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Transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution

Author

Listed:
  • Nicholas D. Leigh

    (Brigham and Women’s Hospital
    Broad Institute of MIT and Harvard)

  • Garrett S. Dunlap

    (Brigham and Women’s Hospital
    Broad Institute of MIT and Harvard)

  • Kimberly Johnson

    (Brigham and Women’s Hospital
    Broad Institute of MIT and Harvard)

  • Rachelle Mariano

    (Brigham and Women’s Hospital)

  • Rachel Oshiro

    (Brigham and Women’s Hospital)

  • Alan Y. Wong

    (Brigham and Women’s Hospital
    Harvard University)

  • Donald M. Bryant

    (Brigham and Women’s Hospital)

  • Bess M. Miller

    (Brigham and Women’s Hospital
    Broad Institute of MIT and Harvard)

  • Alex Ratner

    (Harvard Medical School)

  • Andy Chen

    (Brigham and Women’s Hospital)

  • William W. Ye

    (Brigham and Women’s Hospital)

  • Brian J. Haas

    (Broad Institute of MIT and Harvard)

  • Jessica L. Whited

    (Brigham and Women’s Hospital
    Broad Institute of MIT and Harvard
    Harvard University)

Abstract

Regeneration of complex multi-tissue structures, such as limbs, requires the coordinated effort of multiple cell types. In axolotl limb regeneration, the wound epidermis and blastema have been extensively studied via histology, grafting, and bulk-tissue RNA-sequencing. However, defining the contributions of these tissues is hindered due to limited information regarding the molecular identity of the cell types in regenerating limbs. Here we report unbiased single-cell RNA-sequencing on over 25,000 cells from axolotl limbs and identify a plethora of cellular diversity within epidermal, mesenchymal, and hematopoietic lineages in homeostatic and regenerating limbs. We identify regeneration-induced genes, develop putative trajectories for blastema cell differentiation, and propose the molecular identity of fibroblast-like blastema progenitor cells. This work will enable application of molecular techniques to assess the contribution of these populations to limb regeneration. Overall, these data allow for establishment of a putative framework for adult axolotl limb regeneration.

Suggested Citation

  • Nicholas D. Leigh & Garrett S. Dunlap & Kimberly Johnson & Rachelle Mariano & Rachel Oshiro & Alan Y. Wong & Donald M. Bryant & Bess M. Miller & Alex Ratner & Andy Chen & William W. Ye & Brian J. Haas, 2018. "Transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07604-0
    DOI: 10.1038/s41467-018-07604-0
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    Cited by:

    1. Aiko Kawasumi-Kita & Sang-Woo Lee & Daisuke Ohtsuka & Kaori Niimi & Yoshifumi Asakura & Keiichi Kitajima & Yuto Sakane & Koji Tamura & Haruki Ochi & Ken-ichi T. Suzuki & Yoshihiro Morishita, 2024. "hoxc12/c13 as key regulators for rebooting the developmental program in Xenopus limb regeneration," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Ariel C. Vonk & Xiaofan Zhao & Zheyu Pan & Megan L. Hudnall & Conrad G. Oakes & Gabriela A. Lopez & Sarah C. Hasel-Kolossa & Alexander W. C. Kuncz & Sasha B. Sengelmann & Darian J. Gamble & Thomas P. , 2023. "Single-cell analysis of lizard blastema fibroblasts reveals phagocyte-dependent activation of Hedgehog-responsive chondrogenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Fang Ye & Guodong Zhang & Weigao E. & Haide Chen & Chengxuan Yu & Lei Yang & Yuting Fu & Jiaqi Li & Sulei Fu & Zhongyi Sun & Lijiang Fei & Qile Guo & Jingjing Wang & Yanyu Xiao & Xinru Wang & Peijing , 2022. "Construction of the axolotl cell landscape using combinatorial hybridization sequencing at single-cell resolution," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Béryl Laplace-Builhé & Audrey Barthelaix & Said Assou & Candice Bohaud & Marine Pratlong & Dany Severac & Gautier Tejedor & Patricia Luz-Crawford & Mai Nguyen-Chi & Marc Mathieu & Christian Jorgensen , 2021. "NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Jixing Zhong & Rita Aires & Georgios Tsissios & Evangelia Skoufa & Kerstin Brandt & Tatiana Sandoval-Guzmán & Can Aztekin, 2023. "Multi-species atlas resolves an axolotl limb development and regeneration paradox," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Urban Lendahl & Lars Muhl & Christer Betsholtz, 2022. "Identification, discrimination and heterogeneity of fibroblasts," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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