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Area postrema neurons mediate interleukin-6 function in cancer cachexia

Author

Listed:
  • Qingtao Sun

    (Cold Spring Harbor Laboratory)

  • Daniëlle Lisdonk

    (Cold Spring Harbor Laboratory
    University of Amsterdam)

  • Miriam Ferrer

    (Cold Spring Harbor Laboratory)

  • Bruno Gegenhuber

    (Cold Spring Harbor Laboratory)

  • Melody Wu

    (Cold Spring Harbor Laboratory)

  • Youngkyu Park

    (Cold Spring Harbor Laboratory)

  • David A. Tuveson

    (Cold Spring Harbor Laboratory)

  • Jessica Tollkuhn

    (Cold Spring Harbor Laboratory)

  • Tobias Janowitz

    (Cold Spring Harbor Laboratory)

  • Bo Li

    (Cold Spring Harbor Laboratory
    Westlake Laboratory of Life Sciences and Biomedicine
    Westlake University
    Westlake Institute for Advanced Study)

Abstract

Interleukin-6 (IL-6) has been long considered a key player in cancer cachexia. It is believed that sustained elevation of IL-6 production during cancer progression causes brain dysfunctions, which ultimately result in cachexia. However, how peripheral IL-6 influences the brain remains poorly understood. Here we show that neurons in the area postrema (AP), a circumventricular structure in the hindbrain, is a critical mediator of IL-6 function in cancer cachexia in male mice. We find that circulating IL-6 can rapidly enter the AP and activate neurons in the AP and its associated network. Peripheral tumor, known to increase circulating IL-6, leads to elevated IL-6 in the AP, and causes potentiated excitatory synaptic transmission onto AP neurons and AP network hyperactivity. Remarkably, neutralization of IL-6 in the brain of tumor-bearing mice with an anti-IL-6 antibody attenuates cachexia and the hyperactivity in the AP network, and markedly prolongs lifespan. Furthermore, suppression of Il6ra, the gene encoding IL-6 receptor, specifically in AP neurons with CRISPR/dCas9 interference achieves similar effects. Silencing Gfral-expressing AP neurons also attenuates cancer cachectic phenotypes and AP network hyperactivity. Our study identifies a central mechanism underlying the function of peripheral IL-6, which may serve as a target for treating cancer cachexia.

Suggested Citation

  • Qingtao Sun & Daniëlle Lisdonk & Miriam Ferrer & Bruno Gegenhuber & Melody Wu & Youngkyu Park & David A. Tuveson & Jessica Tollkuhn & Tobias Janowitz & Bo Li, 2024. "Area postrema neurons mediate interleukin-6 function in cancer cachexia," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48971-1
    DOI: 10.1038/s41467-024-48971-1
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    1. Esther B. Florsheim & Nathaniel D. Bachtel & Jaime L. Cullen & Bruna G. C. Lima & Mahdieh Godazgar & Fernando Carvalho & Carolina P. Chatain & Marcelo R. Zimmer & Cuiling Zhang & Gregory Gautier & Pie, 2023. "Immune sensing of food allergens promotes avoidance behaviour," Nature, Nature, vol. 620(7974), pages 643-650, August.
    2. Jer-Yuan Hsu & Suzanne Crawley & Michael Chen & Dina A. Ayupova & Darrin A. Lindhout & Jared Higbee & Alan Kutach & William Joo & Zhengyu Gao & Diana Fu & Carmen To & Kalyani Mondal & Betty Li & Avant, 2017. "Non-homeostatic body weight regulation through a brainstem-restricted receptor for GDF15," Nature, Nature, vol. 550(7675), pages 255-259, October.
    3. Filipa Cardoso & Roel G. J. Klein Wolterink & Cristina Godinho-Silva & Rita G. Domingues & Hélder Ribeiro & Joaquim Alves da Silva & Inês Mahú & Ana I. Domingos & Henrique Veiga-Fernandes, 2021. "Neuro-mesenchymal units control ILC2 and obesity via a brain–adipose circuit," Nature, Nature, vol. 597(7876), pages 410-414, September.
    4. Andre Lima Queiroz & Ezequiel Dantas & Shakti Ramsamooj & Anirudh Murthy & Mujmmail Ahmed & Elizabeth R. M. Zunica & Roger J. Liang & Jessica Murphy & Corey D. Holman & Curtis J. Bare & Gregory Ghahra, 2022. "Blocking ActRIIB and restoring appetite reverses cachexia and improves survival in mice with lung cancer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Carolyn W. Roman & Victor A. Derkach & Richard D. Palmiter, 2016. "Genetically and functionally defined NTS to PBN brain circuits mediating anorexia," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    6. Xu Zhang & Bo Lei & Yuan Yuan & Li Zhang & Lu Hu & Sen Jin & Bilin Kang & Xuebin Liao & Wenzhi Sun & Fuqiang Xu & Yi Zhong & Ji Hu & Hai Qi, 2020. "Brain control of humoral immune responses amenable to behavioural modulation," Nature, Nature, vol. 581(7807), pages 204-208, May.
    7. Anoj Ilanges & Rani Shiao & Jordan Shaked & Ji-Dung Luo & Xiaofei Yu & Jeffrey M. Friedman, 2022. "Brainstem ADCYAP1+ neurons control multiple aspects of sickness behaviour," Nature, Nature, vol. 609(7928), pages 761-771, September.
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