IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30259-x.html
   My bibliography  Save this article

Preventing erosion of X-chromosome inactivation in human embryonic stem cells

Author

Listed:
  • Marissa Cloutier

    (University of Michigan Medical School)

  • Surinder Kumar

    (University of Michigan Medical School
    University of Michigan Medical School)

  • Emily Buttigieg

    (University of Michigan Medical School)

  • Laura Keller

    (University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School)

  • Brandon Lee

    (University of Michigan Medical School)

  • Aaron Williams

    (University of Michigan Medical School)

  • Sandra Mojica-Perez

    (University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School)

  • Indri Erliandri

    (University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School)

  • Andre Monteiro Da Rocha

    (University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School)

  • Kenneth Cadigan

    (Cellular, and Developmental Biology, University of Michigan Medical School)

  • Gary D. Smith

    (University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School
    University of Michigan Medical School)

  • Sundeep Kalantry

    (University of Michigan Medical School)

Abstract

X-chromosome inactivation is a paradigm of epigenetic transcriptional regulation. Female human embryonic stem cells (hESCs) often undergo erosion of X-inactivation upon prolonged culture. Here, we investigate the sources of X-inactivation instability by deriving new primed pluripotent hESC lines. We find that culture media composition dramatically influenced the expression of XIST lncRNA, a key regulator of X-inactivation. hESCs cultured in a defined xenofree medium stably maintained XIST RNA expression and coating, whereas hESCs cultured in the widely used mTeSR1 medium lost XIST RNA expression. We pinpointed lithium chloride in mTeSR1 as a cause of XIST RNA loss. The addition of lithium chloride or inhibitors of GSK-3 proteins that are targeted by lithium to the defined hESC culture medium impeded XIST RNA expression. GSK-3 inhibition in differentiating female mouse embryonic stem cells and epiblast stem cells also resulted in a loss of XIST RNA expression. Together, these data may reconcile observed variations in X-inactivation in hESCs and inform the faithful culture of pluripotent stem cells.

Suggested Citation

  • Marissa Cloutier & Surinder Kumar & Emily Buttigieg & Laura Keller & Brandon Lee & Aaron Williams & Sandra Mojica-Perez & Indri Erliandri & Andre Monteiro Da Rocha & Kenneth Cadigan & Gary D. Smith & , 2022. "Preventing erosion of X-chromosome inactivation in human embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30259-x
    DOI: 10.1038/s41467-022-30259-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30259-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-30259-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ohad Gafni & Leehee Weinberger & Abed AlFatah Mansour & Yair S. Manor & Elad Chomsky & Dalit Ben-Yosef & Yael Kalma & Sergey Viukov & Itay Maza & Asaf Zviran & Yoach Rais & Zohar Shipony & Zohar Mukam, 2013. "Derivation of novel human ground state naive pluripotent stem cells," Nature, Nature, vol. 504(7479), pages 282-286, December.
    2. Paul J. Tesar & Josh G. Chenoweth & Frances A. Brook & Timothy J. Davies & Edward P. Evans & David L. Mack & Richard L. Gardner & Ronald D. G. McKay, 2007. "New cell lines from mouse epiblast share defining features with human embryonic stem cells," Nature, Nature, vol. 448(7150), pages 196-199, July.
    3. Ikuhiro Okamoto & Catherine Patrat & Dominique Thépot & Nathalie Peynot & Patricia Fauque & Nathalie Daniel & Patricia Diabangouaya & Jean-Philippe Wolf & Jean-Paul Renard & Véronique Duranthon & Edit, 2011. "Erratum: Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development," Nature, Nature, vol. 474(7350), pages 239-240, June.
    4. Colleen A. McHugh & Chun-Kan Chen & Amy Chow & Christine F. Surka & Christina Tran & Patrick McDonel & Amy Pandya-Jones & Mario Blanco & Christina Burghard & Annie Moradian & Michael J. Sweredoski & A, 2015. "The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3," Nature, Nature, vol. 521(7551), pages 232-236, May.
    5. Ikuhiro Okamoto & Catherine Patrat & Dominique Thépot & Nathalie Peynot & Patricia Fauque & Nathalie Daniel & Patricia Diabangouaya & Jean-Philippe Wolf & Jean-Paul Renard & Véronique Duranthon & Edit, 2011. "Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development," Nature, Nature, vol. 472(7343), pages 370-374, April.
    6. Emily Maclary & Emily Buttigieg & Michael Hinten & Srimonta Gayen & Clair Harris & Mrinal Kumar Sarkar & Sonya Purushothaman & Sundeep Kalantry, 2014. "Differentiation-dependent requirement of Tsix long non-coding RNA in imprinted X-chromosome inactivation," Nature Communications, Nature, vol. 5(1), pages 1-14, September.
    7. Sundeep Kalantry & Sonya Purushothaman & Randall Bryant Bowen & Joshua Starmer & Terry Magnuson, 2009. "Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation," Nature, Nature, vol. 460(7255), pages 647-651, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Milan Kumar Samanta & Srimonta Gayen & Clair Harris & Emily Maclary & Yumie Murata-Nakamura & Rebecca M. Malcore & Robert S. Porter & Patricia M. Garay & Christina N. Vallianatos & Paul B. Samollow & , 2022. "Activation of Xist by an evolutionarily conserved function of KDM5C demethylase," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Woranop Sukparangsi & Elena Morganti & Molly Lowndes & Hélène Mayeur & Melanie Weisser & Fella Hammachi & Hanna Peradziryi & Fabian Roske & Jurriaan Hölzenspies & Alessandra Livigni & Benoit Gilbert G, 2022. "Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    3. Jonathan M. Werner & John Hover & Jesse Gillis, 2024. "Population variability in X-chromosome inactivation across 10 mammalian species," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    4. Lisa-Marie Appel & Vedran Franke & Johannes Benedum & Irina Grishkovskaya & Xué Strobl & Anton Polyansky & Gregor Ammann & Sebastian Platzer & Andrea Neudolt & Anna Wunder & Lena Walch & Stefanie Kais, 2023. "The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Teresa Robert-Finestra & Beatrice F. Tan & Hegias Mira-Bontenbal & Erika Timmers & Cristina Gontan & Sarra Merzouk & Benedetto Daniele Giaimo & François Dossin & Wilfred F. J. IJcken & John W. M. Mart, 2021. "SPEN is required for Xist upregulation during initiation of X chromosome inactivation," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Siti Razila Abdul Razak & Kazuko Ueno & Naoya Takayama & Naoki Nariai & Masao Nagasaki & Rika Saito & Hideto Koso & Chen-Yi Lai & Miyako Murakami & Koichiro Tsuji & Tatsuo Michiue & Hiromitsu Nakauchi, 2013. "Profiling of MicroRNA in Human and Mouse ES and iPS Cells Reveals Overlapping but Distinct MicroRNA Expression Patterns," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-16, September.
    7. Andrea Lauria & Guohua Meng & Valentina Proserpio & Stefania Rapelli & Mara Maldotti & Isabelle Laurence Polignano & Francesca Anselmi & Danny Incarnato & Anna Krepelova & Daniela Donna & Chiara Levra, 2023. "DNMT3B supports meso-endoderm differentiation from mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Francesco Panariello & Onelia Gagliano & Camilla Luni & Antonio Grimaldi & Silvia Angiolillo & Wei Qin & Anna Manfredi & Patrizia Annunziata & Shaked Slovin & Lorenzo Vaccaro & Sara Riccardo & Valenti, 2023. "Cellular population dynamics shape the route to human pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Kirstin Meyer & Nicholas C. Lammers & Lukasz J. Bugaj & Hernan G. Garcia & Orion D. Weiner, 2023. "Optogenetic control of YAP reveals a dynamic communication code for stem cell fate and proliferation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Andrew Keniry & Natasha Jansz & Linden J. Gearing & Iromi Wanigasuriya & Joseph Chen & Christian M. Nefzger & Peter F. Hickey & Quentin Gouil & Joy Liu & Kelsey A. Breslin & Megan Iminitoff & Tamara B, 2022. "BAF complex-mediated chromatin relaxation is required for establishment of X chromosome inactivation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Yan Bi & Zhifen Tu & Jianfeng Zhou & Xuehao Zhu & Hong Wang & Shaorong Gao & Yixuan Wang, 2022. "Cell fate roadmap of human primed-to-naive transition reveals preimplantation cell lineage signatures," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Kory R Johnson & Barbara S Mallon & Yang C Fann & Kevin G Chen, 2021. "Multivariate meta-analysis reveals global transcriptomic signatures underlying distinct human naive-like pluripotent states," PLOS ONE, Public Library of Science, vol. 16(5), pages 1-24, May.
    13. Raamesh Deshpande & Shikha Sharma & Catherine M Verfaillie & Wei-Shou Hu & Chad L Myers, 2010. "A Scalable Approach for Discovering Conserved Active Subnetworks across Species," PLOS Computational Biology, Public Library of Science, vol. 6(12), pages 1-18, December.
    14. Lisa-Marie Appel & Vedran Franke & Melania Bruno & Irina Grishkovskaya & Aiste Kasiliauskaite & Tanja Kaufmann & Ursula E. Schoeberl & Martin G. Puchinger & Sebastian Kostrhon & Carmen Ebenwaldner & M, 2021. "PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    15. Aditya Kshirsagar & Svetlana Maslov Doroshev & Anna Gorelik & Tsviya Olender & Tamar Sapir & Daisuke Tsuboi & Irit Rosenhek-Goldian & Sergey Malitsky & Maxim Itkin & Amir Argoetti & Yael Mandel-Gutfre, 2023. "LIS1 RNA-binding orchestrates the mechanosensitive properties of embryonic stem cells in AGO2-dependent and independent ways," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    16. Anna Malkowska & Christopher Penfold & Sophie Bergmann & Thorsten E. Boroviak, 2022. "A hexa-species transcriptome atlas of mammalian embryogenesis delineates metabolic regulation across three different implantation modes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    17. Yinuo Wang & Adel Elsherbiny & Linda Kessler & Julio Cordero & Haojie Shi & Heike Serke & Olga Lityagina & Felix A. Trogisch & Mona Malek Mohammadi & Ibrahim El-Battrawy & Johannes Backs & Thomas Wiel, 2022. "Lamin A/C-dependent chromatin architecture safeguards naïve pluripotency to prevent aberrant cardiovascular cell fate and function," Nature Communications, Nature, vol. 13(1), pages 1-24, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30259-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.