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Spatial transcriptomics defines injury specific microenvironments and cellular interactions in kidney regeneration and disease

Author

Listed:
  • Michal Polonsky

    (California Institute of Technology)

  • Louisa M. S. Gerhardt

    (Keck School of Medicine of the University of Southern California
    University of Heidelberg)

  • Jina Yun

    (California Institute of Technology)

  • Kari Koppitch

    (Keck School of Medicine of the University of Southern California)

  • Katsuya Lex Colón

    (California Institute of Technology)

  • Henry Amrhein

    (California Institute of Technology)

  • Barbara Wold

    (California Institute of Technology)

  • Shiwei Zheng

    (Icahn School of Medicine at Mount Sinai)

  • Guo-Cheng Yuan

    (Icahn School of Medicine at Mount Sinai)

  • Matt Thomson

    (California Institute of Technology)

  • Long Cai

    (California Institute of Technology)

  • Andrew P. McMahon

    (Keck School of Medicine of the University of Southern California)

Abstract

Kidney injury disrupts the intricate renal architecture and triggers limited regeneration, together with injury-invoked inflammation and fibrosis. Deciphering the molecular pathways and cellular interactions driving these processes is challenging due to the complex tissue structure. Here, we apply single cell spatial transcriptomics to examine ischemia-reperfusion injury in the mouse kidney. Spatial transcriptomics reveals injury-specific and spatially-dependent gene expression patterns in distinct cellular microenvironments within the kidney and predicts Clcf1-Crfl1 in a molecular interplay between persistently injured proximal tubule cells and their neighboring fibroblasts. Immune cell types play a critical role in organ repair. Spatial analysis identifies cellular microenvironments resembling early tertiary lymphoid structures and associated molecular pathways. Collectively, this study supports a focus on molecular interactions in cellular microenvironments to enhance understanding of injury, repair and disease.

Suggested Citation

  • Michal Polonsky & Louisa M. S. Gerhardt & Jina Yun & Kari Koppitch & Katsuya Lex Colón & Henry Amrhein & Barbara Wold & Shiwei Zheng & Guo-Cheng Yuan & Matt Thomson & Long Cai & Andrew P. McMahon, 2024. "Spatial transcriptomics defines injury specific microenvironments and cellular interactions in kidney regeneration and disease," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51186-z
    DOI: 10.1038/s41467-024-51186-z
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    1. Michael S. Balzer & Tomohito Doke & Ya-Wen Yang & Daniel L. Aldridge & Hailong Hu & Hung Mai & Dhanunjay Mukhi & Ziyuan Ma & Rojesh Shrestha & Matthew B. Palmer & Christopher A. Hunter & Katalin Suszt, 2022. "Single-cell analysis highlights differences in druggable pathways underlying adaptive or fibrotic kidney regeneration," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Massimo Andreatta & Jesus Corria-Osorio & Sören Müller & Rafael Cubas & George Coukos & Santiago J. Carmona, 2021. "Interpretation of T cell states from single-cell transcriptomics data using reference atlases," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Blue B. Lake & Rajasree Menon & Seth Winfree & Qiwen Hu & Ricardo Melo Ferreira & Kian Kalhor & Daria Barwinska & Edgar A. Otto & Michael Ferkowicz & Dinh Diep & Nongluk Plongthongkum & Amanda Knoten , 2023. "An atlas of healthy and injured cell states and niches in the human kidney," Nature, Nature, vol. 619(7970), pages 585-594, July.
    4. Yodai Takei & Jina Yun & Shiwei Zheng & Noah Ollikainen & Nico Pierson & Jonathan White & Sheel Shah & Julian Thomassie & Shengbao Suo & Chee-Huat Linus Eng & Mitchell Guttman & Guo-Cheng Yuan & Long , 2021. "Integrated spatial genomics reveals global architecture of single nuclei," Nature, Nature, vol. 590(7845), pages 344-350, February.
    5. Chee-Huat Linus Eng & Michael Lawson & Qian Zhu & Ruben Dries & Noushin Koulena & Yodai Takei & Jina Yun & Christopher Cronin & Christoph Karp & Guo-Cheng Yuan & Long Cai, 2019. "Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+," Nature, Nature, vol. 568(7751), pages 235-239, April.
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