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The endocannabinoid N-arachidonoyl dopamine is critical for hyperalgesia induced by chronic sleep disruption

Author

Listed:
  • Weihua Ding

    (Harvard Medical School)

  • Liuyue Yang

    (Harvard Medical School)

  • Eleanor Shi

    (Harvard Medical School)

  • Bowon Kim

    (Harvard Medical School)

  • Sarah Low

    (Harvard Medical School)

  • Kun Hu

    (Tuft University School of Medicine)

  • Lei Gao

    (Harvard Medical School)

  • Ping Chen

    (University of Massachusetts Boston)

  • Wei Ding

    (University of Massachusetts Boston)

  • David Borsook

    (Harvard Medical School)

  • Andrew Luo

    (currently at Brandeis University)

  • Jee Hyun Choi

    (Korea Institute of Science and Technology)

  • Changning Wang

    (Harvard Medical School)

  • Oluwaseun Akeju

    (Harvard Medical School)

  • Jun Yang

    (Harvard Medical School)

  • Chongzhao Ran

    (Harvard Medical School)

  • Kristin L. Schreiber

    (Harvard Medical School)

  • Jianren Mao

    (Harvard Medical School)

  • Qian Chen

    (Massachusetts Institute of Technology
    Chinese Academy of Sciences)

  • Guoping Feng

    (Massachusetts Institute of Technology)

  • Shiqian Shen

    (Harvard Medical School)

Abstract

Chronic pain is highly prevalent and is linked to a broad range of comorbidities, including sleep disorders. Epidemiological and clinical evidence suggests that chronic sleep disruption (CSD) leads to heightened pain sensitivity, referred to as CSD-induced hyperalgesia. However, the underlying mechanisms are unclear. The thalamic reticular nucleus (TRN) has unique integrative functions in sensory processing, attention/arousal and sleep spindle generation. We report that the TRN played an important role in CSD-induced hyperalgesia in mice, through its projections to the ventroposterior region of the thalamus. Metabolomics revealed that the level of N-arachidonoyl dopamine (NADA), an endocannabinoid, was decreased in the TRN after CSD. Using a recently developed CB1 receptor (cannabinoid receptor 1) activity sensor with spatiotemporal resolution, CB1 receptor activity in the TRN was found to be decreased after CSD. Moreover, CSD-induced hyperalgesia was attenuated by local NADA administration to the TRN. Taken together, these results suggest that TRN NADA signaling is critical for CSD-induced hyperalgesia.

Suggested Citation

  • Weihua Ding & Liuyue Yang & Eleanor Shi & Bowon Kim & Sarah Low & Kun Hu & Lei Gao & Ping Chen & Wei Ding & David Borsook & Andrew Luo & Jee Hyun Choi & Changning Wang & Oluwaseun Akeju & Jun Yang & C, 2023. "The endocannabinoid N-arachidonoyl dopamine is critical for hyperalgesia induced by chronic sleep disruption," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42283-6
    DOI: 10.1038/s41467-023-42283-6
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    1. Daniel Jimenez-Blasco & Arnau Busquets-Garcia & Etienne Hebert-Chatelain & Roman Serrat & Carlos Vicente-Gutierrez & Christina Ioannidou & Paula Gómez-Sotres & Irene Lopez-Fabuel & Monica Resch-Beushe, 2020. "Glucose metabolism links astroglial mitochondria to cannabinoid effects," Nature, Nature, vol. 583(7817), pages 603-608, July.
    2. Fan Fei & Xia Wang & Cenglin Xu & Jiaying Shi & Yiwei Gong & Heming Cheng & Nanxi Lai & Yeping Ruan & Yao Ding & Shuang Wang & Zhong Chen & Yi Wang, 2022. "Discrete subicular circuits control generalization of hippocampal seizures," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Rosa I. Martinez-Garcia & Bettina Voelcker & Julia B. Zaltsman & Saundra L. Patrick & Tanya R. Stevens & Barry W. Connors & Scott J. Cruikshank, 2020. "Publisher Correction: Two dynamically distinct circuits drive inhibition in the sensory thalamus," Nature, Nature, vol. 585(7825), pages 13-13, September.
    4. Marco Koch & Luis Varela & Jae Geun Kim & Jung Dae Kim & Francisco Hernández-Nuño & Stephanie E. Simonds & Carlos M. Castorena & Claudia R. Vianna & Joel K. Elmquist & Yury M. Morozov & Pasko Rakic & , 2015. "Hypothalamic POMC neurons promote cannabinoid-induced feeding," Nature, Nature, vol. 519(7541), pages 45-50, March.
    5. Yi Li & Weixin Zhong & Daqing Wang & Qiru Feng & Zhixiang Liu & Jingfeng Zhou & Chunying Jia & Fei Hu & Jiawei Zeng & Qingchun Guo & Ling Fu & Minmin Luo, 2016. "Serotonin neurons in the dorsal raphe nucleus encode reward signals," Nature Communications, Nature, vol. 7(1), pages 1-15, April.
    6. Rosa I. Martinez-Garcia & Bettina Voelcker & Julia B. Zaltsman & Saundra L. Patrick & Tanya R. Stevens & Barry W. Connors & Scott J. Cruikshank, 2020. "Two dynamically distinct circuits drive inhibition in the sensory thalamus," Nature, Nature, vol. 583(7818), pages 813-818, July.
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