Mammalian fertility preservation through cryobiology: Value of classical comparative studies and the need for new preservation options

Reproduction, Fertility and Development

Volumn 26, Issue 1, 2014, Pages 91-98

  Comizzoli, Pierre ^a   Wildt, David E ^a  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

Author keywords

Biobanking; Endangered species; Gametes; Gonadal tissues; Long term storage; Universal protocol

Indexed keywords

ANIMAL REPRODUCTIVE PROCEDURES; ARTICLE; CRYOBIOLOGY; CRYOPRESERVATION; ENDANGERED SPECIES; FREEZE THAWING; GAMETE; GERMPLASM; HUMAN; LIVESTOCK; NONHUMAN; OOCYTE; PROGENY; REPRODUCTIVE BEHAVIOR; SEMINAL PLASMA; SPECIES COMPARISON; SPECIES DIFFERENCE; TAXON; TISSUE PRESERVATION; WILDLIFE;

ANIMALS; CRYOPRESERVATION; ENDANGERED SPECIES; FEMALE; FERTILITY; FERTILITY PRESERVATION; HUMANS; MALE; PREGNANCY; REPRODUCTION; SPECIES SPECIFICITY; SPERM BANKS; TIME FACTORS; TISSUE BANKS;

EID: 84889801558     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD13259     Document Type: Article

References (64)

1. Anel, L., Gomes-Alves, S., Alvarez, M., Borragan, S., Anel, E., Nicolas, M., Martinez-Pastor, F., and de Paz, P. (2010). Effect of basic factors of extender composition on post-thawing quality of brown bear electroejaculated spermatozoa. Theriogenology 74, 643-651. doi:10.1016/J.THERIOGENOLOGY.2010.03. 004
2. Arav, A., and Natan, Y. (2009). Directional freezing: a solution to the methodological challenges to preserve large organs. Semin. Reprod. Med. 27, 438-442. doi:10.1055/S-0029-1241052
3. Baker, M. (2012). Biorepositories: building better biobanks. Nature 486, 141-146. doi:10.1038/486141A
4. Cleary, M., Shaw, J. M., Jenkin, G., and Trounson, A. O. (2004). Influence of hormone environment and donor age on cryopreserved common wombat (Vombatus ursinus) ovarian tissue xenografted into nude mice. Reprod. Fertil. Dev. 16, 699-707. doi:10.1071/RD04054
5. Comizzoli, P., and Wildt, D. E. (2012a). On the horizon for fertility preservation in domestic and wild carnivores. Reprod. Domest. Anim. 47(Suppl. 6), 261-265. doi:10.1111/RDA.12010
6. Comizzoli, P., and Wildt, D. E. (2012b). Centrosomal functions and dysfunctions in cat spermatozoa. In 'The Centrosome'. (Ed. H. Schatten.) pp. 49-58. (Humana Press: New York.)
7. Comizzoli, P., Wildt, D. E., and Pukazhenthi, B. S. (2004). Effect of 1,2-propanediol versus 1,2-ethanediol on subsequent oocyte maturation, spindle integrity, fertilization and embryo development in vitro in the domestic cat. Biol. Reprod. 71, 598-604. doi:10.1095/BIOLREPROD. 104.027920
8. Comizzoli, P., Wildt, D. E., and Pukazhenthi, B. S. (2008). Impact of anisosmotic conditions on structural and functional integrity of cumulusoocyte complexes at the germinal vesicle stage in the domestic cat. Mol. Reprod. Dev. 75, 345-354. doi:10.1002/MRD.20769
9. Comizzoli, P., Songsasen, N., and Wildt, D. E. (2010). Protecting and extending fertility for females of wild and endangered mammals. Cancer Treat. Res. 156, 87-100. doi:10.1007/978-1-4419-6518-9-7
10. Comizzoli, P., Songsasen, N., Hagedorn, M., and Wildt, D. E. (2012). Comparative cryobiological traits and requirements for gametes and gonadal tissues collected from wildlife species. Theriogenology 78, 1666-1681. doi:10.1016/J.THERIOGENOLOGY.2012.04.008
11. Critser, J. K., Agca, Y., and Woods, E. (2002). Cryopreservation of immature and mature gametes. In 'Assisted Reproductive Technology: Accomplishment and New Horizons'. (Eds C. J. De Jonge and C. L. R. Barratt.) pp. 144-166. (Cambridge University Press: Cambridge, UK.)
12. Crosier, A. E., Pukazhenthi, B. S., Henghali, J.N., Howard, J., Dickman, A. J., Marker, L., and Wildt, D. E. (2006). Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival. Cryobiology 52, 169-181. doi:10.1016/J.CRYOBIOL.2005.10.011
13. Crowe, J. H., Hoekstra, F. A., and Crowe, L. M. (1992). Anhydrobiosis. Annu. Rev. Physiol. 54, 579-599. doi:10.1146/ANNUREV.PH.54. 030192.003051
14. Ehmcke, J., and Schlatt, S. (2008). Animal models for fertility preservation in the male. Reproduction 136, 717-723. doi:10.1530/REP-08-0093
15. Gilmore, J. A., McGann, L. E., Ashworth, E., Acker, J. P., Raath, J. P., Bush, M., and Critser, J. K. (1998). Fundamental cryobiology of selected African mammalian spermatozoa and its role in biodiversity preservation through the development of genome resource banking. Anim. Reprod. Sci. 53, 277-297. doi:10.1016/S0378-4320(98)00118-3
16. Gosálvez, J., López-Fernández, C., Fernández, J. L., Gouraud, A., and Holt, W. V. (2011). Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol. Reprod. Dev. 78, 951-961. doi:10.1002/MRD.21394
17. Graves-Herring, J. E., Wildt, D. E., and Comizzoli, P. (2013). Retention of structure and function of the cat germinal vesicle after air-drying and storage at suprazero temperature. Biol. Reprod. 88, 139. doi:10.1095/BIOLREPROD. 113.108472
18. Hagedorn, M., Carter, V., Martorana, K., Paresa, M. K., Acker, J., Baums, I. B., Borneman, E. H., Brittsan, M., Byers, M., Henley, M., Laterveer, M., Leong, J. C., McCarthy, M., Meyers, S., Nelson, B. D., Petersen, D., Tiersch, T., Cuevas Uribe, R., and Wildt, D. E. (2012). Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral. PLoS One 7, e33354. doi:10.1371/JOURNAL.PONE.0033354
19. Heo, Y. S., Nagrath, S., Moore, A. L., Malinowska, I., Zenali, M., Kwiatkowski, D., and Toner, M. (2011). Universal vitrification of rare cancer cells from different origins by ultra-fast cooling. Cryobiology 63, 326. doi:10.1016/J.CRYOBIOL.2011.09.076
20. Hermes, R., Göritz, F., Saragusty, J., Sós, E., Molnar, V., Reid, C. E., Schwarzenberger, F., and Hildebrandt, T. B. (2009). First successful artificial insemination with frozen-thawed semen in rhinoceros. Theriogenology 71, 393-399. doi:10.1016/J.THERIOGENOLOGY.2008. 10.008
21. Holt, W. V. (2011). Mechanisms of sperm storage in the female reproductive tract: an interspecies comparison. Reprod. Domest. Anim. 46(Suppl. 2), 68-74. doi:10.1111/J.1439-0531.2011.01862.X
22. Hovatta, O., Foudila, T., Siegberg, R., Johansson, K., von Smitten, K., and Reima, I. (1996). Pregnancy resulting from intracytoplasmic injection of spermatozoa from a frozen-thawed testicular biopsy specimen. Hum. Reprod. 11, 2472-2473. doi:10.1093/OXFORDJOURNALS.HUM REP.A019140
23. Howard, J. G., and Wildt, D. E. (2009). Approaches and efficacy of artificial insemination in felids and mustelids. Theriogenology 71, 130-148. doi:10.1016/J.THERIOGENOLOGY.2008.09.046
24. Huang, Y., Zhang, H., Li, D., Zhang, G., Wei, R., Huang, Z., Zhou, Y., Zhou, Q., Liu, Y., Wildt, D. E., and Hull, V. (2012). Relationship of the estrogen surge and multiple mates to cub paternity in the giant panda (Ailuropoda melanoleuca): implications for optimal timing of copulation or artificial insemination. Biol. Reprod. 87, 112. doi:10.1095/BIOLREPROD.112. 102970
25. Jewgenow, K., Wiedemann, C., Bertelsen, M. F., and Ringleb, J. (2011). Cryopreservation of mammalian ovaries and oocytes. Intl. Zoo. Yrbk 45, 124-132. doi:10.1111/J.1748-1090.2010.00124.X
26. Johnston, S. D., O'Callaghan, P., McGowan, M. R., and Phillips, N. J. (1997). Characteristics of koala (Phascolarctos cinereus adustus) semen collected by artificial vagina. J. Reprod. Fertil. 109, 319-323. doi:10.1530/JRF.0.1090319
27. Kiso, W. K., Brown, J. L., Siewerdt, F., Schmitt, D. L., Olson, D., Crichton, E. G., and Pukazhenthi, B. S. (2011). Liquid semen storage in elephants (Elephas maximus and Loxodonta africana): species differences and storage optimization. J. Androl. 32, 420-431. doi:10.2164/JANDROL. 110.011460
28. Leibo, S. P., and Songsasen, N. (2002). Cryopreservation of gametes and embryos of nondomestic species. Theriogenology 57, 303-326. doi:10.1016/S0093- 691X(01)00673-2
29. Lermen, D., Blömeke, B., Browne, R., Clarke, A., Dyce, P. W., Fixemer, T., Müller, P., Fuhr, G. R., Holt, W. V., Jewgenow, K., Lloyd, R. E., Lötters, S., Paulus, M., Reid, G. M., Rapoport, D. H., Rawson, D., Ringleb, J., Ryder, O. A., Spörl, G., Schmitt, T., Veith, M., and Mueller, P. (2009). Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Mol. Ecol. 18, 1030-1033. doi:10.1111/J.1365-294X. 2008.04062.X
30. Mazur, P., Leibo, S. P., and Seidel, G. E. (2008). Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions. Biol. Reprod. 78, 2-12. doi:10.1095/BIOLREPROD.107.064113
31. McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163-170.
32. Okano, T., Nakamura, S., Komatsu, T., Murase, T., Miyazawa, K., Asano, M., and Tsubota, T. (2006). Characteristics of frozen-thawed spermatozoa cryopreserved with different concentrations of glycerol in captive Japanese black bears (Ursus thibetanus japonicus). J. Vet. Med. Sci. 68, 1101-1104. doi:10.1292/JVMS.68.1101
33. Paris, M. C., Snow, M., Cox, S. L., and Shaw, J. M. (2004). Xenotransplantation: a tool for reproductive biology and animal conservation? Theriogenology 61, 277-291. doi:10.1016/S0093-691X(03)00234-6
34. Pope, C. E., Gómez, M. C., and Dresser, B. L. (2006). In vitro production and transfer of cat embryos in the 21st century. Theriogenology 66, 59-71. doi:10.1016/J.THERIOGENOLOGY.2006.03.014
35. Pukazhenthi, B., Spindler, R., Wildt, D., Bush, L. M., and Howard, J. (2002). Osmotic properties of spermatozoa from felids producing different proportions of pleiomorphisms: influence of adding and removing cryoprotectant. Cryobiology 44, 288-300. doi:10.1016/S0011-2240 (02)00035-4
36. Pukazhenthi, B. S., Lapiana, F., Padilla, L., Santiestevan, J., Coutinho da Silva, M., Alvarenga, M., and Wildt, D. E. (2010). Improved sperm cryopreservation in the critically endangered Przewalski's horse (Equus ferus przewalskii) using different cryoprotectants. Biol. Reprod. 83, 675.
37. Pukazhenthi, B. S., Togna, G. D., Padilla, L., Smith, D., Sanchez, C., Pelican, K., and Sanjur, O. I. (2011). Ejaculate traits and sperm cryopreservation in the endangered Baird's tapir (Tapirus bairdii). J. Androl. 32, 260-270. doi:10.2164/JANDROL.110.011833
38. Robeck, T. R., and O'Brien, J. K. (2004). Effect of cryopreservation methods and precryopreservation storage on bottlenose dolphin (Tursiops truncatus) spermatozoa. Biol. Reprod. 70, 1340-1348. doi:10.1095/BIOLREPROD.103. 025304
39. Robeck, T. R., Gearhart, S. A., Steinman, K. J., Katsumata, E., Loureiro, J. D., and O'Brien, J. K. (2011). In vitro sperm characterization and development of a sperm cryopreservation method using directional solidification in the killer whale (Orcinus orca). Theriogenology 76, 267-279. doi:10.1016/J.THERIOGENOLOGY.2011.02.003
40. Rossato, M., Balercia, G., Lucarelli, G., Foresta, C., and Mantero, F. (2002). Role of seminal osmolarity in the reduction of human sperm motility. Int. J. Androl. 25, 230-235. doi:10.1046/J.1365-2605.2002.00353.X
41. Santymire, R. M., Marinari, P. E., Kreeger, J. S., Wildt, D. E., and Howard, J. (2006). Sperm viability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality. Cryobiology 53, 37-50. doi:10.1016/J.CRYOBIOL.2006.03.009
42. Saragusty, J., and Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1-19. doi:10.1530/REP-10-0236
43. Saragusty, J., Hildebrandt, T. B., Behr, B., Knieriem, A., Kruse, J., and Hermes, R. (2009). Successful cryopreservation of Asian elephant (Elephas maximus) spermatozoa. Anim. Reprod. Sci. 115, 255-266. doi:10.1016/J. ANIREPROSCI.2008.11.010
44. Schiewe, M. C., Bush, M., de Vos, V., and Wildt, D. E. (1991). Semen characteristics, sperm freezing and endocrine profiles in free-ranging wildebeest (Connochaetes taurinus) and greater kudu (Tragelaphus strepsiceros). J. Zoo Wildl. Med. 22, 58-72.
45. Songsasen, N., and Comizzoli, P. (2009). A historic overview of embryos and oocyte preservation in the world of mammalian in vitro fertilization and biotechnology. In 'Preservation of Human Oocytes'. (Eds A. Borini and G. Coticchio.) pp. 1-11. (Informa Healthcare: London.)
46. Songsasen, N., Ratterree, M. S., VandeVoort, C. A., Pegg, D. E., and Leibo, S. P. (2002). Permeability characteristics and osmotic sensitivity of rhesus monkey (Macaca mulatta) oocytes. Hum. Reprod. 17, 1875-1884. doi:10.1093/HUMREP/17.7.1875
47. Songsasen, N., Comizzoli, P., Nagashima, J., Fujihara, M., and Wildt, D. E. (2012). The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro. Reprod. Domest. Anim. 47(Suppl. 6), 13-18. doi:10.1111/RDA.12067
48. Spindler, R. E., Huang, Y., Howard, J. G., Wang, P., Zhang, H., Zhang, G., and Wildt, D. E. (2004). Acrosomal integrity and capacitation are not influenced by sperm cryopreservation in the giant panda. Reproduction 127, 547-556. doi:10.1530/REP.1.00034
49. Stoops, M. A., Bond, J. B., Bateman, H. L., Campbell, M. K., Levens, G. P., Bowsher, T. R., Ferrell, S. T., and Swanson, W. F. (2007). Comparison of different sperm cryopreservation procedures on post-thaw quality and heterologous in vitro fertilisation success in the ocelot (Leopardus pardalis). Reprod. Fertil. Dev. 19, 685-694. doi:10.1071/RD06078
50. Stoops, M. A., Atkinson, M. W., Blumer, E. S., Campbell, M. K., and Roth, T. L. (2010). Semen cryopreservation in the Indian rhinoceros (Rhinoceros unicornis). Theriogenology 73, 1104-1115. doi:10.1016/J.THER IOGENOLOGY.2010.01.011
51. Sturmey, R. G., and Leese, H. J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197-204. doi:10.1530/REP.0. 1260197
52. Tharasanit, T., Manee-In, S., Buarpung, S., Chatdarong, K., Lohachit, C., and Techakumphu, M. (2011). Successful pregnancy following transfer of feline embryos derived from vitrified immature cat oocytes using 'stepwise' cryoprotectant exposure technique. Theriogenology 76, 1442-1449. doi:10.1016/J.THERIOGENOLOGY.2011.06.014
53. Thongtip, N., Mahasawangkul, S., Thitaram, C., Pongsopavijitr, P., Kornkaewrat, K., Pinyopummin, A., Angkawanish, T., Jansittiwate, S., Rungsri, R., Boonprasert, K., Wongkalasin, W., Homkong, P., Dejchaisri, S., Wajjwalku, W., and Saikhun, K. (2009). Successful artificial insemination in the Asian elephant (Elephas maximus) using chilled and frozen-thawed semen. Reprod. Biol. Endocrinol. 7, 75. doi:10.1186/1477-7827-7-75
54. Waimey, K. E., Duncan, F. E., Su, H. I., Smith, K., Wallach, H., Jona, K., Coutifaris, C., Gracia, C. R., Shea, L. D., Brannigan, R. E., Chang, J., Zelinski, M. B., Stouffer, R. L., Taylor, R. L., and Woodruff, T. K. (2013). Future Directions in Oncofertility and Fertility Preservation: a report from the 2011 Oncofertility Consortium Conference. J. Adolesc. Young Adult Oncol. 2, 25-30. doi:10.1089/JAYAO.2012.0035
55. Wildt, D. E., Schiewe, M. C., Schmidt, P.M., Goodrowe, K.L., Howard, J.G., Phillips, L. G., O'Brien, S. J., and Bush, M. (1986). Developing animal model systems for embryo technologies in rare and endangered wildlife. Theriogenology 25, 33-51. doi:10.1016/0093-691X(86)90182-2
56. Wildt, D. E., Bush, M., O'Brien, S. J., Murray, N. D., Taylor, A., and Graves, J. A. (1991). Semen characteristics in free-living koalas (Phascolarctos cinereus). J. Reprod. Fertil. 92, 99-107. doi:10.1530/JRF.0.0920099
57. Wildt, D. E., Rall, W. F., Critser, J. K., Monfort, S. L., and Seal, U. S. (1997). Genome resource banks: 'living collections' for biodiversity conservation. Bioscience 47, 689-698. doi:10.2307/1313209
58. Wildt, D. E., Ellis, S. E., Janssen, D., and Buff, J. (2003). Toward more effective reproductive science in conservation. In 'Reproductive Sciences and Integrated Conservation'. (Eds W. V. Holt, A. Pickard, J. C. Rodger and D. E. Wildt.) pp. 2-20. (Cambridge University Press: Cambridge.)
59. Wildt, D. E., Comizzoli, P., Pukazhenthi, B., and Songsasen, N. (2010). Lessons from biodiversity: the value of nontraditional species to advance reproductive science, conservation, and human health. Mol. Reprod. Dev. 77, 397-409. doi:10.1002/MRD.21137
60. Wolfe, B. A., and Wildt, D. E. (1996). Development to blastocysts of domestic cat oocytes matured and fertilized in vitro after prolonged cold storage. J. Reprod. Fertil. 106, 135-141. doi:10.1530/JRF.0.1060135
61. Woods, E. J., Benson, J. D., Agca, Y., and Critser, J. K. (2004). Fundamental cryobiology of reproductive cells and tissues. Cryobiology 48, 146-156. doi:10.1016/J.CRYOBIOL.2004.03.002
62. Yang, C. R., Miao, D. Q., Zhang, Q. H., Guo, L., Tong, J. S., Wei, Y., Huang, X., Hou, Y., Schatten, H., Liu, Z., and Sun, Q. Y. (2010). Short-term preservation of porcine oocytes in ambient temperature: novel approaches. PLoS One 5, e14242. doi:10.1371/JOURNAL.PONE. 0014242
63. Yavin, S., and Arav, A. (2007). Measurement of essential physical properties of vitrification solutions. Theriogenology 67, 81-89. doi:10.1016/J.THERIOGENOLOGY.2006.09.029
64. Zee, Y. P., Holt, W. V., Gosalvez, J., Allen, C. D., Nicolson, V., Pyne, M., Burridge, M., Carrick, F. N., and Johnston, S. D. (2008). Dimethylacetamide can be used as an alternative to glycerol for the successful cryopreservation of koala (Phascolarctos cinereus) spermatozoa. Reprod. Fertil. Dev. 20, 724-733. doi:10.1071/RD08036