IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31737-y.html
   My bibliography  Save this article

Interchromosomal interaction of homologous Stat92E alleles regulates transcriptional switch during stem-cell differentiation

Author

Listed:
  • Matthew Antel

    (University of Connecticut Health Center)

  • Romir Raj

    (University of Connecticut Health Center)

  • Madona Y. G. Masoud

    (University of Connecticut Health Center)

  • Ziwei Pan

    (The Jackson Laboratory for Genomic Medicine
    University of Connecticut Health Center)

  • Sheng Li

    (The Jackson Laboratory for Genomic Medicine
    University of Connecticut Health Center)

  • Barbara G. Mellone

    (University of Connecticut
    University of Connecticut)

  • Mayu Inaba

    (University of Connecticut Health Center)

Abstract

Pairing of homologous chromosomes in somatic cells provides the opportunity of interchromosomal interaction between homologous gene regions. In the Drosophila male germline, the Stat92E gene is highly expressed in a germline stem cell (GSC) and gradually downregulated during the differentiation. Here we show that the pairing of Stat92E is always tight in GSCs and immediately loosened in differentiating daughter cells, gonialblasts (GBs). Disturbance of Stat92E pairing by relocation of one locus to another chromosome or by knockdown of global pairing/anti-pairing factors both result in a failure of Stat92E downregulation, suggesting that the pairing is required for the decline in transcription. Furthermore, the Stat92E enhancer, but not its transcription, is required for the change in pairing state, indicating that pairing is not a consequence of transcriptional changes. Finally, we show that the change in Stat92E pairing is dependent on asymmetric histone inheritance during the asymmetric division of GSCs. Taken together, we propose that the changes in Stat92E pairing status is an intrinsically programmed mechanism for enabling prompt cell fate switch during the differentiation of stem cells.

Suggested Citation

  • Matthew Antel & Romir Raj & Madona Y. G. Masoud & Ziwei Pan & Sheng Li & Barbara G. Mellone & Mayu Inaba, 2022. "Interchromosomal interaction of homologous Stat92E alleles regulates transcriptional switch during stem-cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31737-y
    DOI: 10.1038/s41467-022-31737-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31737-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31737-y?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. Arjun Raj & Charles S Peskin & Daniel Tranchina & Diana Y Vargas & Sanjay Tyagi, 2006. "Stochastic mRNA Synthesis in Mammalian Cells," PLOS Biology, Public Library of Science, vol. 4(10), pages 1-13, September.
    2. Leslie J. Mateo & Sedona E. Murphy & Antonina Hafner & Isaac S. Cinquini & Carly A. Walker & Alistair N. Boettiger, 2019. "Visualizing DNA folding and RNA in embryos at single-cell resolution," Nature, Nature, vol. 568(7750), pages 49-54, April.
    3. Matthew Wawersik & Allison Milutinovich & Abbie L. Casper & Erika Matunis & Brian Williams & Mark Van Doren, 2005. "Somatic control of germline sexual development is mediated by the JAK/STAT pathway," Nature, Nature, vol. 436(7050), pages 563-567, July.
    4. Diego I. Cattoni & Andrés M. Cardozo Gizzi & Mariya Georgieva & Marco Stefano & Alessandro Valeri & Delphine Chamousset & Christophe Houbron & Stephanie Déjardin & Jean-Bernard Fiche & Inma González &, 2017. "Single-cell absolute contact probability detection reveals chromosomes are organized by multiple low-frequency yet specific interactions," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    5. Mayu Inaba & Michael Buszczak & Yukiko M. Yamashita, 2015. "Nanotubes mediate niche–stem-cell signalling in the Drosophila testis," Nature, Nature, vol. 523(7560), pages 329-332, July.
    6. Swathi Yadlapalli & Yukiko M. Yamashita, 2013. "Chromosome-specific nonrandom sister chromatid segregation during stem-cell division," Nature, Nature, vol. 498(7453), pages 251-254, June.
    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. Guang Shi & D. Thirumalai, 2023. "A maximum-entropy model to predict 3D structural ensembles of chromatin from pairwise distances with applications to interphase chromosomes and structural variants," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Olivier Messina & Flavien Raynal & Julian Gurgo & Jean-Bernard Fiche & Vera Pancaldi & Marcelo Nollmann, 2023. "3D chromatin interactions involving Drosophila insulators are infrequent but preferential and arise before TADs and transcription," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Robin Aguilar & Conor K. Camplisson & Qiaoyi Lin & Karen H. Miga & William S. Noble & Brian J. Beliveau, 2024. "Tigerfish designs oligonucleotide-based in situ hybridization probes targeting intervals of highly repetitive DNA at the scale of genomes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Stuart Aitken & Marie-Cécile Robert & Ross D Alexander & Igor Goryanin & Edouard Bertrand & Jean D Beggs, 2010. "Processivity and Coupling in Messenger RNA Transcription," PLOS ONE, Public Library of Science, vol. 5(1), pages 1-12, January.
    5. Singh, Abhyudai & Vahdat, Zahra & Xu, Zikai, 2019. "Time-triggered stochastic hybrid systems with two timer-dependent resets," OSF Preprints u8fzg, Center for Open Science.
    6. Muir Morrison & Manuel Razo-Mejia & Rob Phillips, 2021. "Reconciling kinetic and thermodynamic models of bacterial transcription," PLOS Computational Biology, Public Library of Science, vol. 17(1), pages 1-30, January.
    7. Marc S Sherman & Barak A Cohen, 2014. "A Computational Framework for Analyzing Stochasticity in Gene Expression," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-13, May.
    8. Rajesh Ramaswamy & Ivo F Sbalzarini & Nélido González-Segredo, 2011. "Noise-Induced Modulation of the Relaxation Kinetics around a Non-Equilibrium Steady State of Non-Linear Chemical Reaction Networks," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-10, January.
    9. Anton J M Larsson & Christoph Ziegenhain & Michael Hagemann-Jensen & Björn Reinius & Tina Jacob & Tim Dalessandri & Gert-Jan Hendriks & Maria Kasper & Rickard Sandberg, 2021. "Transcriptional bursts explain autosomal random monoallelic expression and affect allelic imbalance," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-16, March.
    10. Chen, Aimin & Tian, Tianhai & Chen, Yiren & Zhou, Tianshou, 2022. "Stochastic analysis of a complex gene-expression model," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).
    11. Zachary R Fox & Brian Munsky, 2019. "The finite state projection based Fisher information matrix approach to estimate information and optimize single-cell experiments," PLOS Computational Biology, Public Library of Science, vol. 15(1), pages 1-23, January.
    12. Abhyudai Singh & Mohammad Soltani, 2013. "Quantifying Intrinsic and Extrinsic Variability in Stochastic Gene Expression Models," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-12, December.
    13. Jonathan Liu & Donald Hansen & Elizabeth Eck & Yang Joon Kim & Meghan Turner & Simon Alamos & Hernan Garcia, 2021. "Real-time single-cell characterization of the eukaryotic transcription cycle reveals correlations between RNA initiation, elongation, and cleavage," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-26, May.
    14. Pranidhi Sood & Robert J Johnston Jr. & Edo Kussell, 2012. "Stochastic De-repression of Rhodopsins in Single Photoreceptors of the Fly Retina," PLOS Computational Biology, Public Library of Science, vol. 8(2), pages 1-13, February.
    15. William C. W. Chen & Leonid Gaidukov & Yong Lai & Ming-Ru Wu & Jicong Cao & Michael J. Gutbrod & Gigi C. G. Choi & Rachel P. Utomo & Ying-Chou Chen & Liliana Wroblewska & Manolis Kellis & Lin Zhang & , 2022. "A synthetic transcription platform for programmable gene expression in mammalian cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Sora Yoon & Aditi Chandra & Golnaz Vahedi, 2022. "Stripenn detects architectural stripes from chromatin conformation data using computer vision," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    19. Lijuan Du & Alex Sohr & Yujia Li & Sougata Roy, 2022. "GPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    20. Amy L. Hughes & Aleksander T. Szczurek & Jessica R. Kelley & Anna Lastuvkova & Anne H. Turberfield & Emilia Dimitrova & Neil P. Blackledge & Robert J. Klose, 2023. "A CpG island-encoded mechanism protects genes from premature transcription termination," Nature Communications, Nature, vol. 14(1), pages 1-19, 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_s41467-022-31737-y. 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.