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Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding.

Publication ,  Journal Article
Keeley, DP; Hastie, E; Jayadev, R; Kelley, LC; Chi, Q; Payne, SG; Jeger, JL; Hoffman, BD; Sherwood, DR
Published in: Developmental cell
July 2020

Basement membranes (BMs) are supramolecular matrices built on laminin and type IV collagen networks that provide structural and signaling support to tissues. BM complexity, however, has hindered an understanding of its formation, dynamics, and regulation. Using genome editing, we tagged 29 BM matrix components and receptors in C. elegans with mNeonGreen. Here, we report a common template that initiates BM formation, which rapidly diversifies during tissue differentiation. Through photobleaching studies, we show that BMs are not static-surprisingly, many matrix proteins move within the laminin and collagen scaffoldings. Finally, quantitative imaging, conditional knockdown, and optical highlighting indicate that papilin, a poorly studied glycoprotein, is the most abundant component in the gonadal BM, where it facilitates type IV collagen removal during BM expansion and tissue growth. Together, this work introduces methods for holistic investigation of BM regulation and reveals that BMs are highly dynamic and capable of rapid change to support tissues.

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Published In

Developmental cell

DOI

EISSN

1878-1551

ISSN

1534-5807

Publication Date

July 2020

Volume

54

Issue

1

Start / End Page

60 / 74.e7

Related Subject Headings

  • Motion
  • Laminin
  • Extracellular Matrix
  • Developmental Biology
  • Collagen
  • Caenorhabditis elegans Proteins
  • Caenorhabditis elegans
  • Basement Membrane
  • Animals
  • 3101 Biochemistry and cell biology
 

Citation

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Keeley, D. P., Hastie, E., Jayadev, R., Kelley, L. C., Chi, Q., Payne, S. G., … Sherwood, D. R. (2020). Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding. Developmental Cell, 54(1), 60-74.e7. https://doi.org/10.1016/j.devcel.2020.05.022
Keeley, Daniel P., Eric Hastie, Ranjay Jayadev, Laura C. Kelley, Qiuyi Chi, Sara G. Payne, Jonathan L. Jeger, Brenton D. Hoffman, and David R. Sherwood. “Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding.Developmental Cell 54, no. 1 (July 2020): 60-74.e7. https://doi.org/10.1016/j.devcel.2020.05.022.
Keeley DP, Hastie E, Jayadev R, Kelley LC, Chi Q, Payne SG, et al. Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding. Developmental cell. 2020 Jul;54(1):60-74.e7.
Keeley, Daniel P., et al. “Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding.Developmental Cell, vol. 54, no. 1, July 2020, pp. 60-74.e7. Epmc, doi:10.1016/j.devcel.2020.05.022.
Keeley DP, Hastie E, Jayadev R, Kelley LC, Chi Q, Payne SG, Jeger JL, Hoffman BD, Sherwood DR. Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding. Developmental cell. 2020 Jul;54(1):60-74.e7.
Journal cover image

Published In

Developmental cell

DOI

EISSN

1878-1551

ISSN

1534-5807

Publication Date

July 2020

Volume

54

Issue

1

Start / End Page

60 / 74.e7

Related Subject Headings

  • Motion
  • Laminin
  • Extracellular Matrix
  • Developmental Biology
  • Collagen
  • Caenorhabditis elegans Proteins
  • Caenorhabditis elegans
  • Basement Membrane
  • Animals
  • 3101 Biochemistry and cell biology