Notch regulates vascular collagen IV basement membrane through modulation of lysyl hydroxylase 3 trafficking.

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  • Additional Information
    • Source:
      Publisher: Springer Country of Publication: Germany NLM ID: 9814575 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-7209 (Electronic) Linking ISSN: 09696970 NLM ISO Abbreviation: Angiogenesis Subsets: MEDLINE
    • Publication Information:
      Publication: Dec. 2004- : Berlin : Springer
      Original Publication: London ; Philadelphia : Rapid Science Publishers,
    • Subject Terms:
      Collagen Type IV*/genetics ; Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase*; Basement Membrane ; Endothelial Cells ; Morphogenesis
    • Abstract:
      Collagen type IV (Col IV) is a basement membrane protein associated with early blood vessel morphogenesis and is essential for blood vessel stability. Defects in vascular Col IV deposition are the basis of heritable disorders, such as small vessel disease, marked by cerebral hemorrhage and drastically shorten lifespan. To date, little is known about how endothelial cells regulate the intracellular transport and selective secretion of Col IV in response to angiogenic cues, leaving a void in our understanding of this critical process. Our aim was to identify trafficking pathways that regulate Col IV deposition during angiogenic blood vessel development. We have identified the GTPase Rab10 as a major regulator of Col IV vesicular trafficking during vascular development using both in vitro imaging and biochemistry as well as in vivo models. Knockdown of Rab10 reduced de novo Col IV secretion in vivo and in vitro. Mechanistically, we determined that Rab10 is an indirect mediator of Col IV secretion, partnering with atypical Rab25 to deliver the enzyme lysyl hydroxylase 3 (LH3) to Col IV-containing vesicles staged for secretion. Loss of Rab10 or Rab25 results in depletion of LH3 from Col IV-containing vesicles and rapid lysosomal degradation of Col IV. Furthermore, we demonstrate that Rab10 is Notch responsive, indicating a novel connection between permissive Notch-based vessel maturation programs and vesicle trafficking. Our results illustrate both a new trafficking-based component in the regulated secretion of Col IV and how this vesicle trafficking program interfaces with Notch signaling to fine-tune basement membrane secretion during blood vessel development.
      (© 2021. The Author(s).)
    • Comments:
      Erratum in: Angiogenesis. 2021 Jun 8;:. (PMID: 34101097)
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    • Grant Information:
      R15 HL156106 United States HL NHLBI NIH HHS; 1R56HL148450-01 United States HL NHLBI NIH HHS; R01 HL112626 United States HL NHLBI NIH HHS; R56 HL148450 United States HL NHLBI NIH HHS; R00HL124311 United States HL NHLBI NIH HHS; R00 HL124311 United States HL NHLBI NIH HHS
    • Contributed Indexing:
      Keywords: Angiogenesis; Blood vessels; Collagen IV; Development; Lysyl hydroxlyase 3; Notch1; Rab10; Rab25; Secretion; Small vessel disease; Trafficking; Zebrafish
    • Accession Number:
      0 (Collagen Type IV)
      EC 1.14.11.4 (Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase)
    • Publication Date:
      Date Created: 20210506 Date Completed: 20220211 Latest Revision: 20231111
    • Publication Date:
      20240829
    • Accession Number:
      PMC8487879
    • Accession Number:
      10.1007/s10456-021-09791-9
    • Accession Number:
      33956260