Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0029
Animal Reproduction (AR)
Thematic Section: 37th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Livestock embryonic stem cells for reproductive biotechniques and genetic improvement

Micaela Navarro; Lucia Laiz-Quiroga; Carolina Blüguermann; Adrián Mutto

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Abstract

Embryonic stem cells (ESCs) have proven to be a great in vitro model that faithfully recapitulates the events that occur during in vivo embryogenesis, making them a unique tool to study the cellular and molecular mechanisms that define tissue specification during embryonic development. Livestock ESCs are particularly attractive and have broad prospects including drug selection and human disease modeling, improvement of reproductive biotechniques and agriculture-related applications such as production of genetically modified animals. While mice and human ESCs have been established many years ago, no significant advances were made in livestock species until recently. Nowadays, livestock ESCs are available from cattle, pigs, sheep, horses and rabbits with different states of pluripotency. In this review, we summarize the current advances on livestock ESCs establishment and maintenance along with their present and future applications.

Keywords

embryonic stem cells, genetic engineering, gametogenesis, pluripotency

References

Betters E, Charney RM, García-Castro MI. Electroporation and in vitro culture of early rabbit embryos. Data Brief. 2018;21:316-20. http://doi.org/10.1016/j.dib.2018.09.131. PMid:30364701.

BioRender [Internet]. 2024 [cited 2024 Mar 21]. Available from: https://www.biorender.com/

Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K, Izpisua Belmonte JC, Ross PJ. Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proc Natl Acad Sci USA. 2018;115(9):2090-5. http://doi.org/10.1073/pnas.1716161115. PMid:29440377.

Camargo LSA, Owen JR, Van Eenennaam AL, Ross PJ. Efficient one-step knockout by electroporation of ribonucleoproteins into zona-intact bovine embryos. Front Genet. 2020;11:570069. http://doi.org/10.3389/fgene.2020.570069. PMid:33133156.

Carlson DF, Lancto CA, Zang B, Kim ES, Walton M, Oldeschulte D, Seabury C, Sonstegard TS, Fahrenkrug SC. Production of hornless dairy cattle from genome-edited cell lines. Nat Biotechnol. 2016;34(5):479-81. http://doi.org/10.1038/nbt.3560. PMid:27153274.

Choi K-H, Lee D-K, Kim SW, Woo S-H, Kim D-Y, Lee C-K. Chemically defined media can maintain pig pluripotency network in vitro. Stem Cell Reports. 2019;13(1):221-34. http://doi.org/10.1016/j.stemcr.2019.05.028. PMid:31257130.

Ciccarelli M, Giassetti MI, Miao D, Oatley MJ, Robbins C, Lopez-Biladeau B, Waqas MS, Tibary A, Whitelaw B, Lillico S, Park CH, Park KE, Telugu B, Fan Z, Liu Y, Regouski M, Polejaeva IA, Oatley JM. Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Proc Natl Acad Sci USA. 2020;117(39):24195-204. http://doi.org/10.1073/pnas.2010102117. PMid:32929012.

Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292(5819):154-6. http://doi.org/10.1038/292154a0. PMid:7242681.

Fischer K, Rieblinger B, Hein R, Sfriso R, Zuber J, Fischer A, Klinger B, Liang W, Flisikowski K, Kurome M, Zakhartchenko V, Kessler B, Wolf E, Rieben R, Schwinzer R, Kind A, Schnieke A. Viable pigs after simultaneous inactivation of porcine MHC class I and three xenoreactive antigen genes GGTA1, CMAH and B4GALNT2. Xenotransplantation. 2020;27(1):e12560. http://doi.org/10.1111/xen.12560. PMid:31591751.

Gao X, Nowak-Imialek M, Chen X, Chen D, Herrmann D, Ruan D, Chen ACH, Eckersley-Maslin MA, Ahmad S, Lee YL, Kobayashi T, Ryan D, Zhong J, Zhu J, Wu J, Lan G, Petkov S, Yang J, Antunes L, Campos LS, Fu B, Wang S, Yong Y, Wang X, Xue SG, Ge L, Liu Z, Huang Y, Nie T, Li P, Wu D, Pei D, Zhang Y, Lu L, Yang F, Kimber SJ, Reik W, Zou X, Shang Z, Lai L, Surani A, Tam PPL, Ahmed A, Yeung WSB, Teichmann SA, Niemann H, Liu P. Establishment of porcine and human expanded potential stem cells. Nat Cell Biol. 2019;21(6):687-99. http://doi.org/10.1038/s41556-019-0333-2. PMid:31160711.

Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA. 1980;77(12):7380-4. http://doi.org/10.1073/pnas.77.12.7380. PMid:6261253.

Goszczynski DE, Cheng H, Demyda-Peyrás S, Medrano JF, Wu J, Ross PJ. In vitro breeding: application of embryonic stem cells to animal production. Biol Reprod. 2019;100(4):885-95. http://doi.org/10.1093/biolre/ioy256. PMid:30551176.

Hammer RE, Pursel VG, Rexroad CE Jr, Wall RJ, Bolt DJ, Ebert KM, Palmiter RD, Brinster RL. Production of transgenic rabbits, sheep and pigs by microinjection. Nature. 1985;315(6021):680-3. http://doi.org/10.1038/315680a0. PMid:3892305.

Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M, Hayashi K. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539(7628):299-303. http://doi.org/10.1038/nature20104. PMid:27750280.

Hu ZL, Park CA, Reecy JM. Developmental progress and current status of the Animal QTL. Nucleic Acids Res. 2016;44(D1):D827-33. http://doi.org/10.1093/nar/gkv1233. PMid:26602686.

Hwang YS, Suzuki S, Seita Y, Ito J, Sakata Y, Aso H, Sato K, Hermann BP, Sasaki K. Reconstitution of prospermatogonial specification in vitro from human induced pluripotent stem cells. Nat Commun. 2020;11(1):5656. http://doi.org/10.1038/s41467-020-19350-3. PMid:33168808.

Ideta A, Yamashita S, Seki-Soma M, Yamaguchi R, Chiba S, Komaki H, Ito T, Konishi M, Aoyagi Y, Sendai Y. Generation of exogenous germ cells in the ovaries of sterile NANOS3-null beef cattle. Sci Rep. 2016;6(1):24983. http://doi.org/10.1038/srep24983. PMid:27117862.

Kinoshita M, Kobayashi T, Planells B, Klisch D, Spindlow D, Masaki H, Bornelöv S, Stirparo GG, Matsunari H, Uchikura A, Lamas-Toranzo I, Nichols J, Nakauchi H, Nagashima H, Alberio R, Smith A. Pluripotent stem cells related to embryonic disc exhibit common self-renewal requirements in diverse livestock species. Development. 2021;148(23):dev199901. http://doi.org/10.1242/dev.199901. PMid:34874452.

Kobayashi T, Castillo-Venzor A, Penfold CA, Morgan M, Mizuno N, Tang WWC, Osada Y, Hirao M, Yoshida F, Sato H, Nakauchi H, Hirabayashi M, Surani MA. Tracing the emergence of primordial germ cells from bilaminar disc rabbit embryos and pluripotent stem cells. Cell Rep. 2021;37(2):109812. http://doi.org/10.1016/j.celrep.2021.109812. PMid:34644585.

Kobayashi T, Yamaguchi T, Hamanaka S, Kato-Itoh M, Yamazaki Y, Ibata M, Sato H, Lee YS, Usui J, Knisely AS, Hirabayashi M, Nakauchi H. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell. 2010;142(5):787-99. http://doi.org/10.1016/j.cell.2010.07.039. PMid:20813264.

Kogasaka Y, Murakami S, Yamashita S, Kimura D, Furumoto Y, Iguchi K, Sendai Y. Generation of germ cell-deficient pigs by NANOS3 knockout. J Reprod Dev. 2022;68(6):361-8. http://doi.org/10.1262/jrd.2022-028. PMid:36273893.

Li N, Ma W, Shen Q, Zhang M, Du Z, Wu C, Niu B, Liu W, Hua J. Reconstitution of male germline cell specification from mouse embryonic stem cells using defined factors in vitro. Cell Death Differ. 2019;26(10):2115-24. http://doi.org/10.1038/s41418-019-0280-2. PMid:30683919.

Li S, Edlinger M, Saalfrank A, Flisikowski K, Tschukes A, Kurome M, Zakhartchenko V, Kessler B, Saur D, Kind A, Wolf E, Schnieke A, Flisikowska T. Viable pigs with a conditionally-activated oncogenic KRAS mutation. Transgenic Res. 2015;24(3):509-17. http://doi.org/10.1007/s11248-015-9866-8. PMid:25716163.

Mahdi AK, Medrano JF, Ross PJ. Single-step genome editing of small ruminant embryos by electroporation. Int J Mol Sci. 2022;23(18):10218. http://doi.org/10.3390/ijms231810218. PMid:36142132.

Mueller ML, McNabb BR, Owen JR, Hennig SL, Ledesma AV, Angove ML, Conley AJ, Ross PJ, van Eenennaam AL. Germline ablation achieved via CRISPR/Cas9 targeting of NANOS3 in bovine zygotes. Front Genome Ed. 2023;5:1321243. http://doi.org/10.3389/fgeed.2023.1321243. PMid:38089499.

Navarro M, Soto DA, Pinzon CA, Wu J, Ross PJ. Livestock pluripotency is finally captured in vitro. Reprod Fertil Dev. 2020;32(2):11-39. http://doi.org/10.1071/RD19272. PMid:32188555.

Navarro M, Halstead MM, Rincon G, Mutto A, Ross PJ. bESCs from cloned embryos do not retain transcriptomic or epigenetic memory from somatic donor cells. Reproduction. 2022;164(5):243-57. http://doi.org/10.1530/REP-22-0063. PMid:35951478.

Nichols J, Smith A. Naive and primed pluripotent states. Cell Stem Cell. 2009;4(6):487-92. http://doi.org/10.1016/j.stem.2009.05.015. PMid:19497275.

Niemann H, Kues WA. Transgenic farm animals: an update. Reprod Fertil Dev. 2007;19(6):762-70. http://doi.org/10.1071/RD07040. PMid:17714630.

Park C-H, Jeoung Y-H, Yeddula SGR, Read R, Telugu B. Depletion of NANOS3 causes germ cells loss in pig fetal gonads of both sexes. Reprod Fertil Dev. 2022;35:166. http://doi.org/10.1071/RDv35n2Ab80.

Park KE, Kaucher AV, Powell A, Waqas MS, Sandmaier SES, Oatley MJ, Park CH, Tibary A, Donovan DM, Blomberg LA, Lillico SG, Whitelaw CBA, Mileham A, Telugu BP, Oatley JM. Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep. 2017;7(1):40176. http://doi.org/10.1038/srep40176. PMid:28071690.

Pieri NCG, de Souza AF, Botigelli RC, Pessôa LVF, Recchia K, Machado LS, Glória MH, Castro RVG, Leal DF, Fantinato P No, Martins SMMK, Martins DS, Bressan FF, Andrade AFC. Porcine primordial germ cell-like cells generated from induced pluripotent stem cells under different culture conditions. Stem Cell Rev Rep. 2022;18(5):1639-56. http://doi.org/10.1007/s12015-021-10198-8. PMid:34115317.

Rieblinger B, Fischer K, Kind A, Saller BS, Baars W, Schuster M, Wolf-van Buerck L, Schäffler A, Flisikowska T, Kurome M, Zakhartchenko V, Kessler B, Flisikowski K, Wolf E, Seissler J, Schwinzer R, Schnieke A. Strong xenoprotective function by single-copy transgenes placed sequentially at a permissive locus. Xenotransplantation. 2018;25(2):e12382. http://doi.org/10.1111/xen.12382. PMid:29359453.

Saeki K, Matsumoto K, Kinoshita M, Suzuki I, Tasaka Y, Kano K, Taguchi Y, Mikami K, Hirabayashi M, Kashiwazaki N, Hosoi Y, Murata N, Iritani A. Functional expression of a Delta12 fatty acid desaturase gene from spinach in transgenic pigs. Proc Natl Acad Sci USA. 2004;101(17):6361-6. http://doi.org/10.1073/pnas.0308111101. PMid:15067141.

Shirasawa A, Hayashi M, Shono M, Ideta A, Yoshino T, Hayashi K. Efficient derivation of embryonic stem cells and primordial germ cell-like cells in cattle. J Reprod Dev. 2024;70(2):82-7. http://doi.org/10.1262/jrd.2023-087. PMid:38355134.

Soto DA, Navarro M, Zheng C, Halstead MM, Zhou C, Guiltinan C, Wu J, Ross PJ. Simplification of culture conditions and feeder-free expansion of bovine embryonic stem cells. Sci Rep. 2021;11(1):11045. http://doi.org/10.1038/s41598-021-90422-0. PMid:34040070.

Templeton NS, Roberts DD, Safer B. Efficient gene targeting in mouse embryonic stem cells. Gene Ther. 1997;4(7):700-9. http://doi.org/10.1038/sj.gt.3300457. PMid:9282171.

Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282(5391):1145-7. http://doi.org/10.1126/science.282.5391.1145. PMid:9804556.

Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA. 1995;92(17):7844-8. http://doi.org/10.1073/pnas.92.17.7844. PMid:7544005.

Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y. Conserved role of nanos proteins in germ cell development. Science. 2003;301(5637):1239-41. http://doi.org/10.1126/science.1085222. PMid:12947200.

Vilarino M, Rashid ST, Suchy FP, McNabb BR, Van Der Meulen T, Fine EJ, Ahsan S, Mursaliyev N, Sebastiano V, Diab SS, Huising MO, Nakauchi H, Ross PJ. CRISPR/Cas9 microinjection in oocytes disables pancreas development in sheep. Sci Rep. 2017;7(1):17472. http://doi.org/10.1038/s41598-017-17805-0. PMid:29234093.

Vilarino M, Soto DA, Bogliotti YS, Yu L, Zhang Y, Wang C, Paulson E, Zhong C, Jin M, Belmonte JCI, Wu J, Ross PJ. Derivation of sheep embryonic stem cells under optimized conditions. Reproduction. 2020;160(5):761-72. http://doi.org/10.1530/REP-19-0606. PMid:33065542.

Wall RJ, Powell AM, Paape MJ, Kerr DE, Bannerman DD, Pursel VG, Wells KD, Talbot N, Hawk HW. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat Biotechnol. 2005;23(4):445-51. http://doi.org/10.1038/nbt1078. PMid:15806099.

Wang J, Ren J, Wang Q, Li C, Han Z, Chen T, Sun K, Feng G, Zhang Y, Han J, Zhou Q, Li W, Yu D, Hai T. Nanos3 knockout pigs to model transplantation and reconstruction of the germline. Cell Prolif. 2023;56(5):e13463. http://doi.org/10.1111/cpr.13463. PMid:37094948.

Wilmut I, Bai Y, Taylor J. Somatic cell nuclear transfer: origins, the present position and future opportunities. Philos Trans R Soc Lond B Biol Sci. 2015;370(1680):20140366. http://doi.org/10.1098/rstb.2014.0366. PMid:26416677.

Xiang J, Wang H, Zhang Y, Wang J, Liu F, Han X, Lu Z, Li C, Li Z, Gao Y, Tian Y, Wang Y, Li X. LCDM medium supports the derivation of bovine extended pluripotent stem cells with embryonic and extraembryonic potency in bovine–mouse chimeras from iPSCs and bovine fetal fibroblasts. FEBS J. 2021;288(14):4394-411. http://doi.org/10.1111/febs.15744. PMid:33524211.

Yamashiro C, Sasaki K, Yabuta Y, Kojima Y, Nakamura T, Okamoto I, Yokobayashi S, Murase Y, Ishikura Y, Shirane K, Sasaki H, Yamamoto T, Saitou M. Generation of human oogonia from induced pluripotent stem cells in vitro. Science. 2018;362(6412):356-60. http://doi.org/10.1126/science.aat1674. PMid:30237246.

Yang J, Ryan DJ, Wang W, Tsang JC-H, Lan G, Masaki H, Gao X, Antunes L, Yu Y, Zhu Z, Wang J, Kolodziejczyk AA, Campos LS, Wang C, Yang F, Zhong Z, Fu B, Eckersley-Maslin MA, Woods M, Tanaka Y, Chen X, Wilkinson AC, Bussell J, White J, Ramirez-Solis R, Reik W, Göttgens B, Teichmann SA, Tam PPL, Nakauchi H, Zou X, Lu L, Liu P. Establishment of mouse expanded potential stem cells. Nature. 2017a;550(7676):393-7. http://doi.org/10.1038/nature24052. PMid:29019987.

Yang Y, Liu B, Xu J, Wang J, Wu J, Shi C, Xu Y, Dong J, Wang C, Lai W, Zhu J, Xiong L, Zhu D, Li X, Yang W, Yamauchi T, Sugawara A, Li Z, Sun F, Li X, Li C, He A, Du Y, Wang T, Zhao C, Li H, Chi X, Zhang H, Liu Y, Li C, Duo S, Yin M, Shen H, Belmonte JCI, Deng H. Derivation of pluripotent stem cells with in vivo embryonic and extraembryonic potency. Cell. 2017b;169(2):243-57.e25. http://doi.org/10.1016/j.cell.2017.02.005. PMid:28388409.

Yu L, Wei Y, Sun HX, Mahdi AK, Pinzon Arteaga CA, Sakurai M, Schmitz DA, Zheng C, Ballard ED, Li J, Tanaka N, Kohara A, Okamura D, Mutto AA, Gu Y, Ross PJ, Wu J. Derivation of intermediate pluripotent stem cells amenable to primordial germ cell specification. Cell Stem Cell. 2021;28(3):550-67.e12. http://doi.org/10.1016/j.stem.2020.11.003. PMid:33271070.

Zhao L, Gao X, Zheng Y, Wang Z, Zhao G, Ren J, Zhang J, Wu J, Wu B, Chen Y, Sun W, Li Y, Su J, Ding Y, Gao Y, Liu M, Bai X, Sun L, Cao G, Tang F, Bao S, Liu P, Li X. Establishment of bovine expanded potential stem cells. Proc Natl Acad Sci USA. 2021;118(15):e2018505118. http://doi.org/10.1073/pnas.2018505118. PMid:33833056.

Zhi M, Zhang J, Tang Q, Yu D, Gao S, Gao D, Liu P, Guo J, Hai T, Gao J, Cao S, Zhao Z, Li C, Weng X, He M, Chen T, Wang Y, Long K, Jiao D, Li G, Zhang J, Liu Y, Lin Y, Pang D, Zhu Q, Chen N, Huang J, Chen X, Yao Y, Yang J, Xie Z, Huang X, Liu M, Zhang R, Li Q, Miao Y, Tian J, Huang X, Ouyang H, Liu B, Xie W, Zhou Q, Wei H, Liu Z, Zheng C, Li M, Han J. Generation and characterization of stable pig pregastrulation epiblast stem cell lines. Cell Res. 2022;32(4):383-400. http://doi.org/10.1038/s41422-021-00592-9. PMid:34848870.
 


Submitted date:
03/21/2024

Accepted date:
05/27/2024

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