IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27338-w.html
   My bibliography  Save this article

Structural basis of Ty3 retrotransposon integration at RNA Polymerase III-transcribed genes

Author

Listed:
  • Guillermo Abascal-Palacios

    (The Institute of Cancer Research)

  • Laura Jochem

    (The Institute of Cancer Research)

  • Carlos Pla-Prats

    (Friedrich Miescher Institute for Biomedical Research)

  • Fabienne Beuron

    (The Institute of Cancer Research)

  • Alessandro Vannini

    (The Institute of Cancer Research
    Human Technopole)

Abstract

Retrotransposons are endogenous elements that have the ability to mobilise their DNA between different locations in the host genome. The Ty3 retrotransposon integrates with an exquisite specificity in a narrow window upstream of RNA Polymerase (Pol) III-transcribed genes, representing a paradigm for harmless targeted integration. Here we present the cryo-EM reconstruction at 4.0 Å of an active Ty3 strand transfer complex bound to TFIIIB transcription factor and a tRNA gene. The structure unravels the molecular mechanisms underlying Ty3 targeting specificity at Pol III-transcribed genes and sheds light into the architecture of retrotransposon machinery during integration. Ty3 intasome contacts a region of TBP, a subunit of TFIIIB, which is blocked by NC2 transcription regulator in RNA Pol II-transcribed genes. A newly-identified chromodomain on Ty3 integrase interacts with TFIIIB and the tRNA gene, defining with extreme precision the integration site position.

Suggested Citation

  • Guillermo Abascal-Palacios & Laura Jochem & Carlos Pla-Prats & Fabienne Beuron & Alessandro Vannini, 2021. "Structural basis of Ty3 retrotransposon integration at RNA Polymerase III-transcribed genes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27338-w
    DOI: 10.1038/s41467-021-27338-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27338-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-27338-w?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. Daniel P. Maskell & Ludovic Renault & Erik Serrao & Paul Lesbats & Rishi Matadeen & Stephen Hare & Dirk Lindemann & Alan N. Engelman & Alessandro Costa & Peter Cherepanov, 2015. "Structural basis for retroviral integration into nucleosomes," Nature, Nature, vol. 523(7560), pages 366-369, July.
    2. Gary Male & Alexander von Appen & Sebastian Glatt & Nicholas M. I. Taylor & Michele Cristovao & Helga Groetsch & Martin Beck & Christoph W. Müller, 2015. "Architecture of TFIIIC and its role in RNA polymerase III pre-initiation complex assembly," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    3. Marcus D. Wilson & Ludovic Renault & Daniel P. Maskell & Mohamed Ghoneim & Valerie E. Pye & Andrea Nans & David S. Rueda & Peter Cherepanov & Alessandro Costa, 2019. "Retroviral integration into nucleosomes through DNA looping and sliding along the histone octamer," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Goedele N. Maertens & Stephen Hare & Peter Cherepanov, 2010. "The mechanism of retroviral integration from X-ray structures of its key intermediates," Nature, Nature, vol. 468(7321), pages 326-329, November.
    5. Guillermo Abascal-Palacios & Ewan Phillip Ramsay & Fabienne Beuron & Edward Morris & Alessandro Vannini, 2018. "Structural basis of RNA polymerase III transcription initiation," Nature, Nature, vol. 553(7688), pages 301-306, January.
    6. Zhiqi Yin & Ke Shi & Surajit Banerjee & Krishan K. Pandey & Sibes Bera & Duane P. Grandgenett & Hideki Aihara, 2016. "Crystal structure of the Rous sarcoma virus intasome," Nature, Nature, vol. 530(7590), pages 362-366, February.
    7. Z. Sean Juo & George A. Kassavetis & Jimin Wang & E. Peter Geiduschek & Paul B. Sigler, 2003. "Crystal structure of a transcription factor IIIB core interface ternary complex," Nature, Nature, vol. 422(6931), pages 534-539, April.
    8. Allison Ballandras-Colas & Monica Brown & Nicola J. Cook & Tamaria G. Dewdney & Borries Demeler & Peter Cherepanov & Dmitry Lyumkis & Alan N. Engelman, 2016. "Cryo-EM reveals a novel octameric integrase structure for betaretroviral intasome function," Nature, Nature, vol. 530(7590), pages 358-361, February.
    9. John F. Flanagan & Li-Zhi Mi & Maksymilian Chruszcz & Marcin Cymborowski & Katrina L. Clines & Youngchang Kim & Wladek Minor & Fraydoon Rastinejad & Sepideh Khorasanizadeh, 2005. "Double chromodomains cooperate to recognize the methylated histone H3 tail," Nature, Nature, vol. 438(7071), pages 1181-1185, December.
    10. Matthias K. Vorländer & Heena Khatter & Rene Wetzel & Wim J. H. Hagen & Christoph W. Müller, 2018. "Molecular mechanism of promoter opening by RNA polymerase III," Nature, Nature, vol. 553(7688), pages 295-300, January.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Phong Quoc Nguyen & Sonia Huecas & Amna Asif-Laidin & Adrián Plaza-Pegueroles & Beatrice Capuzzi & Noé Palmic & Christine Conesa & Joël Acker & Juan Reguera & Pascale Lesage & Carlos Fernández-Tornero, 2023. "Structural basis of Ty1 integrase tethering to RNA polymerase III for targeted retrotransposon integration," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Allison Ballandras-Colas & Vidya Chivukula & Dominika T. Gruszka & Zelin Shan & Parmit K. Singh & Valerie E. Pye & Rebecca K. McLean & Gregory J. Bedwell & Wen Li & Andrea Nans & Nicola J. Cook & Hind, 2022. "Multivalent interactions essential for lentiviral integrase function," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    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. Allison Ballandras-Colas & Vidya Chivukula & Dominika T. Gruszka & Zelin Shan & Parmit K. Singh & Valerie E. Pye & Rebecca K. McLean & Gregory J. Bedwell & Wen Li & Andrea Nans & Nicola J. Cook & Hind, 2022. "Multivalent interactions essential for lentiviral integrase function," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Gayan Senavirathne & James London & Anne Gardner & Richard Fishel & Kristine E. Yoder, 2023. "DNA strand breaks and gaps target retroviral intasome binding and integration," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Saurabh Mishra & Shaina H. Hasan & Rima M. Sakhawala & Shereen Chaudhry & Richard J. Maraia, 2021. "Mechanism of RNA polymerase III termination-associated reinitiation-recycling conferred by the essential function of the N terminal-and-linker domain of the C11 subunit," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Haifeng Hou & Yan Li & Mo Wang & Aijun Liu & Zishuo Yu & Ke Chen & Dan Zhao & Yanhui Xu, 2021. "Structural insights into RNA polymerase III-mediated transcription termination through trapping poly-deoxythymidine," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Phong Quoc Nguyen & Sonia Huecas & Amna Asif-Laidin & Adrián Plaza-Pegueroles & Beatrice Capuzzi & Noé Palmic & Christine Conesa & Joël Acker & Juan Reguera & Pascale Lesage & Carlos Fernández-Tornero, 2023. "Structural basis of Ty1 integrase tethering to RNA polymerase III for targeted retrotransposon integration," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Xinhao Hou & Mingjing Xu & Chengming Zhu & Jianing Gao & Meili Li & Xiangyang Chen & Cheng Sun & Björn Nashan & Jianye Zang & Ying Zhou & Shouhong Guang & Xuezhu Feng, 2023. "Systematic characterization of chromodomain proteins reveals an H3K9me1/2 reader regulating aging in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Monica Naughtin & Zofia Haftek-Terreau & Johan Xavier & Sam Meyer & Maud Silvain & Yan Jaszczyszyn & Nicolas Levy & Vincent Miele & Mohamed Salah Benleulmi & Marc Ruff & Vincent Parissi & Cédric Vaill, 2015. "DNA Physical Properties and Nucleosome Positions Are Major Determinants of HIV-1 Integrase Selectivity," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-28, June.
    8. Li Wang & Jiali Yu & Zishuo Yu & Qianmin Wang & Wanjun Li & Yulei Ren & Zhenguo Chen & Shuang He & Yanhui Xu, 2022. "Structure of nucleosome-bound human PBAF complex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Kevin Van Bortle & David P. Marciano & Qing Liu & Tristan Chou & Andrew M. Lipchik & Sanjay Gollapudi & Benjamin S. Geller & Emma Monte & Rohinton T. Kamakaka & Michael P. Snyder, 2022. "A cancer-associated RNA polymerase III identity drives robust transcription and expression of snaR-A noncoding RNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Caojie Liu & Qiuchan Xiong & Qiwen Li & Weimin Lin & Shuang Jiang & Danting Zhang & Yuan Wang & Xiaobo Duan & Ping Gong & Ning Kang, 2022. "CHD7 regulates bone-fat balance by suppressing PPAR-γ signaling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    11. Joke J F A van Vugt & Martijn de Jager & Magdalena Murawska & Alexander Brehm & John van Noort & Colin Logie, 2009. "Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-14, July.
    12. Hannah O. Ajoge & Tyler M. Renner & Kasandra Bélanger & Matthew Greig & Samar Dankar & Hinissan P. Kohio & Macon D. Coleman & Emmanuel Ndashimye & Eric J. Arts & Marc-André Langlois & Stephen D. Barr, 2023. "Antiretroviral APOBEC3 cytidine deaminases alter HIV-1 provirus integration site profiles," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Corina Maritz & Reihaneh Khaleghi & Michelle N. Yancoskie & Sarah Diethelm & Sonja Brülisauer & Natalia Santos Ferreira & Yang Jiang & Shana J. Sturla & Hanspeter Naegeli, 2023. "ASH1L-MRG15 methyltransferase deposits H3K4me3 and FACT for damage verification in nucleotide excision repair," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Yichen Zhong & Hakimeh Moghaddas Sani & Bishnu P. Paudel & Jason K. K. Low & Ana P. G. Silva & Stefan Mueller & Chandrika Deshpande & Santosh Panjikar & Xavier J. Reid & Max J. Bedward & Antoine M. Oi, 2022. "The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families," Nature Communications, Nature, vol. 13(1), pages 1-17, 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:12:y:2021:i:1:d:10.1038_s41467-021-27338-w. 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.