IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-44120-2.html
   My bibliography  Save this article

USP7/Maged1-mediated H2A monoubiquitination in the paraventricular thalamus: an epigenetic mechanism involved in cocaine use disorder

Author

Listed:
  • Julian Cheron

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Leonardo Beccari

    (Centro de Biología Molecular Severo Ochoa, CSIC-UAM
    Université Claude Bernard Lyon 1, Pathophysiology and Genetics of Neuron and Muscle, CNRS UMR 5261, INSERM U1315)

  • Perrine Hagué

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Romain Icick

    (INSERM UMRS_1144, Université Paris Cité)

  • Chloé Despontin

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory)

  • Teresa Carusone

    (European Molecular Biology Laboratory)

  • Matthieu Defrance

    (Interuniversity Institute of Bioinformatics in Brussels, Université Libre de Bruxelles (ULB))

  • Sagar Bhogaraju

    (European Molecular Biology Laboratory)

  • Elena Martin-Garcia

    (Universitat Pompeu Fabra (UPF)
    Hospital del Mar Medical Research Institute (IMIM)
    Universitat Autònoma de Barcelona)

  • Roberto Capellan

    (Universitat Pompeu Fabra (UPF)
    Hospital del Mar Medical Research Institute (IMIM))

  • Rafael Maldonado

    (Universitat Pompeu Fabra (UPF)
    Hospital del Mar Medical Research Institute (IMIM))

  • Florence Vorspan

    (INSERM UMRS_1144, Université Paris Cité)

  • Jérôme Bonnefont

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Institut de Recherches en Biologie Humaine et Moléculaire (IRIBHM))

  • Alban de Kerchove d’Exaerde

    (Université Libre de Bruxelles (ULB), ULB Neuroscience Institute, Neurophysiology Laboratory
    WELBIO)

Abstract

The risk of developing drug addiction is strongly influenced by the epigenetic landscape and chromatin remodeling. While histone modifications such as methylation and acetylation have been studied in the ventral tegmental area and nucleus accumbens (NAc), the role of H2A monoubiquitination remains unknown. Our investigations, initially focused on the scaffold protein melanoma-associated antigen D1 (Maged1), reveal that H2A monoubiquitination in the paraventricular thalamus (PVT) significantly contributes to cocaine-adaptive behaviors and transcriptional repression induced by cocaine. Chronic cocaine use increases H2A monoubiquitination, regulated by Maged1 and its partner USP7. Accordingly, Maged1 specific inactivation in thalamic Vglut2 neurons, or USP7 inhibition, blocks cocaine-evoked H2A monoubiquitination and cocaine locomotor sensitization. Additionally, genetic variations in MAGED1 and USP7 are linked to altered susceptibility to cocaine addiction and cocaine-associated symptoms in humans. These findings unveil an epigenetic modification in a non-canonical reward pathway of the brain and a potent marker of epigenetic risk factors for drug addiction in humans.

Suggested Citation

  • Julian Cheron & Leonardo Beccari & Perrine Hagué & Romain Icick & Chloé Despontin & Teresa Carusone & Matthieu Defrance & Sagar Bhogaraju & Elena Martin-Garcia & Roberto Capellan & Rafael Maldonado & , 2023. "USP7/Maged1-mediated H2A monoubiquitination in the paraventricular thalamus: an epigenetic mechanism involved in cocaine use disorder," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44120-2
    DOI: 10.1038/s41467-023-44120-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44120-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44120-2?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. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    2. Ed S. Lein & Michael J. Hawrylycz & Nancy Ao & Mikael Ayres & Amy Bensinger & Amy Bernard & Andrew F. Boe & Mark S. Boguski & Kevin S. Brockway & Emi J. Byrnes & Lin Chen & Li Chen & Tsuey-Ming Chen &, 2007. "Genome-wide atlas of gene expression in the adult mouse brain," Nature, Nature, vol. 445(7124), pages 168-176, January.
    3. Wei Yang & Yun-Hwa Lee & Amanda E. Jones & Jessica L. Woolnough & Dewang Zhou & Qian Dai & Qiang Wu & Keith E. Giles & Tim M. Townes & Hengbin Wang, 2014. "The histone H2A deubiquitinase Usp16 regulates embryonic stem cell gene expression and lineage commitment," Nature Communications, Nature, vol. 5(1), pages 1-15, September.
    4. Haithem Barbour & Salima Daou & Michael Hendzel & El Bachir Affar, 2020. "Polycomb group-mediated histone H2A monoubiquitination in epigenome regulation and nuclear processes," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. Qi Cao & Xiaoju Wang & Meng Zhao & Rendong Yang & Rohit Malik & Yuanyuan Qiao & Anton Poliakov & Anastasia K. Yocum & Yong Li & Wei Chen & Xuhong Cao & Xia Jiang & Arun Dahiya & Clair Harris & Felix Y, 2014. "The central role of EED in the orchestration of polycomb group complexes," Nature Communications, Nature, vol. 5(1), pages 1-13, May.
    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. C. W. Ryan & S. L. Regan & E. F. Mills & B. T. McGrath & E. Gong & Y. T. Lai & J. B. Sheingold & K. Patel & T. Horowitz & A. Moccia & Y. C. Tsan & A. Srivastava & S. L. Bielas, 2024. "RING1 missense variants reveal sensitivity of DNA damage repair to H2A monoubiquitination dosage during neurogenesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. 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.
    3. S. Vickovic & B. Lötstedt & J. Klughammer & S. Mages & Å Segerstolpe & O. Rozenblatt-Rosen & A. Regev, 2022. "SM-Omics is an automated platform for high-throughput spatial multi-omics," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Poonam Dhillon & Kelly Ann Mulholland & Hailong Hu & Jihwan Park & Xin Sheng & Amin Abedini & Hongbo Liu & Allison Vassalotti & Junnan Wu & Katalin Susztak, 2023. "Increased levels of endogenous retroviruses trigger fibroinflammation and play a role in kidney disease development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Gaylor Boulay & Liliane C. Broye & Rui Dong & Sowmya Iyer & Rajendran Sanalkumar & Yu-Hang Xing & Rémi Buisson & Shruthi Rengarajan & Beverly Naigles & Benoît Duc & Angela Volorio & Mary E. Awad & Raf, 2024. "EWS-WT1 fusion isoforms establish oncogenic programs and therapeutic vulnerabilities in desmoplastic small round cell tumors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Léa J. Becker & Clémentine Fillinger & Robin Waegaert & Sarah H. Journée & Pierre Hener & Beyza Ayazgok & Muris Humo & Meltem Karatas & Maxime Thouaye & Mithil Gaikwad & Laetitia Degiorgis & Marie des, 2023. "The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    9. Xiaohe Lin & Junjie Yin & Yifan Wang & Jing Yao & Qingshun Q. Li & Vit Latzel & Oliver Bossdorf & Yuan-Ye Zhang, 2024. "Environment-induced heritable variations are common in Arabidopsis thaliana," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Quentin I. B. Lemaître & Natascha Bartsch & Ian U. Kouzel & Henriette Busengdal & Gemma Sian Richards & Patrick R. H. Steinmetz & Fabian Rentzsch, 2023. "NvPrdm14d-expressing neural progenitor cells contribute to non-ectodermal neurogenesis in Nematostella vectensis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Songming Tang & Xuejian Cui & Rongxiang Wang & Sijie Li & Siyu Li & Xin Huang & Shengquan Chen, 2024. "scCASE: accurate and interpretable enhancement for single-cell chromatin accessibility sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Raúl F. Pérez & Patricia Tezanos & Alfonso Peñarroya & Alejandro González-Ramón & Rocío G. Urdinguio & Javier Gancedo-Verdejo & Juan Ramón Tejedor & Pablo Santamarina-Ojeda & Juan José Alba-Linares & , 2024. "A multiomic atlas of the aging hippocampus reveals molecular changes in response to environmental enrichment," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    13. Yanming Ren & Zongyao Huang & Lingling Zhou & Peng Xiao & Junwei Song & Ping He & Chuanxing Xie & Ran Zhou & Menghan Li & Xiangqun Dong & Qing Mao & Chao You & Jianguo Xu & Yanhui Liu & Zhigang Lan & , 2023. "Spatial transcriptomics reveals niche-specific enrichment and vulnerabilities of radial glial stem-like cells in malignant gliomas," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Wei Liu & Xu Liao & Ziye Luo & Yi Yang & Mai Chan Lau & Yuling Jiao & Xingjie Shi & Weiwei Zhai & Hongkai Ji & Joe Yeong & Jin Liu, 2023. "Probabilistic embedding, clustering, and alignment for integrating spatial transcriptomics data with PRECAST," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    15. Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Michael R. Kelly & Kamila Wisniewska & Matthew J. Regner & Michael W. Lewis & Andrea A. Perreault & Eric S. Davis & Douglas H. Phanstiel & Joel S. Parker & Hector L. Franco, 2022. "A multi-omic dissection of super-enhancer driven oncogenic gene expression programs in ovarian cancer," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    18. E. R. Velasco & A. Florido & Á Flores & E. Senabre & A. Gomez-Gomez & A. Torres & A. Roca & S. Norrholm & E. L. Newman & P. Das & R. A. Ross & A. Lori & O. J. Pozo & K. J. Ressler & L. L. Garcia-Estev, 2022. "PACAP-PAC1R modulates fear extinction via the ventromedial hypothalamus," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    19. Benjamin L. Walker & Qing Nie, 2023. "NeST: nested hierarchical structure identification in spatial transcriptomic data," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Ioanna Tzani & Marina Castro-Rivadeneyra & Paul Kelly & Lisa Strasser & Lin Zhang & Martin Clynes & Barry L. Karger & Niall Barron & Jonathan Bones & Colin Clarke, 2024. "Detection of host cell microprotein impurities in antibody drug products," Nature Communications, Nature, vol. 15(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:14:y:2023:i:1:d:10.1038_s41467-023-44120-2. 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.