IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47311-7.html
   My bibliography  Save this article

Compensatory growth and recovery of cartilage cytoarchitecture after transient cell death in fetal mouse limbs

Author

Listed:
  • Chee Ho H’ng

    (Monash University)

  • Shanika L. Amarasinghe

    (Monash University
    Monash University)

  • Boya Zhang

    (Monash University)

  • Hojin Chang

    (Monash University
    Dentistry & Health Sciences. The University of Melbourne)

  • Xinli Qu

    (Monash University)

  • David R. Powell

    (Monash University)

  • Alberto Rosello-Diez

    (Monash University
    University of Cambridge)

Abstract

A major question in developmental and regenerative biology is how organ size and architecture are controlled by progenitor cells. While limb bones exhibit catch-up growth (recovery of a normal growth trajectory after transient developmental perturbation), it is unclear how this emerges from the behaviour of chondroprogenitors, the cells sustaining the cartilage anlagen that are progressively replaced by bone. Here we show that transient sparse cell death in the mouse fetal cartilage is repaired postnatally, via a two-step process. During injury, progression of chondroprogenitors towards more differentiated states is delayed, leading to altered cartilage cytoarchitecture and impaired bone growth. Then, once cell death is over, chondroprogenitor differentiation is accelerated and cartilage structure recovered, including partial rescue of bone growth. At the molecular level, ectopic activation of mTORC1 correlates with, and is necessary for, part of the recovery, revealing a specific candidate to be explored during normal growth and in future therapies.

Suggested Citation

  • Chee Ho H’ng & Shanika L. Amarasinghe & Boya Zhang & Hojin Chang & Xinli Qu & David R. Powell & Alberto Rosello-Diez, 2024. "Compensatory growth and recovery of cartilage cytoarchitecture after transient cell death in fetal mouse limbs," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47311-7
    DOI: 10.1038/s41467-024-47311-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47311-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47311-7?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. Joseph T. Rodgers & Katherine Y. King & Jamie O. Brett & Melinda J. Cromie & Gregory W. Charville & Katie K. Maguire & Christopher Brunson & Namrata Mastey & Ling Liu & Chang-Ru Tsai & Margaret A. Goo, 2014. "mTORC1 controls the adaptive transition of quiescent stem cells from G0 to GAlert," Nature, Nature, vol. 510(7505), pages 393-396, June.
    2. Phillip T. Newton & Lei Li & Baoyi Zhou & Christoph Schweingruber & Maria Hovorakova & Meng Xie & Xiaoyan Sun & Lakshmi Sandhow & Artem V. Artemov & Evgeny Ivashkin & Simon Suter & Vyacheslav Dyachuk , 2019. "A radical switch in clonality reveals a stem cell niche in the epiphyseal growth plate," Nature, Nature, vol. 567(7747), pages 234-238, March.
    3. Henry M. Kronenberg, 2003. "Developmental regulation of the growth plate," Nature, Nature, vol. 423(6937), pages 332-336, May.
    4. Smyth Gordon K, 2004. "Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 3(1), pages 1-28, February.
    5. Shanmugam Muruganandan & Rachel Pierce & Dian Astari Teguh & Rocio Fuente Perez & Nicole Bell & Brandon Nguyen & Katherine Hohl & Brian D. Snyder & Mark W. Grinstaff & Hannah Alberico & Dori Woods & Y, 2022. "A FoxA2+ long-term stem cell population is necessary for growth plate cartilage regeneration after injury," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Jeffrey T Leek & John D Storey, 2007. "Capturing Heterogeneity in Gene Expression Studies by Surrogate Variable Analysis," PLOS Genetics, Public Library of Science, vol. 3(9), pages 1-12, September.
    7. Kimberly L. Cooper & Seungeun Oh & Yongjin Sung & Ramachandra R. Dasari & Marc W. Kirschner & Clifford J. Tabin, 2013. "Multiple phases of chondrocyte enlargement underlie differences in skeletal proportions," Nature, Nature, vol. 495(7441), pages 375-378, March.
    8. Bo Yan & Zhongmin Zhang & Dadi Jin & Chen Cai & Chunhong Jia & Wen Liu & Ting Wang & Shengfa Li & Haiyan Zhang & Bin Huang & Pinglin Lai & Hua Wang & Anling Liu & Chun Zeng & Daozhang Cai & Yu Jiang &, 2016. "mTORC1 regulates PTHrP to coordinate chondrocyte growth, proliferation and differentiation," Nature Communications, Nature, vol. 7(1), pages 1-15, September.
    9. Koji Mizuhashi & Wanida Ono & Yuki Matsushita & Naoko Sakagami & Akira Takahashi & Thomas L. Saunders & Takashi Nagasawa & Henry M. Kronenberg & Noriaki Ono, 2018. "Resting zone of the growth plate houses a unique class of skeletal stem cells," Nature, Nature, vol. 563(7730), pages 254-258, November.
    10. Anjali P. Kusumbe & Saravana K. Ramasamy & Ralf H. Adams, 2014. "Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone," Nature, Nature, vol. 507(7492), pages 323-328, March.
    11. Anjali P. Kusumbe & Saravana K. Ramasamy & Ralf H. Adams, 2014. "Correction: Corrigendum: Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone," Nature, Nature, vol. 513(7519), pages 574-574, September.
    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. Marketa Kaucka & Alberto Joven Araus & Marketa Tesarova & Joshua D. Currie & Johan Boström & Michaela Kavkova & Julian Petersen & Zeyu Yao & Anass Bouchnita & Andreas Hellander & Tomas Zikmund & Ahmed, 2022. "Altered developmental programs and oriented cell divisions lead to bulky bones during salamander limb regeneration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Masayuki Tsukasaki & Noriko Komatsu & Takako Negishi-Koga & Nam Cong-Nhat Huynh & Ryunosuke Muro & Yutaro Ando & Yuka Seki & Asuka Terashima & Warunee Pluemsakunthai & Takeshi Nitta & Takashi Nakamura, 2022. "Periosteal stem cells control growth plate stem cells during postnatal skeletal growth," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Aaron Warren & Ryan M. Porter & Olivia Reyes-Castro & Md Mohsin Ali & Adriana Marques-Carvalho & Ha-Neui Kim & Landon B. Gatrell & Ernestina Schipani & Intawat Nookaew & Charles A. O’Brien & Roy Morel, 2023. "The NAD salvage pathway in mesenchymal cells is indispensable for skeletal development in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Young-Woong Kim & Greta Zara & HyunJun Kang & Sergio Branciamore & Denis O’Meally & Yuxin Feng & Chia-Yi Kuan & Yingjun Luo & Michael S. Nelson & Alex B. Brummer & Russell Rockne & Zhen Bouman Chen & , 2022. "Integration of single-cell transcriptomes and biological function reveals distinct behavioral patterns in bone marrow endothelium," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Leek Jeffrey T & Storey John D., 2011. "The Joint Null Criterion for Multiple Hypothesis Tests," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 10(1), pages 1-22, June.
    6. Cheng-Hai Zhang & Yao Gao & Han-Hwa Hung & Zhu Zhuo & Alan J. Grodzinsky & Andrew B. Lassar, 2022. "Creb5 coordinates synovial joint formation with the genesis of articular cartilage," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Joschka Heil & Victor Olsavszky & Katrin Busch & Kay Klapproth & Carolina Torre & Carsten Sticht & Kajetan Sandorski & Johannes Hoffmann & Hiltrud Schönhaber & Johanna Zierow & Manuel Winkler & Christ, 2021. "Bone marrow sinusoidal endothelium controls terminal erythroid differentiation and reticulocyte maturation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    8. Stephen Salerno Jr. & Mahya Mehrmohamadi & Maria V Liberti & Muting Wan & Martin T Wells & James G Booth & Jason W Locasale, 2017. "RRmix: A method for simultaneous batch effect correction and analysis of metabolomics data in the absence of internal standards," PLOS ONE, Public Library of Science, vol. 12(6), pages 1-19, June.
    9. Yuki Matsushita & Angel Ka Yan Chu & Chiaki Tsutsumi-Arai & Shion Orikasa & Mizuki Nagata & Sunny Y. Wong & Joshua D. Welch & Wanida Ono & Noriaki Ono, 2022. "The fate of early perichondrial cells in developing bones," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Yuki Matsushita & Jialin Liu & Angel Ka Yan Chu & Chiaki Tsutsumi-Arai & Mizuki Nagata & Yuki Arai & Wanida Ono & Kouhei Yamamoto & Thomas L. Saunders & Joshua D. Welch & Noriaki Ono, 2023. "Bone marrow endosteal stem cells dictate active osteogenesis and aggressive tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    11. Shanmugam Muruganandan & Rachel Pierce & Dian Astari Teguh & Rocio Fuente Perez & Nicole Bell & Brandon Nguyen & Katherine Hohl & Brian D. Snyder & Mark W. Grinstaff & Hannah Alberico & Dori Woods & Y, 2022. "A FoxA2+ long-term stem cell population is necessary for growth plate cartilage regeneration after injury," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Kynon J. M. Benjamin & Ria Arora & Arthur S. Feltrin & Geo Pertea & Hunter H. Giles & Joshua M. Stolz & Laura D’Ignazio & Leonardo Collado-Torres & Joo Heon Shin & William S. Ulrich & Thomas M. Hyde &, 2024. "Sex affects transcriptional associations with schizophrenia across the dorsolateral prefrontal cortex, hippocampus, and caudate nucleus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. M. Gabriele Bixel & Kishor K. Sivaraj & Melanie Timmen & Vishal Mohanakrishnan & Anusha Aravamudhan & Susanne Adams & Bong-Ihn Koh & Hyun-Woo Jeong & Kai Kruse & Richard Stange & Ralf H. Adams, 2024. "Angiogenesis is uncoupled from osteogenesis during calvarial bone regeneration," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    14. Jianping Wang & Bin Zhao & Jingmin Che & Peng Shang, 2023. "Hypoxia Pathway in Osteoporosis: Laboratory Data for Clinical Prospects," IJERPH, MDPI, vol. 20(4), pages 1-22, February.
    15. Aaron C Ericsson & J Wade Davis & William Spollen & Nathan Bivens & Scott Givan & Catherine E Hagan & Mark McIntosh & Craig L Franklin, 2015. "Effects of Vendor and Genetic Background on the Composition of the Fecal Microbiota of Inbred Mice," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-19, February.
    16. Hossain, Ahmed & Beyene, Joseph & Willan, Andrew R. & Hu, Pingzhao, 2009. "A flexible approximate likelihood ratio test for detecting differential expression in microarray data," Computational Statistics & Data Analysis, Elsevier, vol. 53(10), pages 3685-3695, August.
    17. Xiaohong Li & Guy N Brock & Eric C Rouchka & Nigel G F Cooper & Dongfeng Wu & Timothy E O’Toole & Ryan S Gill & Abdallah M Eteleeb & Liz O’Brien & Shesh N Rai, 2017. "A comparison of per sample global scaling and per gene normalization methods for differential expression analysis of RNA-seq data," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-22, May.
    18. Ambroise Jérôme & Bearzatto Bertrand & Robert Annie & Macq Benoit & Gala Jean-Luc, 2012. "Combining Multiple Laser Scans of Spotted Microarrays by Means of a Two-Way ANOVA Model," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(3), pages 1-20, February.
    19. J. McClatchy & R. Strogantsev & E. Wolfe & H. Y. Lin & M. Mohammadhosseini & B. A. Davis & C. Eden & D. Goldman & W. H. Fleming & P. Conley & G. Wu & L. Cimmino & H. Mohammed & A. Agarwal, 2023. "Clonal hematopoiesis related TET2 loss-of-function impedes IL1β-mediated epigenetic reprogramming in hematopoietic stem and progenitor cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Alexandra Gyurdieva & Stefan Zajic & Ya-Fang Chang & E. Andres Houseman & Shan Zhong & Jaegil Kim & Michael Nathenson & Thomas Faitg & Mary Woessner & David C. Turner & Aisha N. Hasan & John Glod & Ro, 2022. "Biomarker correlates with response to NY-ESO-1 TCR T cells in patients with synovial sarcoma," Nature Communications, Nature, vol. 13(1), pages 1-18, 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:15:y:2024:i:1:d:10.1038_s41467-024-47311-7. 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.