IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52783-8.html
   My bibliography  Save this article

The lncRNA SNHG26 drives the inflammatory-to-proliferative state transition of keratinocyte progenitor cells during wound healing

Author

Listed:
  • Dongqing Li

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Zhuang Liu

    (Karolinska Institutet)

  • Letian Zhang

    (Karolinska Institutet)

  • Xiaowei Bian

    (Karolinska Institutet)

  • Jianmin Wu

    (Wenzhou Medical University)

  • Li Li

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Yongjian Chen

    (Karolinska Institutet)

  • Lihua Luo

    (Karolinska Institutet)

  • Ling Pan

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Lingzhuo Kong

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Yunting Xiao

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jiating Wang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Xiya Zhang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Wang Wang

    (East China Normal University)

  • Maria Toma

    (Karolinska Institutet)

  • Minna Piipponen

    (Karolinska Institutet)

  • Pehr Sommar

    (Karolinska University Hospital)

  • Ning Xu Landén

    (Karolinska Institutet)

Abstract

The cell transition from an inflammatory phase to a subsequent proliferative phase is crucial for wound healing, yet the driving mechanism remains unclear. By profiling lncRNA expression changes during human skin wound healing and screening lncRNA functions, we identify SNHG26 as a pivotal regulator in keratinocyte progenitors underpinning this phase transition. Snhg26-deficient mice exhibit impaired wound repair characterized by delayed re-epithelization accompanied by exacerbated inflammation. Single-cell transcriptome analysis combined with gain-of-function and loss-of-function of SNHG26 in vitro and ex vivo reveals its specific role in facilitating inflammatory-to-proliferative state transition of keratinocyte progenitors. A mechanistic study unravels that SNHG26 interacts with and relocates the transcription factor ILF2 from inflammatory genomic loci, such as JUN, IL6, IL8, and CCL20, to the genomic locus of LAMB3. Collectively, our findings suggest that lncRNAs play cardinal roles in expediting tissue repair and regeneration and may constitute an invaluable reservoir of therapeutic targets in reparative medicine.

Suggested Citation

  • Dongqing Li & Zhuang Liu & Letian Zhang & Xiaowei Bian & Jianmin Wu & Li Li & Yongjian Chen & Lihua Luo & Ling Pan & Lingzhuo Kong & Yunting Xiao & Jiating Wang & Xiya Zhang & Wang Wang & Maria Toma &, 2024. "The lncRNA SNHG26 drives the inflammatory-to-proliferative state transition of keratinocyte progenitor cells during wound healing," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52783-8
    DOI: 10.1038/s41467-024-52783-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52783-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52783-8?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. Markus Kretz & Zurab Siprashvili & Ci Chu & Dan E. Webster & Ashley Zehnder & Kun Qu & Carolyn S. Lee & Ross J. Flockhart & Abigail F. Groff & Jennifer Chow & Danielle Johnston & Grace E. Kim & Robert, 2013. "Control of somatic tissue differentiation by the long non-coding RNA TINCR," Nature, Nature, vol. 493(7431), pages 231-235, January.
    2. Suoqin Jin & Christian F. Guerrero-Juarez & Lihua Zhang & Ivan Chang & Raul Ramos & Chen-Hsiang Kuan & Peggy Myung & Maksim V. Plikus & Qing Nie, 2021. "Inference and analysis of cell-cell communication using CellChat," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    3. Anamaria Necsulea & Magali Soumillon & Maria Warnefors & Angélica Liechti & Tasman Daish & Ulrich Zeller & Julie C. Baker & Frank Grützner & Henrik Kaessmann, 2014. "The evolution of lncRNA repertoires and expression patterns in tetrapods," Nature, Nature, vol. 505(7485), pages 635-640, 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. Fan Zhang & Haijuan Zhang & Shengfu Wang & Mingying Gao & Kaiyi Du & Xinyuan Chen & Yang Lu & Qianqian Hu & Anyu Du & Shenghu Du & Jian Wang & Keqing Shi & Zimiao Chen & Zhuo Li & Zhenglin Li & Jian X, 2025. "A dynamically phase-adaptive regulating hydrogel promotes ultrafast anti-fibrotic wound healing," Nature Communications, Nature, vol. 16(1), pages 1-20, 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. Xiaochen Wang & Maosheng Cheng & Shuang Chen & Caihua Zhang & Rongsong Ling & Shuqing Qiu & Ke Chen & Bin Zhou & Qiuli Li & Wenbin Lei & Demeng Chen, 2025. "Resistance to anti-LAG-3 plus anti-PD-1 therapy in head and neck cancer is mediated by Sox9+ tumor cells interaction with Fpr1+ neutrophils," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    2. Yanchuan Li & Huamei Li & Cheng Peng & Ge Meng & Yijun Lu & Honglin Liu & Li Cui & Huan Zhou & Zhu Xu & Lingyun Sun & Lihong Liu & Qing Xiong & Beicheng Sun & Shiping Jiao, 2024. "Unraveling the spatial organization and development of human thymocytes through integration of spatial transcriptomics and single-cell multi-omics profiling," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    3. Tim Flerlage & Jeremy Chase Crawford & E. Kaitlynn Allen & Danielle Severns & Shaoyuan Tan & Sherri Surman & Granger Ridout & Tanya Novak & Adrienne Randolph & Alina N. West & Paul G. Thomas, 2023. "Single cell transcriptomics identifies distinct profiles in pediatric acute respiratory distress syndrome," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Shirong Cao & Yu Pan & Andrew S. Terker & Juan Pablo Arroyo Ornelas & Yinqiu Wang & Jiaqi Tang & Aolei Niu & Sarah Abu Kar & Mengdi Jiang & Wentian Luo & Xinyu Dong & Xiaofeng Fan & Suwan Wang & Matth, 2023. "Epidermal growth factor receptor activation is essential for kidney fibrosis development," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Christopher Bono & Yang Liu & Alexander Ferrena & Aneesa Valentine & Deyou Zheng & Bernice E. Morrow, 2023. "Single-cell transcriptomics uncovers a non-autonomous Tbx1-dependent genetic program controlling cardiac neural crest cell development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Jingyang Qian & Xin Shao & Hudong Bao & Yin Fang & Wenbo Guo & Chengyu Li & Anyao Li & Hua Hua & Xiaohui Fan, 2025. "Identification and characterization of cell niches in tissue from spatial omics data at single-cell resolution," Nature Communications, Nature, vol. 16(1), pages 1-21, December.
    7. Lichun Ma & Sophia Heinrich & Limin Wang & Friederike L. Keggenhoff & Subreen Khatib & Marshonna Forgues & Michael Kelly & Stephen M. Hewitt & Areeba Saif & Jonathan M. Hernandez & Donna Mabry & Roman, 2022. "Multiregional single-cell dissection of tumor and immune cells reveals stable lock-and-key features in liver cancer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Qingnan Liang & Yuefan Huang & Shan He & Ken Chen, 2023. "Pathway centric analysis for single-cell RNA-seq and spatial transcriptomics data with GSDensity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Maximilian Reck & David P. Baird & Stefan Veizades & Callum Sutherland & Rachel M. B. Bell & Heeyoun Hur & Carolynn Cairns & Piotr P. Janas & Ross Campbell & Andy Nam & Wei Yang & Nathan Schurman & Cl, 2025. "Multiomic analysis of human kidney disease identifies a tractable inflammatory and pro-fibrotic tubular cell phenotype," Nature Communications, Nature, vol. 16(1), pages 1-23, December.
    10. Faith H. Brennan & Yang Li & Cankun Wang & Anjun Ma & Qi Guo & Yi Li & Nicole Pukos & Warren A. Campbell & Kristina G. Witcher & Zhen Guan & Kristina A. Kigerl & Jodie C. E. Hall & Jonathan P. Godbout, 2022. "Microglia coordinate cellular interactions during spinal cord repair in mice," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    11. Sandra Curras-Alonso & Juliette Soulier & Thomas Defard & Christian Weber & Sophie Heinrich & Hugo Laporte & Sophie Leboucher & Sonia Lameiras & Marie Dutreix & Vincent Favaudon & Florian Massip & Tho, 2023. "An interactive murine single-cell atlas of the lung responses to radiation injury," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Brandon M. Lehrich & Evan R. Delgado & Tyler M. Yasaka & Silvia Liu & Catherine Cao & Yuqing Liu & Mohammad N. Taheri & Xiangnan Guan & Hartmut Koeppen & Sucha Singh & Vik Meadows & Jia-Jun Liu & Anya, 2025. "Precision targeting of β-catenin induces tumor reprogramming and immunity in hepatocellular cancers," Nature Communications, Nature, vol. 16(1), pages 1-26, December.
    13. Ilmatar Rooda & Jasmin Hassan & Jie Hao & Magdalena Wagner & Elisabeth Moussaud-Lamodière & Kersti Jääger & Marjut Otala & Katri Knuus & Cecilia Lindskog & Kiriaki Papaikonomou & Sebastian Gidlöf & Ce, 2024. "In-depth analysis of transcriptomes in ovarian cortical follicles from children and adults reveals interfollicular heterogeneity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Moujtaba Y. Kasmani & Paytsar Topchyan & Ashley K. Brown & Ryan J. Brown & Xiaopeng Wu & Yao Chen & Achia Khatun & Donia Alson & Yue Wu & Robert Burns & Chien-Wei Lin & Matthew R. Kudek & Jie Sun & We, 2023. "A spatial sequencing atlas of age-induced changes in the lung during influenza infection," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    15. Wei Yang & Li-Bo Liu & Feng-Liang Liu & Yan-Hua Wu & Zi-Da Zhen & Dong-Ying Fan & Zi-Yang Sheng & Zheng-Ran Song & Jia-Tong Chang & Yong-Tang Zheng & Jing An & Pei-Gang Wang, 2023. "Single-cell RNA sequencing reveals the fragility of male spermatogenic cells to Zika virus-induced complement activation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Luke Simpson & Andrew Strange & Doris Klisch & Sophie Kraunsoe & Takuya Azami & Daniel Goszczynski & Triet Minh & Benjamin Planells & Nadine Holmes & Fei Sang & Sonal Henson & Matthew Loose & Jennifer, 2024. "A single-cell atlas of pig gastrulation as a resource for comparative embryology," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    17. Erick Armingol & Hratch M. Baghdassarian & Cameron Martino & Araceli Perez-Lopez & Caitlin Aamodt & Rob Knight & Nathan E. Lewis, 2022. "Context-aware deconvolution of cell–cell communication with Tensor-cell2cell," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Baptiste Lamarthée & Jasper Callemeyn & Yannick Van Herck & Asier Antoranz & Dany Anglicheau & Patrick Boada & Jan Ulrich Becker & Tim Debyser & Frederik De Smet & Katrien De Vusser & Maëva Eloudzeri , 2023. "Transcriptional and spatial profiling of the kidney allograft unravels a central role for FcyRIII+ innate immune cells in rejection," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    19. Shawyon P. Shirazi & Nicholas M. Negretti & Christopher S. Jetter & Alexandria L. Sharkey & Shriya Garg & Meghan E. Kapp & Devan Wilkins & Gabrielle Fortier & Saahithi Mallapragada & Nicholas E. Banov, 2025. "Bronchopulmonary dysplasia with pulmonary hypertension associates with semaphorin signaling loss and functionally decreased FOXF1 expression," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    20. Shenghao Li & Hui Guo & Simai Zhang & Yizhou Li & Menglong Li, 2023. "Attention-based deep clustering method for scRNA-seq cell type identification," PLOS Computational Biology, Public Library of Science, vol. 19(11), pages 1-19, November.

    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_s41467-024-52783-8. 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.