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Pericyte ALK5/TIMP3 Axis Contributes to Endothelial Morphogenesis in the Developing Brain.

Jui M Dave1, Teodelinda Mirabella2, Scott D Weatherbee3

  • 1Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, 300 George Street, Room 773J, New Haven, CT 06511, USA; Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA.

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Pericyte activin receptor-like kinase 5 (Alk5) is crucial for blood-brain barrier (BBB) development. Its absence in mice causes brain bleeds, but restoring tissue inhibitor of metalloproteinase 3 (TIMP3) helps.

Keywords:
ALK5TIMP3blood vesselblood-brain barrierendothelial cellsgerminal matrix hemorrhageintracranial hemorrhagepericytesvascular development

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Area of Science:

  • Neuroscience
  • Developmental Biology
  • Vascular Biology

Background:

  • The murine embryonic blood-brain barrier (BBB) comprises endothelial cells (ECs), pericytes (PCs), and basement membrane.
  • Pericytes (PCs) are vital for vascular stability, yet their signaling pathways regulating EC morphogenesis during BBB development are unknown.

Purpose of the Study:

  • To investigate the role of transforming growth factor β (TGF-β) receptor activin receptor-like kinase 5 (Alk5) in pericytes (PCs) during blood-brain barrier (BBB) development.
  • To explore the underlying mechanisms of germinal matrix hemorrhage-intraventricular hemorrhage (GMH-IVH) in Alk5-deficient PC murine models.

Main Methods:

  • Generation of murine embryos with conditional knockout of Alk5 specifically in brain pericytes (PCs).
  • Histological and molecular analysis of germinal matrix (GM) microvessels in wild-type and mutant embryos.
  • Assessment of endothelial cell (EC) proliferation, basement membrane composition, and matrix metalloproteinase (MMP) activity.
  • Administration of tissue inhibitor of matrix metalloproteinase 3 (TIMP3) to mutant embryos and evaluation of its therapeutic effects.

Main Results:

  • Murine embryos lacking PC Alk5 exhibit severe germinal matrix hemorrhage-intraventricular hemorrhage (GMH-IVH).
  • Mutant GM microvessels show abnormal dilation, reduced PC coverage, EC hyperproliferation, decreased collagen, and increased MMP activity.
  • Alk5-deficient PCs downregulate tissue inhibitor of matrix metalloproteinase 3 (TIMP3).
  • TIMP3 administration to mutants ameliorates EC abnormalities and reduces GMH-IVH.

Conclusions:

  • Pericyte (PC) activin receptor-like kinase 5 (Alk5) plays a critical role in regulating brain endothelial cell (EC) morphogenesis during blood-brain barrier (BBB) development.
  • Downregulation of tissue inhibitor of matrix metalloproteinase 3 (TIMP3) by PCs lacking Alk5 contributes to BBB defects.
  • TIMP3 represents a potential therapeutic agent for germinal matrix hemorrhage-intraventricular hemorrhage (GMH-IVH).