal transgenesis. It also has potential application in the preservation and restoration of fertility in males with diseases/treatments affecting spermatogenesis. Consequently, the cryopreservation of SSC and GS cells is becoming pivotal in assisted reproductive technology (ART) for male reproduction. Cryopreservation of testis-derived stem cells is particularly indispensable for fertility preservation in pre-pubertal males, who have not yet begun their sperm production. This chapter provides an overview of the indications, applications, and strategies of fertility preservation through the cryopreservation of testicular stem cells. Recent advances on freezing and vitrification techniques, assessment of cryopreservation-induced injuries, and methods of their amelioration are also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrishami M, Anzar M, Yang Y, Honaramooz A (2010) Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology 73:86–96

    Article  CAS  PubMed  Google Scholar 

  • Aliakbari F, Gilani MA, Amidi F, Baazm M, Korouji M, Izadyar F, Yazdekhasti H, Abbasi M (2016) Improving the efficacy of cryopreservation of spermatogonia stem cells by antioxidant supplements. Cell Reprogram 18:87–95

    Article  CAS  PubMed  Google Scholar 

  • Anserini P, Chiodi S, Spinelli S, Costa M, Conte N, Copello F, Bacigalupo A (2002) Semen analysis following allogeneic bone marrow transplantation. Additional data for evidence-based counselling. Bone Marrow Transplant 30:447–451

    Article  CAS  PubMed  Google Scholar 

  • Arkoun B, Galas L, Dumont L, Rives A, Saulnier J, Delessard M, Rondanino C, Rives N (2019) Vitamin E but not GSH decreases reactive oxygen species accumulation and enhances sperm production during in vitro maturation of frozen-thawed prepubertal mouse testicular tissue. Int J Mol Sci 20:5380

    Article  CAS  PubMed Central  Google Scholar 

  • Avarbock MR, Brinster CJ, Brinster RL (1996) Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat Med 2:693–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baert Y, Goossens E, van Saen D, Ning L, Tournaye H (2012) Orthotopic grafting of cryopreserved prepubertal testicular tissue: in search of a simple yet effective cryopreservation protocol. Fertil Steril 97:1151–1152

    Article  Google Scholar 

  • Bashawat M, Braun BC, Müller K (2020) Cell survival after cryopreservation of dissociated testicular cells from feline species. Cryobiology 97:191–197

    Article  CAS  PubMed  Google Scholar 

  • Batzer FR, Hurwitz JM, Caplan A (2003) Postmortem parenthood and the need for a protocol with posthumous sperm procurement. Fertil Steril 79:1263–1269

    Article  PubMed  Google Scholar 

  • Bebbere D, Pinna S, Nieddu S, Natan D, Arav A, Ledda S (2019) Gene expression analysis of ovine prepubertal testicular tissue vitrified with a novel cryodevice (E.Vit). J Assist Reprod Genet 36:2145–2154

    Article  PubMed  PubMed Central  Google Scholar 

  • Bielanski A, Nadin-Davis S, Sapp T, Lutze-Wallace C (2000) Viral contamination of embryos cryopreserved in liquid nitrogen. Cryobiology 40:110–116

    Article  CAS  PubMed  Google Scholar 

  • Boroujeni MB, Peidayesh F, Pirnia A, Boroujeni NB, Ahmadi SAY, Gholami M (2019) Effect of selenium on freezing-thawing damage of mice spermatogonial stem cell: a model to preserve fertility in childhood cancers. Stem Cell Investig 6:36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt JS, Cruz Ithier MA, Rosen T, Ashkinadze E (2019) Advanced paternal age, infertility, and reproductive risks: a review of the literature. Prenat Diagn 39:81–87

    Article  PubMed  Google Scholar 

  • Braye A, Tournaye H, Goossens E (2019) Setting up a cryopreservation programme for immature testicular tissue: lessons learned after more than 15 years of experience. Clin Med Insights Reprod Health 13:1179558119886342

    Article  PubMed  PubMed Central  Google Scholar 

  • Bujan L, Sergerie M, Moinard N, Martinet S, Porte L, Massip P, Pasquier C, Daudin M (2007) Decreased semen volume and spermatozoa motility in HIV-1-infected patients under antiretroviral treatment. J Androl 28:444–452

    Article  PubMed  Google Scholar 

  • Check ML, Check JH, Summers-Chase D, Choe JK, Check DJ, Nazari A (2002) Live birth after posthumous testicular sperm aspiration and intracytoplasmic sperm injection with cryopreserved sperm: case report. Clin Exp Obstet Gynecol 29:95–96

    CAS  PubMed  Google Scholar 

  • Cheung RCF, Ng TB, Wong JH (2017) Antifreeze proteins from diverse organisms and their applications: an overview. Curr Protein Pept Sci 18:262–283

    Article  CAS  PubMed  Google Scholar 

  • Costa GMJ, Avelar GF, Lacerda S, Figueiredo AFA, Tavares AO, Rezende-Neto JV, Martins FGP, França LR (2017) Horse spermatogonial stem cell cryopreservation: feasible protocols and potential biotechnological applications. Cell Tissue Res 370:489–500

    Article  CAS  PubMed  Google Scholar 

  • Crha I, Ventruba P, Zakova J, Huser M, Kubesova B, Hudecek R, Jarkovsky J (2009) Survival and infertility treatment in male cancer patients after sperm banking. Fertil Steril 91:2344–2348

    Article  PubMed  Google Scholar 

  • Curaba M, Verleysen M, Amorim CA, Dolmans MM, Van Langendonckt A, Hovatta O, Wyns C, Donnez J (2011) Cryopreservation of prepubertal mouse testicular tissue by vitrification. Fertil Steril 95:1229–1234

    Article  CAS  PubMed  Google Scholar 

  • da Silva AM, Bezerra LGP, Praxedes ECG, Moreira SSJ, de Souza CMP, de Oliveira MF, Pereira AF, Comizzoli P, Silva AR (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

    Article  PubMed  Google Scholar 

  • de Michele F, Poels J, Weerens L, Petit C, Evrard Z, Ambroise J, Gruson D, Wyns C (2017) Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum Reprod 32:32–45

    PubMed  Google Scholar 

  • Del Vento F, Vermeulen M, Ucakar B, Poels J, Rieux A, Wyns C (2019) Significant benefits of nanoparticles containing a necrosis inhibitor on mice testicular tissue autografts outcomes. Int J Mol Sci 20:5833

    Article  PubMed Central  Google Scholar 

  • Docampo MJ, Hadziselimovic F (2015) Molecular pathology of cryptorchidism-induced infertility. Sex Dev 9:269–278

    Article  CAS  PubMed  Google Scholar 

  • Dohle GR (2010) Male infertility in cancer patients: review of the literature. Int J Urol 17:327–331

    Article  PubMed  Google Scholar 

  • Dong WZ, Hua JL, Shen WZ, Dou ZY (2010) In vitro production of haploid sperm cells from male germ cells of foetal cattle. Anim Reprod Sci 118:103–109

    Article  CAS  PubMed  Google Scholar 

  • Dong L, Gul M, Hildorf S, Pors SE, Kristensen SG, Hoffmann ER, Cortes D, Thorup J, Andersen CY (2019) Xeno-free propagation of spermatogonial stem cells from infant boys. Int J Mol Sci 20:5390

    Article  CAS  PubMed Central  Google Scholar 

  • Duca Y, Di Cataldo A, Russo G, Cannata E, Burgio G, Compagnone M, Alamo A, Condorelli RA, La Vignera S, Calogero AE (2019) Testicular function of childhood cancer survivors: who is worse? J Clin Med 8:2204

    Article  CAS  PubMed Central  Google Scholar 

  • Dumont L, Arkoun B, Jumeau F, Milazzo JP, Bironneau A, Liot D, Wils J, Rondanino C, Rives N (2015) Assessment of the optimal vitrification protocol for pre-pubertal mice testes leading to successful in vitro production of flagellated spermatozoa. Andrology 3:611–625

    Article  CAS  PubMed  Google Scholar 

  • Fahy GM, Wowk B, Wu J, Paynter S (2004) Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology 48:22–35

    Article  CAS  PubMed  Google Scholar 

  • Feng LX, Ravindranath N, Dym M (2000) Stem cell factor/c-kit up-regulates cyclin D3 and promotes cell cycle progression via the phosphoinositide 3-kinase/p70 S6 kinase pathway in spermatogonia. J Biol Chem 275:25572–25576

    Article  CAS  PubMed  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  CAS  PubMed  Google Scholar 

  • Fode M, Krogh-Jespersen S, Brackett NL, Ohl DA, Lynne CM, Sønksen J (2012) Male sexual dysfunction and infertility associated with neurological disorders. Asian J Androl 14:61–68

    Article  PubMed  Google Scholar 

  • Fountain D, Ralston M, Higgins N, Gorlin JB, Uhl L, Wheeler C, Antin JH, Churchill WH, Benjamin RJ (1997) Liquid nitrogen freezers: a potential source of microbial contamination of hematopoietic stem cell components. Transfusion 37:585–591

    Article  CAS  PubMed  Google Scholar 

  • Frederickx V, Michiels A, Goossens E, De Block G, Van Steirteghem AC, Tournaye H (2004) Recovery, survival and functional evaluation by transplantation of frozen-thawed mouse germ cells. Hum Reprod 19:948–953

    Article  CAS  PubMed  Google Scholar 

  • Fuchs EF, Burt RA (2002) Vasectomy reversal performed 15 years or more after vasectomy: correlation of pregnancy outcome with partner age and with pregnancy results of in vitro fertilization with intracytoplasmic sperm injection. Fertil Steril 77:516–519

    Article  PubMed  Google Scholar 

  • Fujita K, Tsujimura A, Miyagawa Y, Kiuchi H, Matsuoka Y, Takao T, Takada S, Nonomura N, Okuyama A (2006) Isolation of germ cells from leukemia and lymphoma cells in a human in vitro model: potential clinical application for restoring human fertility after anticancer therapy. Cancer Res 66:11166–11171

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Liu C, Wu B, Cui H, Zhao Y, Duan Y, Gao F, Gu Q, Wang H, Li W (2020) Effects of different biomaterials and cellular status on testicular cell self-organization. Adv Biosyst 2020:1900292

    Article  Google Scholar 

  • Geens M, Van de Velde H, De Block G, Goossens E, Van Steirteghem A, Tournaye H (2007) The efficiency of magnetic-activated cell sorting and fluorescence-activated cell sorting in the decontamination of testicular cell suspensions in cancer patients. Hum Reprod 22:733–742

    Article  CAS  PubMed  Google Scholar 

  • Gholami M, Saki G, Hemadi M, Khodadadi A, Mohamma-di-Asl J (2013) Effect of melatonin on the expression of apoptotic genes in vitrified-thawed spermatogonia stem cells type A of 6-day-old mice. Iran J Basic Med Sci 16:906–909

    PubMed  PubMed Central  Google Scholar 

  • Ginsberg JP, Carlson CA, Lin K, Hobbie WL, Wigo E, Wu X, Brinster RL, Kolon TF (2010) An experimental protocol for fertility preservation in prepubertal boys recently diagnosed with cancer: a report of acceptability and safety. Hum Reprod 25:37–41

    Article  CAS  PubMed  Google Scholar 

  • Goossens E, Frederickx V, Geens M, De Block G, Tournaye H (2008) Cryosurvival and spermatogenesis after allografting prepubertal mouse tissue: comparison of two cryopreservation protocols. Fertil Steril 89:725–727

    Article  PubMed  Google Scholar 

  • Goossens E, Bilgec T, Van Saen D, Tournaye H (2011) Mouse germ cells go through typical epigenetic modifications after intratesticular tissue grafting. Hum Reprod 26:3388–3400

    Article  CAS  PubMed  Google Scholar 

  • Gouk SS, Loh YF, Kumar SD, Watson PF, Kuleshova LL (2011) Cryopreservation of mouse testicular tissue: prospect for harvesting spermatogonial stem cells for fertility preservation. Fertil Steril 95:2399–2403

    Article  PubMed  Google Scholar 

  • Green DM, Kawashima T, Stovall M, Leisenring W, Sklar CA, Mertens AC, Donaldson SS, Byrne J, Robison LL (2010) Fertility of male survivors of childhood cancer: a report from the Childhood Cancer Survivor Study. J Clin Oncol 28:332–339

    Article  PubMed  Google Scholar 

  • Gül M, Dong L, Wang D, Diri MA, Andersen CY (2020) Surrogate testes: allogeneic spermatogonial stem cell transplantation within an encapsulation device may restore male fertility. Med Hypotheses 139:109634

    Article  PubMed  Google Scholar 

  • Gupta MK, Lee HT (2010) Cryopreservation of oocytes and embryos by vitrification. Clin Exp Reprod Med 37:267–291

    Google Scholar 

  • Gupta MK, Uhm SJ, Lee HT (2007) Cryopreservation of immature and in vitro matured porcine oocytes by solid surface vitrification. Theriogenology 67:238–248

    Article  CAS  PubMed  Google Scholar 

  • Gupta MK, Uhm SJ, Lee HT (2010) Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil Steril 93:2602–2607

    Article  PubMed  Google Scholar 

  • Gurtovenko AA, Anwar J (2007) Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B 111:10453–10460

    Article  CAS  PubMed  Google Scholar 

  • Ha SJ, Kim BG, Lee YA, Kim YH, Kim BJ, Jung SE, Pang MG, Ryu BY (2016) Effect of antioxidants and apoptosis inhibitors on cryopreservation of murine germ cells enriched for spermatogonial stem cells. PLoS One 11:e0161372

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M, Shuttleworth JJ, McFarland D, Hobbs RM, Pandolfi PP, Schatten GP, Orwig KE (2007) Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 25:2330–2338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hermann BP, Sukhwani M, Salati J, Sheng Y, Chu T, Orwig KE (2011) Separating spermatogonia from cancer cells in contaminated prepubertal primate testis cell suspensions. Hum Reprod 26:3222–3231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrid M, Nagy P, Juhasz J, Morrell JM, Billah M, Khazanehdari K, Skidmore JA (2019) Donor sperm production in heterologous recipients by testis germ cell transplantation in the dromedary camel. Reprod Fertil Dev 31:538–546

    Article  CAS  PubMed  Google Scholar 

  • Higaki S, Kuwata N, Tanaka K, Tooyama I, Fujioka Y, Sakai N, Takada T (2017) Successful vitrification of whole juvenile testis in the critically endangered cyprinid honmoroko (Gnathopogon caerulescens). Zygote 25:652–661

    Article  CAS  PubMed  Google Scholar 

  • Hofmann MC, Braydich-Stolle L, Dym M (2005) Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 279:114–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou M, Andersson M, Zheng C, Sundblad A, Söder O, Jahnukainen K (2007) Decontamination of leukemic cells and enrichment of germ cells from testicular samples from rats with Roser’s T-cell leukemia by flow cytometric sorting. Reproduction 134:767–779

    Article  CAS  PubMed  Google Scholar 

  • Hou M, Andersson M, Zheng C, Sundblad A, Söder O, Jahnukainen K (2009) Immunomagnetic separation of normal rat testicular cells from Roser’s T-cell leukaemia cells is ineffective. Int J Androl 32:66–73

    Article  PubMed  Google Scholar 

  • Huang JY, Chen HY, Park JY, Tan SL, Chian RC (2008) Comparison of spindle and chromosome configuration in in vitro- and in vivo-matured mouse oocytes after vitrification. Fertil Steril 90:1424–1432

    Article  PubMed  Google Scholar 

  • Hurwitz JM, Batzer FR (2004) Posthumous sperm procurement: demand and concerns. Obstet Gynecol Surv 59:806–808

    Article  PubMed  Google Scholar 

  • Ibtisham F, Honaramooz A (2020) Spermatogonial stem cells for in vitro spermatogenesis and in vivo restoration of fertility. Cell 9:745

    Article  CAS  Google Scholar 

  • Iwatani M, Ikegami K, Kremenska Y, Hattori N, Tanaka S, Yagi S, Shiota K (2006) Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cells 24:2549–2556

    Article  CAS  PubMed  Google Scholar 

  • Izadyar F, Matthijs-Rijsenbilt JJ, den Ouden K, Creemers LB, Woelders H, de Rooij DG (2002) Development of a cryopreservation protocol for type A spermatogonia. J Androl 23:537–545

    CAS  PubMed  Google Scholar 

  • Jahnukainen K, Hou M, Petersen C, Setchell B, Söder O (2001) Intratesticular transplantation of testicular cells from leukemic rats causes transmission of leukemia. Cancer Res 61:706–710

    CAS  PubMed  Google Scholar 

  • Jung SE, Ahn JS, Kim YH, Kim BJ, Won JH, Ryu BY (2020a) Effective cryopreservation protocol for preservation of male primate (Macaca fascicularis) prepubertal fertility. Reprod Biomed Online 41(6):1070–1083

    Article  CAS  PubMed  Google Scholar 

  • Jung SE, Kim M, Ahn JS, Kim YH, Kim BJ, Yun MH, Auh JH, Ryu BY (2020b) Effect of equilibration time and temperature on murine spermatogonial stem cell cryopreservation. Biopreserv Biobank 18:213–221

    Article  CAS  PubMed  Google Scholar 

  • Kadam P, Ntemou E, Baert Y, Van Laere S, Van Saen D, Goossens E (2018) Co-transplantation of mesenchymal stem cells improves spermatogonial stem cell transplantation efficiency in mice. Stem Cell Res Ther 9:317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadam P, Ntemou E, Onofre J, Van Saen D, Goossens E (2019) Does co-transplantation of mesenchymal and spermatogonial stem cells improve reproductive efficiency and safety in mice? Stem Cell Res Ther 10:310

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Shinohara T (2003) Restoration of fertility in infertile mice by transplantation of cryopreserved male germline stem cells. Hum Reprod 18:2660–2667

    Article  CAS  PubMed  Google Scholar 

  • Kaneko H, Kikuchi K, Nakai M, Somfai T, Noguchi J, Tanihara F, Ito J, Kashiwazaki N (2013) Generation of live piglets for the first time using sperm retrieved from immature testicular tissue cryopreserved and grafted into nude mice. PLoS One 8:e70989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaul G, Kaur J, Rafeeqi TA (2010) Ultrasound guided transplantation of enriched and cryopreserved spermatogonial cell suspension in goats. Reprod Domest Anim 45:e249–e254

    Article  CAS  PubMed  Google Scholar 

  • Kawai K, Li YS, Song MF, Kasai H (2010) DNA methylation by dimethyl sulfoxide and methionine sulfoxide triggered by hydroxyl radical and implications for epigenetic modifications. Bioorg Med Chem Lett 20:260–265

    Article  CAS  PubMed  Google Scholar 

  • Kee K, Angeles VT, Flores M, Nguyen HN, Reijo Pera RA (2009) Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462:222–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keros V, Rosenlund B, Hultenby K, Aghajanova L, Levkov L, Hovatta O (2005) Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod 20:1676–1687

    Article  CAS  PubMed  Google Scholar 

  • Keros V, Hultenby K, Borgström B, Fridström M, Jahnukainen K, Hovatta O (2007) Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment. Hum Reprod 22:1384–1395

    Article  CAS  PubMed  Google Scholar 

  • Kim YM, Uhm SJ, Gupta MK, Yang JS, Lim JG, Das ZC, Heo YT, Chung HJ, Kong IK, Kim NH, Lee HT, Ko DH (2012) Successful vitrification of bovine blastocysts on paper container. Theriogenology 78:1085–1093

    Article  CAS  PubMed  Google Scholar 

  • Kim KJ, Lee YA, Kim BJ, Kim YH, Kim BG, Kang HG, Jung SE, Choi SH, Schmidt JA, Ryu BY (2015) Cryopreservation of putative pre-pubertal bovine spermatogonial stem cells by slow freezing. Cryobiology 70:175–183

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Lee JH, Hur YB, Lee CW, Park SH, Koo BW (2017) Marine antifreeze proteins: structure, function, and application to cryopreservation as a potential cryoprotectant. Mar Drugs 15:27

    Article  PubMed Central  Google Scholar 

  • Kirpatovskii VI, Efremov GD, Frolova EV (2018) Ectopic organogenesis after allotransplantation of freshly removed or cryopreserved neonatal testicle under the renal capsule in rats. Bull Exp Biol Med 166:268–273

    Article  CAS  PubMed  Google Scholar 

  • Koppes EA, Redel BK, Johnson MA, Skvorak KJ, Ghaloul-Gonzalez L, Yates ME, Lewis DW, Gollin SM, Wu YL, Christ SE, Yerle M, Leshinski A, Spate LD, Benne JA, Murphy SL, Samuel MS, Walters EM, Hansen SA, Wells KD, Lichter-Konecki U, Wagner RA, Newsome JT, Dobrowolski SF, Vockley J, Prather RS, Nicholls RD (2020) A porcine model of phenylketonuria generated by CRISPR/Cas9 genome editing. JCI Insight 5:141523

    Article  PubMed  Google Scholar 

  • Kristensen TN, Hoffmann AA, Pertoldi C, Stronen AV (2015) What can livestock breeders learn from conservation genetics and vice versa? Front Genet 6:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumari N, Gupta MK, Singh RK (2016) Open encapsulation-vitrification for cryopreservation of algae. Cryobiology 73:232–239

    Article  CAS  PubMed  Google Scholar 

  • Lakhoo K, Davies J, Chakraborty S, Berg S, Tennyson R, Fowler D, Manek S, Verrill C, Lane S (2019) Development of a new reproductive tissue cryopreservation clinical service for children: the Oxford programme. Pediatr Surg Int 35:1271–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee PA, Coughlin MT (2001) Fertility after bilateral cryptorchidism. Evaluation by paternity, hormone, and semen data. Horm Res 55:28–32

    CAS  PubMed  Google Scholar 

  • Lee YA, Kim YH, Kim BJ, Jung MS, Auh JH, Seo JT, Park YS, Lee SH, Ryu BY (2013a) Cryopreservation of mouse spermatogonial stem cells in dimethylsulfoxide and polyethylene glycol. Biol Reprod 89:109

    Article  PubMed  Google Scholar 

  • Lee YA, Kim YH, Kim BJ, Kim BG, Kim KJ, Auh JH, Schmidt JA, Ryu BY (2013b) Cryopreservation in trehalose preserves functional capacity of murine spermatogonial stem cells. PLoS One 8:e54889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YA, Kim YH, Ha SJ, Kim BJ, Kim KJ, Jung MS, Kim BG, Ryu BY (2014a) Effect of sugar molecules on the cryopreservation of mouse spermatogonial stem cells. Fertil Steril 101:1165–1175

    Article  CAS  PubMed  Google Scholar 

  • Lee YA, Kim YH, Ha SJ, Kim KJ, Kim BJ, Kim BG, Choi SH, Kim IC, Schmidt JA, Ryu BY (2014b) Cryopreservation of porcine spermatogonial stem cells by slow-freezing testis tissue in trehalose. J Anim Sci 92:984–995

    Article  CAS  PubMed  Google Scholar 

  • Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, Pinotti R, Swan SH (2017) Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update 23:646–659

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Leng M, Ma T, Yu D, Shi H, Shi Q (2009) Cryopreservation has no effect on meiotic recombination and synapsis in testicular tissues. Fertil Steril 91:1404–1407

    Article  CAS  PubMed  Google Scholar 

  • Li H, Bian YL, Schreurs N, Zhang XG, Raza SHA, Fang Q, Wang LQ, Hu JH (2018) Effects of five cryoprotectants on proliferation and differentiation-related gene expression of frozen-thawed bovine calf testicular tissue. Reprod Domest Anim 53:1211–1218

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Nie YH, Zhang CC, Cai YJ, Wang Y, Lu HP, Li YZ, Cheng C, Qiu ZL, Sun Q (2016) Generation of macaques with sperm derived from juvenile monkey testicular xenografts. Cell Res 26:139–142

    Article  PubMed  Google Scholar 

  • Lukusa AK, Vermylen C, Vanabelle B, Curaba M, Brichard B, Chantrain C, Dupont S, Ferrant A, Wyns C (2009) Bone marrow transplantation or hydroxyurea for sickle cell anemia: long-term effects on semen variables and hormone profiles. Pediatr Hematol Oncol 26:186–194

    Article  PubMed  Google Scholar 

  • Makala H, Pothana L, Sonam S, Malla A, Goel S (2015) Regeneration of Leydig cells in ectopically autografted adult mouse testes. Reproduction 149:259–268

    Article  CAS  PubMed  Google Scholar 

  • Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Phys 247:C125–C142

    Article  CAS  Google Scholar 

  • Men H, Agca Y, Riley LK, Critser JK (2006) Improved survival of vitrified porcine embryos after partial delipation through chemically stimulated lipolysis and inhibition of apoptosis. Theriogenology 66:2008–2016

    Article  CAS  PubMed  Google Scholar 

  • Meneghel J, Kilbride P, Morris JG, Fonseca F (2019) Physical events occurring during the cryopreservation of immortalized human T cells. PLoS One 14:e0217304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohaqiq M, Movahedin M, Mazaheri Z, Amirjannati N (2019) In vitro transplantation of spermatogonial stem cells isolated from human frozen-thawed testis tissue can induce spermatogenesis under 3-dimensional tissue culture conditions. Biol Res 52:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Morimoto H, Iwata K, Ogonuki N, Inoue K, Atsuo O, Kanatsu-Shinohara M, Morimoto T, Yabe-Nishimura C, Shinohara T (2013) ROS are required for mouse spermatogonial stem cell self-renewal. Cell Stem Cell 12:774–786

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Nabeshima Y, Yoshida S (2007) Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12:195–206

    Article  CAS  PubMed  Google Scholar 

  • Navid S, Rastegar T, Baazm M, Alizadeh R, Talebi A, Gholami K, Khosravi-Farsani S, Koruji M, Abbasi M (2017) In vitro effects of melatonin on colonization of neonate mouse spermatogonial stem cells. Syst Biol Reprod Med 63:370–381

    Article  CAS  PubMed  Google Scholar 

  • Nicopoullos JD, Almeida P, Vourliotis M, Gilling-Smith C (2011) A decade of the sperm-washing programme: correlation between markers of HIV and seminal parameters. HIV Med 12:195–201

    Article  CAS  PubMed  Google Scholar 

  • Noguchi J, Ohnuma K, Ozawa M, Karja NW, Fahrudin M, Somfai T, Kikuchi K, Kaneko H (2006) Successful long term culture of immature porcine sertoli cells in the reconstructed testicular cell cord. J Reprod Dev 52:383–389

    Article  CAS  PubMed  Google Scholar 

  • Ntemou E, Kadam P, Van Saen D, Wistuba J, Mitchell RT, Schlatt S, Goossens E (2019) Complete spermatogenesis in intratesticular testis tissue xenotransplants from immature non-human primate. Hum Reprod 34:403–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oblette A, Rives N, Dumont L, Rives A, Verhaeghe F, Jumeau F, Rondanino C (2017) Assessment of sperm nuclear quality after in vitro maturation of fresh or frozen/thawed mouse pre-pubertal testes. Mol Hum Reprod 23:674–684

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Dobrinski I, Avarbock MR, Brinster RL (2000) Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med 6:29–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onions VJ, Mitchell MR, Campbell BK, Webb R (2008) Ovarian tissue viability following whole ovine ovary cryopreservation: assessing the effects of sphingosine-1-phosphate inclusion. Hum Reprod 23:606–618

    Article  CAS  PubMed  Google Scholar 

  • Onofre J, Baert Y, Faes K, Goossens E (2016) Cryopreservation of testicular tissue or testicular cell suspensions: a pivotal step in fertility preservation. Hum Reprod Update 22:744–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onofre J, Kadam P, Baert Y, Goossens E (2020) Testicular tissue cryopreservation is the preferred method to preserve spermatogonial stem cells prior to transplantation. Reprod Biomed Online 40:261–269

    Article  CAS  PubMed  Google Scholar 

  • Pacchiarotti J, Ramos T, Howerton K, Greilach S, Zaragoza K, Olmstead M, Izadyar F (2013) Developing a clinical-grade cryopreservation protocol for human testicular tissue and cells. Biomed Res Int 2013:930962

    Article  PubMed  PubMed Central  Google Scholar 

  • Park KE, Kaucher AV, Powell A, Waqas MS, Sandmaier SE, Oatley MJ, Park CH, Tibary A, Donovan DM, Blomberg LA, Lillico SG, Whitelaw CB, Mileham A, Telugu BP, Oatley JM (2017) Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep 7:40176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patra T, Gupta MK (2019) Cryopreservation of murine testicular Leydig cells by modified solid surface vitrification with supplementation of antioxidants. Cryobiology 88:38–46

    Article  CAS  PubMed  Google Scholar 

  • Patra T, Gupta MK (2020) Evaluation of sodium alginate for encapsulation-vitrification of testicular Leydig cells. Int J Biol Macromol 153:128–137

    Article  CAS  PubMed  Google Scholar 

  • Patra T, Pathak D, Gupta MK (2021) Strategies for cryopreservation of testicular cells and tissues in cancer and genetic diseases. Cell Tissue Res 385:1–19. https://doi.org/10.1007/s00441-021-03437-4

    Article  PubMed  Google Scholar 

  • Pelzman DL, Orwig KE, Hwang K (2020) Progress in translational reproductive science: testicular tissue transplantation and in vitro spermatogenesis. Fertil Steril 113:500–509

    Article  PubMed  Google Scholar 

  • Pendergraft SS, Sadri-Ardekani H, Atala A, Bishop CE (2017) Three-dimensional testicular organoid: a novel tool for the study of human spermatogenesis and gonadotoxicity in vitro. Biol Reprod 96:720–732

    Article  PubMed  Google Scholar 

  • Perrard MH, Sereni N, Schluth-Bolard C, Blondet A, Plotton I, Morel-Journel N, Lejeune H, David L, Durand P (2016) Complete human and rat ex vivo spermatogenesis from fresh or frozen testicular tissue. Biol Reprod 95:89

    Article  PubMed  Google Scholar 

  • Pietzak EJ 3rd, Tasian GE, Tasian SK, Brinster RL, Carlson C, Ginsberg JP, Kolon TF (2015) Histology of testicular biopsies obtained for experimental fertility preservation protocol in boys with cancer. J Urol 194:1420–1424

    Article  PubMed  PubMed Central  Google Scholar 

  • Pirnia A, Parivar K, Hemadi M, Yaghmaei P, Gholami M (2017) Stemness of spermatogonial stem cells encapsulated in alginate hydrogel during cryopreservation. Andrologia 49:12650

    Article  Google Scholar 

  • Poels J, Van Langendonckt A, Dehoux JP, Donnez J, Wyns C (2012) Vitrification of non-human primate immature testicular tissue allows maintenance of proliferating spermatogonial cells after xenografting to recipient mice. Theriogenology 77:1008–1013

    Article  CAS  PubMed  Google Scholar 

  • Poels J, Van Langendonckt A, Many MC, Wese FX, Wyns C (2013) Vitrification preserves proliferation capacity in human spermatogonia. Hum Reprod 28:578–589

    Article  CAS  PubMed  Google Scholar 

  • Poels J, Abou-Ghannam G, Herman S, Van Langendonckt A, Wese FX, Wyns C (2014) In search of better spermatogonial preservation by supplementation of cryopreserved human immature testicular tissue xenografts with N-acetylcysteine and testosterone. Front Surg 1:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Poels J, Abou-Ghannam G, Decamps A, Leyman M, Rieux A, Wyns C (2016) Transplantation of testicular tissue in alginate hydrogel loaded with VEGF nanoparticles improves spermatogonial recovery. J Control Release 234:79–89

    Article  CAS  PubMed  Google Scholar 

  • Portela JMD, de Winter-Korver CM, van Daalen SKM, Meißner A, de Melker AA, Repping S, van Pelt AMM (2019) Assessment of fresh and cryopreserved testicular tissues from (pre)pubertal boys during organ culture as a strategy for in vitro spermatogenesis. Hum Reprod 34:2443–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pothana L, Makala H, Devi L, Varma VP, Goel S (2015) Germ cell differentiation in cryopreserved, immature, Indian spotted mouse deer (Moschiola indica) testes xenografted onto mice. Theriogenology 83:625–633

    Article  CAS  PubMed  Google Scholar 

  • Pothana L, Devi L, Goel S (2017) Cryopreservation of adult cervid testes. Cryobiology 74:103–109

    Article  CAS  PubMed  Google Scholar 

  • Pukazhenthi BS, Neubauer K, Jewgenow K, Howard J, Wildt DE (2006) The impact and potential etiology of teratospermia in the domestic cat and its wild relatives. Theriogenology 66:112–121

    Article  PubMed  Google Scholar 

  • Pukazhenthi BS, Nagashima J, Travis AJ, Costa GM, Escobar EN, França LR, Wildt DE (2015) Slow freezing, but not vitrification supports complete spermatogenesis in cryopreserved, neonatal sheep testicular xenografts. PLoS One 10:e0123957

    Article  PubMed  PubMed Central  Google Scholar 

  • Redden E, Davey R, Borjigin U, Hutton K, Hinch G, Hope S, Hill J, Herrid M (2009) Large quantity cryopreservation of bovine testicular cells and its effect on enrichment of type A spermatogonia. Cryobiology 58:190–195

    Article  CAS  PubMed  Google Scholar 

  • Rezaei Topraggaleh T, Rezazadeh Valojerdi M, Montazeri L, Baharvand H (2019) A testis-derived macroporous 3D scaffold as a platform for the generation of mouse testicular organoids. Biomater Sci 7:1422–1436

    Article  CAS  PubMed  Google Scholar 

  • Sá R, Cremades N, Malheiro I, Sousa M (2012) Cryopreservation of human testicular diploid germ cell suspensions. Andrologia 44:366–372

    Article  PubMed  Google Scholar 

  • Sadri-Ardekani H, Atala A (2014) Testicular tissue cryopreservation and spermatogonial stem cell transplantation to restore fertility: from bench to bedside. Stem Cell Res Ther 5:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakib S, Uchida A, Valenzuela-Leon P, Yu Y, Valli-Pulaski H, Orwig K, Ungrin M, Dobrinski I (2019) Formation of organotypic testicular organoids in microwell culture. Biol Reprod 100:1648–1660

    Article  PubMed  PubMed Central  Google Scholar 

  • Saragusty J, Walzer C, Petit T, Stalder G, Horowitz I, Hermes R (2010) Cooling and freezing of epididymal sperm in the common hippopotamus (Hippopotamus amphibius). Theriogenology 74:1256–1263

    Article  CAS  PubMed  Google Scholar 

  • Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T (2011) In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471:504–507

    Article  CAS  PubMed  Google Scholar 

  • Sayed Mahdi N, Azarbani F, Pirnia A, Abbaszadeh A, Gholami M (2018) The effect of caffeic acid on spermatogonial stem cell-type a cryopreservation. Rep Biochem Mol Biol 7:85–93

    PubMed  PubMed Central  Google Scholar 

  • Schrans-Stassen BH, Saunders PT, Cooke HJ, de Rooij DG (2001) Nature of the spermatogenic arrest in Dazl −/− mice. Biol Reprod 65:771–776

    Article  CAS  PubMed  Google Scholar 

  • Shetty G, Mitchell JM, Lam TNA, Wu Z, Zhang J, Hill L, Tailor RC, Peters KA, Penedo MC, Orwig KE, Meistrich ML (2018) Donor spermatogenesis in de novo formed seminiferous tubules from transplanted testicular cells in rhesus monkey testis. Hum Reprod 33:2249–2255

    PubMed  PubMed Central  Google Scholar 

  • Shetty G, Mitchell JM, Meyer JM, Wu Z, Lam TNA, Phan TT, Zhang J, Hill L, Tailor RC, Peters KA, Penedo MC, Hanna C, Orwig KE, Meistrich ML (2020) Restoration of functional sperm production in irradiated pubertal rhesus monkeys by spermatogonial stem cell transplantation. Andrology 8:1428–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, Robker RL, Richards JS, McGinnis LK, Biggers JD, Eppig JJ, Bronson RT, Elledge SJ, Weinberg RA (1996) Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 384:470–474

    Article  CAS  PubMed  Google Scholar 

  • Snowden JA, Badoglio M, Labopin M, Giebel S, McGrath E, Marjanovic Z, Burman J, Moore J, Rovira M, Wulffraat NM, Kazmi M, Greco R, Snarski E, Kozak T, Kirgizov K, Alexander T, Bader P, Saccardi R, Farge D (2017) Evolution, trends, outcomes, and economics of hematopoietic stem cell transplantation in severe autoimmune diseases. Blood Adv 1:2742–2755

    Article  PubMed  PubMed Central  Google Scholar 

  • Song W, Zhao W, Yang Q, Wang X, Jin H, Yao G, Peng Z, Shi S, Yang H, Sun Y (2016) Effect of rapid cryopreservation on meiotic recombination in human spermatocytes. Microsc Res Tech 79:923–928

    Article  CAS  PubMed  Google Scholar 

  • Su XJ, Yuan W, Huang GY, Olsen J, Li J (2015) Paternal age and offspring congenital heart defects: a national cohort study. PLoS One 10:e0121030

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka A, Nagayoshi M, Takemoto Y, Tanaka I, Kusunoki H, Watanabe S, Kuroda K, Takeda S, Ito M, Yanagimachi R (2015) Fourteen babies born after round spermatid injection into human oocytes. Proc Natl Acad Sci U S A 112:14629–14634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka A, Suzuki K, Nagayoshi M, Takemoto Y, Watanabe S, Takeda S, Irahara M, Kuji N, Yamagata Z, Yanagimachi R (2018) Ninety babies born after round spermatid injection into oocytes: survey of their development from fertilization to 2 years of age. Fertil Steril 110:443–451

    Article  PubMed  Google Scholar 

  • Taylor JL, Debost JPG, Morton SU, Wigdor EM, Heyne HO, Lal D, Howrigan DP, Bloemendal A, Larsen JT, Kosmicki JA, Weiner DJ, Homsy J, Seidman JG, Seidman CE, Agerbo E, McGrath JJ, Mortensen PB, Petersen L, Daly MJ, Robinson EB (2019) Paternal-age-related de novo mutations and risk for five disorders. Nat Commun 10:3043

    Article  PubMed  PubMed Central  Google Scholar 

  • Tedder RS, Zuckerman MA, Goldstone AH, Hawkins AE, Fielding A, Briggs EM, Irwin D, Blair S, Gorman AM, Patterson KG et al (1995) Hepatitis B transmission from contaminated cryopreservation tank. Lancet 346:137–140

    Article  CAS  PubMed  Google Scholar 

  • Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA, Clark AM (2009) Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod 24:2061–2070

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Ma K, Pei CB, Zhang SH, Li X, Zhou Y, Yan B, Wang HY, Ma LH (2019) Relative safety of various spermatogenic stem cell purification methods for application in spermatogenic stem cell transplantation. Stem Cell Res Ther 10:382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travers A, Milazzo JP, Perdrix A, Metton C, Bironneau A, Macé B, Rives N (2011) Assessment of freezing procedures for rat immature testicular tissue. Theriogenology 76:981–990

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui T, Hesabi B, Moons DS, Pandolfi PP, Hansel KS, Koff A, Kiyokawa H (1999) Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity. Mol Cell Biol 19:7011–7019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unni S, Kasiviswanathan S, D'Souza S, Khavale S, Mukherjee S, Patwardhan S, Bhartiya D (2012) Efficient cryopreservation of testicular tissue: effect of age, sample state, and concentration of cryoprotectant. Fertil Steril 97:200–208

    Article  CAS  PubMed  Google Scholar 

  • Valli-Pulaski H, Peters KA, Gassei K, Steimer SR, Sukhwani M, Hermann BP, Dwomor L, David S, Fayomi AP, Munyoki SK, Chu T, Chaudhry R, Cannon GM, Fox PJ, Jaffe TM, Sanfilippo JS, Menke MN, Lunenfeld E, Abofoul-Azab M, Sender LS, Messina J, Klimpel LM, Gosiengfiao Y, Rowell EE, Hsieh MH, Granberg CF, Reddy PP, Sandlow JI, Huleihel M, Orwig KE (2019) Testicular tissue cryopreservation: 8 years of experience from a coordinated network of academic centers. Hum Reprod 34:966–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vermeulen M, Poels J, de Michele F, Rieux A, Wyns C (2017) Restoring fertility with cryopreserved prepubertal testicular tissue: perspectives with hydrogel encapsulation, nanotechnology, and bioengineered scaffolds. Ann Biomed Eng 45:1770–1781

    Article  PubMed  Google Scholar 

  • Vermeulen M, Del Vento F, de Michele F, Poels J, Wyns C (2018) Development of a cytocompatible scaffold from pig immature testicular tissue allowing human sertoli cell attachment, proliferation and functionality. Int J Mol Sci 19:227

    Article  PubMed Central  Google Scholar 

  • Vermeulen M, Del Vento F, Kanbar M, Pyr Dit Ruys S, Vertommen D, Poels J, Wyns C (2019) Generation of organized porcine testicular organoids in solubilized hydrogels from decellularized extracellular matrix. Int J Mol Sci 20:5476

    Article  CAS  PubMed Central  Google Scholar 

  • Vialard F, Bailly M, Bouazzi H, Albert M, Pont JC, Mendes V, Bergere M, Gomes DM, de Mazancourt P, Selva J (2012) The high frequency of sperm aneuploidy in klinefelter patients and in nonobstructive azoospermia is due to meiotic errors in euploid spermatocytes. J Androl 33:1352–1359

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Li L, Xie Q, Hou Z, Yu X, Ma M, Huang T (2014) Factors affecting sperm fertilizing capacity in men infected with HIV. J Med Virol 86:1467–1472

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Karlsson JOM, Aksan A (2019) FTIR analysis of molecular changes associated with warming injury in cryopreserved leukocytes. Langmuir 35:7552–7559

    Article  CAS  PubMed  Google Scholar 

  • Weng L, Chen C, Zuo J, Li W (2011) Molecular dynamics study of effects of temperature and concentration on hydrogen-bond abilities of ethylene glycol and glycerol: implications for cryopreservation. J Phys Chem A 115:4729–4737

    Article  CAS  PubMed  Google Scholar 

  • Wikström AM, Dunkel L (2008) Testicular function in Klinefelter syndrome. Horm Res 69:317–326

    PubMed  Google Scholar 

  • Wu X, Goodyear SM, Abramowitz LK, Bartolomei MS, Tobias JW, Avarbock MR, Brinster RL (2012) Fertile offspring derived from mouse spermatogonial stem cells cryopreserved for more than 14 years. Hum Reprod 27:1249–1259

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Zhou H, Fan X, Zhang Y, Zhang M, Wang Y, Xie Z, Bai M, Yin Q, Liang D, Tang W, Liao J, Zhou C, Liu W, Zhu P, Guo H, Pan H, Wu C, Shi H, Wu L, Tang F, Li J (2015) Correction of a genetic disease by CRISPR-Cas9-mediated gene editing in mouse spermatogonial stem cells. Cell Res 25:67–79

    Article  CAS  PubMed  Google Scholar 

  • Wyns C, Curaba M, Martinez-Madrid B, Van Langendonckt A, François-Xavier W, Donnez J (2007) Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice. Hum Reprod 22:1603–1611

    Article  PubMed  Google Scholar 

  • Wyns C, Van Langendonckt A, Wese FX, Donnez J, Curaba M (2008) Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue. Hum Reprod 23:2402–2414

    Article  PubMed  Google Scholar 

  • Xie Y, Chen H, Luo D, Yang X, Yao J, Zhang C, Lv L, Guo Z, Deng C, Li Y, Liang X, Sun X, Liu G (2020) Inhibiting necroptosis of spermatogonial stem cell as a novel strategy for male fertility preservation. Stem Cells Dev 29:475–487

    Article  CAS  PubMed  Google Scholar 

  • Yango P, Altman E, Smith JF, Klatsky PC, Tran ND (2014) Optimizing cryopreservation of human spermatogonial stem cells: comparing the effectiveness of testicular tissue and single cell suspension cryopreservation. Fertil Steril 102:1491–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokonishi T, Sato T, Komeya M, Katagiri K, Kubota Y, Nakabayashi K, Hata K, Inoue K, Ogonuki N, Ogura A, Ogawa T (2014) Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun 5:4320

    Article  CAS  PubMed  Google Scholar 

  • Yu Z, Ji P, Cao J, Zhu S, Li Y, Zheng L, Chen X, Feng L (2009) Dazl promotes germ cell differentiation from embryonic stem cells. J Mol Cell Biol 1:93–103

    Article  CAS  PubMed  Google Scholar 

  • Yuan Z, Hou R, Wu J (2009) Generation of mice by transplantation of an adult spermatogonial cell line after cryopreservation. Cell Prolif 42:123–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XG, Wang YH, Han C, Hu S, Wang LQ, Hu JH (2015) Effects of trehalose supplementation on cell viability and oxidative stress variables in frozen-thawed bovine calf testicular tissue. Cryobiology 70:246–252

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Wang C, Zhang Y, Jiang Y, Qin Y, Pang D, Zhang G, Liu H, Xie Z, Yuan H, Ouyang H, Wang J, Tang X (2020) A CRISPR-engineered swine model of COL2A1 deficiency recapitulates altered early skeletal developmental defects in humans. Bone 137:115450

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grant from Indian Council of Medical Research (ICMR), Government of India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mukesh Kumar Gupta .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Patra, T., Bhaskar, R., Gupta, M.K. (2021). Cryopreservation of Testicular Stem Cells and Its Application in Veterinary Science. In: Choudhary, R.K., Choudhary, S. (eds) Stem Cells in Veterinary Science. Springer, Singapore. https://doi.org/10.1007/978-981-16-3464-2_9

Download citation

Publish with us

Policies and ethics