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Subventricular zone cytogenesis provides trophic support for neural repair in a mouse model of stroke

Author

Listed:
  • Michael R. Williamson

    (University of Texas at Austin
    Baylor College of Medicine)

  • Stephanie P. Le

    (University of Texas at Austin)

  • Ronald L. Franzen

    (University of Texas at Austin
    Baylor College of Medicine)

  • Nicole A. Donlan

    (University of Texas at Austin)

  • Jill L. Rosow

    (University of Texas at Austin)

  • Mathilda S. Nicot-Cartsonis

    (University of Texas Medical Branch at Galveston)

  • Alexis Cervantes

    (Baylor College of Medicine
    Baylor College of Medicine)

  • Benjamin Deneen

    (Baylor College of Medicine
    Baylor College of Medicine)

  • Andrew K. Dunn

    (University of Texas at Austin
    University of Texas at Austin)

  • Theresa A. Jones

    (University of Texas at Austin
    University of Texas at Austin)

  • Michael R. Drew

    (University of Texas at Austin
    University of Texas at Austin)

Abstract

Stroke enhances proliferation of neural precursor cells within the subventricular zone (SVZ) and induces ectopic migration of newborn cells towards the site of injury. Here, we characterize the identity of cells arising from the SVZ after stroke and uncover a mechanism through which they facilitate neural repair and functional recovery. With genetic lineage tracing, we show that SVZ-derived cells that migrate towards cortical photothrombotic stroke in mice are predominantly undifferentiated precursors. We find that ablation of neural precursor cells or conditional knockout of VEGF impairs neuronal and vascular reparative responses and worsens recovery. Replacement of VEGF is sufficient to induce neural repair and recovery. We also provide evidence that CXCL12 from peri-infarct vasculature signals to CXCR4-expressing cells arising from the SVZ to direct their ectopic migration. These results support a model in which vasculature surrounding the site of injury attracts cells from the SVZ, and these cells subsequently provide trophic support that drives neural repair and recovery.

Suggested Citation

  • Michael R. Williamson & Stephanie P. Le & Ronald L. Franzen & Nicole A. Donlan & Jill L. Rosow & Mathilda S. Nicot-Cartsonis & Alexis Cervantes & Benjamin Deneen & Andrew K. Dunn & Theresa A. Jones & , 2023. "Subventricular zone cytogenesis provides trophic support for neural repair in a mouse model of stroke," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42138-0
    DOI: 10.1038/s41467-023-42138-0
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    References listed on IDEAS

    as
    1. Moises Freitas-Andrade & Cesar H. Comin & Peter Dyken & Julie Ouellette & Joanna Raman-Nair & Nicole Blakeley & Qing Yan Liu & Sonia Leclerc & Youlian Pan & Ziying Liu & Micaël Carrier & Karan Thakur , 2023. "Astroglial Hmgb1 regulates postnatal astrocyte morphogenesis and cerebrovascular maturation," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Stefano Pluchino & Lucia Zanotti & Barbara Rossi & Elena Brambilla & Linda Ottoboni & Giuliana Salani & Marianna Martinello & Alessandro Cattalini & Alessandra Bergami & Roberto Furlan & Giancarlo Com, 2005. "Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism," Nature, Nature, vol. 436(7048), pages 266-271, July.
    3. Kelly A. Tennant & Stephanie L. Taylor & Emily R. White & Craig E. Brown, 2017. "Optogenetic rewiring of thalamocortical circuits to restore function in the stroke injured brain," Nature Communications, Nature, vol. 8(1), pages 1-14, August.
    4. Michael Lattke & Robert Goldstone & James K. Ellis & Stefan Boeing & Jerónimo Jurado-Arjona & Nicolás Marichal & James I. MacRae & Benedikt Berninger & Francois Guillemot, 2021. "Extensive transcriptional and chromatin changes underlie astrocyte maturation in vivo and in culture," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    5. Nader Sanai & Anthony D. Tramontin & Alfredo Quiñones-Hinojosa & Nicholas M. Barbaro & Nalin Gupta & Sandeep Kunwar & Michael T. Lawton & Michael W. McDermott & Andrew T. Parsa & José Manuel-García Ve, 2004. "Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration," Nature, Nature, vol. 427(6976), pages 740-744, February.
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