IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34735-2.html
   My bibliography  Save this article

Hypothermia evoked by stimulation of medial preoptic nucleus protects the brain in a mouse model of ischaemia

Author

Listed:
  • Shuai Zhang

    (Southern University of Science and Technology)

  • Xinpei Zhang

    (Southern University of Science and Technology)

  • Haolin Zhong

    (Southern University of Science and Technology)

  • Xuanyi Li

    (Southern University of Science and Technology)

  • Yujie Wu

    (Southern University of Science and Technology)

  • Jun Ju

    (Southern University of Science and Technology)

  • Bo Liu

    (Southern University of Science and Technology)

  • Zhenyu Zhang

    (Southern University of Science and Technology)

  • Hai Yan

    (Southern University of Science and Technology)

  • Yizheng Wang

    (Fudan University)

  • Kun Song

    (Southern University of Science and Technology)

  • Sheng-Tao Hou

    (Southern University of Science and Technology)

Abstract

Therapeutic hypothermia at 32-34 °C during or after cerebral ischaemia is neuroprotective. However, peripheral cold sensor-triggered hypothermia is ineffective and evokes vigorous counteractive shivering thermogenesis and complications that are difficult to tolerate in awake patients. Here, we show in mice that deep brain stimulation (DBS) of warm-sensitive neurones (WSNs) in the medial preoptic nucleus (MPN) produces tolerable hypothermia. In contrast to surface cooling-evoked hypothermia, DBS mice exhibit a torpor-like state without counteractive shivering. Like hypothermia evoked by chemogenetic activation of WSNs, DBS in free-moving mice elicits a rapid lowering of the core body temperature to 32-34 °C, which confers significant brain protection and motor function reservation. Mechanistically, activation of WSNs contributes to DBS-evoked hypothermia. Inhibition of WSNs prevents DBS-evoked hypothermia. Maintaining the core body temperature at normothermia during DBS abolishes DBS-mediated brain protection. Thus, the MPN is a DBS target to evoke tolerable therapeutic hypothermia for stroke treatment.

Suggested Citation

  • Shuai Zhang & Xinpei Zhang & Haolin Zhong & Xuanyi Li & Yujie Wu & Jun Ju & Bo Liu & Zhenyu Zhang & Hai Yan & Yizheng Wang & Kun Song & Sheng-Tao Hou, 2022. "Hypothermia evoked by stimulation of medial preoptic nucleus protects the brain in a mouse model of ischaemia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34735-2
    DOI: 10.1038/s41467-022-34735-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34735-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-34735-2?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. Zhi Zhang & Fernando M. C. V. Reis & Yanlin He & Jae W. Park & Johnathon R. DiVittorio & Nilla Sivakumar & J. Edward van Veen & Sandra Maesta-Pereira & Michael Shum & India Nichols & Megan G. Massa & , 2020. "Estrogen-sensitive medial preoptic area neurons coordinate torpor in mice," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. Sinisa Hrvatin & Senmiao Sun & Oren F. Wilcox & Hanqi Yao & Aurora J. Lavin-Peter & Marcelo Cicconet & Elena G. Assad & Michaela E. Palmer & Sage Aronson & Alexander S. Banks & Eric C. Griffith & Mich, 2020. "Neurons that regulate mouse torpor," Nature, Nature, vol. 583(7814), pages 115-121, July.
    3. Daniel Kroeger & Gianna Absi & Celia Gagliardi & Sathyajit S. Bandaru & Joseph C. Madara & Loris L. Ferrari & Elda Arrigoni & Heike Münzberg & Thomas E. Scammell & Clifford B. Saper & Ramalingam Vetri, 2018. "Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Carol Kilkenny & William J Browne & Innes C Cuthill & Michael Emerson & Douglas G Altman, 2010. "Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research," PLOS Biology, Public Library of Science, vol. 8(6), pages 1-5, June.
    5. Tohru M. Takahashi & Genshiro A. Sunagawa & Shingo Soya & Manabu Abe & Katsuyasu Sakurai & Kiyomi Ishikawa & Masashi Yanagisawa & Hiroshi Hama & Emi Hasegawa & Atsushi Miyawaki & Kenji Sakimura & Masa, 2020. "A discrete neuronal circuit induces a hibernation-like state in rodents," Nature, Nature, vol. 583(7814), pages 109-114, July.
    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. Shaowen Qian & Sumei Yan & Ruiqi Pang & Jing Zhang & Kai Liu & Zhiyue Shi & Zhaoqun Wang & Penghui Chen & Yanjie Zhang & Tiantian Luo & Xianli Hu & Ying Xiong & Yi Zhou, 2022. "A temperature-regulated circuit for feeding behavior," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. 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.
    3. Airi Jo-Watanabe & Toshiki Inaba & Takahiro Osada & Ryota Hashimoto & Tomohiro Nishizawa & Toshiaki Okuno & Sayoko Ihara & Kazushige Touhara & Nobutaka Hattori & Masatsugu Oh-Hora & Osamu Nureki & Tak, 2024. "Bicarbonate signalling via G protein-coupled receptor regulates ischaemia-reperfusion injury," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Dean A Fergusson & Marc T Avey & Carly C Barron & Mathew Bocock & Kristen E Biefer & Sylvain Boet & Stephane L Bourque & Isidora Conic & Kai Chen & Yuan Yi Dong & Grace M Fox & Ronald B George & Neil , 2019. "Reporting preclinical anesthesia study (REPEAT): Evaluating the quality of reporting in the preclinical anesthesiology literature," PLOS ONE, Public Library of Science, vol. 14(5), pages 1-15, May.
    5. M Polyakova & M L Schroeter & B M Elzinga & S Holiga & P Schoenknecht & E R de Kloet & M L Molendijk, 2015. "Brain-Derived Neurotrophic Factor and Antidepressive Effect of Electroconvulsive Therapy: Systematic Review and Meta-Analyses of the Preclinical and Clinical Literature," PLOS ONE, Public Library of Science, vol. 10(11), pages 1-18, November.
    6. Kimberley E Wever & Carlijn R Hooijmans & Niels P Riksen & Thomas B Sterenborg & Emily S Sena & Merel Ritskes-Hoitinga & Michiel C Warlé, 2015. "Determinants of the Efficacy of Cardiac Ischemic Preconditioning: A Systematic Review and Meta-Analysis of Animal Studies," PLOS ONE, Public Library of Science, vol. 10(11), pages 1-17, November.
    7. Bettina Bert & Céline Heinl & Justyna Chmielewska & Franziska Schwarz & Barbara Grune & Andreas Hensel & Matthias Greiner & Gilbert Schönfelder, 2019. "Refining animal research: The Animal Study Registry," PLOS Biology, Public Library of Science, vol. 17(10), pages 1-12, October.
    8. Xiao-meng Xu & Guang-yan Cai & Ru Bu & Wen-juan Wang & Xue-yuan Bai & Xue-feng Sun & Xiang-mei Chen, 2015. "Beneficial Effects of Caloric Restriction on Chronic Kidney Disease in Rodent Models: A Meta-Analysis and Systematic Review," PLOS ONE, Public Library of Science, vol. 10(12), pages 1-15, December.
    9. Zhongwei Xu & Bingze Xu & Susanna L. Lundström & Àlex Moreno-Giró & Danxia Zhao & Myriam Martin & Erik Lönnblom & Qixing Li & Alexander Krämer & Changrong Ge & Lei Cheng & Bibo Liang & Dongmei Tong & , 2023. "A subset of type-II collagen-binding antibodies prevents experimental arthritis by inhibiting FCGR3 signaling in neutrophils," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Nathalie Percie du Sert & Viki Hurst & Amrita Ahluwalia & Sabina Alam & Marc T Avey & Monya Baker & William J Browne & Alejandra Clark & Innes C Cuthill & Ulrich Dirnagl & Michael Emerson & Paul Garne, 2020. "The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research," PLOS Biology, Public Library of Science, vol. 18(7), pages 1-12, July.
    11. Vivian Leung & Frédérik Rousseau-Blass & Guy Beauchamp & Daniel S J Pang, 2018. "ARRIVE has not ARRIVEd: Support for the ARRIVE (Animal Research: Reporting of in vivo Experiments) guidelines does not improve the reporting quality of papers in animal welfare, analgesia or anesthesi," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-13, May.
    12. Claudia Kurreck & Esmeralda Castaños-Vélez & Dorette Freyer & Sonja Blumenau & Ingo Przesdzing & Rene Bernard & Ulrich Dirnagl, 2020. "Improving quality of preclinical academic research through auditing: A feasibility study," PLOS ONE, Public Library of Science, vol. 15(10), pages 1-15, October.
    13. Simon Bate & Natasha A Karp, 2014. "A Common Control Group - Optimising the Experiment Design to Maximise Sensitivity," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-12, December.
    14. Laura Maxim & Jeroen P van der Sluijs, 2014. "Qualichem In Vivo: A Tool for Assessing the Quality of In Vivo Studies and Its Application for Bisphenol A," PLOS ONE, Public Library of Science, vol. 9(1), pages 1-16, January.
    15. Beverly S Muhlhausler & Frank H Bloomfield & Matthew W Gillman, 2013. "Whole Animal Experiments Should Be More Like Human Randomized Controlled Trials," PLOS Biology, Public Library of Science, vol. 11(2), pages 1-6, February.
    16. Sarah Driessen & Lambert Bodewein & Dagmar Dechent & David Graefrath & Kristina Schmiedchen & Dominik Stunder & Thomas Kraus & Anne-Kathrin Petri, 2020. "Biological and health-related effects of weak static magnetic fields (≤ 1 mT) in humans and vertebrates: A systematic review," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-18, June.
    17. Constance Holman & Sophie K Piper & Ulrike Grittner & Andreas Antonios Diamantaras & Jonathan Kimmelman & Bob Siegerink & Ulrich Dirnagl, 2016. "Where Have All the Rodents Gone? The Effects of Attrition in Experimental Research on Cancer and Stroke," PLOS Biology, Public Library of Science, vol. 14(1), pages 1-12, January.
    18. Thirumalai Diraviyam & Bin Zhao & Yuan Wang & Ruediger Schade & Antonysamy Michael & Xiaoying Zhang, 2014. "Effect of Chicken Egg Yolk Antibodies (IgY) against Diarrhea in Domesticated Animals: A Systematic Review and Meta-Analysis," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-14, May.
    19. 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.
    20. Bertha Estrella & Elena N. Naumova & Magda Cepeda & Trudy Voortman & Peter D. Katsikis & Hemmo A. Drexhage, 2019. "Effects of Air Pollution on Lung Innate Lymphoid Cells: Review of In Vitro and In Vivo Experimental Studies," IJERPH, MDPI, vol. 16(13), pages 1-15, July.

    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_s41467-022-34735-2. 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.