Derivation of sheep embryonic stem cells under optimized conditions

in Reproduction
View More View Less
  • 1 Department of Animal Science, University of California Davis, Davis, California, USA
  • 2 Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA
  • 3 Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, Dallas, Texas, USA
  • 4 Gene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, California, USA

Correspondence should be addressed to J Wu or P J Ross; Email: Jun2.Wu@utsouthwestern.edu or pross@ucdavis.edu
Restricted access

Until recently, it has been difficult to derive and maintain stable embryonic stem cells lines from livestock species. Sheep ESCs with characteristics similar to those described for rodents and primates have not been produced. We report the derivation of sheep ESCs under a chemically defined culture system containing fibroblast growth factor 2 (FGF2) and a tankyrase/Wnt inhibitor (IWR1). We also show that several culture conditions used for stabilizing naïve and intermediate pluripotency states in humans and mice were unsuitable to maintain ovine pluripotency in vitro. Sheep ESCs display a smooth dome-shaped colony morphology, and maintain an euploid karyotype and stable expression of pluripotency markers after more than 40 passages. We further demonstrate that IWR1 and FGF2 are essential for the maintenance of an undifferentiated state in de novo derived sheep ESCs. The derivation of stable pluripotent cell lines from sheep blastocysts represents a step forward toward understanding pluripotency regulation in livestock species and developing novel biomedical and agricultural applications.

 

     An official journal of

    Society for Reproduction and Fertility

 

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 230 230 207
Full Text Views 59 59 52
PDF Downloads 34 34 28
  • Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K & Izpisua Belmonte JC 2018 Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. PNAS 115 20902095. (https://doi.org/10.1073/pnas.1716161115)

    • Search Google Scholar
    • Export Citation
  • Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL & Smith A 2008 Capture of authentic embryonic stem cells from rat blastocysts. Cell 135 12871298. (https://doi.org/10.1016/j.cell.2008.12.007)

    • Search Google Scholar
    • Export Citation
  • Chen G, Gulbranson DR, Hou Z, Bolin JM, Ruotti V, Probasco MD, Smuga-Otto K, Howden SE, Diol NR & Propson NE 2011 Chemically defined conditions for human iPSC derivation and culture. Nat ure Methods 8 424429. (https://doi.org/10.1038/nmeth.1593)

    • Search Google Scholar
    • Export Citation
  • Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR & Ma’ayan A 2013 Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14 128. (https://doi.org/10.1186/1471-2105-14-128)

    • Search Google Scholar
    • Export Citation
  • Choi KH, Lee DK, Kim SW, Woo SH, Kim DY & Lee CK 2019 Chemically defined media can maintain pig pluripotency network in vitro. Stem Cell Reports 13 221234. (https://doi.org/10.1016/j.stemcr.2019.05.028)

    • Search Google Scholar
    • Export Citation
  • Chung YG, Eum JH, Lee JE, Shim SH, Sepilian V, Hong SW, Lee Y, Treff NR, Choi YH & Kimbrel EA 2014 Human somatic cell nuclear transfer using adult cells. Cell Stem Cell 14 777780. (https://doi.org/10.1016/j.stem.2014.03.015)

    • Search Google Scholar
    • Export Citation
  • De Los Angeles A, Ferrari F, Xi R, Fujiwara Y, Benvenisty N, Deng H, Hochedlinger K, Jaenisch R, Lee S & Leitch HG 2015 Hallmarks of pluripotency. Nature 525 469478. (https://doi.org/10.1038/nature15515)

    • Search Google Scholar
    • Export Citation
  • Ezashi T, Telugu BP & Roberts RM 2012 Induced pluripotent stem cells from pigs and other ungulate species: an alternative to embryonic stem cells? Reprod uction in Domest ic Anim als 47 (Supplement 4) 9297. (https://doi.org/10.1111/j.1439-0531.2012.02061.x)

    • Search Google Scholar
    • Export Citation
  • Ezashi T, Yuan Y & Roberts RM 2016 Pluripotent stem cells from domesticated mammals. Annu al Rev iew of Anim al Biosci ences 4 223253. (https://doi.org/10.1146/annurev-animal-021815-111202)

    • Search Google Scholar
    • Export Citation
  • Factor DC, Corradin O, Zentner GE, Saiakhova A, Song L, Chenoweth JG, McKay RD, Crawford GE, Scacheri PC & Tesar PJ 2014 Epigenomic comparison reveals activation of ‘seed’ enhancers during transition from naive to primed pluripotency. Cell Stem Cell 14 854863. (https://doi.org/10.1016/j.stem.2014.05.005)

    • Search Google Scholar
    • Export Citation
  • Gafni O, Weinberger L, Mansour AA, Manor YS, Chomsky E, Ben-Yosef D, Kalma Y, Viukov S, Maza I & Zviran A 2013 Derivation of novel human ground state naive pluripotent stem cells. Nature 504 282286. (https://doi.org/10.1038/nature12745)

    • Search Google Scholar
    • Export Citation
  • Gandolfi F, Pennarossa G, Maffei S & Brevini T 2012 Why is it so difficult to derive pluripotent stem cells in domestic ungulates? Reprod uction in Domest ic Anim als 47 (Supplement 5) 1117. (https://doi.org/10.1111/j.1439-0531.2012.02106.x)

    • Search Google Scholar
    • Export Citation
  • Gao Y, Wu H, Wang Y, Liu X, Chen L, Li Q, Cui C, Liu X, Zhang J & Zhang Y 2017 Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol ogy 18 13. (https://doi.org/10.1186/s13059-016-1144-4)

    • Search Google Scholar
    • Export Citation
  • Gao X, Nowak-Imialek M, Chen X, Chen D, Herrmann D, Ruan D, Chen ACH, Eckersley-Maslin MA, Ahmad S & Lee YL 2019 Establishment of porcine and human expanded potential stem cells. Nat ure Cell Biol ogy 21 687699. (https://doi.org/10.1038/s41556-019-0333-2)

    • Search Google Scholar
    • Export Citation
  • Guo G, von Meyenn F, Santos F, Chen Y, Reik W, Bertone P, Smith A & Nichols J 2016 Naive pluripotent stem cells derived directly from isolated cells of the human inner cell mass. Stem Cell Reports 6 437446. (https://doi.org/10.1016/j.stemcr.2016.02.005)

    • Search Google Scholar
    • Export Citation
  • Hanna J, Cheng AW, Saha K, Kim J, Lengner CJ, Soldner F, Cassady JP, Muffat J, Carey BW & Jaenisch R 2010 Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. PNAS 107 92229227. (https://doi.org/10.1073/pnas.1004584107)

    • Search Google Scholar
    • Export Citation
  • Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, Charlat O, Wiellette E, Zhang Y & Wiessner S 2009 Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461 614620. (https://doi.org/10.1038/nature08356)

    • Search Google Scholar
    • Export Citation
  • Irie N, Weinberger L, Tang WW, Kobayashi T, Viukov S, Manor YS, Dietmann S, Hanna JH & Surani MA 2015 SOX17 is a critical specifier of human primordial germ cell fate. Cell 160 253268. (https://doi.org/10.1016/j.cell.2014.12.013)

    • Search Google Scholar
    • Export Citation
  • Kirubakaran P, Kothandan G, Cho SJ & Muthusamy K 2014 Molecular insights on TNKS1/TNKS2 and inhibitor-IWR1 interactions. Mol ecular Biosyst ems 10 281293. (https://doi.org/10.1039/c3mb70305c)

    • Search Google Scholar
    • Export Citation
  • Koh S & Piedrahita JA 2014 From ‘ES-like’ cells to induced pluripotent stem cells: a historical perspective in domestic animals. Theriogenology 81 103111. (https://doi.org/10.1016/j.theriogenology.2013.09.009)

    • Search Google Scholar
    • Export Citation
  • Ludwig TE, Bergendahl V, Levenstein ME, Yu J, Probasco MD & Thomson JA 2006 Feeder-independent culture of human embryonic stem cells. Nat ure Methods 3 637646. (https://doi.org/10.1038/nmeth902)

    • Search Google Scholar
    • Export Citation
  • Mahla RS 2016 Stem cells applications in regenerative medicine and disease therapeutics. Int ernational J ournal of Cell Biol ogy 2016 6940283. (https://doi.org/10.1155/2016/6940283)

    • Search Google Scholar
    • Export Citation
  • Malaver-Ortega LF, Sumer H, Liu J & Verma PJ 2012 The state of the art for pluripotent stem cells derivation in domestic ungulates. Theriogenology 78 17491762. (https://doi.org/10.1016/j.theriogenology.2012.03.031)

    • Search Google Scholar
    • Export Citation
  • Navarro M, Soto DA, Pinzon CA, Wu J & Ross PJ 2019 Livestock pluripotency is finally captured in vitro. Reproduction, Fertility , and Development 32 1139. (https://doi.org/10.1071/RD19272)

    • Search Google Scholar
    • Export Citation
  • Nichols J & Smith A 2009 Naive and primed pluripotent states. Cell Stem Cell 4 487492. (https://doi.org/10.1016/j.stem.2009.05.015)

  • Park KE & Telugu BP 2013 Role of stem cells in large animal genetic engineering in the TALENs-CRISPR era. Reprod uction, Fertility, and Development 26 6573. (https://doi.org/10.1071/RD13258)

    • Search Google Scholar
    • Export Citation
  • Rashid T, Kobayashi T & Nakauchi H 2014 Revisiting the flight of Icarus: making human organs from PSCs with large animal chimeras. Cell Stem Cell 15 406409. (doi:10.1016/j.stem.2014.09.013)

    • Search Google Scholar
    • Export Citation
  • Rideout WM 3rd, Wakayama T, Wutz A, Eggan K, Jackson-Grusby L, Dausman J, Yanagimachi R & Jaenisch R 2000 Generation of mice from wild-type and targeted ES cells by nuclear cloning. Nat ure Genet ics 24 109110. (https://doi.org/10.1038/72753)

    • Search Google Scholar
    • Export Citation
  • Scheerlinck JP, Snibson KJ, Bowles VM & Sutton P 2008 Biomedical applications of sheep models: from asthma to vaccines. Trends in Biotechnol ogy 26 259266. (https://doi.org/10.1016/j.tibtech.2008.02.002)

    • Search Google Scholar
    • Export Citation
  • Sokol SY 2011 Maintaining embryonic stem cell pluripotency with Wnt signaling. Development 138 43414350. (https://doi.org/10.1242/dev.066209)

    • Search Google Scholar
    • Export Citation
  • Soto DA & Ross PJ 2016 Pluripotent stem cells and livestock genetic engineering. Transgenic Res earch 25 289306. (https://doi.org/10.1007/s11248-016-9929-5)

    • Search Google Scholar
    • Export Citation
  • Takashima Y, Guo G, Loos R, Nichols J, Ficz G, Krueger F, Oxley D, Santos F, Clarke J & Mansfield W 2014 Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158 12541269. (https://doi.org/10.1016/j.cell.2014.08.029)

    • Search Google Scholar
    • Export Citation
  • Tandon S & Jyoti S 2012 Embryonic stem cells: an alternative approach to developmental toxicity testing. J ournal of Pharm acy and Bioallied Sci ences 4 96100. (https://doi.org/10.4103/0975-7406.94808)

    • Search Google Scholar
    • Export Citation
  • Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL & McKay RD 2007 New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448 196199. (https://doi.org/10.1038/nature05972)

    • Search Google Scholar
    • Export Citation
  • Theunissen TW, Powell BE, Wang H, Mitalipova M, Faddah DA, Reddy J, Fan ZP, Maetzel D, Ganz K, Shi L et al. 2014 Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15 471487. (https://doi.org/10.1016/j.stem.2014.07.002)

    • Search Google Scholar
    • Export Citation
  • Tomizawa M, Shinozaki F, Sugiyama T, Yamamoto S, Sueishi M & Yoshida T 2013 Activin A is essential for feeder-free culture of human induced pluripotent stem cells. J ournal of Cell ular Biochem istry 114 584588. (https://doi.org/10.1002/jcb.24395)

    • Search Google Scholar
    • Export Citation
  • Tribulo P, Leao BCDS, Lehloenya KC, Mingoti GZ & Hansen PJ 2017 Consequences of endogenous and exogenous WNT signaling for development of the preimplantation bovine embryo. Biol ogy of Reprod uction 96 11291141. (https://doi.org/10.1093/biolre/iox048)

    • Search Google Scholar
    • Export Citation
  • Tsukiyama T & Ohinata Y 2014 A modified EpiSC culture condition containing a GSK3 inhibitor can support germline-competent pluripotency in mice. PL o S O NE 9 e95329. (https://doi.org/10.1371/journal.pone.0095329)

    • Search Google Scholar
    • Export Citation
  • Vilarino M, Rashid ST, Suchy FP, McNabb BR, van der Meulen T, Fine EJ, Ahsan SD, Mursaliyev N, Sebastiano V & Diab SS 2017 CRISPR/Cas9 microinjection in oocytes disables pancreas development in sheep. Sci entific Rep orts 7 17472. (https://doi.org/10.1038/s41598-017-17805-0)

    • Search Google Scholar
    • Export Citation
  • Wu J, Okamura D, Li M, Suzuki K, Luo C, Ma L, He Y, Li Z, Benner C & Tamura I 2015 An alternative pluripotent state confers interspecies chimaeric competency. Nature 521 316321. (https://doi.org/10.1038/nature14413)

    • Search Google Scholar
    • Export Citation
  • Wu J, Greely HT, Jaenisch R, Nakauchi H, Rossant J & Belmonte JC 2016 Stem cells and interspecies chimaeras. Nature 540 5159. (https://doi.org/10.1038/nature20573)

    • Search Google Scholar
    • Export Citation
  • Wu J, Platero-Luengo A, Sakurai M, Sugawara A, Gil MA, Yamauchi T, Suzuki K, Bogliotti YS, Cuello C & Morales Valencia M 2017 Interspecies chimerism with mammalian pluripotent stem cells. Cell 168 473 .e15486.e15. (https://doi.org/10.1016/j.cell.2016.12.036)

    • Search Google Scholar
    • Export Citation
  • Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P & Smith A 2008 The ground state of embryonic stem cell self-renewal. Nature 453 519523. (https://doi.org/10.1038/nature06968)

    • Search Google Scholar
    • Export Citation
  • Zhao Y, Lin J, Wang L, Chen B, Zhou C, Chen T, Guo M, He S, Zhang N & Liu C 2011 Derivation and characterization of ovine embryonic stem-like cell lines in semi-defined medium without feeder cells. J ournal of Experimental Zoology : Part A, Ecological Genetics and Physiology 315 639648. (https://doi.org/10.1002/jez.715)

    • Search Google Scholar
    • Export Citation