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Cited by 108Animal Genetics and ReproductionReproductive biology and impacts on aquatic speciesReproductive Biology and Fertility

Resurrecting biodiversity: Advanced assisted reproductive technologies and biobanking

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Bolton, Rhiannon L, Mooney, Andrew, Pettit, Matt T, Bolton, Anthony E, Morgan, Lucy, Drake, Gabby J, Appeltant, Ruth, Walker, Susan L +2 more·2022·Reproduction and Fertility
DOI 10.1530/raf-22-0005PMC PMC9346332
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Abstract

Biodiversity is defined as the presence of a variety of living organisms on the Earth that is essential for human survival. However, anthropogenic activities are causing the sixth mass extinction, threatening even our own species. For many animals, dwindling numbers are becoming fragmented populations with low genetic diversity, threatening long-term species viability. With extinction rates 1000–10,000 times greater than natural, ex situ and in situ conservation programmes need additional support to save species. The indefinite storage of cryopreserved (−196°C) viable cells and tissues (cryobanking), followed by assisted or advanced assisted reproductive technology (ART: utilisation of oocytes and spermatozoa to generate offspring; aART: utilisation of somatic cell genetic material to generate offspring), may be the only hope for species’ long-term survival. As such, cryobanking should be considered a necessity for all future conservation strategies. Following cryopreservation, ART/aART can be used to reinstate lost genetics back into a population, resurrecting biodiversity. However, for this to be successful, species-specific protocol optimisation and increased knowledge of basic biology for many taxa are required. Current ART/aART is primarily focused on mammalian taxa; however, this needs to be extended to all, including to some of the most endangered species: amphibians. Gamete, reproductive tissue and somatic cell cryobanking can fill the gap between losing genetic diversity today and future technological developments. This review explores species prioritisation for cryobanking and the successes and challenges of cryopreservation and multiple ARTs/aARTs. We here discuss the value of cryobanking before more species are lost and the potential of advanced reproductive technologies not only to halt but also to reverse biodiversity loss. Lay summary: The world is undergoing its sixth mass extinction; however, unlike previous events, the latest is caused by human activities and is resulting in the largest loss of biodiversity (all living things on Earth) for 65 million years. With an extinction rate 1000–10,000-fold greater than natural, this catastrophic decline in biodiversity is threatening our own survival. As the number of individuals within a species declines, genetic diversity reduces, threatening their long-term existence. In this review, the authors summarise approaches to indefinitely preserve living cells and tissues at low temperatures (cryobanking) and the technologies required to resurrect biodiversity. In the future when appropriate techniques become available, these living samples can be thawed and used to reinstate genetic diversity and produce live young ones of endangered species, enabling their long-term survival. The successes and challenges of genome resource cryopreservation are discussed to enable a move towards a future of stable biodiversity.

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  • The existence of biobanks and available germplasm from endangered and extinct-in-the-wild species creates opportunities to reintroduce genetic potential that does not currently exist in the extant population.

    “The existence of biobanks and available germplasm from endangered and extinct-in-the-wild species thus creates opportunities to reintroduce genetic potential that does not currently exist in the extant population [88][89][90][91].”

    From The Concept of Agency, Animal Wellbeing, and the Practical Realities of Ex Situ Breeding Programs in Zoos and Aquariums (2024) · cites this paper as [88]

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References 317 · Cited by 108

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  1. Abe Y Asano T Ali M Suzuki H 2010 Vitrification of canine cumulus-oocyte complexes in DAP213 with a cryotop holder. Reproductive Medicine and Biology 9 115– 120. (10.1007/s12522-010-0045-6) 29662428 PMC5891781 · DOI
  2. Allen CD Burridge M Mulhall S Chafer ML Nicolson VN Pyne M Zee YP Jago SC Lundie-Jenkins G Holt WV 2008 Successful artificial insemination in the koala (Phascolarctos cinereus) using extended and extended-chilled semen collected by electroejaculation. Biology of Reproduction 78 661– 666. (10.1095/biolreprod.107.064824) 18094357 · DOI
  3. Andrabi SMH Maxwell WMC 2007 A review on reproductive biotechnologies for conservation of endangered mammalian species. Animal Reproduction Science 99 223– 243. (10.1016/j.anireprosci.2006.07.002) 16919407 · DOI · Paper page
  4. Andrae CS Oliveira ECS Ferraz MAMM Nagashima JB 2021 Cryopreservation of grey wolf (Canis lupus) testicular tissue. Cryobiology 100 173– 179. (10.1016/j.cryobiol.2021.01.010) 33482146 · DOI
  5. Appeltant R Somfai T Santos ECS Dang-Nguyen TQ Nagai T Kikuchi K 2017 Effects of vitrification of cumulus-enclosed porcine oocytes at the germinal vesicle stage on cumulus expansion, nuclear progression and cytoplasmic maturation. Reproduction, Fertility, and Development 29 2419– 2429. (10.1071/RD16386) 28502309 · DOI
  6. Arav A 2014 Cryopreservation of oocytes and embryos. Theriogenology 81 96– 102. (10.1016/j.theriogenology.2013.09.011) 24274414 · DOI
  7. Arregui L Rathi R Zeng W Honaramooz A Gomendio M Roldan ER Dobrinski I 2008 Xenografting of adult mammalian testis tissue. Animal Reproduction Science 106 65– 76. (10.1016/j.anireprosci.2007.03.026) 17512146 PMC2386512 · DOI
  8. Asa CS Bauman JE Coonan TJ Gray MM 2007 Evidence for induced estrus or ovulation in a canid, the island fox (Urocyon littoralis). Journal of Mammalogy 88 436– 440. (10.1644/05-MAMM-A-295R2.1) · DOI
  9. Asano A Tajima A 2017 Development and preservation of avian sperm. Advances in Experimental Medicine and Biology 1001 59– 73. (10.1007/978-981-10-3975-1_4) 28980229 · DOI
  10. Asturiano JF Cabrita E Horváth Á 2017 Progress, challenges and perspectives on fish gamete cryopreservation: a mini-review. General and Comparative Endocrinology 245 69– 76. (10.1016/j.ygcen.2016.06.019) 27318279 · DOI
  11. Bailey JL Bilodeau JF Cormier N 2000 Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon. Journal of Andrology 21 1– 7. 10670514
  12. Bailey JL Lessard C Jacques J Brèque C Dobrinski I Zeng W Galantino-Homer HL 2008 Cryopreservation of boar semen and its future importance to the industry. Theriogenology 70 1251– 1259. (10.1016/j.theriogenology.2008.06.014) 18653225 · DOI
  13. Bajerski F Bürger A Glasmacher B Keller ERJ Müller K Mühldorfer K Nagel M Rüdel H Müller T Schenkel J 2020 Factors determining microbial colonization of liquid nitrogen storage tanks used for archiving biological samples. Applied Microbiology and Biotechnology 104 131– 144. (10.1007/s00253-019-10242-1) 31781817 PMC6942587 · DOI
  14. Ballou JD 1984 Strategies for maintaining genetic diversity in captive populations through reproductive technology. Zoo Biology 3 311– 323. (10.1002/zoo.1430030404) · DOI
  15. Ballou JD Lees C Faust LJ Long S Lynch C Bingaman Lackey L & Foose TJ 2010 Demographic and genetic management of captive populations Aug 15;219. In Wild mammals in captivity: principles and techniques for zoo management 2nd Edition. Eds DG Kleiman, KV Thompson and CK Baer. The University of Chicago Press
  16. Benesova B Trefil P 2016 Possibilities for preserving genetic resources in birds. World’s Poultry Science Journal 72 629– 642. (10.1017/S0043933916000489) · DOI
  17. Benirschke K 1984 The frozen zoo concept. Zoo Biology 3 325– 328. (10.1002/zoo.1430030405) · DOI
  18. Ben-Nun IF Montague SC Houck ML Tran HT Garitaonandia I Leonardo TR Wang YC Charter SJ Laurent LC Ryder OA 2011 Induced pluripotent stem cells from highly endangered species. Nature Methods 8 829– 831. (10.1038/nmeth.1706) 21892153 · DOI
  19. Ben-Nun IF Montague SC Houck ML Ryder O Loring JF 2015 Generation of induced pluripotent stem cells from mammalian endangered species. In Cell Reprogramming: Methods and Protocols. Eds Verma PJ Sumer H. New York, NY: Springer. 26621593
  20. Bhak JS Lee SL Ock SA Mohana Kumar B Choe SY Rho GJ 2006 Developmental rate and ploidy of embryos produced by nuclear transfer with different activation treatments in cattle. Animal Reproduction Science 92 37– 49. (10.1016/j.anireprosci.2005.04.016) 15979829 · DOI
  21. Bhat MH Sharma V Khan FA Naykoo NA Yaqoob SH Ruby K Khan HM Fazili MR Ganai NA Shah RA 2014 Comparison of slow freezing and vitrification on ovine immature oocytes. Cryo Letters 35 77– 82. 24872161
  22. Blesbois E Grasseau I Seigneurin F 2005 Membrane fluidity and the ability of domestic bird spermatozoa to survive cryopreservation. Reproduction 129 371– 378. (10.1530/rep.1.00454) 15749963 · DOI
  23. Borges AA Pereira AF 2019 Potential role of intraspecific and interspecific cloning in the conservation of wild mammals. Zygote 27 111– 117. (10.1017/S0967199419000170) 31182179 · DOI
  24. Borges AA Santos MVO Nascimento LE Lira GPO Praxedes ÉA Oliveira MF Silva AR Pereira AF 2020 Production of collared peccary (Pecari tajacu Linnaeus, 1758) parthenogenic embryos following different oocyte chemical activation and in vitro maturation conditions. Theriogenology 142 320– 327. 31711691
  25. Boutelle S Lenahan K Krisher R Bauman KL Asa CS Silber S 2011 Vitrification of oocytes from endangered Mexican gray wolves (Canis lupus baileyi). Theriogenology 75 647– 654. (10.1016/j.theriogenology.2010.10.004) 21111469 · DOI
  26. Briski O Salamone DF 2022 Past, present and future of ICSI in livestock species. Animal Reproduction Science In press. (10.1016/j.anireprosci.2022.106925) 35148927 · DOI
  27. Browne RK Clulow J Mahony M 2001 Short-term storage of cane toad (Bufo marinus) gametes. Reproduction 121 167– 173. (10.1530/rep.0.1210167) 11226040 · DOI
  28. Browne RK Clulow J Mahony M 2002 The short-term storage and cryopreservation of spermatozoa from hylid and myobatrachid frogs. Cryo Letters 23 129– 136. 12050781
  29. Browne RK Seratt J Vance C Kouba A 2006 Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reproductive Biology and Endocrinology 4 34. (10.1186/1477-7827-4-34) PMC1524778 16790071 · DOI
  30. Browne RK Silla AJ Upton R Della-Togna G Marcec-Greaves R Shishova NV Uteshev VK Proaño B Pérez OD Mansour N 2019 Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133 187– 200. (10.1016/j.theriogenology.2019.03.035) 31155034 · DOI
  31. Byrne PG Silla AJ 2010 Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered southern corroboree frog, Pseudophryne corroboree. Reproductive Biology and Endocrinology 8 144. (10.1186/1477-7827-8-144) PMC3014959 21114857 · DOI
  32. Carballo L Battistotti A Teltscher K Lierz M Bublat A Valcu M Kempenaers B 2019 Sperm morphology and evidence for sperm competition among parrots. Journal of Evolutionary Biology 32 856– 867. (10.1111/jeb.13487) 31245887 PMC6852422 · DOI
  33. Cardoso B Sánchez-Ajofrín I Castaño C García-Álvarez O Esteso MC Maroto-Morales A Iniesta-Cuerda M Garde JJ Santiago-Moreno J Soler AJ 2020 Optimization of sperm cryopreservation protocol for peregrine falcon (Falco peregrinus). Animals 10 691. (10.3390/ani10040691) PMC7222757 32316152 · DOI
  34. Ceballos G Ehrlich PR 2018 The misunderstood sixth mass extinction. Science 360 1080– 10 81. 29880679
  35. Chatdarong K 2011 Gamete rescues from gonads of wild animal post mortem. Thai Journal of Veterinary Medicine 41 99– 102.
  36. Che-Castaldo J Gray SM Rodriguez-Clark KM Schad Eebes K Faust LJ 2021 Expected demographic and genetic declines not found in most zoo and aquarium populations. Frontiers in Ecology and the Environment 19 435– 442. (10.1002/fee.2362) · DOI
  37. Chemnick LG Houck ML Ryder OA 2009 Banking of genetic resources: the Frozen Zoo® at the San Diego Zoo. In Conservation Genetics in the Age of Genomics, pp. 124– 130. Eds Amato G Desalle R Rosenblum HC Ryder OA. New York, NY, USA: Columbio University Press.
  38. Cheng TL Rovito SM Wake DB Vredenburg VT 2011 Coincident mass extirpation of Neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. PNAS 108 9502– 9507. (10.1073/pnas.1105538108) 21543713 PMC3111304 · DOI
  39. Chian RC Kuwayama M Tan L Tan J Kato O Nagai T 2004 High survival rate of bovine oocytes matured in vitro following vitrification. Journal of Reproduction and Development 50 685– 696. (10.1262/jrd.50.685) 15647621 · DOI
  40. Choudhary KK Kavya KM Jerome A Sharma RK 2016 Advances in reproductive biotechnologies. Veterinary World 9 388– 395. (10.14202/vetworld.2016.388-395) 27182135 PMC4864481 · DOI
  41. Clarke AG 2009 The Frozen Ark Project: the role of zoos and aquariums in preserving the genetic material of threatened animals. International Zoo Yearbook 43 222– 230. (10.1111/j.1748-1090.2008.00074.x) · DOI
  42. Clérico G Taminelli G Veronesi JC Polola J Pagura N Pinto C Sansinena M 2021 Mitochondrial function, blastocyst development and live foals born after ICSI of immature vitrified/warmed equine oocytes matured with or without melatonin. Theriogenology 160 40– 49. (10.1016/j.theriogenology.2020.10.036) 33171351 · DOI
  43. Clulow J Clulow S 2016 Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reproduction, Fertility, and Development 28 1116– 1132. (10.1071/RD15466) 27246622 · DOI
  44. Clulow J Upton R Trudeau VL Clulow S 2019b Amphibian assisted reproductive technologies: moving from technology to application. Advances in Experimental Medicine and Biology 1200 413– 463. (10.1007/978-3-030-23633-5_14) 31471805 · DOI
  45. Comizzoli P 2015 Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian Journal of Andrology 17 640– 645. (10.4103/1008-682X.153849) 25966625 PMC4492057 · DOI
  46. Comizzoli P 2020 Birth of a giant panda cub after artificial insemination with frozen-thawed semen: a powerful reminder about the key role of biopreservation and biobanking for wildlife conservation. Biopreservation and Biobanking 18 349– 350. (10.1089/bio.2020.29076.pjc) 32936003 · DOI
  47. Comizzoli P Holt WV 2019 Breakthroughs and new horizons in reproductive biology of rare and endangered animal species. Biology of Reproduction 101 514– 525. (10.1093/biolre/ioz031) 30772911 · DOI
  48. Comizzoli P Wildt DE 2017 Cryobanking biomaterials from wild animal species to conserve genes and biodiversity: relevance to human biobanking and biomedical research. In Biobanking of Human Biospecimens: Principles and Practice. Eds Hainaut P Vaught J Zatloukal K Pasterk M. Cham: Springer International Publishing.
  49. Comizzoli P Songsasen N Hagedorn M Wildt DE 2012 Comparative cryobiological traits and requirements for gametes and gonadal tissues collected from wildlife species. Theriogenology 78 1666– 1681. (10.1016/j.theriogenology.2012.04.008) 22704386 · DOI
  50. Comizzoli P Brown JL Holt WV 2019 Reproductive science as an essential component of conservation biology: new edition. In Reproductive Sciences in Animal Conservation. Eds Comizzoli P Brown JL Holt WV. Cham: Springer International Publishing.
  51. Conforti VA Adania CH Gonzalez PG De Oliveira C Swanson WF 2009 155 Novel recipient synchronization regimens for successful embryo transfer in the Brazilian ocelot following long-term frozen embryo storage. Reproduction, Fertility and Development 21 176– 177. (10.1071/RDv21n1Ab155) · DOI
  52. Crabbé E Verheyen G Tournaye H Van Steirteghem A 1997 The use of enzymatic procedures to recover testicular germ cells. Human Reproduction 12 1682– 1687. (10.1093/humrep/12.8.1682) 9308793 · DOI
  53. Curry MR 2000 Cryopreservation of semen from domestic livestock. Reviews of Reproduction 5 46– 52. (10.1530/ror.0.0050046) 10711735 · DOI
  54. 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. (10.1016/j.cryobiol.2019.10.199) 31678072 · DOI
  55. Damiani P Gomez M Cole A Pope E Aguilar R Hammond B Nel L Cortez C Vaccaro J Sarrat E 2004 The production of intracytoplasmic sperm injection lion (Panthera leo) embyros using spermatozoa collected by percutaneous epididymal sperm aspiration from vasectomized males. Reproduction, Fertility and Development 16 223– 224. (10.1071/RDv16n1Ab204) · DOI
  56. De Mori B Spiriti MM Pollastri I Normando S Biasetti P Florio D Andreucci F Colleoni S Galli C Göritz F 2021 An ethical assessment tool (ETHAS) to evaluate the application of assisted reproductive technologies in mammals’ conservation: the case of the northern white rhinoceros (Ceratotherium simum cottoni). Animals 11 312. (10.3390/ani11020312) PMC7911958 33530613 · DOI
  57. Diwan AD Harke SN Panche AN Panche AN 2020 Cryobanking of fish and shellfish egg, embryos and larvae: an overview. Frontiers in Marine Science 7 251. (10.3389/fmars.2020.00251) · DOI
  58. Doudna JA Charpentier E 2014 Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346 1258096. (10.1126/science.1258096) 25430774 · DOI · Paper page
  59. Eppig JJ O’Brien MJ 1996 Development in vitro of mouse oocytes from primordial follicles. Biology of Reproduction 54 197– 207. (10.1095/biolreprod54.1.197) 8838017 · DOI
  60. Fayomi AP Peters K Sukhwani M Valli-Pulaski H Shetty G Meistrich ML Houser L Robertson N Roberts V Ramsey C 2019 Autologous grafting of cryopreserved prepubertal rhesus testis produces sperm and offspring. Science 363 1314– 1319. (10.1126/science.aav2914) 30898927 PMC6598202 · DOI
  61. Fernandez-Gonzalez L Jewgenow K 2017 Cryopreservation of feline oocytes by vitrification using commercial kits and slush nitrogen technique. Reproduction in Domestic Animals 52 (Supplement 2) 230– 234. (10.1111/rda.12837) 27885726 · DOI
  62. Fernandez-Gonzalez L Huebinger J Jewgenow K 2021 Comparison of different materials for self-pressurized vitrification of feline oocytes – first results. Animals 11 1314. (10.3390/ani11051314) PMC8147606 34063659 · DOI
  63. Ficetola GF Rondinini C Bonardi A Baisero D Padoa-Schioppa E 2015 Habitat availability for amphibians and extinction threat: a global analysis. Diversity and Distributions 21 302– 311. (10.1111/ddi.12296) · DOI
  64. Figueiredo JR Hulshof SCJ Van Den Hurk R Ectors FJ Fontes RS Nusgens B Bevers MM Beckers JF 1993 Development of a combined new mechanical and enzymatic method for the isolation of intact preantral follicles from fetal, calf and adult bovine ovaries. Theriogenology 40 789– 799. (10.1016/0093-691x(9390214-p) 16727360 · DOI
  65. Figueiredo JR Hulshof SCJ Van Den Hurk R Bevers MM Thiry M Nusgens B Beckers JF 1994a The physiological status of the ovarian donor affects in vitro development of isolated bovine preantral follicles. Theriogenology 42 1303– 1310. (10.1016/0093-691X(9490250-M) · DOI
  66. Figueiredo JR Hulshof SCJ Van Den Hurk R Nusgens B Bevers MM Ectors FJ Beckers JF 1994b Preservation of oocyte and granulosa cell morphology in bovine preantral follicles cultured in vitro. Theriogenology 41 1333– 1346. (10.1016/0093-691x(9490492-2) 16727488 · DOI
  67. Folch J Cocero MJ Chesné P Alabart JL Domínguez V Cognié Y Roche A Fernández-Árias A Martí JI Sánchez P 2009 First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71 1026– 1034. (10.1016/j.theriogenology.2008.11.005) 19167744 · DOI
  68. Friedrich Ben-Nun IF Montague SC Houck ML Tran HT Garitaonandia I Leonardo TR Wang YC Charter SJ Laurent LC Ryder OA 2011 Induced pluripotent stem cells from highly endangered species. Nature Methods 8 829– 831. (10.1038/nmeth.1706) 21892153 · DOI
  69. Fuku E Kojima T Shioya Y Marcus GJ Downey BR 1992 In vitro fertilization and development of frozen-thawed bovine oocytes. Cryobiology 29 485– 492. (10.1016/0011-2240(9290051-3) 1395686 · DOI
  70. Fuller BJ 2004 Cryoprotectants: the essential antifreezes to protect life in the frozen state. Cryo Letters 25 375– 388. 15660165
  71. Fuller B Paynter S 2004 Fundamentals of cryobiology in reproductive medicine. Reproductive Biomedicine Online 9 680– 691. (10.1016/s1472-6483(1061780-4) 15670420 · DOI
  72. García-Martínez T Mogas T Mullen SF Martínez-Rodero I Gulieva RE Higgins AZ 2021 Effect of cryoprotectant concentration on bovine oocyte permeability and comparison of two membrane permeability modelling approaches. Scientific Reports 11 15387. (10.1038/s41598-021-94884-0) PMC8319298 34321576 · DOI
  73. Gastal GDA Aguiar FLN Rodrigues APR Scimeca JM Apgar GA Banz WJ Feugang JM Gastal EL 2018 Cryopreservation and in vitro culture of white-tailed deer ovarian tissue. Theriogenology 113 253– 260. (10.1016/j.theriogenology.2018.03.003) 29574135 · DOI
  74. Gillis AB Guy EL Kouba AJ Allen PJ Marcec-Greaves RM Kouba CK 2021a Short-term storage of tiger salamander (Ambystoma tigrinum) spermatozoa: the effect of collection type, temperature and time. PLoS ONE 16 e0245047. 33428658 PMC7799794
  75. Gillis JD Penfold LM Mylniczenko ND 2021b Initial characterization of male southern stingray (Hypanus americanus) reproductive parameters and preliminary investigation of sperm cryopreservation. Animals 11 2716. (10.3390/ani11092716) PMC8468634 34573681 · DOI
  76. Girgin MU Broguiere N Hoehnel S Brandenberg N Mercier B Arias AM Lutolf MP 2021 Bioengineered embryoids mimic post-implantation development in vitro. Nature Communications 12 5140. (10.1038/s41467-021-25237-8) PMC8390504 34446708 · DOI
  77. Gómez MC Pope CE Giraldo A Lyons LA Harris RF King AL Cole A Godke RA Dresser BL 2004 Birth of African wildcat cloned kittens born from domestic cats. Cloning and Stem Cells 6 247– 258. (10.1089/clo.2004.6.247) 15671671 · DOI
  78. Gómez MC Pope CE Kutner RH Ricks DM Lyons LA Ruhe M Dumas C Lyons J López M Dresser BL 2008 Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning and Stem Cells 10 469– 483. (10.1089/clo.2008.0021) 18795868 · DOI
  79. Gouveia C Huyser C Egli D Pepper MS 2020 Lessons learned from somatic cell nuclear transfer. International Journal of Molecular Sciences 21 2314. (10.3390/ijms21072314) PMC7177533 32230814 · DOI
  80. Guan WJ Liu CQ Li CY Liu D Zhang WX Ma YH 2010 Establishment and cryopreservation of a fibroblast cell line derived from Bengal tiger (Panthera tigris tigris). Cryo Letters 31 130– 138. 20687455
  81. Guenther JF Seki S Kleinhans FW Edashige K Roberts DM Mazur P 2006 Extra- and intra-cellular ice formation in stage I and II Xenopus laevis oocytes. Cryobiology 52 401– 416. (10.1016/j.cryobiol.2006.02.002) 16600207 · DOI
  82. Gurdon JB Laskey RA Reeves OR 1975 The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs. Journal of Embryology and Experimental Morphology 34 93– 112. (10.1242/dev.34.1.93) 1102625 · DOI
  83. Hagedorn M Carter V Martorana K Paresa MK Acker J Baums IB Borneman E Brittsan M Byers M Henley M 2012 Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral. PLoS ONE 7 e33354. (10.1371/journal.pone.0033354) PMC3297639 22413020 · DOI
  84. Hagedorn M Carter VL Henley EM Van Oppen MJH Hobbs R Spindler RE 2017 Producing coral offspring with cryopreserved sperm: a tool for coral reef restoration. Scientific Reports 7 14432. (10.1038/s41598-017-14644-x) PMC5663941 29089578 · DOI
  85. Hagedorn M Page CA Oneill K Flores DM Tichy L Chamberland VF Lager C Zuchowicz N Lohr K Blackburn H 2018 Successful demonstration of assisted gene flow in the threatened coral Acropora palmata across genetically- isolated Caribbean populations using cryopreserved sperm. bioRxiv 492447. (10.1101/492447) · DOI
  86. Hagedorn M Spindler R Daly J 2019 Cryopreservation as a tool for reef restoration: 2019. Advances in Experimental Medicine and Biology 1200 489– 505. (10.1007/978-3-030-23633-5_16) 31471807 · DOI
  87. Hajian M Hosseini SM Forouzanfar M Abedi P Ostadhosseini S Hosseini L Moulavi F Gourabi H Shahverdi AH Vosough Taghi Dizaj A 2011 ‘Conservation cloning’ of vulnerable Esfahan mouflon (Ovis orientalis isphahanica): in vitro and in vivo studies. European Journal of Wildlife Research 57 959– 969. (10.1007/s10344-011-0510-5) · DOI
  88. Hamano S Koikeda A Kuwayama M Nagai T 1992 Full-term development of in vitro-matured, vitrified and fertilized bovine oocytes. Theriogenology 38 1085– 1090. (10.1016/0093-691x(9290122-8) 16727206 · DOI
  89. Hamazaki N Kyogoku H Araki H Miura F Horikawa C Hamada N Shimamoto S Hikabe O Nakashima K Kitajima TS 2021 Reconstitution of the oocyte transcriptional network with transcription factors. Nature 589 264– 269. (10.1038/s41586-020-3027-9) 33328630 · DOI
  90. Herrick JR 2019 Assisted reproductive technologies for endangered species conservation: developing sophisticated protocols with limited access to animals with unique reproductive mechanisms. Biology of Reproduction 100 1158– 1170. (10.1093/biolre/ioz025) 30770538 · DOI · Paper page
  91. Hewitt R Watson P 2013 Defining biobank. Biopreservation and Biobanking 11 309– 315. (10.1089/bio.2013.0042) 24835262 · DOI · Paper page
  92. Hikabe O Hamazaki N Nagamatsu G Obata Y Hirao Y Hamada N Shimamoto S Imamura T Nakashima K Saitou M 2016 Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539 299– 303. (10.1038/nature20104) 27750280 · DOI
  93. Hildebrandt TB Hermes R Goeritz F Appeltant R Colleoni S De Mori B Diecke S Drukker M Galli C Hayashi K 2021 The ART of bringing extinction to a freeze–History and future of species conservation, exemplified by rhinos. Theriogenology 169 76– 88. (10.1016/j.theriogenology.2021.04.006) 33940218 · DOI
  94. Hinkle K Orwig KE Valli-Pulaski H Taylor S Van Leeuwen K Carpentieri D Walsh A 2021 Cryopreservation of ovarian tissue for pediatric fertility. Biopreservation and Biobanking 19 130– 135. (10.1089/bio.2020.0124) 33847512 · DOI
  95. Hoban S Bruford M D’Urban Jackson J Lopes-Fernandes M Heuertz M Hohenlohe PA Paz-Vinas I Sjögren-Gulve P Segelbacher G Vernesi C 2020 Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved. Biological Conservation 248 108654. (10.1016/j.biocon.2020.108654) · DOI
  96. Hobbs RJ O’Brien JK Spindler RE 2019 Strategic gene banking for conservation: the ins and outs of a living bank. In Scientific Foundations of Zoos and Aquariums: Their Role in Conservation and Research. Eds Kaufman AB Bashaw MJ Maple TL. Cambridge: Cambridge University Press.
  97. Holt WV 2000 Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53 47– 58. (10.1016/s0093-691x(9900239-3) 10735061 · DOI
  98. Holt WV Lloyd RE 2009 Artificial insemination for the propagation of CANDES: the reality! Theriogenology 71 228– 235. (10.1016/j.theriogenology.2008.09.003) 18922568 · DOI
  99. Holt WV Pickard AR Prather RS 2004 Wildlife conservation and reproductive cloning. Reproduction 127 317– 324. (10.1530/rep.1.00074) 15016951 · DOI
  100. Houck ML 2019 Fibroblast cell culture and cryopreservation of endangered vertebrates. Cryobiology 91 153– 154. (10.1016/j.cryobiol.2019.10.037) · DOI
  101. Howard JG Lynch C Santymire RM Marinari PE Wildt DE 2016 Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Animal Conservation 19 102– 111. (10.1111/acv.12229) · DOI
  102. Howell LG Frankham R Rodger JC Witt RR Clulow S Upton RMO Clulow J 2021 Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme. Conservation Letters 14 e12776. (10.1111/conl.12776) 38600658 · DOI
  103. Hübner K Fuhrmann G Christenson LK Kehler J Reinbold R De La Fuente R Wood J Strauss JF 3rd Boiani M Schöler HR 2003 Derivation of oocytes from mouse embryonic stem cells. Science 300 1251– 1256. (10.1126/science.1083452) 12730498 · DOI
  104. Huffmeyer AA Sikich JA Vickers TW Riley SP & Wayne RK 2022 First reproductive signs of inbreeding depression in Southern California male mountain lions (Puma concolor). Theriogenology 177 157– 164. (10.1016/j.theriogenology.2021.10.016) 34710647 · DOI
  105. Hulshof SCJ Figueiredo JR Beckers JF Bevers MM Van Der Donk JA Van Den Hurk R 1995 Effects of fetal bovine serum, FSH and 17β-estradiol on the culture of bovine preantral follicles. Theriogenology 44 217– 226. (10.1016/0093-691x(9500171-4) 16727721 · DOI
  106. Hunt CJ 2017 Cryopreservation: vitrification and controlled rate cooling. Methods in Molecular Biology 1590 41– 77. (10.1007/978-1-4939-6921-0_5) 28353262 · DOI
  107. Hurtt AE Landim-Alvarenga F Seidel Jr GE Squires EL 2000 Vitrification of immature and mature equine and bovine oocytes in an ethylene glycol, Ficoll and sucrose solution using open-pulled straws. Theriogenology 54 119– 128. (10.1016/s0093-691x(0000330-7) 10990353 · DOI
  108. Hwang I Jeong YW Kim JJ Lee HJ Kang M Park KB Park JH Kim YW Kim WT Shin T 2012 Successful cloning of coyotes through interspecies somatic cell nuclear transfer (iSCNT) using domestic dog oocytes. Biology of Reproduction 87 56– 56. 23217630
  109. Inoue K Wakao H Ogonuki N Miki H Seino K Nambu-Wakao R Noda S Miyoshi H Koseki H Taniguchi M 2005 Generation of cloned mice by direct nuclear transfer from natural killer T cells. Current Biology 15 1114– 1118. (10.1016/j.cub.2005.05.021) 15964276 · DOI
  110. Ishikura Y Ohta H Sato T Murase Y Yabuta Y Kojima Y Yamashiro C Nakamura T Yamamoto T Ogawa T 2021 In vitro reconstitution of the whole male germ-cell development from mouse pluripotent stem cells. Cell Stem Cell 28 2167.e9– 2179.e9. (10.1016/j.stem.2021.08.005) 34496297 · DOI
  111. IUCN SSC Amphibian Specialist Group 2017 Leptodactylus fallax. The IUCN Red List of Threatened Species 2017 e.T57125A3055585. (10.2305/IUCN.UK.2017-3.RLTS.T57125A3055585.en). Accessed on 21 January 2022. · DOI
  112. Janssen DL Edwards ML Koster JA Lanza RP Ryder OA 2004 Postnatal management of chryptorchid banteng calves cloned by nuclear transfer utilizing frozen fibroblast cultures and enucleated cow ova. Reproduction, Fertility and Development 16 224– 224. (10.1071/RDv16n1Ab206) · DOI
  113. Jeon Y Nam YH Cheong SA Kwak SS Lee E Hyun SH 2016 Absence of nucleolus formation in raccoon dog-porcine interspecies somatic cell nuclear transfer embryos results in embryonic developmental failure. Journal of Reproduction and Development 62 345– 350. (10.1262/jrd.2015-175) 27064112 PMC5004789 · DOI
  114. Jewgenow K Zahmel J 2020 Preservation of female genetic resources in feline species. Theriogenology 156 124– 129. (10.1016/j.theriogenology.2020.06.040) 32698038 · DOI
  115. Jia BY Xiang DC Quan GB Zhang B Shao QY Hong QH Wu GQ 2019 Transcriptome analysis of porcine immature oocytes and surrounding cumulus cells after vitrification and in vitro maturation. Theriogenology 134 90– 97. (10.1016/j.theriogenology.2019.05.019) 31158735 · DOI
  116. Jia B Xiang D Fu X Shao Q Hong Q Quan G Wu G 2020 Proteomic changes of porcine oocytes after vitrification and subsequent in vitro maturation: a tandem mass tag-based quantitative analysis. Frontiers in Cell and Developmental Biology 8 614577. (10.3389/fcell.2020.614577) PMC7785821 33425922 · DOI
  117. Joaquim DC Borges ED Viana IGR Navarro PA Vireque AA 2017 Risk of contamination of gametes and embryos during cryopreservation and measures to prevent cross-contamination. BioMed Research International 2017 1840417. (10.1155/2017/1840417) PMC5584362 28890894 · DOI
  118. Johnston SD Holt WV 2019 Using the koala (Phascolarctos cinereus) as a case study to illustrate the development of artificial breeding technology in marsupials: an update. In Reproductive Sciences in Animal Conservation. Eds Comizzoli P Brown JL Holt WV. Cham: Springer International Publishing. 31471803
  119. Johnson JA Altwegg R Evans DM Ewen JG Gordon IJ Pettorelli N Young JK 2016 Is there a future for genome-editing technologies in conservation? Animal Conservation 19 97– 101. (10.1111/acv.12273) · DOI
  120. Kaneko T Ito H Sakamoto H Onuma M & Inoue-Murayama M. 2014 Sperm preservation by freeze-drying for the conservation of wild animals. PloS one 9 e113381. (10.1371/journal.pone.0113381) 25409172 PMC4237436 · DOI
  121. Keogh LM Byrne PG Silla AJ 2017 The effect of gentamicin on sperm motility and bacterial abundance during chilled sperm storage in the Booroolong frog. General and Comparative Endocrinology 243 51– 59. (10.1016/j.ygcen.2016.11.005) 27823953 · DOI
  122. Kochan J Niżański W Moreira N Cubas ZS Nowak A Prochowska S Partyka A Młodawska W Skotnicki J 2019 ARTs in wild felid conservation programmes in Poland and in the world. Journal of Veterinary Research 63 457– 464. (10.2478/jvetres-2019-0043) 31572828 PMC6749728 · DOI
  123. Kong HS Hong YH Lee J Youm HW Lee JR Suh CS Kim SH 2021 Antifreeze protein supplementation during the warming of vitrified bovine ovarian tissue can improve the ovarian tissue quality after xenotransplantation. Frontiers in Endocrinology 12 672619. (10.3389/fendo.2021.672619) PMC8194858 34122348 · DOI
  124. Korody ML Ford SM Nguyen TD Pivaroff CG Valiente-Alandi I Peterson SE Ryder OA Loring JF 2021 Rewinding extinction in the northern white rhinoceros: genetically diverse induced pluripotent stem cell bank for genetic rescue. Stem Cells and Development 30 177– 189. (10.1089/scd.2021.0001) 33406994 PMC7891310 · DOI
  125. Kouba A Willis E Vance CK Hasenstab S Reichling S Krebs J Linhoff L Snoza M Langhorne C Germano J 2012 116 Development of assisted reproduction technologies for the endangered Mississippi gopher frog (rana sevosa) and sperm transfer for in vitro fertilization. Reproduction, Fertility and Development 24 170. (10.1071/RDv24n1Ab116) · DOI
  126. Kouba AJ Lloyd RE Houck ML Silla AJ Calatayud N Trudeau VL Clulow J Molinia F Langhorne C Vance C 2013 Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biological Conservation 164 10– 21. (10.1016/j.biocon.2013.03.010) · DOI
  127. Lagutina I Fulka H Lazzari G Galli C 2013 Interspecies somatic cell nuclear transfer: advancements and problems. Cellular Reprogramming 15 374– 384. (10.1089/cell.2013.0036) 24033141 PMC3787369 · DOI
  128. Lanza RP Cibelli JB Diaz F Moraes CT Farin PW Farin CE Hammer CJ West MD Damiani P 2000 Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2 79– 90. (10.1089/152045500436104) 16218862 · DOI
  129. Lanzendorf SE Holmgren WJ Schaffer N Hatasaka H Wentz AC Jeyendran RS 1992 In vitro fertilization and gamete micromanipulation in the lowland gorilla. Journal of Assisted Reproduction and Genetics 9 358– 364. (10.1007/BF01203960) 1472815 · DOI
  130. Lawson B Clulow S Mahony MJ Clulow J 2013 Towards gene banking amphibian maternal germ lines: short-term incubation, cryoprotectant tolerance and cryopreservation of embryonic cells of the frog, Limnodynastes peronei. PLoS ONE 4 e60760. PMC3618038 23577155
  131. Lee WY Park HJ Lee R Lee KH Kim YH Ryu BY Kim NH Kim JH Kim JH Moon SH 2013 Establishment and in vitro culture of porcine spermatogonial germ cells in low temperature culture conditions. Stem Cell Research 11 1234– 1249. (10.1016/j.scr.2013.08.008) 24041805 · DOI
  132. Lee SG Mikhalchenko AE Yim SH Lobanov AV Park JK Choi KH Bronson RT Lee CK Park TJ Gladyshev VN 2017 Naked mole rat induced pluripotent stem cells and their contribution to interspecific chimera. Stem Cell Reports 9 1706– 1720. (10.1016/j.stemcr.2017.09.013) 29107591 PMC5829328 · DOI
  133. Lee J Lee Y Lee GS Lee ST Lee E 2019 Comparative study of the developmental competence of cloned pig embryos derived from spermatogonial stem cells and fetal fibroblasts. Reproduction of Domestic Animals 54 1258– 1264. (10.1111/rda.13507) 31283039 · DOI
  134. Lee AR Park JH Shim SH Hong K La H Park KS Lee DR 2021 Genome stabilization by RAD51-stimulatory compound 1 enhances efficiency of somatic cell nuclear transfer-mediated reprogramming and full-term development of cloned mouse embryos. Cell Proliferation 54 e13059. (10.1111/cpr.13059) PMC8249786 34021643 · DOI
  135. Lees CM Wilcken J 2009 Sustaining the Ark: the challenges faced by zoos in maintaining viable populations. International Zoo Yearbook 43 6– 18. (10.1111/j.1748-1090.2008.00066.x) · DOI
  136. Leibo SP 1980 Water permeability and its activation energy of fertilized and unfertilized mouse ova. Journal of Membrane Biology 53 179– 188. (10.1007/BF01868823) 7190193 · DOI
  137. Leibo SP Songsasen N 2002 Cryopreservation of gametes and embryos of non-domestic species. Theriogenology 57 303– 326. (10.1016/s0093-691x(0100673-2) 11775977 · DOI
  138. Li LF Yue H Ma J Guan WJ Ma YH 2009 Establishment and characterization of a fibroblast line from Simmental cattle. Cryobiology 59 63– 68. (10.1016/j.cryobiol.2009.04.009) 19426723 · DOI
  139. Li P Hu H Yang S Tian R Zhang Z Zhang W Ma M Zhu Y Guo X Huang Y 2013 Differentiation of induced pluripotent stem cells into male germ cells in vitro through embryoid body formation and retinoic acid or testosterone induction. BioMed Research International 2013 608728. (10.1155/2013/608728) PMC3591174 23509752 · DOI
  140. Lima GL Luz VB Lunardi FO Souza ALP Peixoto GCX Rodrigues APR Oliveira MF Santos RR Silva AR 2019 Effect of cryoprotectant type and concentration on the vitrification of collared peccary (Pecari tajacu) ovarian tissue. Animal Reproduction Science 205 126– 133. (10.1016/j.anireprosci.2019.04.012) 31047761 · DOI
  141. Lima DBC Silva LDMD Marinari P Comizzoli P 2020 Long-term preservation of testicular tissue integrity and viability using vitrification in the endangered black-footed ferret (Mustela nigripes). Animals 10 1865. (10.3390/ani10101865) PMC7602014 33066219 · DOI
  142. Lindau R Vondra S Spreckels J Solders M Svensson-Arvelund J Berg G Pollheimer J Kaipe H Jenmalm MC Ernerudh J 2021 Decidual stromal cells support tolerance at the human foetal-maternal interface by inducing regulatory M2 macrophages and regulatory T-cells. Journal of Reproductive Immunology 146 103330. (10.1016/j.jri.2021.103330) 34049032 · DOI
  143. Liu C Guo Y Lu T Li X Guan W Ma Y 2014 Establishment and genetic characteristics analysis of in vitro culture a fibroblast cell line derived from Wuzhishan miniature pig. Cryobiology 68 281– 287. (10.1016/j.cryobiol.2014.02.009) 24556363 · DOI
  144. Liu T Dou H Xiang X Li L Li Y Lin L Pang X Zhang Y Chen Y Luan J 2015 Factors determining the efficiency of porcine somatic cell nuclear transfer: data analysis with over 200,000 reconstructed embryos. Cellular Reprogramming 17 463– 471. (10.1089/cell.2015.0037) 26655078 PMC4677548 · DOI
  145. Liu Z Cai Y Wang Y Nie Y Zhang C Xu Y Zhang X Lu Y Wang Z Poo M 2018 Cloning of macaque monkeys by somatic cell nuclear transfer. Cell 172 881.e7– 887.e7. (10.1016/j.cell.2018.01.020) 29395327 · DOI
  146. Locatelli Y Calais L Duffard N Lardic L Monniaux D Piver P Mermillod P Bertoldo MJ 2019 In vitro survival of follicles in prepubertal ewe ovarian cortex cryopreserved by slow freezing or non-equilibrium vitrification. Journal of Assisted Reproduction and Genetics 36 1823– 1835. (10.1007/s10815-019-01532-8) 31376104 PMC6731053 · DOI
  147. Loi P Ptak G Barboni B Fulka Jr J Cappai P Clinton M 2001 Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nature Biotechnology 19 962– 964. (10.1038/nbt1001-962) 11581663 · DOI
  148. Long CR Westhusin ME Golding MC 2014 Reshaping the transcriptional frontier: epigenetics and somatic cell nuclear transfer. Molecular Reproduction and Development 81 183– 193. (10.1002/mrd.22271) 24167064 PMC3953569 · DOI
  149. Lopes CA Alves AM Jewgenow K Báo SN de Figueiredo JR 2016 Cryopreservation of canine ovarian cortex using DMSO or 1,3-propanediol. Theriogenology 86 1165– 1174. (10.1016/j.theriogenology.2016.04.006) 27160447 · DOI
  150. Lopes KRF Praxedes ECG Campos LB Bezerra MB Lima GL Saraiva MVA Silva AR 2018 Vitrification of ovarian tissue of Brazilian North-eastern donkeys (Equus asinus) using different cryoprotectants. Reproduction in Domestic Animals 53 1060– 1067. (10.1111/rda.13203) 29809292 · DOI
  151. López A Ducolomb Y Casas E Retana-Márquez S Betancourt M Casillas F 2021 Effects of porcine immature oocyte vitrification on actin microfilament distribution and chromatin integrity during early embryo development in vitro. Frontiers in Cell and Developmental Biology 9 636765. (10.3389/fcell.2021.636765) PMC8093386 33959606 · DOI
  152. Lu Y West FD Jordan BJ Beckstead RB Jordan ET Stice SL 2015 Generation of avian induced pluripotent stem cells. Methods in Molecular Biology 1330 89– 99. (10.1007/978-1-4939-2848-4_9) 26621592 · DOI
  153. Lucci CM Kacinskis MA Lopes LHR Rumpf R Baoa SN 2004 Effect of different cryoprotectants on the structural preservation of follicles in frozen zebu bovine (Bos indicus) ovarian tissue. Theriogenology 61 1101– 1114. (10.1016/j.theriogenology.2003.06.004) 15036998 · DOI
  154. Lueders I Luther I Scheepers G Van Der Horst G 2012 Improved semen collection method for wild felids: urethral catheterization yields high sperm quality in African lions (Panthera leo). Theriogenology 78 696– 701. (10.1016/j.theriogenology.2012.02.026) 22538007 · DOI
  155. Lujić J Marinović Z Sušnik Bajec S Djurdjevič I Kása E Urbányi B Horváth Á 2017 First successful vitrification of salmonid ovarian tissue. Cryobiology 76 154– 157. (10.1016/j.cryobiol.2017.04.005) 28438562 · DOI
  156. Luvoni GC Pellizzari P 2000 Embryo development in vitro of cat oocytes cryopreserved at different maturation stages. Theriogenology 53 1529– 1540. (10.1016/S0093-691X(0000295-8) 10883841 · DOI
  157. Ma Y Gu M Chen L Shen H Pan Y Pang Y Miao S Tong R Huang H Zhu Y 2021 Recent advances in critical nodes of embryo engineering technology. Theranostics 11 7391– 7424. (10.7150/thno.58799) 34158857 PMC8210615 · DOI
  158. Maclellan LJ Carnevale EM Coutinho Da Silva MA Scoggin CF Bruemmer JE Squires EL 2002 Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology 58 911– 919. (10.1016/s0093-691x(0200920-2) 12212891 · DOI
  159. Macpherson AJ De Agüero MG Ganal-Vonarburg SC 2017 How nutrition and the maternal microbiota shape the neonatal immune system. Nature Reviews: Immunology 17 508– 517. (10.1038/nri.2017.58) 28604736 · DOI · Paper page
  160. Magalhães LC Bhat MH Freitas JLS Melo LM Teixeira DIA Pinto LCA Câmara LMC Duarte JMB & Freitas VJF 2017 The effects of cryopreservation on different passages of fibroblast cell culture in brown brocket deer (Mazama gouazoubira). Biopreservation and Biobanking15 463– 468. (10.1089/bio.2017.0060) 28922611 · DOI
  161. Manoli DS Subramanyam D Carey C Sudin E Van Westerhuyzen JA Bales KL Blelloch R Shah NM 2012 Generation of induced pluripotent stem cells from the prairie vole. PLoS ONE 7 e38119. (10.1371/journal.pone.0038119) PMC3365000 22675440 · DOI
  162. Marchetto MCN Narvaiza I Denli AM Benner C Lazzarini TA Nathanson JL Paquola ACM Desai KN Herai RH Weitzman MD 2013 Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503 525– 529. (10.1038/nature12686) 24153179 PMC4064720 · DOI
  163. Martinez F 2017 Update on fertility preservation from the Barcelona International Society for Fertility Preservation-ESHRE-ASRM 2015 expert meeting: indications, results and future perspectives. Human Reproduction 32 1802– 1811. (10.1093/humrep/dex218) 29117320 PMC5850800 · DOI
  164. Martínez-Fresneda L Castaño C Bóveda P Tesfaye D Schellander K Santiago-Moreno J García-Vázquez FA 2019 Epididymal and ejaculated sperm differ on their response to the cryopreservation and capacitation processes in mouflon (Ovis musimon). Scientific Reports 9 15659. (10.1038/s41598-019-52057-0) PMC6821854 31666633 · DOI
  165. Martin-Wintle MS Kersey DC Wintle NJ Aitken-Palmer C Owen MA Swaisgood RR. 2019 Comprehensive breeding techniques for the giant panda. In Reproductive Sciences in Animal Conservation. pp 275– 308; Eds P Comizzoli, JL Brown & WV Holt Cham: Springer International Publishing. 31471801
  166. Mastromonaco GF Songsasen N 2020 Chapter 7 – Reproductive technologies for the conservation of wildlife and endangered species. In Reproductive Technologies in Animals. Ed Presicce GA Academic Press.
  167. Mestre-Citrinovitz AC Sestelo AJ Ceballos MB Barañao JL Saragüeta P 2016 Isolation of primary fibroblast culture from wildlife: the Panthera onca case to preserve a South American endangered species. Current Protocols in Molecular Biology 116 28.7.1– 28.7.14. (10.1002/cpmb.25) 27723084 · DOI
  168. Mitchell RT Williams SA 2022 A fertile future: fertility preservation special series. Reproduction and Fertility 3 C1– C3. (10.1530/RAF-22-0001) 35350654 PMC8956825 · DOI
  169. Mo X Li N Wu S 2014 Generation and characterization of bat-induced pluripotent stem cells. Theriogenology 82 283– 293. (10.1016/j.theriogenology.2014.04.001) 24853281 PMC7103130 · DOI
  170. Moawad AR Zhu J Choi I Amarnath D Chen W Campbell KH 2013 Production of good-quality blastocyst embryos following IVF of ovine oocytes vitrified at the germinal vesicle stage using a cryoloop. Reproduction, Fertility, and Development 25 1204– 1215. (10.1071/RD12215) 23336581 · DOI
  171. Montfort SL 2014. “ Mayday Mayday Mayday”, the Millennium Ark Is Sinking! In Reproductive Sciences in Animal Conservation, Advances in Experimental Medicine and Biology; W V Holt, JL Brown, P Comizzoli (eds.) 753, Springer Science+Business Media New York. pp 15– 31. (10.1007/978-1-4939-0820-2_2) 25091904 · DOI
  172. Mooney A 2021 The value of ex situ collections for global biodiversity conservation in the wild. PhD Thesis. Trinity College Dublin, School of Natural Sciences.
  173. Moro LN Hiriart MI Buemo C Jarazo J Sestelo A Veraguas D Rodriguez-Alvarez L Salamone DF 2015 Cheetah interspecific SCNT followed by embryo aggregation improves in vitro development but not pluripotent gene expression. Reproduction 150 1– 10. (10.1530/REP-15-0048) 25820926 · DOI
  174. Morrow CJ Penfold LM Wolfe BA 2009 Artificial insemination in deer and non-domestic bovids. Theriogenology 71 149– 165. (10.1016/j.theriogenology.2008.09.001) 18986694 · DOI
  175. Mouttham L Comizzoli P 2016 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 73 187– 195. (10.1016/j.cryobiol.2016.07.013) 27475292 · DOI
  176. Mrowiec P Bugno-Poniewierska M Młodawska W 2021 The perspective of the incompatible of nucleus and mitochondria in interspecies somatic cell nuclear transfer for endangered species. Reproduction in Domestic Animals 56 199– 207. (10.1111/rda.13864) 33190359 · DOI
  177. Na RS Zhao QJ Jin DP Su XH Chen XW Guan WJ Ma YH 2010 Establishment and biological characteristics of Ujumqin sheep fibroblast line. Cytotechnology 62 43– 52. (10.1007/s10616-010-9260-6) 20383581 PMC3303005 · DOI
  178. Nakayama K Chinen S Teshima J Tamada Y Hirabayashi M Hochi S 2020 Silk fibroin sheet multilayer suitable for vitrification of in vitro-matured bovine oocytes. Theriogenology 145 109– 114. (10.1016/j.theriogenology.2020.01.052) 32014616 · DOI
  179. Nowak A Kochan J Świętek E Kij B Prochowska S Witarski W Bugno-Poniewierska M Niżański W 2020 Survivability and developmental competences of domestic cat (Felis catus) oocytes after Cryotech method vitrification. Reproduction in Domestic Animals 55 992– 997. (10.1111/rda.13741) 32516454 · DOI
  180. O’Brien JK Robeck TR 2006 Development of sperm sexing and associated assisted reproductive technology for sex preselection of captive bottlenose dolphins (Tursiops truncatus). Reproduction, Fertility, and Development 18 319– 329. (10.1071/rd05108) 16554007 · DOI
  181. Oh HJ Kim MK Jang G Kim HJ Hong SG Park JE Park K Park C Sohn SH Kim DY 2008 Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology 70 638– 647. (10.1016/j.theriogenology.2008.04.032) 18534672 · DOI
  182. Okita K Nagata N Yamanaka S 2011 Immunogenicity of induced pluripotent stem cells. Circulation Research 109 720– 721. (10.1161/RES.0b013e318232e187) 21921270 · DOI
  183. Okotrub KA Mokrousova VI Amstislavsky SY Surovtsev NV 2018 Lipid droplet phase transition in freezing cat embryos and oocytes probed by Raman spectroscopy. Biophysical Journal 115 577– 587. (10.1016/j.bpj.2018.06.019) 30099990 PMC6084414 · DOI
  184. Ortiz-Escribano N Bogado Pascottini O Woelders H Vandenberghe L De Schauwer C Govaere J Van Den Abbeel E Vullers T Ververs C Roels K 2018 An improved vitrification protocol for equine immature oocytes, resulting in a first live foal. Equine Veterinary Journal 50 391– 397. (10.1111/evj.12747) 28833413 · DOI
  185. Otoi T Yamamoto K Koyama N Suzuki T 1995 In vitro fertilization and development of immature and mature bovine oocytes cryopreserved by ethylene glycol with sucrose. Cryobiology 32 455– 460. (10.1006/cryo.1995.1045) 7587284 · DOI
  186. Penfold LM O’Brien JK 2012 Chapter 78 – Importation of nondomestic ruminant semen for management of zoological populations using artificial insemination. In: Fowler’s Zoo and Wild Animal Medicine: Current Therapy, vol. 7, pp. 604– 611. Eds Miller & Fowler ME Elsevier Inc.
  187. Penfold LM Gillis JD Pye GW Pope EC 2021 Chapter 8 – Quality control practices and prevention of disease transmission in exotic and wild species. In Manual of the International Embryo Technology Society, 5th ed., pp. 8– 13. International Embryo Technology Society.
  188. Peng L Zhou Y Xu W Jiang M Li H Long M Liu W Liu J Zhao X Xiao Y 2019 Generation of stable induced pluripotent stem-like cells from adult zebra fish fibroblasts. International Journal of Biological Sciences 15 2340– 2349. (10.7150/ijbs.34010) 31595152 PMC6775306 · DOI
  189. Peter RE Lin HR Van Der Kraak G 1988 Induced ovulation and spawning of cultured freshwater fish in China: advances in application of GnRH analogues and dopamine antagonists. Aquaculture 74 1– 10. (10.1016/0044-8486(8890080-4) · DOI
  190. Pillai VV Kei TG Reddy SE Das M Abratte C Cheong SH Selvaraj V 2019 Induced pluripotent stem cell generation from bovine somatic cells indicates unmet needs for pluripotency sustenance. Animal Science Journal 90 1149– 1160. (10.1111/asj.13272) 31322312 · DOI
  191. 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. (10.1016/j.theriogenology.2011.10.015) 22153273 · DOI
  192. Poo S Hinkson KM 2019 Applying cryopreservation to anuran conservation biology. Conservation Science and Practice 1 e91. (10.1111/csp2.91) · DOI
  193. 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. (10.1016/j.theriogenology.2014.10.028) 25467768 · DOI
  194. Pothana L Venna NK Devi L Singh A Chatterjee I Goel S 2016 Cryopreservation of adult primate testes. European Journal of Wildlife Research 62 619– 626. (10.1007/s10344-016-1024-y) · DOI
  195. Pothana L Devi L Goel S 2017 Cryopreservation of adult cervid testes. Cryobiology 74 103– 109. (10.1016/j.cryobiol.2016.11.008) 27890704 · DOI
  196. Praxedes ÉCG Lima GL Silva AM Apolinário C Bezerra JAB Souza ALP Oliveira MF Rodrigues APR Silva AR 2017 Characterisation and cryopreservation of the ovarian preantral follicle population from Spix’s yellow-toothed cavies (Galea spixii Wagler, 1831). Reproduction, Fertility and Development 29 594– 602. 28442066
  197. Prentice JR Anzar M 2010 Cryopreservation of Mammalian oocyte for conservation of animal genetics. Veterinary Medicine International 2011 146405. (10.4061/2011/146405) PMC2945659 20886016 · DOI
  198. Pukazhenthi BS Wildt DE 2004 Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reproduction, Fertility, and Development 16 33– 46. (10.10371/RD03076) 14972101 · DOI
  199. Purdy PH 2006 A review on goat sperm cryopreservation. Small Ruminant Research 63 215– 225. (10.1016/j.smallrumres.2005.02.015) · DOI
  200. Purohit GN Meena H Solanki K 2012 Effects of vitrification on immature and in vitro matured, denuded and cumulus compact goat oocytes and their subsequent fertilization. Journal of Reproduction and Infertility 13 53– 59. 23926524 PMC3719371

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Authors
Bolton, R. L., Mooney, A., Pettit, M. T., Bolton, A. E., Morgan, L., Drake, G. J., Appeltant, R., Walker, S. L., Gillis, J. D., & Hvilsom, C.
Affiliations
  • Nature’s SAFE, Chapel Field Stud, Ash Lane, Whitchurch, Shropshire, UK
  • Dublin Zoo, Phoenix Park, Dublin 8, Ireland
  • Gemini Genetics, Chapel Field Stud, Ash Lane, Whitchurch, UK
  • Chester Zoo (GB)
  • John Radcliffe Hospital (GB)
  • South-East Zoo Alliance for Reproduction & Conservation, Yulee, Florida, USA
  • Copenhagen Zoo (DK)
Corresponding author
Bolton, Rhiannon L
ORCID
Venue
Reproduction and Fertility
Publisher
Bioscientifica
Published
2022-07-01
Volume
3
Issue
3
Pages
R121-R146
ISSN
2633-8386 (ISSN-L)
DOI
10.1530/raf-22-0005
PMC
PMC9346332
OpenAlex
W4283742304
Cited by
108
References
317
Citations by year
2026: 27 · 2025: 31 · 2024: 31 · 2023: 17 · 2022: 2
FWCI
3.32
Type
journal article
Language
en
Open access
Licence
Locations
  • Reproduction and Fertility (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • University of Chicago
  • University of Oxford
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Animal Genetics and Reproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords
assisted reproduction, biobanking, cryopreservation, species conservation, threatened species, genetic diversity, biodiversity loss, sixth mass extinction, somatic cell nuclear transfer, amphibians, species prioritization, genomic resources
MeSH terms
Animals, Conservation of Natural Resources, Humans, Male, Mammals, Biological Specimen Banks, Reproductive Techniques, Assisted, Biodiversity, Endangered Species

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