IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-35977-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-35977-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-35977-4?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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. David T. Scadden, 2006. "The stem-cell niche as an entity of action," Nature, Nature, vol. 441(7097), pages 1075-1079, June.
    8. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Mingyi Zhang & Tingwei Guo & Fei Pei & Jifan Feng & Junjun Jing & Jian Xu & Takahiko Yamada & Thach-Vu Ho & Jiahui Du & Prerna Sehgal & Yang Chai, 2024. "ARID1B maintains mesenchymal stem cell quiescence via inhibition of BCL11B-mediated non-canonical Activin signaling," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

    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. Lijun Wang & Xiuling You & Dengfeng Ruan & Rui Shao & Hai-Qiang Dai & Weiliang Shen & Guo-Liang Xu & Wanlu Liu & Weiguo Zou, 2022. "TET enzymes regulate skeletal development through increasing chromatin accessibility of RUNX2 target genes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Xingxing Ren & Qiuyuan Liu & Peirong Zhou & Tingyue Zhou & Decai Wang & Qiao Mei & Richard A. Flavell & Zhanju Liu & Mingsong Li & Wen Pan & Shu Zhu, 2024. "DHX9 maintains epithelial homeostasis by restraining R-loop-mediated genomic instability in intestinal stem cells," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Katarzyna M. Sitnik & Fran Krstanović & Natascha Gödecke & Ulfert Rand & Tobias Kubsch & Henrike Maaß & Yeonsu Kim & Ilija Brizić & Luka Čičin-Šain, 2023. "Fibroblasts are a site of murine cytomegalovirus lytic replication and Stat1-dependent latent persistence in vivo," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Yadong Qi & Jiamin He & Yawen Zhang & Qiwei Ge & Qiwen Wang & Luyi Chen & Jilei Xu & Lan Wang & Xueqin Chen & Dingjiacheng Jia & Yifeng Lin & Chaochao Xu & Ying Zhang & Tongyao Hou & Jianmin Si & Shuj, 2023. "Heat-inactivated Bifidobacterium adolescentis ameliorates colon senescence through Paneth-like-cell-mediated stem cell activation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Shuting Li & Chia-Wen Lu & Elia C. Diem & Wang Li & Melanie Guderian & Marc Lindenberg & Friederike Kruse & Manuela Buettner & Stefan Floess & Markus R. Winny & Robert Geffers & Hans-Hermann Richnow &, 2022. "Acetyl-CoA-Carboxylase 1-mediated de novo fatty acid synthesis sustains Lgr5+ intestinal stem cell function," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Liang Yang & Zifeng Ruan & Xiaobing Lin & Hao Wang & Yanmin Xin & Haite Tang & Zhijuan Hu & Yunhao Zhou & Yi Wu & Junwei Wang & Dajiang Qin & Gang Lu & Kerry M. Loomes & Wai-Yee Chan & Xingguo Liu, 2024. "NAD+ dependent UPRmt activation underlies intestinal aging caused by mitochondrial DNA mutations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Marco Calafiore & Ya-Yuan Fu & Paola Vinci & Viktor Arnhold & Winston Y. Chang & Suze A. Jansen & Anastasiya Egorova & Shuichiro Takashima & Jason Kuttiyara & Takahiro Ito & Jonathan Serody & Susumu N, 2023. "A tissue-intrinsic IL-33/EGF circuit promotes epithelial regeneration after intestinal injury," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Jong Hoon Won & Jacob S. Choi & Joon-Il Jun, 2022. "CCN1 interacts with integrins to regulate intestinal stem cell proliferation and differentiation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Shruthi Kalgudde Gopal & Ruoxuan Dai & Ania Maria Stefanska & Meshal Ansari & Jiakuan Zhao & Pushkar Ramesh & Johannes W. Bagnoli & Donovan Correa-Gallegos & Yue Lin & Simon Christ & Ilias Angelidis &, 2023. "Wound infiltrating adipocytes are not myofibroblasts," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Simone Isling Pærregaard & Line Wulff & Sophie Schussek & Kristoffer Niss & Urs Mörbe & Johan Jendholm & Kerstin Wendland & Anna T. Andrusaite & Kevin F. Brulois & Robert J. B. Nibbs & Katarzyna Sitni, 2023. "The small and large intestine contain related mesenchymal subsets that derive from embryonic Gli1+ precursors," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Ihab Ansari & Llorenç Solé-Boldo & Meshi Ridnik & Julian Gutekunst & Oliver Gilliam & Maria Korshko & Timur Liwinski & Birgit Jickeli & Noa Weinberg-Corem & Michal Shoshkes-Carmel & Eli Pikarsky & Era, 2023. "TET2 and TET3 loss disrupts small intestine differentiation and homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Qi Liu & Charles A Herring & Quanhu Sheng & Jie Ping & Alan J Simmons & Bob Chen & Amrita Banerjee & Wei Li & Guoqiang Gu & Robert J Coffey & Yu Shyr & Ken S Lau, 2018. "Quantitative assessment of cell population diversity in single-cell landscapes," PLOS Biology, Public Library of Science, vol. 16(10), pages 1-29, October.
    13. Lingchi Kong & Xin Gao & Xiangyun Yao & Haijiao Xie & Qinglin Kang & Wei Sun & Zhengwei You & Yun Qian & Cunyi Fan, 2024. "Multilevel neurium-mimetic individualized graft via additive manufacturing for efficient tissue repair," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Fengwei Zhang & Wei Qiao & Ji-an Wei & Zhengyi Tao & Congjia Chen & Yefeng Wu & Minghui Lin & Ka Man Carmen Ng & Li Zhang & Kelvin Wai-Kwok Yeung & Billy Kwok Chong Chow, 2024. "Secretin-dependent signals in the ventromedial hypothalamus regulate energy metabolism and bone homeostasis in mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Victoria H. Ng & Zachary Spencer & Leif R. Neitzel & Anmada Nayak & Matthew A. Loberg & Chen Shen & Sara N. Kassel & Heather K. Kroh & Zhenyi An & Christin C. Anthony & Jamal M. Bryant & Amanda Lawson, 2023. "The USP46 complex deubiquitylates LRP6 to promote Wnt/β-catenin signaling," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    16. Jina Yun & Simon Hansen & Otto Morris & David T. Madden & Clare Peters Libeu & Arjun J. Kumar & Cameron Wehrfritz & Aaron H. Nile & Yingnan Zhang & Lijuan Zhou & Yuxin Liang & Zora Modrusan & Michelle, 2023. "Senescent cells perturb intestinal stem cell differentiation through Ptk7 induced noncanonical Wnt and YAP signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Ruiye Bi & Qing Yin & Haohan Li & Xianni Yang & Yiru Wang & Qianli Li & Han Fang & Peiran Li & Ping Lyu & Yi Fan & Binbin Ying & Songsong Zhu, 2023. "A single-cell transcriptional atlas reveals resident progenitor cell niche functions in TMJ disc development and injury," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Stephen J. Gaudino & Ankita Singh & Huakang Huang & Jyothi Padiadpu & Makheni Jean-Pierre & Cody Kempen & Tej Bahadur & Kiyoshi Shiomitsu & Richard Blumberg & Kenneth R. Shroyer & Semir Beyaz & Natali, 2024. "Intestinal IL-22RA1 signaling regulates intrinsic and systemic lipid and glucose metabolism to alleviate obesity-associated disorders," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. Zhdanov, Vladimir P., 2009. "Signal propagation in stem-cell niches," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 388(18), pages 3791-3797.
    20. Joana Silva & Ferhat Alkan & Sofia Ramalho & Goda Snieckute & Stefan Prekovic & Ana Krotenberg Garcia & Santiago Hernández-Pérez & Rob Kammen & Danielle Barnum & Liesbeth Hoekman & Maarten Altelaar & , 2022. "Ribosome impairment regulates intestinal stem cell identity via ZAKɑ activation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    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:14:y:2023:i:1:d:10.1038_s41467-023-35977-4. 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.