INTERSPECIES SOMATIC CELL NUCLEAR TRANSFER IN WILD FELIDS: A SYSTEMATIC REVIEW AND META-ANALYSIS
Abstract
The aim of this work was to systematically review scientific articles on interspecies somatic cell nuclear transfer (iSCNT) in wild cats using domestic cat oocytes. In addition, two meta-analyses were performed using the Comprehensive Meta-Analysis V4 program to evaluate the effect of iSCNT on embryonic division and blastocyst formation compared to the intraspecies technique with somatic cells and oocytes from domestic cat (SCNTc-c). The meta-analysis was performed using a randomized model and the effect size was determined using the relative risk (RR). Sixteen scientific articles were selected from a total of 248 and 3230 initial references in PubMed and ScienceDirect, respectively. The articles report embryonic cleavage rates of 27.5% to 96.7% and a maximum blastocyst formation rate of 41.5%. Only 2 of the 8 articles obtained live offspring, with an efficiency of approximately 1% of the total number of embryos transferred. The risk of bias of the 10 articles selected for the meta-analysis was low. No significant differences (p>0.05) were found in the embryonic division between the iSCNT and the SCNTc-c. However, a lower (p=0.016; RR=0.4) probability of blastocyst formation was observed in the experimental group of iSCNT compared to SCNTc-c. In conclusion, the bibliography on iSCNT in wild cats is scarce and studies very different species, which makes meta-analyses difficult. Although embryonic division up to the 2-4 cell stage is similar in iSCNT and SCNTc-c, blastocyst formation is less when the somatic cell is from a felid species other than the cat.
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Beyhan, Z., Iager, A. E., & Cibelli, J. B. (2007). Interspecies nuclear transfer: implications for embryonic stem cell biology. Cell Stem Cell, 1(5), 502–512.
Borges, A. A., & Pereira, A. F. (2019). Potential role of intraspecific and interspecific cloning in the conservation of wild mammals. Zygote (Cambridge, England), 27(3), 111–117.
Cordova, A., King, W. A., & Mastromonaco, G. F. (2017). Choosing a culture medium for SCNT and iSCNT reconstructed embryos: from domestic to wildlife species. Journal of Animal Science and Technology, 59, 24.
Folch, J., Cocero, M. J., Chesné, P., Alabart, J. L., Domínguez, V., Cognié, Y., Roche, A., Fernández-Arias, A., Martí, J. I., Sánchez, P., Echegoyen, E., Beckers, J. F., Bonastre, A. S., & Vignon, X. (2009). First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology, 71(6), 1026–1034.
Galli, C., & Lazzari, G. (2021). Current applications of SCNT in advanced breeding and genome editing in livestock. Reproduction, 162(1), 23-32.
Goeritz, F., Painer, J., Jewgenow, K., Hermes, R., Rasmussen, K., Dehnhard, M., & Hildebrandt, T. (2012). Embryo retrieval after hormonal treatment to control ovarian function and non-surgical artificial insemination in African lions (Panthera leo). Reproduction in domestic animals, 47(6), 156–160.
Gómez, M. C., Biancardi, M. N., Jenkins, J. A., Dumas, C., Galiguis, J., Wang, G., & Earle Pope, C. (2012). Scriptaid and 5-aza-2'deoxycytidine enhanced expression of pluripotent genes and in vitro developmental competence in interspecies black-footed cat cloned embryos. Reproduction in Domestic Animals, 47(6), 130-135.
Gómez, M. C., Jenkins, J. A., Giraldo, A., Harris, R. F., King, A., Dresser, B. L., & Pope, C. E. (2003). Nuclear transfer of synchronized African wild cat somatic cells into enucleated domestic cat oocytes. Biology of Reproduction, 69(3), 1032-1041.
Gómez, M. C., Pope, C. E., & Dresser, B. L. (2006). Nuclear transfer in cats and its application. Theriogenology, 66(1), 72-81.
Gómez, M. C., Pope, C. E., Biancardi, M. N., Dumas, C., Galiguis, J., Morris, A. C., Wang, G., & Dresser, B. L. (2011). 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 Reprogramming, 13(4), 315-329.
Gómez, M. C., Pope, C. E., Giraldo, A., Lyons, L. A., Harris, R. F., King, A. L., Cole, A., Godke, R. A., & Dresser, B. L. (2004). Birth of African Wildcat cloned kittens born from domestic cats. Cloning and Stem Cells, 6(3), 247-258.
Gómez, M. C., Pope, C. E., Kutner, R. H., Ricks, D. M., Lyons, L. A., Ruhe, M., Dumas, C., Lyons, J., López, M., Dresser, B. L., & Reiser, J. (2008). Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning and Stem Cells, 10(4), 469-483.
Herrick, J. R., Campbell, M., Levens, G., Moore, T., Benson, K., D'Agostino, J., West, G., Okeson, D. M., Coke, R., Portacio, S. C., Leiske, K., Kreider, C., Polumbo, P. J., & Swanson, W. F. (2010). In vitro fertilization and sperm cryopreservation in the black-footed cat (Felis nigripes) and sand cat (Felis margarita). Biology of reproduction, 82(3), 552–562.
Higgins, J. P. T., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M. J., & Welch, V. A. (2022). Cochrane Handbook for Systematic Reviews of Interventions Version 6.3 (Updated February 2022). Cochrane.
Hoffert, K. A., Anderson, G. B., Wildt, D. E., & Roth, T. L. (1997). Transition from maternal to embryonic control of development in IVM/IVF domestic cat embryos. Molecular reproduction and development, 48(2), 208–215.
Holt, W. V., Pickard, A. R., & Prather, R. S. (2004). Wildlife conservation and reproductive cloning. Reproduction (Cambridge, England), 127(3), 317–324.
Howard, J. G., Lynch, C., Santymire, R. M., Marinari, P. E., & Wildt, D. E. (2016). Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Animal Conservation, 19(2), 102-111.
Imsoonthornruksa, S., Sangmalee, A., Srirattana, K., Parnpai, R., & Ketudat-Cairns, M. (2012). Development of intergeneric and intrageneric somatic cell nuclear transfer (SCNT) cat embryos and the determination of telomere length in cloned offspring. Cell Reprogramming, 14(1), 79-87.
IUCN. (2022). The IUCN Red List of Threatened Species. Version 2022-2. https://www.iucnredlist.org.
Kitiyanant, Y., Saikhun, J., & Pavasuthipaisit, K. (2003). Somatic cell nuclear transfer in domestic cat oocytes treated with IGF-I for in vitro maturation. Theriogenology, 59(8), 1775–1786.
Lee, H. S., Yu, X. F., Bang, J. I., Cho, S. J., Deb, G. K., Kim, B. W., & Kong, I. K. (2010). Enhanced histone acetylation in somatic cells induced by a histone deacetylase inhibitor improved inter-generic cloned leopard cat blastocysts. Theriogenology, 74(8), 1439-1449.
León-Quinto, T., Simón, M. A., Cadenas, R., Jones, J., Martínez-Hernández, F. J., Moreno, J. M., Vargas, A., Martínez, F., & 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. Animal Reproduction Science, 112(3-4), 347-361.
Loi, P., Modlinski, J. A., & Ptak, G. (2011). Interspecies somatic cell nuclear transfer: a salvage tool seeking first aid. Theriogenology, 76(2), 217-228.
Loi, P., Ptak, G., Barboni, B., Fulka, J. J. R., 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.
Mastromonaco, G. F., & King, W. A. (2007). Cloning in companion animal, non-domestic and endangered species: Can the technology become a practical reality? Reproduction, Fertility and Development, 19, 748-758
Memili, E., & First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote (Cambridge, England), 8(1), 87–96.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., Altman, D., Antes, G., Atkins, D., Barbour, V., Barrowman, N., Berlin, J. A., Clark, J., Clarke, M., Cook, D., D’Amico, R., Deeks, J. J., Devereaux, P. J., Dickersin, K., Egger, M., Ernst, E., ... Tugwell, P. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Medicine, 6(7).
Moro, L. N., Hiriart, M. I., Buemo, C., Jarazo, J., Sestelo, A., Veraguas, D., ... & Stover, J. (2015)a. Cheetah interspecific SCNT followed by embryo aggregation improves in vitro development but not pluripotent gene expression. Reproduction, 150(1), 1-10.
Moro, L. N., Jarazo, J., Buemo, C., Hiriart, M. I., Sestelo, A., & Salamone, D. F. (2015)b. Tiger, Bengal and Domestic Cat Embryos Produced by Homospecific and Interspecific Zona-Free Nuclear Transfer. Reproduction in Domestic Animals, 50(5), 849–857.
Moulavi, F., Hosseini, S. M., Tanhaie-Vash, N., Ostadhosseini, S., Hosseini, S. H., Hajinasrollah, M., Asghari MH, Gourabi H, Shahverdi A, Vosough AD., Nasr-Esfahani, M. H. (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, 197-203.
Mrowiec, A., Waleń, M., Łukaszuk, K., & Smorąg, Z. (2020). Mitochondrial DNA Replication Disorders and Cancer: Epigenetic Regulation of MUT-Related Genes in Carcinogenesis. International Journal of Molecular Sciences, 21(7), 2524.
Seaby, R. P., Alexander, B., King, W. A., & Mastromonaco, G. F. (2013). In vitro development of bison embryos using interspecies somatic cell nuclear transfer. Reprod Domest Anim, 48(6), 881–887.
Shahverdi, M., Akbarinejad, V., Dalman, A., Hajinasrollah, M., Vodjgani, M., Tanhaei Vash, N., Nasr-Esfahani, M. H., & Eftekhari-Yazdi, P. (2022). Effect of Mechanical Micro-Vibrations on The Efficiency of Leopard Inter-Species Somatic Cell Nuclear Transfer. Cell Journal, 24(10), 612-619.
Spindler, R. E., Crichton, E. G., Agca, Y., Loskutoff, N., Critser, J., Gardner, D. K., & Wildt, D. E. (2006). Improved felid embryo development by group culture is maintained with heterospecific companions. Theriogenology, 66(1), 82–92.
Takeda, K., Akagi, S., Kaneyama, K., Kojima, T., Takahashi, S., Imai, H., Yamanaka, M., Onishi, A., & Hanada, H. (2003). Proliferation of donor mitochondrial DNA in nuclear transfer calves (Bos taurus) derived from cumulus cells. Molecular Reproduction and Development, 64(4), 429–437.
Thongphakdee, A., Numchaisrika, P., Omsongkram, S., Chatdarong, K., Kamolnorranath, S., Dumnui, S., & Techakumphu, M. (2006). In vitro development of marbled cat embryos derived from interspecies somatic cell nuclear transfer. Reproduction in Domestic Animals, 41(3), 219-226.
Thongphakdee, A., Siriaroonrat, B., Manee-in, S., Klincumhom, N., Kamolnorranath, S., Chatdarong, K., & Techakumphu, M. (2010). Intergeneric somatic cell nucleus transfer in marbled cat and flat-headed cat. Theriogenology, 73(1), 120-128.
Thongphakdee, A., Sukparangsi, W., Comizzoli, P., & Chatdarong, K. (2020). Reproductive biology and biotechnologies in wild felids. Theriogenology, 150, 360-373.
Trounson A. (2001). Nucler transfer in human medicine and animal breeding. Reproduction, fertility, and development, 13(1), 31–39.
Veraguas, D., Aguilera, C., Echeverry, D., Saez-Ruiz, D., Castro, F. O., & Rodriguez-Alvarez, L. (2020). Embryo aggregation allows the production of kodkod (Leopardus guigna) blastocysts after interspecific SCNT. Theriogenology, 158, 148-157.
Wilmut, I., Schnieke, A. E., McWhir, J., Kind, A. J., & Campbell, K. H. S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature, 385(6619), 810-813.
Yamochi, T., Kida, Y., Oh, N., Ohta, S., Amano, T., Anzai, M., ... & Niwa, K. (2013). Development of interspecies cloned embryos reconstructed with rabbit (Oryctolagus cuniculus) oocytes and cynomolgus monkey (Macaca fascicularis) fibroblast cell nuclei. Zygote, 21(4), 358–366.
Yin, X. J., Lee, Y., Lee, H., Kim, N., Kim, L., Shin, H., & Kong, I. (2006)a. 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, 66(2), 275-282.
Yin, X. J., Lee, Y. H., Jin, J. Y., Kim, N. H., & Kong, I. K. (2006)b. Nuclear and microtubule remodeling and in vitro development of nuclear transferred cat oocytes with skin fibroblasts of the domestic cat (Felis silvestris catus) and leopard cat (Prionailurus bengalensis). Animal Reproduction Science, 95(3-4), 307-315.
Zuo, Y., Su, G., Cheng, L., Liu, K., Feng, Y., Wei, Z., Bai, C., Cao, G., & Li, G. (2017). Coexpression analysis identifies nuclear reprogramming barriers of somatic cell nuclear transfer embryos. Oncotarget, 8(39), 65847–65859.
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