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Sensory nerve niche regulates mesenchymal stem cell homeostasis via FGF/mTOR/autophagy axis

Author

Listed:
  • Fei Pei

    (University of Southern California
    Wuhan University)

  • Li Ma

    (University of Southern California)

  • Junjun Jing

    (University of Southern California)

  • Jifan Feng

    (University of Southern California)

  • Yuan Yuan

    (University of Southern California)

  • Tingwei Guo

    (University of Southern California)

  • Xia Han

    (University of Southern California)

  • Thach-Vu Ho

    (University of Southern California)

  • Jie Lei

    (University of Southern California)

  • Jinzhi He

    (University of Southern California)

  • Mingyi Zhang

    (University of Southern California)

  • Jian-Fu Chen

    (University of Southern California)

  • Yang Chai

    (University of Southern California)

Abstract

Mesenchymal stem cells (MSCs) reside in microenvironments, referred to as niches, which provide structural support and molecular signals. Sensory nerves are niche components in the homeostasis of tissues such as skin, bone marrow and hematopoietic system. However, how the sensory nerve affects the behavior of MSCs remains largely unknown. Here we show that the sensory nerve is vital for mesenchymal tissue homeostasis and maintenance of MSCs in the continuously growing adult mouse incisor. Loss of sensory innervation leads to mesenchymal disorder and a decrease in MSCs. Mechanistically, FGF1 from the sensory nerve directly acts on MSCs by binding to FGFR1 and activates the mTOR/autophagy axis to sustain MSCs. Modulation of mTOR/autophagy restores the MSCs and rescues the mesenchymal tissue disorder of Fgfr1 mutant mice. Collectively, our study provides insights into the role of sensory nerves in the regulation of MSC homeostasis and the mechanism governing it.

Suggested Citation

  • Fei Pei & Li Ma & Junjun Jing & Jifan Feng & Yuan Yuan & Tingwei Guo & Xia Han & Thach-Vu Ho & Jie Lei & Jinzhi He & Mingyi Zhang & Jian-Fu Chen & Yang Chai, 2023. "Sensory nerve niche regulates mesenchymal stem cell homeostasis via FGF/mTOR/autophagy axis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35977-4
    DOI: 10.1038/s41467-023-35977-4
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    1. Toru Fukuda & Shu Takeda & Ren Xu & Hiroki Ochi & Satoko Sunamura & Tsuyoshi Sato & Shinsuke Shibata & Yutaka Yoshida & Zirong Gu & Ayako Kimura & Chengshan Ma & Cheng Xu & Waka Bando & Koji Fujita & , 2013. "Sema3A regulates bone-mass accrual through sensory innervations," Nature, Nature, vol. 497(7450), pages 490-493, May.
    2. Hao Chen & Bo Hu & Xiao Lv & Shouan Zhu & Gehua Zhen & Mei Wan & Amit Jain & Bo Gao & Yu Chai & Mi Yang & Xiao Wang & Ruoxian Deng & Lei Wang & Yong Cao & Shuangfei Ni & Shen Liu & Wen Yuan & Huajiang, 2019. "Prostaglandin E2 mediates sensory nerve regulation of bone homeostasis," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Toshiro Sato & Johan H. van Es & Hugo J. Snippert & Daniel E. Stange & Robert G. Vries & Maaike van den Born & Nick Barker & Noah F. Shroyer & Marc van de Wetering & Hans Clevers, 2011. "Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts," Nature, Nature, vol. 469(7330), pages 415-418, January.
    4. Jae Myoung Suh & Johan W. Jonker & Maryam Ahmadian & Regina Goetz & Denise Lackey & Olivia Osborn & Zhifeng Huang & Weilin Liu & Eiji Yoshihara & Theo H. van Dijk & Rick Havinga & Weiwei Fan & Yun-Qia, 2014. "Endocrinization of FGF1 produces a neomorphic and potent insulin sensitizer," Nature, Nature, vol. 513(7518), pages 436-439, September.
    5. Christian F. Guerrero-Juarez & Priya H. Dedhia & Suoqin Jin & Rolando Ruiz-Vega & Dennis Ma & Yuchen Liu & Kosuke Yamaga & Olga Shestova & Denise L. Gay & Zaixin Yang & Kai Kessenbrock & Qing Nie & Wa, 2019. "Single-cell analysis reveals fibroblast heterogeneity and myeloid-derived adipocyte progenitors in murine skin wounds," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    6. Seungyong Lee & Charles Hwang & Simone Marini & Robert J. Tower & Qizhi Qin & Stefano Negri & Chase A. Pagani & Yuxiao Sun & David M. Stepien & Michael Sorkin & Carrie A. Kubiak & Noelle D. Visser & C, 2021. "NGF-TrkA signaling dictates neural ingrowth and aberrant osteochondral differentiation after soft tissue trauma," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    7. Sean C. Bendall & Morag H. Stewart & Pablo Menendez & Dustin George & Kausalia Vijayaragavan & Tamra Werbowetski-Ogilvie & Veronica Ramos-Mejia & Anne Rouleau & Jiabi Yang & Marc Bossé & Gilles Lajoie, 2007. "IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro," Nature, Nature, vol. 448(7157), pages 1015-1021, August.
    8. David T. Scadden, 2006. "The stem-cell niche as an entity of action," Nature, Nature, vol. 441(7097), pages 1075-1079, June.
    9. Xin Gao & Dachuan Zhang & Chunliang Xu & Huihui Li & Kathleen M. Caron & Paul S. Frenette, 2021. "Nociceptive nerves regulate haematopoietic stem cell mobilization," Nature, Nature, vol. 589(7843), pages 591-596, January.
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