Somatic Cells, Stem Cells, and Induced Pluripotent Stem Cells: How Do They Now Contribute to Conservation?

  • Gabriela F. Mastromonaco
  • L. Antonio González-Grajales
  • Melissa Filice
  • Pierre Comizzoli
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 753)


More than a decade has now passed since the birth of the first endangered species produced from an adult somatic cell reprogrammed by somatic cell nuclear transfer. At that time, advances made in domestic and laboratory animal species provided the necessary foundation for attempting cutting-edge technologies on threatened and endangered species. In addition to nuclear transfer, spermatogonial stem cell transplantation and induction of pluripotent stem cells have also been explored. Although many basic scientific questions have been answered and more than 30 wild species have been investigated, very few successes have been reported. The majority of studies document numerous obstacles that still need to be overcome to produce viable gametes or embryos for healthy offspring production. This chapter provides an overview of somatic cell and stem cell technologies in different taxa (mammals, fishes, birds, reptiles and amphibians) and evaluates the potential and impact of these approaches for animal species conservation.


Cell culture Stem cell Cloning Somatic cell nuclear transfer Biobanking 


  1. Anizet MP, Huwe B, Pays A, Picard JJ. Characterization of a new cell line, XL2, obtained from Xenopus laevis and determination of optimal culture conditions. In Vitro. 1981;17:267–74.PubMedGoogle Scholar
  2. Benkeddache D, Bodinier P, Joly T, Berchiche M, Vignon X. Recovery of viable cells from rabbit skin biopsies after storage at -20°C for up to 10 days. Cell Tissue Bank. 2012;13:479–86.PubMedGoogle Scholar
  3. Ben-Nun IF, Montague SC, Houck ML, Tran HT, Garitaonandia I, Leonardo TR, et al. Induced pluripotent stem cells from highly endangered species. Nat Methods. 2011;8:829–31.PubMedGoogle Scholar
  4. Berg DK, Li C, Asher G, Wells DN, Oback B. Red deer cloned from antler stem cells and their differentiated progeny. Biol Reprod. 2007;77:384–94.PubMedGoogle Scholar
  5. Bhuiyan MMU, Suzuki Y, Watanabe H, Lee E, Hirayama H, Matsuoka K, et al. Production of Sei whale (Balaenoptera borealis) cloned embryos by inter- and intra-species somatic cell nuclear transfer. J Reprod Dev. 2010;56:131–9.PubMedGoogle Scholar
  6. Bols NC, Dayeh VR, Lee LEJ, Schirmer K. Use of fish cell lines in the toxicology and ecotoxicology of fish. Piscine cell lines in environmental toxicology. In: Mommsen TP, Moon TW, editors. Biochemistry and molecular biology of fishes, vol. 6. Amsterdam: Elsevier; 2005. p. 43–84.Google Scholar
  7. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. Isolation and multilineage differentiation of bovine bone marrow mesenchymal stem cells. Cell Tissue Res. 2005;319:243–53.PubMedGoogle Scholar
  8. Briggs R, King TJ. Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs. Proc Natl Acad Sci U S A. 1952;38:455–63.PubMedPubMedCentralGoogle Scholar
  9. Briggs R, Signoret J, Humphrey RR. Transplantation of nuclei of various cell types from neurulae of the Mexican axolotl (Ambystoma mexicanum). Dev Biol. 1964;10:233–46.PubMedGoogle Scholar
  10. Bruno J, Reich N, Lucas JJ. Globin synthesis in hybrid cells constructed by transplantation of dormant avian erythrocyte nuclei into enucleated fibroblasts. Mol Cell Biol. 1981;1:1163–76.PubMedPubMedCentralGoogle Scholar
  11. Bubenshchikova E, Kaftanovskaya E, Hattori M, Kinoshita M, Adachi T, Hashimoto H, et al. Nuclear transplants from adult somatic cells generated by a novel method using diploidized eggs as recipients in medaka fish (Oryzias latipes). Cloning Stem Cells. 2008;10:443–52.PubMedGoogle Scholar
  12. Bui HT, Wakayama S, Kishigami S, Kim JH, Van Thuan N, Wakayama T. The cytoplasm of mouse germinal vesicle stage oocytes can enhance somatic cell nuclear reprogramming. Development. 2008;135:3935–45.PubMedGoogle Scholar
  13. Bui HT, Dn K, Kang MH, Oh MH, Park MR, Park WJ, et al. Epigenetic reprogramming in somatic cells induced by extract from germincal vesicle stage pig oocytes. Development. 2012;139:4330–40.PubMedGoogle Scholar
  14. Bui LC, Vignon X, Campion E, Laloy E, Lavergne Y, Ty LV, et al. Use of interspecies nuclear transfer to study the early embryonic development and nuclear activities of the endangered species Pseudoryx nghetinhensis (saola). Theriogenology. 2002;57:427 [abstract].Google Scholar
  15. Campbell KHS, Fisher P, Chen WC, Choi I, Kelly RDW, Lee J-H, et al. Somatic cell nuclear transfer: past, present and future perspectives. Theriogenology. 2007;68:S214–31.PubMedGoogle Scholar
  16. Cecil JT, Nigrelli RF. Cell cultures from marine mammals. J Wildl Dis. 1970;6:494–5.PubMedGoogle Scholar
  17. Chakraborty N, Biswas D, Parker W, Moyer P, Elliott GD. A role for microwave processing in the dry preservation of mammalian cells. Biotechnol Bioeng. 2008;100:782–96.PubMedGoogle Scholar
  18. Chakraborty N, Chang A, Elmoazzen H, Menze MA, Hand SC, Toner M. A spin-drying technique for lyopreservation of mammalian cells. Ann Biomed Eng. 2011;39:1582–91.PubMedGoogle Scholar
  19. Chang C, Lee I, Ye F, Tarantal AF. Comparison of growth and differentiation of fetal and adult rhesus monkey mesenchymal stem cells. Stem Cells Dev. 2006;15:209–20.Google Scholar
  20. Chavatte-Palmer P, Camous S, Jammes H, Le Cleac’h N, Guillomot M, Lee RS. Review: placental perturbations induce the developmental abnormalities often observed in bovine somatic cell nuclear transfer. Placenta. 2012;33(Suppl):S99–104.PubMedGoogle Scholar
  21. Chen D-Y, Wen D-C, Zhang Y-P, Sun Q-Y, Han Z-M, Liu Z-H, et al. Interspecies Implantation and mitochondria fate of panda-rabbit cloned embryos. Biol Reprod. 2002;67:637–42.PubMedGoogle Scholar
  22. Cheng C, Lian W, Hsiao F, Liu I, Lin S, Lee Y, et al. Isolation and characterization of novel murine epiphysis derived mesenchymal stem cells. PLoS One. 2012;7:e36085. doi: 10.1371/journal.pone.0036085.PubMedPubMedCentralGoogle Scholar
  23. Choresca Jr CH, Kang JT, Han JE, Kim JH, Shin SP, Jun JW, et al. Effect of storage media and time on fin explants culture in the goldfish, Carassius auratus. Afr J Biotech. 2012;11:6599–602.Google Scholar
  24. Clarke AG. The Frozen Ark Project: the role of zoos and aquariums in preserving the genetic material of threatened animals. Int Zoo Yb. 2009;43:222–30.Google Scholar
  25. Clark HF, Cohen MM, Karzon DT. Characterization of reptilian cell lines established at incubation temperatures of 23 to 36°. Exp Biol Med. 1970;133:1039–47.Google Scholar
  26. Cummins JM. Mitochondria: potential roles in embryogenesis and nucleocytoplasmic transfer. Hum Reprod Update. 2001;7:217–28.PubMedGoogle Scholar
  27. Das ZC, Gupta MK, Uhm SJ, Lee HT. Lyophilized somatic cells direct embryonic development after whole cell intracytoplasmic injection into pig oocytes. Cryobiology. 2010;61:220–4.PubMedGoogle Scholar
  28. De Robertis EM, Gurdon JB. Gene activation in somatic nuclei after injection into amphibian oocytes. Proc Natl Acad Sci U S A. 1977;74:2470–4.PubMedPubMedCentralGoogle Scholar
  29. Ding X, Wang Y, Zhang D, Wang Y, Guo Z, Zhang Y. Increased pre-implantation development of cloned bovine embryos treated with 5-aza-2’-deoxycytidine and trichostatin A. Theriogenology. 2008;70:622–30.PubMedGoogle Scholar
  30. Dobrinski I, Travis AJ. Germ cell transplantation for the propagation of companion animals, non-domestic and endangered species. Reprod Fertil Dev. 2007;19:732–9.PubMedGoogle Scholar
  31. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Kraus DS, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.PubMedGoogle Scholar
  32. Dominko T, Mitalipova M, Haley B, Beyhan Z, Memili E, McKusick B, et al. Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol Reprod. 1999;60:1496–502.PubMedGoogle Scholar
  33. Duarte MM, Montes de Oca H, Diniz CR, Fortes-Dias CL. Primary culture of venom gland cells from the South American rattlesnake (Crotalus durissus terrificus). Toxicon. 1999;37:1673–82.PubMedGoogle Scholar
  34. Dyce PW, Liu J, Tayade C, Kidder GM, Betts DH, Li J. In vitro and in vivo germ line potential of stem cells derived from newborn mouse skin. PLoS One. 2011a;6:e20339. doi: 10.1371/journal. pone.0020339.
  35. Dyce PW, Shen W, Huynh E, Shao H, Villagómez DA, Kidder GM, et al. Analysis of oocyte-like cells differentiated from porcine fetal skin-derived stem cells. Stem Cells Dev. 2011b;20:809–19.PubMedGoogle Scholar
  36. Dyce PW, Zhu H, Craig J, Li J. Stem cells with multilineage potential derived from porcine skin. Biochem Biophys Res Commun. 2004;316:651–8.PubMedGoogle Scholar
  37. Eagle H. Nutrition needs of mammalian cells in tissue culture. Science. 1955;122:501–4.PubMedGoogle Scholar
  38. Ezaz T, O’Meally D, Quinn AE, Sarre SD, Georges A, Marshall Graves JA. A simple non-invasive protocol to establish primary cell lines from tail and toe explants for cytogenetic studies in Australian dragon lizards (Squamata: Agamidae). Cytotechnology. 2008;58:135–9.PubMedPubMedCentralGoogle Scholar
  39. Fink T, Rasmussen JG, Emmersen J, Fahlman A, Brunberg S, Josefsson J, et al. Adipose-derived stem cells from the brown bear (Ursus arctos) spontaneously undergo chondrogenic and osteogenic differentiation. Stem Cell Res. 2011;7:89–95.PubMedGoogle Scholar
  40. Folch J, Cocero MJ, Chesné P, Alabart JL, Domínguez V, Cognié Y, et al. First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology. 2009;71:1026–34.PubMedGoogle Scholar
  41. Freshney RI. Culture of animal cells: A manual of basic technique. 5th ed. Hoboken, NJ: John Wiley and Sons Inc.; 2005.Google Scholar
  42. Gallien C-L, Aimar C, Guillet F. Nucleocytoplasmic interactions during ontogenesis in individuals obtained by intra- and interspecific nuclear transplantation in the genus Pleurodels (Urodele Amphibian): morphology, analysis of two enzymatic systems (LDH and MDH) and immunity reactions. Dev Biol. 1973;33:154–70.PubMedGoogle Scholar
  43. Gomez MC, Pope CE, Biancardi MN, Dumas C, Galiguis J, Morris AC, et al. Trichostatin A modified histone covalent pattern and enhanced expression of pluripotent genes in interspecies black-footed cat cloned embryos but did not improve in vitro and in vivo viability. Cell Reprogram. 2011;13:315–29.PubMedGoogle Scholar
  44. Gómez MC, Pope CE, Kutner RH, Ricks DM, Lyons LA, Ruhe M, et al. Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning Stem Cells. 2008;4:469–83.Google Scholar
  45. Gómez MC, Pope CE, Lopez M, Dumas C, Giraldo A, Dresser BL. Chromosomal aneuploidy in African wildcat somatic cells and cloned embryos. Cloning Stem Cells. 2006;8:69–78.PubMedGoogle Scholar
  46. Gómez MC, Pope CE, Giraldo A, Lyons LA, Harris RF, King AL, et al. Birth of African wildcat cloned kittens born from domestic cats. Cloning Stem Cells. 2004;6:247–58.PubMedGoogle Scholar
  47. Gómez MC, Jenkins JA, Giraldo A, Harris RF, King A, Dresser BL, et al. Nuclear transfer of synchronized African wild cat somatic cells into enucleated domestic cat oocytes. Biol Reprod. 2003;69:1032–41.PubMedGoogle Scholar
  48. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, et al. Multipotential stem cells from adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci. 1996;16:1091–100.PubMedGoogle Scholar
  49. Grunow B, Noglick S, Kruse C, Gebert M. Isolation of cells from Atlantic sturgeon Acipenser oxyrinchus oxyrinchus and optimization of culture conditions. Aquat Biol. 2011;14:67–75.Google Scholar
  50. Guan W, He X, Li L, Liang H, Zhao Q, Pu Y, et al. Establishment and biological characterization of fibroblast cell line from the Langshan chicken. Cell Prolif. 2010;43:157–63.PubMedGoogle Scholar
  51. Gurdon JB. The transplantation of nuclei between two subspecies of Xenopus laevis. Heredity. 1961;16:305–15.Google Scholar
  52. Gurdon JB, Wilmut I. Nuclear transfer to eggs and oocytes. Cold Spring Harb Perspect Biol. 2011;3:a002659. doi: 10.1101/cshperspect.a002659.PubMedPubMedCentralGoogle Scholar
  53. Hajian M, Hosseini SM, Forouzanfar M, Abedi P, Ostadhosseini S, Hosseini L, et al. “Conservation cloning” of vulnerable Esfahan mouflon (Ovis orientalis isphahanica): in vitro and in vivo studies. Eur J Wildl Res. 2011;57:959–69.Google Scholar
  54. Han JE, Choresca Jr CH, Koo OJ, Oh HJ, Hong SG, Kin JH, et al. Establishment of glass catfish (Kryptopterus bicirrhis) fin-derived cells. Cell Biol Intl Rep. 2011;18(1):e00008. doi: 10.1042/CBR20110002.Google Scholar
  55. Hao Y, Wax D, Zhong Z, Murphy C, Ross JW, Rieke A, et al. Porcine skin-derived stem cells can serve as donor cells for nuclear transfer. Cloning Stem Cells. 2009;11:101–9.PubMedPubMedCentralGoogle Scholar
  56. Hashem MA, Bhandari BP, Kang SK, Lee BC. Cell cycle analysis and interspecies nuclear transfer of in vitro cultured skin fibroblasts of the Siberian tiger (Panthera tigris altaica). Mol Reprod Dev. 2007;74:403–11.PubMedGoogle Scholar
  57. Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338:971–5.PubMedGoogle Scholar
  58. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146:519–32.PubMedGoogle Scholar
  59. Hebert PD, Cywinska A, Ball SL, deWaard JR. Biological identifications through DNA barcodes. Proc Biol Sci. 2003;270:313–21.PubMedPubMedCentralGoogle Scholar
  60. Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y, et al. Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell. 2012;11:715–26.PubMedPubMedCentralGoogle Scholar
  61. Hochedlinger K, Jaenisch R. Nuclear reprogramming and pluripotency. Nature. 2006;441:1061–7.PubMedGoogle Scholar
  62. Hochedlinger K, Jaenisch R. Nuclear transplantation: Lessons from frogs and mice. Curr Opin Cell Biol. 2002;14:741–8.PubMedGoogle Scholar
  63. Hochedlinger K, Plath K. Epigenetic reprogramming and induced pluripotency. Development. 2009;136:509–23.PubMedPubMedCentralGoogle Scholar
  64. Holt WV, Moore HDM. Semen banking – Is it now feasible for captive endangered species? Oryx. 1988;22:172–8.Google Scholar
  65. Holt WV, Pickard AR, Prather RS. Wildlife conservation and reproductive cloning. Reproduction. 2004;127:317–24.PubMedGoogle Scholar
  66. Hong N, Li Z, Hong Y. Fish stem cell cultures. Int J Biol Sci. 2011;7:392–402.PubMedPubMedCentralGoogle Scholar
  67. Houck M. Establishing and cryopreserving cell cultures: procedures developed for the Frozen Zoo®. Biopreserv Biobank. 2012;10:66 [abstract].Google Scholar
  68. Hutton SR, Pevny LH. Isolation, culture, and isolation of progenitor cells from the central nervous system. Cold Spring Harb Protoc. 2008. doi: 10.1101/pdb.prot5077.Google Scholar
  69. Hwang W, Kim K, Kim G, Jin Y, Kim Y, Chung H, et al. Interspecies somatic cell nuclear transfer for the production of endangered Korean tiger (Panthera tigris altaica). Theriogenology. 2001;55:271 [abstract].Google Scholar
  70. Ikumi S, Sawai K, Takeuchi Y, Iwayama H, Ishikawa H, Ohsumi S, et al. Interspecies somatic cell nuclear transfer for in vitro production of Antarctic minke whale (Balaenoptera bonaerensis) embryos. Cloning Stem Cells. 2004;6:284–93.PubMedGoogle Scholar
  71. IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. (
  72. Jeon BG, Coppola G, Perrault SD, Rho GJ, Betts DH, King WA. S-adenosylhomocysteine treatment of adult female fibroblasts alters X-chromosome inactivation and improves in vitro embryo development after somatic cell nuclear transfer. Reproduction. 2008;135:815–26.PubMedGoogle Scholar
  73. Jiang Y, Kelly R, Peters A, Fulka H, Dickinson A, Mitchell DA, et al. Interspecies somatic cell nuclear transfer is dependent on compatible mitochondrial DNA and reprogramming factors. PLoS ONE. 2011;6:e14805. doi: 10.1371/journal.pone.0014805.PubMedPubMedCentralGoogle Scholar
  74. Kenyon L, Moraes CT. Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. Proc Natl Acad Sci U S A. 1997;94:9131–5.PubMedPubMedCentralGoogle Scholar
  75. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V, et al. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature. 2008;454:646–50.PubMedGoogle Scholar
  76. Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, Hwang WS, et al. Endangered wolves cloned from adult somatic cells. Cloning Stem Cells. 2007;9:130–7.PubMedGoogle Scholar
  77. Kjelland ME, Kraemer D. Feathers and post-hatch eggshells: Sources of fibroblast cells for conserving genetic diversity. Avian Biol Res. 2012;5:123–30.Google Scholar
  78. Koch TG, Heerkens T, Thomsen PD, Betts DH. Isolation of mesenchymal stem cells from equine umbilical cord blood. BMC Biotechnol. 2007;7:26. doi: 10.1186/1472-6750-7-26.PubMedPubMedCentralGoogle Scholar
  79. Kumar BM, St. John E, Mackie PM, King WA, Mastromonaco GF. In vitro development of wood bison (Bison bison athabascae) embryos by interspecies somatic cell nuclear transfer. Reprod Fertil Dev. 2009;21:178 [abstract].Google Scholar
  80. Lakra WS, Bhonde RR. Development of a primary cell culture from the caudal fin of an Indian major carp, Labeo rohita (Ham). Asian Fisheries Sci. 1996;9:149–52.Google Scholar
  81. Lakra WS, Goswami M. Development and characterization of a continuous cell line PSCF from Puntius sophore. J Fish Biol. 2011;78:987–1001.PubMedGoogle Scholar
  82. Lakra WS, Goswami M, Rajaswaminathan T, Rathore G. Development and characterization of two new cell lines from common carp, Cyprinus carpio (Linn). Biol Res. 2010;43:385–92.PubMedGoogle Scholar
  83. Lakra WS, Goswami M, Rajaswaminathan T, Joy KP. Development, characterization, conservation and storage of fish cell lines: a review. Fish Physiol Biochem. 2011;37:1–20.PubMedGoogle Scholar
  84. Lannan CN. Fish cell culture: A protocol for quality control. J Tissue Cult Methods. 1994;16:95–8.Google Scholar
  85. Lanza RP, Cibelli JB, Diaz F, Moraes CT, Farin PW, Farin CE, et al. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning. 2000;2:79–90.PubMedGoogle Scholar
  86. Laskey RA. The use of antibiotics in the preparation of amphibian cell cultures from highly contaminated material. J Cell Sci. 1970;7:653–9.PubMedGoogle Scholar
  87. Le Bail P-Y, Depince A, Chenais N, Mahe S, Maisse G, Labbe C. Optimization of somatic cell injection in the perspective of nuclear transfer in goldfish. BMC Dev Biol. 2010;10:64. doi: 10.1186/1471-213X-10-64.PubMedPubMedCentralGoogle Scholar
  88. Lee HS, Yu XF, Bang JI, Cho SJ, Deb GK, Kim BW, et al. Enhanced histone acetylation in somatic cells induced by a histone deacetylase inhibitor improved inter-generic cloned leopard cat blastocysts. Theriogenology. 2010;74:1439–49.PubMedGoogle Scholar
  89. Lee E, Bhuiyan MM, Watanabe H, Matsuoka K, Fujise Y, Ishikawa H, et al. Production of cloned sei whale (Balaenoptera borealis) embryos by interspecies somatic cell nuclear transfer using enucleated pig oocytes. J Vet Sci. 2009;10:285–92.PubMedPubMedCentralGoogle Scholar
  90. Lee B, Wirtu GG, Damiani P, Pope E, Dresser BL, Hwang W, et al. Blastocyst development after intergeneric nuclear transfer of mountain bongo antelope somatic cells into bovine oocytes. Cloning Stem Cells. 2003;5:25–33.PubMedGoogle Scholar
  91. Lee K-Y, Huang H, Ju B, Yang Z, Lin S. Cloned zebrafish by nuclear transfer from long-term cultured cells. Nat Biotechnol. 2002;20:795–9.PubMedGoogle Scholar
  92. Lees CM, Wilcken J. Sustaining the ark: The challenges faced by zoos in maintaining viable populations. Int Zoo Yb. 2009;43:6–18.Google Scholar
  93. León-Quinto T, Simón MA, Sánchez A, Martín F, Soria B. Cryobanking the genetic diversity in the critically endangered Iberian lynx (Lynx pardinus) from skin biopsies. Investigating the cryopreservation and culture ability of highly valuable explants and cells. Cryobiology. 2011;62:145–51.PubMedGoogle Scholar
  94. Li Y, Dai Y, Du W, Zhao C, Wang H, Wang L, et al. Cloned endangered species takin (Budorcas taxicolor) by inter-species nuclear transfer and comparison of the blastocyst development with yak (Bos grunniens) and bovine. Mol Reprod Dev. 2006a;73:189–95.PubMedGoogle Scholar
  95. Li Z, Sun X, Chen J, Liu X, Wisely SM, Zhou Q, et al. Cloned ferrets produced by somatic cell nuclear transfer. Dev Biol. 2006b;293:439–48.PubMedPubMedCentralGoogle Scholar
  96. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature. 2011;471:68–73.PubMedPubMedCentralGoogle Scholar
  97. Liu P-C, Wang C-Y, Lin S-L, Lin C-C, Hung S-W, Chang C-H, et al. Establishment of a soft shell turtle, Pelodiscus sinensis, embryo primary cell culture for studies of soft shell turtle poxvirus-like virus replication and characteristics. Afr J Microbiol Res. 2012;6:960–7.Google Scholar
  98. Liu S-Z, Zhou Z-M, Chen T, Zhang Y-L, Wen D-C, Kou Z-H, et al. Blastocysts produced by nuclear transfer between chicken blastodermal cells and rabbit oocytes. Mol Reprod Dev. 2004;69:296–302.PubMedGoogle Scholar
  99. Loi P, Matsukawa K, Ptak G, Clinton M, Fulka Jr J, Nathan Y, et al. Freeze-dried somatic cells direct embryonic development after nuclear transfer. PLoS One. 2008;3:e2978. doi: 10.1371/journal.pone.0002978.PubMedPubMedCentralGoogle Scholar
  100. Loi P, Beaujean N, Khochbin S, Fulka Jr J, Ptak G. Asymmetric nuclear reprogramming in somatic cell nuclear transfer? Bioessays. 2007;30:66–74.Google Scholar
  101. Loi P, Ptak G, Barboni B, Fulka Jr J, Cappai P, Clinton M. Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotechnol. 2001;19:962–4.PubMedGoogle Scholar
  102. Lu Y, West FD, Jordan BJ, Mumaw JL, Jordan ET, Gallegos-Cardenas A, et al. Avian-induced pluripotent stem cells derived using human reprogramming factors. Stem Cells Dev. 2012;21:394–403.PubMedGoogle Scholar
  103. Luvoni GC, Chigioni S, Beccaglia M. Embryo production in dogs: from in vitro fertilization to cloning. Reprod Domest Anim. 2006;41:286–90.PubMedGoogle Scholar
  104. Mancia A, Spyropoulos DD, McFee WE, Newton DA, Baatz JE. Cryopreservation and in vitro culture of primary cell types from lung tissue of a stranded pygmy sperm whale (Kogia breviceps). Comp Biochem Phys C. 2012;155:136–42.Google Scholar
  105. Manoli DS, Subramanyam D, Carey C, Sudin E, Van Westerhuyzen JA, Bales KL, et al. Generation of induced pluripotent stem cells from the prairie vole. PLoS One. 2012;7:e38119. doi: 10.1371/journal.pone.0038119.PubMedPubMedCentralGoogle Scholar
  106. Mastromonaco GF, Paris MCJ, Krisher RL, Paris DBBP. Consensus discussion on artificial insemination in companion animal, non-domestic and endangered species (CANDES). Embryo Transfer Newsletter. 2011;29(2):10–2.Google Scholar
  107. Mastromonaco GF, King WA. Cloning in companion animal, non-domestic and endangered species: can the technology become a practical reality? Reprod Fertil Dev. 2007;19:748–61.PubMedGoogle Scholar
  108. Mastromonaco GF, Favetta LA, Smith LC, Filion F, King WA. The influence of nuclear content on developmental competence of gaur x cattle hybrid in vitro fertilized and somatic cell nuclear transfer embryos. Biol Reprod. 2007;76:514–23.PubMedGoogle Scholar
  109. Mastromonaco GF, Perrault SD, Betts DH, King WA. Role of chromosome stability and telomere length in the production of viable cell lines for somatic cell nuclear transfer. BMC Dev Biol. 2006;6:41. doi: 10.1186/1471-213X-6-41.PubMedPubMedCentralGoogle Scholar
  110. Mauger P-E, Le Bail PY, Labbé C. Cryobanking of fish somatic cells: optimizations of fin explants culture and fin cell cryopreservation. Comp Biochem Phys B. 2006;144:29–37.Google Scholar
  111. Maya-Soriano MJ, Holt WV, Lloyd RE. Biobanked amphibian samples confirmed to species level using 16S rRNA DNA barcodes. Biopreserv Biobank. 2012;10:22–8.PubMedGoogle Scholar
  112. Minematsu T, Tajima A, Kanai Y. Attempt to produce nuclear transferred primordial germ cells using electrofusion in domestic chicken. Anim Sci J. 2004;75:271–4.Google Scholar
  113. Moore MK, Work TM, Balazs GH, Docherty DE. Preparation, cryopreservation, and growth of cells prepared from the green turtle (Chelonia mydas). Methods Cell Sci. 1997;19:161–8.Google Scholar
  114. Moresco KA, Stallknecht DE, Swayne DE. Evaluation and attempted optimization of avian embryos and cell culture methods for efficient isolation and propagation of low pathogenicity avian influenza virus. Avian Dis. 2010;54:622–6.PubMedGoogle Scholar
  115. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005;14:R47–58.PubMedGoogle Scholar
  116. Na RS, Bai CY, Jin DP, Su XH, Feng BG, Guan WJ, et al. Establishment and biological characteristics of Qingyuan partridge chicken fibroblast line. Poult Sci. 2010;89:1207–16.PubMedGoogle Scholar
  117. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2007;26:101–6.PubMedGoogle Scholar
  118. Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell. 2006;11:125–32.PubMedGoogle Scholar
  119. Nel-Themaat L, Gomez MC, Pope CE, Lopez M, Wirtu G, Jenkins JA, et al. Cloned embryos from semen. Part 2: Intergeneric nuclear transfer of semen-derived eland (Taurotragus oryx) epithelial cells into bovine oocytes. Cloning Stem Cells. 2008;10:161–72.PubMedGoogle Scholar
  120. Nel-Themaat L, Gómez MC, Damiani P, Wirtu G, Bl D, Bondioli KR, et al. Isolation, culture and characterization of somatic cells derived from semen and mild of endangered sheep and eland antelope. Reprod Fertil Dev. 2007;19:576–84.PubMedGoogle Scholar
  121. Ng S-C, Chen N, Yip W-Y, Liow S-L, Tong G-Q, Martelli B, et al. The first cell cycle after transfer of somatic cell nuclei in a non-human primate. Development. 2004;131:2475–84.PubMedGoogle Scholar
  122. Nowak JA, Fuchs E. Isolation and culture of epithelial stem cells. Methods Mol Biol. 2009;482:215–32.PubMedPubMedCentralGoogle Scholar
  123. Oh HT, Kim MK, Jang G, Kim HJ, Hong SG, Park JE, et al. Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology. 2008;70:638–47.PubMedGoogle Scholar
  124. Oh B-C, Kim J-T, Shin N-S, Kwon S-W, Kang S-K, Lee B-C, et al. Production of blastocysts after intergeneric nuclear transfer of goral (Naemorhedus goral) somatic cells into bovine oocytes. J Vet Med Sci. 2006;68:1167–71.PubMedGoogle Scholar
  125. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science. 2008;322:949–52.PubMedGoogle Scholar
  126. Okita K, Ichisaka T, Yamanaka S. Generation of gemline-competent induced pluripotent stem cells. Nature. 2007;448:313–8.PubMedGoogle Scholar
  127. Ono T, Mizutani E, Li C, Wakayama T. Nuclear transfer preserves the nuclear genome of freeze-dried mouse cells. J Reprod Dev. 2008;54:486–91.PubMedGoogle Scholar
  128. Peat JR, Reik W. Incomplete methylation reprogramming in SCNT embryos. Nat Genet. 2012;44:965–6.PubMedGoogle Scholar
  129. Pereira RJ, Napolitano A, Garcia-Pereira FL, Baldo CF, Suhr ST, King LE, et al. Conservation of avian germplasm by xenogeneic transplantation of spermatogonia from sexually mature donors. Stem Cells Dev. 2012. doi: 10.1089/scd.2012.0497.PubMedCentralGoogle Scholar
  130. Peruffo A, Panin M, Suman M, Mazzariol S, Ballarin C, Giurisato M, et al. Research strategies and development possibilities of a marine mammal tissue bank: conservation biology and biomolecular science. In: Isobe T, Nomiyama K, Subramanian A, Tanabe S, editors. Interdisciplinary studies on environmental chemistry, Environmental Specimen Bank: exploring possibilities of setting up ESB’s in developing countries, vol. 4. Tokyo: Terrapub; 2010. p. 87–93.Google Scholar
  131. Petitte JN. Avian germplasm preservation: embryonic stem cells or primordial germ cells? Poultry Sci. 2006;85:237–42.Google Scholar
  132. Portz C, Lopes de Almeida L, Bianco Jr A, Reck H, Franco AC, Canal CW. Comparison of different cell cultures for replication of infectious laryngotracheitis virus from chickens. Acta Sci Vet. 2008;36:101–5.Google Scholar
  133. Prasanna I, Lakra WS, Ogale SN, Bhonde RR. Cell culture from fin explants of endangered golden mahseer, Tor putitora (Hamilton). Curr Sci. 2000;79:93–8.Google Scholar
  134. Rathore G, Kumar G, Rajaswaminathan T, Sood N, Singh V, Abidi R, et al. Primary cell culture from fin explants of Labeo rohita (Ham.). Indian J Fish. 2007;54:93–7.Google Scholar
  135. Rawson D. Fish biobanking: current activies, lessons, and opportunities. Biopreserv Biobank. 2012;10:68 [abstract].Google Scholar
  136. Rideout III WM, Eggan K, Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science. 2001;293:1093–8.PubMedGoogle Scholar
  137. Rolf HJ, Kierdorf U, Kierdorf H, Schulz J, Seymour N, Schliephake H, et al. Localization and characterization of STRO-1+ cells in the deer pedicle and regenerating antler. PLoS One. 2008;3:e2064. doi: 10.1371/journal.pone.0002064.PubMedPubMedCentralGoogle Scholar
  138. Sangalli JR, De Bem TH, Perecin F, Chiaratti MR, Oliveira LJ, de Araujo RR, et al. Treatment of nuclear-donor cells or cloned zygotes with chromatin-modifying agents increases histone acetylation but does not improve full-term development of cloned cattle. Cell Reprogram. 2012;14:235–47.PubMedGoogle Scholar
  139. Sansinena MJ, Hylan D, Hebert K, Denniston RS, Godke RA. Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology. 2005;63:1081–91.PubMedGoogle Scholar
  140. Saragusty J. Genome banking for vertebrates wildlife conservation. In: Katkov I, editor. Current frontiers in cryobiology. Croatia: Intech; 2012. p. 293–368.Google Scholar
  141. Signoret J, David J-C, Lefresne J, Houillon C. Control of DNA ligase molecular forms in nucleocytoplasmic combinations of axolotl and Pleurodeles. Dev Biol. 1983;80:3368–71.Google Scholar
  142. Silva RC, Costa GM, Lacerda SM, Batlouni SR, Soares JM, Avelar GF, et al. Germ cell transplantation in felids: a potential approach to preserving endangered species. J Androl. 2012;33:264–76.PubMedGoogle Scholar
  143. Sinzelle L, Thuret R, Hwang H-Y, Herszberg B, Paillard E, Bronchain OJ, et al. Characterization of a novel Xenopus tropicalis cell line as a model for in vitro studies. Genesis. 2012;50:316–24.PubMedPubMedCentralGoogle Scholar
  144. Slimane Bureau W, Bordignon V, Leveilée C, Smith LC, King WA. Assessment of chromosomal abnormalities in bovine nuclear transfer embryos and in their donor cells. Cloning Stem Cells. 2003;5:123–32.PubMedGoogle Scholar
  145. Srirattana K, Imsoonthornruksa S, Laowtammathron C, Sangmalee A, Tunwattana W, Thongprapai T, et al. Full-term development of gaur-bovine interspecies somatic cell nuclear transfer embryos: effect of trichostatin A treatment. Cell Reprogram. 2012;14:248–57.PubMedGoogle Scholar
  146. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science. 2008;322:945–9.PubMedPubMedCentralGoogle Scholar
  147. Stephenson NG. Effects of temperature on reptilian and other cells. J Embryol Exp Morph. 1966;16:455–67.PubMedGoogle Scholar
  148. Su X, Jin D, Li C, Yue H, Pu Y, Ma Y, et al. Establishment of Big Bone chicken fibroblast cell bank and study of its biological characteristics. Belg J Zool. 2011;141:14–23.Google Scholar
  149. Sun Y-H, Chen S-P, Wang Y-P, Hu W, Zhu Z-Y. Cytoplasmic impact on cross-genus cloned fish derived from transgenic common carp (Cyrprinus carpio) nuclei and goldfish (Carassius auratus) enucleated eggs. Biol Reprod. 2005;72:510–5.PubMedGoogle Scholar
  150. Sweat JM, Dunigan DD, Wright SD. Characterization of kidney epithelial cells from the Florida manatee, Trichechus manatus latirostris. In Vitro Cell Dev Biol Anim. 2001;37:386–94.Google Scholar
  151. Tanaka D, Takahashi A, Takai A, Ohta H, Ueno K. Attempt at cloning high-quality goldfish breed ‘Ranchu’ by fin-cultured cell nuclear transplantation. Zygote. 2010;20:79–85.PubMedGoogle Scholar
  152. Takahashi K, Tanabe K, Ohnuke M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.PubMedGoogle Scholar
  153. Tao Y, Liu J, Zhang Y, Zhang M, Fang J, Han W, et al. Fibroblast cell line establishment, cryopreservation and interspecies embryos reconstruction in red panda (Ailurus fulgens). Zygote. 2009;17:117–24.PubMedGoogle Scholar
  154. Tayfur Tecirlioglu R, Trounson AO. Embryonic stem cells in companion animals (horses, dogs and cats): present status and future prospects. Reprod Fert Dev. 2007;19:740–7.Google Scholar
  155. Thongphakdee A, Siriaroonrat B, Manee-in S, Klincumhom N, Kamolnorranath S, Chatdarong K, et al. Intergeneric somatic cell nucleus transfer in marbled cat and flat-headed cat. Theriogenology. 2010;73:120–8.PubMedGoogle Scholar
  156. Thongphakdee A, Numchaisrika P, Omsongkram S, Chatdarong K, Kamolnorranath S, Dumnui S, et al. In vitro development of marbled cat embryos derived from interspecies somatic cell nuclear transfer. Reprod Dom Anim. 2006;41:219–26.Google Scholar
  157. Till JE, McCulloch EA. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961;14:213–22.PubMedGoogle Scholar
  158. Tilly JL, Telfer EE. Purification of germline stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock? Mol Hum Reprod. 2009;15:393–8.PubMedPubMedCentralGoogle Scholar
  159. Torvar H, Navarrete F, Rodriguez L, Skewes O, Castro FO. Cold storage of biopsies from wild endangered native Chilean species in field conditions and subsequent isolation of primary culture cell lines. In Vitro Cell Dev Biol. 2008;44:309–20.Google Scholar
  160. Travis AJ, Kim Y, Meyers-Wallen V. Development of new stem cell-based technologies for carnivore reproduction research. Reprod Domest Anim. 2009;44 Suppl 2:22–8.PubMedPubMedCentralGoogle Scholar
  161. Tryon RC, Johnson SL. Clonal and lineage analysis of melanocyte stem cells and their progeny in the zebrafish. Methods Mol Biol. 2012;916:181–95.PubMedPubMedCentralGoogle Scholar
  162. Ty LV, Hanh NV, Uoc NT, Duc NG, Thanh NT, Bui LC, et al. Preliminary results of cell cryobanking and embryo production of black bear (Ursus thibetanus) by interspecies somatic cell nuclear transfer. Theriogenology. 2003;59:290 [abstract].Google Scholar
  163. Venegas F, Guillomot M, Vignon X, Servely J-L, Audouard C, Montiel E, et al. Obtaiment of pudu (Pudu pudu) deer embryos by the somatic nuclear transfer technique. Int J Morphol. 2006;24:285–92.Google Scholar
  164. Veprintsev BN, Rott NN. Conserving genetic resources of animal species. Nature. 1979;280:633–4.Google Scholar
  165. Verma R, Holland MK, Temple-Smith P, Verma PJ. Inducing pluripotency in somatic cells from the snow leopard (Panthera uncia), an endangered felid. Theriogenology. 2012;77:220–8.PubMedGoogle Scholar
  166. Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell. 2004;116:639–48.PubMedGoogle Scholar
  167. Wang K, Beyhan Z, Rodriguez RM, Ross PJ, Iager AE, Kaiser GG, et al. Bovine ooplasm partially remodels primate somatic nuclei following somatic cell nuclear transfer. Cloning Stem Cells. 2009;11:187–202.PubMedGoogle Scholar
  168. Wang L, Peng T, Zhu H, Lv Z, Liu T, Shuai Z, et al. In vitro development of reconstructed ibex (Capra ibex) embryos by nuclear transfer using goat (Capra hircus) oocytes. Small Ruminant Res. 2007;73:135–41.Google Scholar
  169. Wani NA, Wernery U, Hassan FAH, Wernery R, Skidmore JA. Production of the first cloned camel by somatic cell nuclear transfer. Biol Reprod. 2010;82:373–9.PubMedGoogle Scholar
  170. Wakamatsu Y. Novel method for the nuclear transfer of adult somatic cells in medaka fish (Oryzias latipes): use of diploidized eggs as recipients. Develop Growth Differ. 2008;50:427–36.Google Scholar
  171. Wen D-C, Bi C-M, Xu Y, Yang C-X, Zhu Z-Y, Sun Q-Y, et al. Hybrid embryos produced by transferring panda or cat somatic nuclei into rabbit MII oocytes can develop to blastocyst in vitro. J Exp Zool Part A. 2005;303A:689–97.Google Scholar
  172. White KL, Bunch TD, Mitalipov S, Reed WA. Establishment of pregnancy after the transfer of nuclear transfer embryos produced from the fusion of argali (Ovis ammon) nuclei into domestic sheep (Ovis aries) enucleated oocytes. Cloning. 1999;1:47–54.PubMedGoogle Scholar
  173. Wildt DE. Genetic resource banks for conserving wildlife species. Justification, examples and becoming organized on a global basis. Anim Reprod Sci. 1992;28:247–57.Google Scholar
  174. Williams JB, Shin T, Liu L, Flores-Foxworth G, Romano J, Blue-McClendon A, et al. Cloning of exotic/endangered species: desert bighorn sheep. Methods Mol Biol. 2006;348:169–82.PubMedGoogle Scholar
  175. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell AH. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997;385:810–3.PubMedGoogle Scholar
  176. Wu DM, Schneiderman T, Burgett J, Gokhale P, Barthel L, Raymond PA. Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retine. Invest Ophthalmol Vis Sci. 2001;42:2115–24.PubMedGoogle Scholar
  177. Xi Y, Nada Y, Soh T, Fujihara N, Hattori M. Establishment of feather follicle stem cells as potential vehicles for delivering exogenous genes in birds. J Reprod Dev. 2003;49:213–9.PubMedGoogle Scholar
  178. Xiong X-R, Wang L-J, Zi X-D, Ma L, Xu W-B, Wang Y-S, et al. Epigenetic reprogramming of yak iSCNT embryos after donor cell pre-treatment with oocyte extracts. Anim Reprod Sci. 2012;133:229–36.PubMedGoogle Scholar
  179. Yan SY, Tu M, Yang HY, Mao ZG, Zhao ZY, Fu LJ, et al. Developmental incompatibility between cell nucleus and cytoplasm as revealed by nuclear transplantation experiments in teleost of different families and orders. Int J Dev Biol. 1990;34:255–66.PubMedGoogle Scholar
  180. Yan SY, Lu DY, Du M, Li GS, Lin LT, Jin GQ, et al. Nuclear transplantation in teleosts. Hybrid fish from the nucleus of crucian and the cytoplasm of carp. Sci Sin B. 1984;27:1029–34.PubMedGoogle Scholar
  181. Yang CX, Han ZM, Wen DC, Sun QY, Zhang KY, Zhang LS, et al. In vitro development and mitochondrial fate of macaca-rabbit cloned embryos. Mol Reprod Dev. 2003;65:396–401.PubMedGoogle Scholar
  182. Yin X, Lee Y, Lee H, Kim N, Kim L, Shin H, et al. In vitro production and initiation of pregnancies in inter-genus nuclear transfer embryos derived from leopard cat (Prionailurus bengalensis) nuclei fused with domestic cat (Felis silverstris catus) enucleated oocytes. Theriogenology. 2006;66:275–82.PubMedGoogle Scholar
  183. Yoshizaki G, Okutsu T, Morita T, Terasawa M, Yazawa R, Takeuchi Y. Biological characteristics of fish germ cells and their application to developmental biotechnology. Reprod Domest Anim. 2012;47 Suppl 4:187–92.PubMedGoogle Scholar
  184. Zeng CJ, Qing YE, Fang SG. Establishment and characterization of liver, heart and muscel cell lines derived from the Chinese alligator (Alligator sinensis). Chinese Sci Bull. 2011;56:2576–9.Google Scholar
  185. Zhao Z-J, Ouyang Y-C, Nan C-L, Lei Z-L, Song X, Sun Q-Y, et al. Rabbit oocyte cytoplasm supports development of nuclear transfer embryos derived from the somatic cells of the camel and Tibetan antelope. J Reprod Dev. 2006;52:449–59.PubMedGoogle Scholar
  186. Zhou Q, Yang SH, Ding CH, He XC, Xie YH, Hildebrandt TB, et al. A comparative approach to somatic cell nuclear transfer in the rhesus monkey. Hum Reprod. 2006;21:2564–71.PubMedGoogle Scholar
  187. Zhu H, Craig JA, Dyce PW, Sunnen N, Li J. Embryos derived from porcine skin-derived stem cells exhibit enhanced preimplantation development. Biol Reprod. 2004;71:1890–7.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Gabriela F. Mastromonaco
    • 1
    • 2
  • L. Antonio González-Grajales
    • 1
    • 2
  • Melissa Filice
    • 1
    • 2
  • Pierre Comizzoli
    • 3
  1. 1.Reproductive Physiology, Toronto ZooTorontoCanada
  2. 2.Department of Biomedical SciencesUniversity of GuelphGuelphCanada
  3. 3.Smithsonian Conservation Biology Institute, National Zoological ParkWashington, DCUSA

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