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Potential role of intraspecific and interspecific cloning in the conservation of wild mammals

Published online by Cambridge University Press:  11 June 2019

Alana Azevedo Borges
Affiliation:
Laboratory of Animal Biotechnology, Federal Rural University of Semi-Arid, Mossoró, RN, Brazil
Alexsandra Fernandes Pereira*
Affiliation:
Laboratory of Animal Biotechnology, Federal Rural University of Semi-Arid, Mossoró, RN, Brazil
*
*Address for correspondence: Alexsandra Fernandes Pereira. Laboratory of Animal Biotechnology, Federal Rural University of Semi-Arid, Av. Francisco Mota, 572, Mossoró, RN, 59625-900, Brazil. Tel: +55 84 3317 8361. E-mail address: [email protected]

Summary

Intraspecific and interspecific cloning via somatic cell nuclear transfer (iSCNT) is a biotechnique with great possibilities for wild mammals because it allows the maintenance of biodiversity by recovering species, nuclear reprogramming for the production of pluripotency-induced cells, and studies related to embryonic development. Nevertheless, many areas in cloning, especially those associated with wild mammals, are still in question because of the difficulty in obtaining cytoplasmic donor cells (or cytoplasts). Conversely, donor cell nuclei (or karyoplasts) are widely obtained from the skin of living or post-mortem individuals and often maintained in somatic cell banks. Moreover, the creation of karyoplast–cytoplast complexes by fusion followed by activation and embryo development is one of the most difficult steps that requires further clarification to avoid genetic failures. Although difficult, cloning different species, such as wild carnivores and ungulates, can be successful via iSCNT with embryo development and the birth of offspring. Thus, novel research in the area that contributes to the conservation of biodiversity and knowledge of the physiology of species continues. The present review presents the failures and successes that occurred with the application of the technique in wild mammals, with the goal of helping future work on cloning via iSCNT.

Type
Review Article
Copyright
© Cambridge University Press 2019 

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References

Berg, DK, Li, C, Asher, G, Wells, DN and Oback, B (2007) Red deer cloned from antler stem cells and their differentiated progeny. Biol Reprod 77, 384394.Google Scholar
Borges, AA, Bezerra, FVB, Costa, FN, Queiroz Neta, LB, Santos, MVO, Oliveira, MF, Silva, AR and Pereira, AF (2017a) Histomorphological characterization of collared peccary (Pecari tajacu Linnaeus, 1758) ear integumentary system. Arq Bras Med Vet Zootec 69, 948954.Google Scholar
Borges, AA, Lima, GL, Queiroz Neta, LB, Santos, MVO, Oliveira, MF, Silva, AR and Pereira, AF (2017b) Conservation of somatic tissue derived from collared peccaries (Pecari tajacu Linnaeus, 1758) using direct or solid-surface vitrification techniques. Cytotechnology 69, 643654.Google Scholar
Borges, AA, Lira, GPO, Nascimento, LE, Queiroz Neta, LB, Santos, MVO, Oliveira, MF, Silva, AR and Pereira, AF (2018a) Influence of cryopreservation solution on the in vitro culture of skin tissues derived from collared peccary (Pecari tajacu Linnaeus, 1758) Biopreserv Biobank 16, 7781.Google Scholar
Borges, AA, Queiroz Neta, LB, Santos, MVO, Oliveira, MF, Silva, AR and Pereira, AF (2018b) Combination of ethylene glycol with sucrose increases survival rate after vitrification of somatic tissue of collared peccaries (Pecari tajacu Linnaeus, 1758) Pesq Vet Bras 38, 350356.Google Scholar
Borges, AA, Santos, MVO, Queiroz Neta, LB, Oliveira, MF, Silva, AR and Pereira, AF (2018c) In vitro maturation of collared peccary (Pecari tajacu Linnaeus, 1758) oocytes after different incubation times. Pesq Vet Bras 38, 18631868.Google Scholar
Brahmasani, SR, Yelisetti, UM, Katari, V, Komjeti, S, Lakshmikantan, U, Pawar, RM and Sisinthy, S (2013) Developmental ability after parthenogenetic activation of in vitro matured oocytes collected postmortem from deers. Small Rumin Res 113, 128135.Google Scholar
Do, VH and Taylor-Robinson, A (2014) Somatic cell nuclear transfer in mammals reprogramming mechanism and factors affecting success. Clon Transgen 3, 129.Google Scholar
Fernandez-Gonzalez, L, Hribal, R, Stagegaard, J, Zahmel, J and Jewgenow, K (2015) Production of lion (Panthera leo) blastocysts after in vitro maturation of oocytes and intracytoplasmic sperm injection. Theriogenology 83, 995999.Google Scholar
Folch, J, Cocero, M, Chesné, P, Alabart, J, Domínguez, V, Cognié, Y, Roche, A, Fernández-Arias, A, Martí, J and Sánchez, P (2009) First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71, 10261034.Google Scholar
Goeritz, F, Painer, J, Jewgenow, K, Hermes, R, Rasmussen, K, Dehnhard, M and Hildebrandt, T (2012) Embryo retrieval after hormonal treatment to control ovarian function and non-surgical artificial insemination in African lions (Panthera leo) Reprod Domest Anim 47, 156160.Google Scholar
Gómez, MC, Jenkins, JA, Giraldo, A, Harris, RF, King, A, Dresser, BL and Pope, CE (2003) Nuclear transfer of synchronized African wild cat somatic cells into enucleated domestic cat oocytes. Biol Reprod 69, 10321041.Google Scholar
Gómez, MC, Pope, CE, Giraldo, A, Lyons, LA, Harris, RF, King, AL, Cole, A, Godke, RA and Dresser, BL (2004) Birth of African wild cat cloned kittens born from domestic cats. Cloning Stem Cells 6, 247258.Google Scholar
Gómez, MC, Pope, CE, Kutner, RH, Ricks, DM, Lyons, LA, Ruhe, M, Dumas, C, Lyons, J, López, M and Dresser, BL (2008) Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning Stem Cells 10, 469484.Google Scholar
González-Grajales, LA, Favetta, LA, King, WA and Mastromonaco, GF (2016) Lack of effects of ooplasm transfer on early development of interspecies somatic cell nuclear transfer bison embryos. BMC Dev Biol 16, 36.Google Scholar
Herrick, J, Campbell, M, Levens, G, Moore, T, Benson, K, D’Agostino, J, West, G, Okeson, D, Coke, R and Portacio, S (2010) In vitro fertilization and sperm cryopreservation in the black-footed cat (Felis nigripes) and sand cat (Felis margarita) Biol Reprod 82, 552562.Google Scholar
Howard, J, Lynch, C, Santymire, R, Marinari, P and Wildt, D (2016) Recovery of gene diversity using long‐term cryopreserved spermatozoa and artificial insemination in the endangered black‐footed ferret. Anim Conserv 19, 102111.Google Scholar
Ikumi, S, Sawai, K, Takeuchi, Y, Iwayama, H, Ishikawa, H, Ohsumi, S and Fukui, Y (2004) Interspecies somatic cell nuclear transfer for in vitro production of Antarctic minke whale (Balaenoptera bonaerensis) embryos. Cloning Stem Cells 6, 284293.Google Scholar
Kato, H, Anzai, M, Mitani, T, Morita, M, Nishiyama, Y, Nakao, A, Kondo, K, Lazarev, PA, Ohtani, T and Shibata, Y (2009) Recovery of cell nuclei from 15,000 years old mammoth tissues and its injection into mouse enucleated matured oocytes. Proc Jpn Acad Ser B Phys Biol Sci 85, 240247.Google Scholar
Kim, MK, Jang, G, Oh, HJ, Yuda, F, Kim, HJ, Hwang, WS, Hossein, MS, Kim, JJ, Shin, NS and Kang, SK (2007) Endangered wolves cloned from adult somatic cells. Cloning Stem Cells 9, 130137.Google Scholar
Lanza, RP, Cibelli, JB, Diaz, F, Moraes, CT, Farin, PW, Farin, CE, Hammer, CJ, West, MD and Damiani, P (2000) Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2, 7990.Google Scholar
Lee, B, Wirtu, GG, Damiani, P, Pope, E, Dresser, BL, Hwang, W and Bavister, BD (2003) Blastocyst development after intergeneric nuclear transfer of mountain bongo antelope somatic cells into bovine oocytes. Cloning Stem Cells 5, 2533.Google Scholar
León-Quinto, T, Simon, MA, Cadenas, R, Jones, J, Martinez-Hernandez, FJ, Moreno, JM, Vargas, A, Martinez-Hernandez, FJ and Soria, B (2009) Developing biological resource banks as a supporting tool for wildlife reproduction and conservation: the Iberian lynx bank as a model for other endangered species. Anim Reprod Sci 112, 347361.Google Scholar
León-Quinto, T, Simón, MA, Cadenas, R, Martínez, Á and Serna, A (2014) Different cryopreservation requirements in foetal versus adult skin cells from an endangered mammal, the Iberian lynx (Lynx pardinus) Cryobiology 68, 227233.Google Scholar
Li, Y, Dai, Y, Du, W, Zhao, C, Wang, L, Wang, H, Liu, Y, Li, R and Li, N (2007) In vitro development of yak (Bos grunniens) embryos generated by interspecies nuclear transfer. Anim Reprod Sci 101, 4559.Google Scholar
Liu, Z, Cai, Y, Wang, Y, Nie, Y, Zhang, C, Xu, Y, Zhang, X, Lu, Y, Wang, Z and Poo, M (2018) Cloning of macaque monkeys by somatic cell nuclear transfer. Cell 172, 881887.Google Scholar
Loi, P, Modlinski, J and Ptak, G (2011) Interspecies somatic cell nuclear transfer: a salvage tool seeking first aid. Theriogenology 76, 217228.Google Scholar
Loi, P, Ptak, G, Barboni, B, Fulka, J Jr, Cappai, P and Clinton, M (2001) Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotech 19, 962.Google Scholar
Lorthongpanich, C, Laowtammathron, C, Chan, AWS, Ketudat-Cairns, M and Parnpai, R (2008) Development of interspecies cloned monkey embryos reconstructed with bovine enucleated oocytes. J Reprod Dev 54, 306313.Google Scholar
Macías-García, B, González-Fernández, L, Matilla, E, Hernández, N, Mijares, J, and Sánchez-Margallo, FM (2018) Oocyte holding in the Iberian red deer (Cervus elaphus hispanicus): Effect of initial oocyte quality and epidermal growth factor addition on in vitro maturation. Reprod Domest Anim 53, 243248.Google Scholar
Mestre-Citrinovitz, AC, Sestelo, AJ, Ceballos, MB, Baranao, JL and Saragueta, P (2016) Isolation of primary fibroblast culture from wildlife: the Panthera onca case to preserve a South American endangered species. Curr Protoc Mol Biol 116, 28.7.128.7.14.Google Scholar
Moro, LN, Hiriart, MI, Buemo, C, Jarazo, J, Sestelo, A, Veraguas, D, Rodriguez-Alvarez, L and Salamone, DF (2015) Cheetah interspecific SCNT followed by embryo aggregation improves in vitro development but not pluripotent gene expression. Reproduction 150, 110.Google Scholar
Moulavi, F, Hosseini, SM, Tanhaie-Vash, N, Ostadhosseini, S, Hosseini, SH, Hajinasrollah, M, Asghari, M, Gourabi, H, Shahverdi, A and Vosough, A (2017) Interspecies somatic cell nuclear transfer in Asiatic cheetah using nuclei derived from post-mortem frozen tissue in absence of cryo-protectant and in vitro matured domestic cat oocytes. Theriogenology 90, 197203.Google Scholar
Oh, H, Kim, M, Jang, G, Kim, H, Hong, S, Park, J, Park, K, Park, C, Sohn, S and Kim, DY (2008) Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology 70, 638647.Google Scholar
Pan, X, Zhang, Y, Guo, Z and Wang, F (2014) Development of interspecies nuclear transfer embryos reconstructed with argali (Ovis ammon) somatic cells and sheep ooplasm. Cell Biol Inter 38, 211218.Google Scholar
Pereira, AF and Freitas, VJF (2009) Cloning in ruminants: progress and current perspectives. Rev Bras Reprod Anim 33, 118128.Google Scholar
Pereira, AF, Feltrin, C, Almeida, KC, Carneiro, IS, Avelar, SRG, Alcântara Neto, AS, Sousa, FC, Melo, CHS, Moura, RR, Teixeira, DIA, Bertolini, LR, Freitas, VJF and Bertolini, M (2013) Analysis of factors contributing to the efficiency of the in vitro production of transgenic goat embryos (Capra hircus) by handmade cloning (HMC) Small Rumin Res 109, 163172.Google Scholar
Pereira, AF, Melo, LM, Freitas, VJF and Salamone, DF (2015) Phosphorylated H2AX in parthenogenetically activated, in vitro fertilized and cloned bovine embryos. Zygote 23, 485493.Google Scholar
Pereira, AF, Santos, MLT, Borges, AA, Queiroz Neta, LB, Santos, MVO and Feitosa, AKN (2014) Isolation and characterization of skin-derived donor cells for nuclear transfer. Acta Vet Brasilica 8, 311316.Google Scholar
Pereira, AF, Silva, AR, Lima, GL and Silva, AM (2016) Somatic and gonadal tissue cryopreservation: an alternative tool for the germplasm conservation in wild mammals. In: Melanie Walton (ed.). Germplasm: Characteristics, Diversity and Preservation. Nova Science Publishers, New York, pp. 80117.Google Scholar
Priya, D, Selokar, N, Raja, A, Saini, M, Sahare, A, Nala, N, Palta, P, Chauhan, M, Manik, R and Singla, S (2014) Production of wild buffalo (Bubalus arnee) embryos by interspecies somatic cell nuclear transfer using domestic buffalo (Bubalus bubalis) oocytes. Reprod Dom Anim 49, 343351.Google Scholar
Queiroz Neta, LB, Lira, GPO, Borges, AA Santos, MVO, Silva, MB, Oliveira, LRM, Silva, AR, Oliveira, MF and Pereira, AF (2018) Influence of storage time and nutrient medium on recovery of fibroblast-like cells from refrigerated collared peccary (Pecari tajacu Linnaeus, 1758) skin. In Vitro Cell Dev Biol Anim 54, 486495.Google Scholar
Rao, BS, Mahesh, YU, Lakshmikantan, UR, Suman, K, Charan, KV and Shivaji, S (2010) Developmental competence of oocytes recovered from postmortem ovaries of the endangered Indian blackbuck (Antilope cervicapra). J Reprod Dev 56, 623629.Google Scholar
Rho, GJ, Hahnel, AC and Betteridge, KJ (2001) Comparison of oocyte maturation times and of three methods of sperm preparation for their effects on the production of goat embryos in vitro. Theriogenology 56, 503516.Google Scholar
Ruiz, J, Landeo, L, Mendoza, J, Correa, J, Silva, M and Ratto, MH (2015) In vitro developmental competence of alpaca (Vicugna pacos) and llama (Lama glama) oocytes after parthenogenetic activation. Small Rumin Res 133, 148152.Google Scholar
Saini, M, Selokar, N, Raja, A, Sahare, A, Singla, S, Chauhan, M, Manik, R and Palta, P (2015) Effect of donor cell type on developmental competence, quality, gene expression, and epigenetic status of interspecies cloned embryos produced using cells from wild buffalo and oocytes from domestic buffalo. Theriogenology 84, 101108.Google Scholar
Sansinena, M, Hylan, D, Hebert, K, Denniston, R and Godke, R (2005) Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology 63, 10811091.Google Scholar
Santos, MLT, Borges, AA, Queiroz Neta, LB, Santos, MVO, Oliveira, MF, Silva, AR and Pereira, AF (2016) In vitro culture of somatic cells derived from ear tissue of collared peccary (Pecari tajacu Linnaeus, 1758) in medium with different requirements. Pesq Vet Bras 36, 11941202.Google Scholar
Saragusty, J, Diecke, S, Drukker, M, Durrant, B, Friedrich Ben‐Nun, I, Galli, C, Göritz, F, Hayashi, K, Hermes, R and Holtze, S (2016) Rewinding the process of mammalian extinction. Zool Biol 35, 280292.Google Scholar
Sharma, R, Sharma, H, Ahlawat, S, Aggarwal, R, Vij, P and Tantia, M (2018) First attempt on somatic cell cryopreservation of critically endangered Camelus bactrianus of India. Gene Rep 10, 109115.Google Scholar
Song, J, Hua, S, Song, K and Zhang, Y (2007) Culture, characteristics and chromosome complement of Siberian tiger fibroblasts for nuclear transfer. In Vitro Cell Dev Biol Anim 43, 203209.Google Scholar
Sparman, ML, Tachibana, M and Mitalipov, SM (2010) Cloning of non-human primates: the road “less traveled by”. Int J Dev Biol 54, 1671.Google Scholar
Sukparangsi, W, Bootsri, R, Sikeao, W, Karoon, S and Thongphakdee, A (2018) Establishment of induced pluripotent stem cells from fishing cat and clouded leopard using integration-free method for wildlife conservation. Reprod Fertil Dev 30, 230.Google Scholar
Tulake, K, Yanagawa, Y, Takahashi, Y, Katagiri, S, Higaki, S, Koyama, K, Wang, X and Li, H (2014) Effects of ovarian storage condition on in vitro maturation of Hokkaido sika deer (Cervus nippon yesoensis) oocytes. Jpn J Vet Res 62, 187192.Google Scholar
Wang, L, Peng, T, Zhu, H, Lv, Z, Liu, T, Shuai, Z, Gao, H, Cai, T, Cao, X and Wang, H (2007) In vitro development of reconstructed ibex (Capra ibex) embryos by nuclear transfer using goat (Capra hircus) oocytes. Small Rumin Res 73, 135141.Google Scholar
Wani, NA, Vettical, BS and Hong, SB (2017) First cloned Bactrian camel (Camelus bactrianus) calf produced by interspecies somatic cell nuclear transfer: A step towards preserving the critically endangered wild Bactrian camels. PLoS One 12, e0177800.Google Scholar
Yamochi, T, Kida, Y, Oh, N, Ohta, S, Amano, T, Anzai, M, Kato, H, Kishigami, S, Mitani, T and Matsumoto, K (2013) Development of interspecies cloned embryos reconstructed with rabbit (Oryctolagus cuniculus) oocytes and cynomolgus monkey (Macaca fascicularis) fibroblast cell nuclei. Zygote 21, 358366.Google Scholar
Yelisetti, UM, Komjeti, S, Katari, VC, Sisinthy, S and Brahmasani, SR (2016) Interspecies nuclear transfer using fibroblasts from leopard, tiger, and lion ear piece collected postmortem as donor cells and rabbit oocytes as recipients. In Vitro Cell Dev Biol Anim 52, 632645.Google Scholar
Yin, Y, Tang, L, Zhang, P, Kong, D, Wang, Z, Guan, J and Li, Z (2013) Optimizing the conditions for in vitro maturation and artificial activation of sika deer (Cervus nippon hortulorum) oocytes. Reprod Domest Anim 48, 2732.Google Scholar
Zhao, ZJ, Ouyang, YC, Nan, CL, Lei, ZL, Song, XF, Sun, QY and Chen, DY, (2006) Rabbit oocyte cytoplasm supports development of nuclear transfer embryos derived from the somatic cells of the camel and Tibetan antelope. J Reprod Dev 52, 449459.Google Scholar
Zhu, HY, Kang, JD, Li, S, Jin, JX, Hong, Y, Jin, L, Guo, Q, Gao, QS, Yan, CG and Yin, XJ (2014) Production of rhesus monkey cloned embryos expressing monomeric red fluorescent protein by interspecies somatic cell nuclear transfer. Biochem Biophys Res Commun 6, 3843.Google Scholar