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Violet-light suppression of thermogenesis by opsin 5 hypothalamic neurons

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  • Kevin X. Zhang

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    University of Cincinnati, College of Medicine)

  • Shane D’Souza

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

  • Brian A. Upton

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    University of Cincinnati, College of Medicine)

  • Stace Kernodle

    (University of Michigan, School of Public Health)

  • Shruti Vemaraju

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center)

  • Gowri Nayak

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center)

  • Kevin D. Gaitonde

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    University of Cincinnati, College of Medicine)

  • Amanda L. Holt

    (Yale University)

  • Courtney D. Linne

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    University of Cincinnati, College of Medicine)

  • April N. Smith

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center)

  • Nathan T. Petts

    (Cincinnati Children’s Hospital Medical Center)

  • Matthew Batie

    (Cincinnati Children’s Hospital Medical Center)

  • Rajib Mukherjee

    (Cincinnati Children’s Hospital Medical Center)

  • Durgesh Tiwari

    (Cincinnati Children’s Hospital Medical Center)

  • Ethan D. Buhr

    (University of Washington Medical School)

  • Russell N. Gelder

    (University of Washington Medical School
    University of Washington Medical School
    University of Washington Medical School)

  • Christina Gross

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

  • Alison Sweeney

    (Yale University)

  • Joan Sanchez-Gurmaches

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    Cincinnati Children’s Hospital Medical Center)

  • Randy J. Seeley

    (University of Michigan, School of Public Health
    University of Michigan, School of Public Health)

  • Richard A. Lang

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

Abstract

The opsin family of G-protein-coupled receptors are used as light detectors in animals. Opsin 5 (also known as neuropsin or OPN5) is a highly conserved opsin that is sensitive to visible violet light1,2. In mice, OPN5 is a known photoreceptor in the retina3 and skin4 but is also expressed in the hypothalamic preoptic area (POA)5. Here we describe a light-sensing pathway in which POA neurons that express Opn5 regulate thermogenesis in brown adipose tissue (BAT). We show that Opn5 is expressed in glutamatergic warm-sensing POA neurons that receive synaptic input from several thermoregulatory nuclei. We further show that Opn5 POA neurons project to BAT and decrease its activity under chemogenetic stimulation. Opn5-null mice show overactive BAT, increased body temperature, and exaggerated thermogenesis when cold-challenged. Moreover, violet photostimulation during cold exposure acutely suppresses BAT temperature in wild-type mice but not in Opn5-null mice. Direct measurements of intracellular cAMP ex vivo show that Opn5 POA neurons increase cAMP when stimulated with violet light. This analysis thus identifies a violet light-sensitive deep brain photoreceptor that normally suppresses BAT thermogenesis.

Suggested Citation

  • Kevin X. Zhang & Shane D’Souza & Brian A. Upton & Stace Kernodle & Shruti Vemaraju & Gowri Nayak & Kevin D. Gaitonde & Amanda L. Holt & Courtney D. Linne & April N. Smith & Nathan T. Petts & Matthew B, 2020. "Violet-light suppression of thermogenesis by opsin 5 hypothalamic neurons," Nature, Nature, vol. 585(7825), pages 420-425, September.
  • Handle: RePEc:nat:nature:v:585:y:2020:i:7825:d:10.1038_s41586-020-2683-0
    DOI: 10.1038/s41586-020-2683-0
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    Citations

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    Cited by:

    1. Tadataka Tsuji & Vladimir Tolstikov & Yang Zhang & Tian Lian Huang & Henrique Camara & Meghan Halpin & Niven R. Narain & King-Wai Yau & Matthew D. Lynes & Michael A. Kiebish & Yu-Hua Tseng, 2024. "Light-responsive adipose-hypothalamus axis controls metabolic regulation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Oliver Tejero & Filip Pamula & Mitsumasa Koyanagi & Takashi Nagata & Pavel Afanasyev & Ishita Das & Xavier Deupi & Mordechai Sheves & Akihisa Terakita & Gebhard F. X. Schertler & Matthew J. Rodrigues , 2024. "Active state structures of a bistable visual opsin bound to G proteins," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Ruina Wang & Lei Xiao & Jianbo Pan & Guangsen Bao & Yunmei Zhu & Di Zhu & Jun Wang & Chengfeng Pei & Qinfeng Ma & Xian Fu & Ziruoyu Wang & Mengdi Zhu & Guoxiang Wang & Ling Gong & Qiuping Tong & Min J, 2023. "Natural product P57 induces hypothermia through targeting pyridoxal kinase," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Wen Z. Yang & Hengchang Xie & Xiaosa Du & Qian Zhou & Yan Xiao & Zhengdong Zhao & Xiaoning Jia & Jianhui Xu & Wen Zhang & Shuang Cai & Zhangjie Li & Xin Fu & Rong Hua & Junhao Cai & Shuang Chang & Jin, 2023. "A parabrachial-hypothalamic parallel circuit governs cold defense in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Ahmed Wagdi & Daniela Malan & Udhayabhaskar Sathyanarayanan & Janosch S. Beauchamp & Markus Vogt & David Zipf & Thomas Beiert & Berivan Mansuroglu & Vanessa Dusend & Mark Meininghaus & Linn Schneider , 2022. "Selective optogenetic control of Gq signaling using human Neuropsin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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