Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0030
Animal Reproduction (AR)
Thematic Section: 37th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Haploid embryos and embryonic stem cells to produce offspring with predetermined parental genomes in cattle

Lawrence Charles Smith; Luis Aguila Paredes; Rafael Vilar Sampaio; Ricardo Perecin Nociti; Jacinthe Therrien; Flavio Vieira Meirelles

Downloads: 0
Views: 141

Abstract

Selection strategies are performed post-fertilization when the random combination of paternal and maternal genomes has already occurred. It would be greatly advantageous to eliminate meiotic uncertainty by selecting genetically superior gametes before fertilization. To achieve this goal, haploid embryonic cells and embryonic stem cell lineages could be derived, genotyped, and used to substitute gametes. On the paternal side, androgenetic development can be achieved by removing the maternal chromosomes from the oocyte before or after fertilization. We have shown that once developed into an embryo, haploid cells can be removed for genotyping and, if carrying the selected genome, be used to replace sperm at fertilization. A similar strategy can be used on the maternal side by activating the oocyte parthenogenetically and using some embryonic cells for genotyping while the remaining are used to produce diploid embryos by fertilization. Placed together, both androgenetic and parthenogenetic haploid cells that have been genotyped to identify optimal genomes can be used to produce offspring with predetermined genomes. Successes and problems in developing such a breeding platform to achieve this goal are described and discussed below.

Keywords

genomics, haploid, embryo, embryonic stem cells, bovine

References

Aguila L, Nociti RP, Sampaio RV, Therrien J, Meirelles FV, Felmer RN, Smith LC. Haploid androgenetic development of bovine embryos reveals imbalanced WNT signaling and impaired cell fate differentiationdagger. Biol Reprod. 2023;109(6):821-38. http://doi.org/10.1093/biolre/ioad124. PMid:37788061.

Aguila L, Suzuki J, Hill ABT, Garcia M, Mattos K, Therrien J, Smith LC. Dysregulated gene expression of imprinted and x-linked genes: a link to poor development of bovine haploid androgenetic embryos. Front Cell Dev Biol. 2021;9:640712. http://doi.org/10.3389/fcell.2021.640712. PMid:33869192.

Gibbs RA, Taylor JF, Van Tassell CP, Barendse W, Eversole KA, Gill CA, Green RD, Hamernik DL, Kappes SM, Lien S, Matukumalli LK, McEwan JC, Nazareth LV, Schnabel RD, Weinstock GM, Wheeler DA, Ajmone-Marsan P, Boettcher PJ, Caetano AR, Garcia JF, Hanotte O, Mariani P, Skow LC, Sonstegard TS, Williams JL, Diallo B, Hailemariam L, Martinez ML, Morris CA, Silva LO, Spelman RJ, Mulatu W, Zhao K, Abbey CA, Agaba M, Araujo FR, Bunch RJ, Burton J, Gorni C, Olivier H, Harrison BE, Luff B, Machado MA, Mwakaya J, Plastow G, Sim W, Smith T, Thomas MB, Valentini A, Williams P, Womack J, Woolliams JA, Liu Y, Qin X, Worley KC, Gao C, Jiang H, Moore SS, Ren Y, Song XZ, Bustamante CD, Hernandez RD, Muzny DM, Patil S, San Lucas A, Fu Q, Kent MP, Vega R, Matukumalli A, McWilliam S, Sclep G, Bryc K, Choi J, Gao H, Grefenstette JJ, Murdoch B, Stella A, Villa-Angulo R, Wright M, Aerts J, Jann O, Negrini R, Goddard ME, Hayes BJ, Bradley DG, Barbosa da Silva M, Lau LP, Liu GE, Lynn DJ, Panzitta F, Dodds KG. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science. 2009;324(5926):528-32. http://doi.org/10.1126/science.1167936. PMid:19390050.

Cao S, Wang F, Chen Z, Liu Z, Mei C, Wu H, Huang J, Li C, Zhou L, Liu L. Isolation and culture of primary bovine embryonic stem cell colonies by a novel method. J Exp Zool Part A Ecol Genet Physiol. 2009;311(5):368-76. http://doi.org/10.1002/jez.535. PMid:19340839.

Cheng WM, Sun XL, An L, Zhu SE, Li XH, Li Y, Tian JH. Effect of different parthenogenetic activation methods on the developmental competence of in vitro matured porcine oocytes. Anim Biotechnol. 2007;18(2):131-41. http://doi.org/10.1080/10495390601096148. PMid:17453653.

Cibelli JB, Grant KA, Chapman KB, Cunniff K, Worst T, Green HL, Walker SJ, Gutin PH, Vilner L, Tabar V, Dominko T, Kane J, Wettstein PJ, Lanza RP, Studer L, Vrana KE, West MD. Parthenogenetic stem cells in nonhuman primates. Science. 2002;295(5556):819. http://doi.org/10.1126/science.1065637. PMid:11823632.

Elling U, Taubenschmid J, Wirnsberger G, O’Malley R, Demers SP, Vanhaelen Q, Shukalyuk AI, Schmauss G, Schramek D, Schnuetgen F, von Melchner H, Ecker JR, Stanford WL, Zuber J, Stark A, Penninger JM. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell. 2011;9(6):563-74. http://doi.org/10.1016/j.stem.2011.10.012. PMid:22136931.

Georges M. Towards sequence-based genomic selection of cattle. Nat Genet. 2014;46(8):807-9. http://doi.org/10.1038/ng.3048. PMid:25070799.

Hayes BJ, Bowman PJ, Chamberlain AJ, Goddard ME. Invited review: genomic selection in dairy cattle: progress and challenges. J Dairy Sci. 2009;92(2):433-43. http://doi.org/10.3168/jds.2008-1646. PMid:19164653.

He ZQ, Xia BL, Wang YK, Li J, Feng GH, Zhang LL, Li YH, Wan HF, Li TD, Xu K, Yuan XW, Li YF, Zhang XX, Zhang Y, Wang L, Li W, Zhou Q. Generation of mouse haploid somatic cells by small molecules for genome-wide genetic screening. Cell Rep. 2017;20(9):2227-37. http://doi.org/10.1016/j.celrep.2017.07.081. PMid:28854370.

Hu M, Zhao Z, TuanMu LC, Wei H, Gao F, Li L, Ying J, Zhang S. Analysis of imprinted gene expression and implantation in haploid androgenetic mouse embryos. Andrologia. 2015;47(1):102-8. http://doi.org/10.1111/and.12222. PMid:24387305.

Kokubu C, Takeda J. When half is better than the whole: advances in haploid embryonic stem cell technology. Cell Stem Cell. 2014;14(3):265-7. http://doi.org/10.1016/j.stem.2014.02.001. PMid:24607398.

Lagutina I, Lazzari G, Duchi R, Galli C. Developmental potential of bovine androgenetic and parthenogenetic embryos: a comparative study. Biol Reprod. 2004;70(2):400-5. http://doi.org/10.1095/biolreprod.103.021972. PMid:14561645.

Latham KE, Akutsu H, Patel B, Yanagimachi R. Comparison of gene expression during preimplantation development between diploid and haploid mouse embryos. Biol Reprod. 2002;67(2):386-92. http://doi.org/10.1095/biolreprod67.2.386. PMid:12135871.

Latham KE, Patel B, Bautista FD, Hawes SM. Effects of X chromosome number and parental origin on X-linked gene expression in preimplantation mouse embryos. Biol Reprod. 2000;63(1):64-73. http://doi.org/10.1095/biolreprod63.1.64. PMid:10859243.

Leeb M, Wutz A. Derivation of haploid embryonic stem cells from mouse embryos. Nature. 2011;479(7371):131-4. http://doi.org/10.1038/nature10448. PMid:21900896.

Leeb M, Dietmann S, Paramor M, Niwa H, Smith A. Genetic exploration of the exit from self-renewal using haploid embryonic stem cells. Cell Stem Cell. 2014;14(3):385-93. http://doi.org/10.1016/j.stem.2013.12.008. PMid:24412312.

Li W, Shuai L, Wan H, Dong M, Wang M, Sang L, Feng C, Luo GZ, Li T, Li X, Wang L, Zheng QY, Sheng C, Wu HJ, Liu Z, Liu L, Wang L, Wang XJ, Zhao XY, Zhou Q. Androgenetic haploid embryonic stem cells produce live transgenic mice. Nature. 2012;490(7420):407-11. http://doi.org/10.1038/nature11435. PMid:23023130.

Li W, Li X, Li T, Jiang MG, Wan H, Luo GZ, Feng C, Cui X, Teng F, Yuan Y, Zhou Q, Gu Q, Shuai L, Sha J, Xiao Y, Wang L, Liu Z, Wang XJ, Zhao XY, Zhou Q. Genetic modification and screening in rat using haploid embryonic stem cells. Cell Stem Cell. 2014;14(3):404-14. http://doi.org/10.1016/j.stem.2013.11.016. PMid:24360884.

Li Z, Wan H, Feng G, Wang L, He Z, Wang Y, Wang XJ, Li W, Zhou Q, Hu B. Birth of fertile bimaternal offspring following intracytoplasmic injection of parthenogenetic haploid embryonic stem cells. Cell Res. 2016;26(1):135-8. http://doi.org/10.1038/cr.2015.151. PMid:26680005.

Li H, Guo A, Xie Z, Tu W, Yu J, Wang H, Zhao J, Zhong C, Kang J, Li J, Huang S, Shen L. Stabilization of mouse haploid embryonic stem cells with combined kinase and signal modulation. Sci Rep. 2017;7(1):13222. http://doi.org/10.1038/s41598-017-13471-4. PMid:29038567.

Meuwissen TH, Hayes BJ, Goddard ME. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 2001;157(4):1819-29. http://doi.org/10.1093/genetics/157.4.1819. PMid:11290733.

Navara CS, First NL, Schatten G. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev Biol. 1994;162(1):29-40. http://doi.org/10.1006/dbio.1994.1064. PMid:8125194.

Pashaiasl M, Khodadadi K, Holland MK, Verma PJ. The efficient generation of cell lines from bovine parthenotes. Cell Reprogram. 2010;12(5):571-9. http://doi.org/10.1089/cell.2009.0118. PMid:20936907.

Sagi I, Chia G, Golan-Lev T, Peretz M, Weissbein U, Sui L, Sauer MV, Yanuka O, Egli D, Benvenisty N. Derivation and differentiation of haploid human embryonic stem cells. Nature. 2016;532(7597):107-11. http://doi.org/10.1038/nature17408. PMid:26982723.

Sagi I, De Pinho JC, Zuccaro MV, Atzmon C, Golan-Lev T, Yanuka O, Prosser R, Sadowy A, Perez G, Cabral T, Glaser B, Tsang SH, Goland R, Sauer MV, Lobo R, Benvenisty N, Egli D. Distinct imprinting signatures and biased differentiation of human androgenetic and parthenogenetic embryonic stem cells. Cell Stem Cell. 2019;25(3):419-432 e9. http://doi.org/10.1016/j.stem.2019.06.013. PMid:31491396.

Sathananthan AH, Selvaraj K, Girijashankar ML, Ganesh V, Selvaraj P, Trounson AO. From oogonia to mature oocytes: inactivation of the maternal centrosome in humans. Microsc Res Tech. 2006;69(6):396-407. http://doi.org/10.1002/jemt.20299. PMid:16718650.

Schaeffer LR. Strategy for applying genome-wide selection in dairy cattle. J Anim Breed Genet. 2006;123(4):218-23. http://doi.org/10.1111/j.1439-0388.2006.00595.x. PMid:16882088.

Schatten G, Simerly C, Schatten H. Maternal inheritance of centrosomes in mammals? Studies on parthenogenesis and polyspermy in mice. Proc Natl Acad Sci USA. 1991;88(15):6785-9. http://doi.org/10.1073/pnas.88.15.6785. PMid:1862101.

Shuai L, Zhou Q. Haploid embryonic stem cells serve as a new tool for mammalian genetic study. Stem Cell Res Ther. 2014;5(1):20. http://doi.org/10.1186/scrt409. PMid:24499606.

Singh KP, Kaushik R, Garg V, Sharma R, George A, Singh MK, Manik RS, Palta P, Singla SK, Chauhan MS. Expression pattern of pluripotent markers in different embryonic developmental stages of buffalo (Bubalus bubalis) embryos and putative embryonic stem cells generated by parthenogenetic activation. Cell Reprogram. 2012;14(6):530-8. http://doi.org/10.1089/cell.2012.0032. PMid:23194456.

Takahashi S, Lee J, Kohda T, Matsuzawa A, Kawasumi M, Kanai-Azuma M, Kaneko-Ishino T, Ishino F. Induction of the G2/M transition stabilizes haploid embryonic stem cells. Development. 2014;141(20):3842-7. http://doi.org/10.1242/dev.110726. PMid:25252944.

Vichera G, Olivera R, Sipowicz P, Radrizzani M, Salamone D. Sperm genome cloning used in biparental bovine embryo reconstruction. Reprod Fertil Dev. 2011;23(6):769-79. http://doi.org/10.1071/RD10252. PMid:21791178.

Wan H, He Z, Dong M, Gu T, Luo GZ, Teng F, Xia B, Li W, Feng C, Li X, Li T, Shuai L, Fu R, Wang L, Wang XJ, Zhao XY, Zhou Q. Parthenogenetic haploid embryonic stem cells produce fertile mice. Cell Res. 2013;23(11):1330-3. http://doi.org/10.1038/cr.2013.126. PMid:24018377.

Wang H, Zhang W, Yu J, Wu C, Gao Q, Li X, Li Y, Zhang J, Tian Y, Tan T, Ji W, Li L, Yu Y, Shuai L. Genetic screening and multipotency in rhesus monkey haploid neural progenitor cells. Development. 2018;145(11):dev160531. http://doi.org/10.1242/dev.160531. PMid:29784672.

Winger QA, De La Fuente R, King WA, Armstrong DT, Watson AJ. Bovine parthenogenesis is characterized by abnormal chromosomal complements: implications for maternal and paternal co-dependence during early bovine development. Dev Genet. 1997;21(2):160-6. http://doi.org/10.1002/(SICI)1520-6408(1997)21:2<160::AID-DVG5>3.0.CO;2-5. PMid:9332973.

Wutz A. Haploid animal cells. Development. 2014;141(7):1423-6. http://doi.org/10.1242/dev.102202. PMid:24644259.

Yang H, Liu Z, Ma Y, Zhong C, Yin Q, Zhou C, Shi L, Cai Y, Zhao H, Wang H, Tang F, Wang Y, Zhang C, Liu XY, Lai D, Jin Y, Sun Q, Li J. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res. 2013;23(10):1187-200. http://doi.org/10.1038/cr.2013.93. PMid:23856644.

Yang H, Shi L, Wang BA, Liang D, Zhong C, Liu W, Nie Y, Liu J, Zhao J, Gao X, Li D, Xu GL, Li J. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell. 2012;149(3):605-17. http://doi.org/10.1016/j.cell.2012.04.002. PMid:22541431.

Zhang XM, Wu K, Zheng Y, Zhao H, Gao J, Hou Z, Zhang M, Liao J, Zhang J, Gao Y, Li Y, Li L, Tang F, Chen ZJ, Li J. In vitro expansion of human sperm through nuclear transfer. Cell Res. 2020;30(4):356-9. http://doi.org/10.1038/s41422-019-0265-1. PMid:31853003.

Zhong C, Zhang M, Yin Q, Zhao H, Wang Y, Huang S, Tao W, Wu K, Chen ZJ, Li J. Generation of human haploid embryonic stem cells from parthenogenetic embryos obtained by microsurgical removal of male pronucleus. Cell Res. 2016;26(6):743-6. http://doi.org/10.1038/cr.2016.59. PMid:27185278.
 


Submitted date:
03/18/2024

Accepted date:
05/13/2024

66bb9909a953951da3245023 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections