A novel role for Lh3 dependent ECM modifications during neural crest cell migration in zebrafish.

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  • Author(s): Banerjee S;Banerjee S; Isaacman-Beck J; Schneider VA; Granato M
  • Source:
    PloS one [PLoS One] 2013; Vol. 8 (1), pp. e54609. Date of Electronic Publication: 2013 Jan 18.
  • Publication Type:
    Journal Article; Research Support, N.I.H., Extramural; Research Support, U.S. Gov't, Non-P.H.S.
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Public Library of Science Country of Publication: United States NLM ID: 101285081 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1932-6203 (Electronic) Linking ISSN: 19326203 NLM ISO Abbreviation: PLoS One Subsets: MEDLINE
    • Publication Information:
      Original Publication: San Francisco, CA : Public Library of Science
    • Subject Terms:
      Collagen Type XVIII/*metabolism ; Extracellular Matrix/*metabolism ; Glycosyltransferases/*metabolism ; Neural Crest/*growth & development ; Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase/*metabolism ; Zebrafish/*metabolism ; Zebrafish Proteins/*metabolism; Animals ; Cell Adhesion ; Cell Differentiation ; Cell Movement ; Collagen Type XVIII/genetics ; Embryonic Development/genetics ; Glycosyltransferases/genetics ; Mutation ; Neural Crest/cytology ; Neural Crest/metabolism ; Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase/genetics ; Protein Processing, Post-Translational ; Somites/growth & development ; Somites/metabolism ; Zebrafish/embryology ; Zebrafish/genetics ; Zebrafish Proteins/genetics
    • Abstract:
      During vertebrate development, trunk neural crest cells delaminate along the entire length of the dorsal neural tube and initially migrate as a non-segmented sheet. As they enter the somites, neural crest cells rearrange into spatially restricted segmental streams. Extracellular matrix components are likely to play critical roles in this transition from a sheet-like to a stream-like mode of migration, yet the extracellular matrix components and their modifying enzymes critical for this transition are largely unknown. Here, we identified the glycosyltransferase Lh3, known to modify extracellular matrix components, and its presumptive substrate Collagen18A1, to provide extrinsic signals critical for neural crest cells to transition from a sheet-like migration behavior to migrating as a segmental stream. Using live cell imaging we show that in lh3 null mutants, neural crest cells fail to transition from a sheet to a stream, and that they consequently enter the somites as multiple streams, or stall shortly after entering the somites. Moreover, we demonstrate that transgenic expression of lh3 in a small subset of somitic cells adjacent to where neural crest cells switch from sheet to stream migration restores segmental neural crest cell migration. Finally, we show that knockdown of the presumptive Lh3 substrate Collagen18A1 recapitulates the neural crest cell migration defects observed in lh3 mutants, consistent with the notion that Lh3 exerts its effect on neural crest cell migration by regulating post-translational modifications of Collagen18A1. Together these data suggest that Lh3-Collagen18A1 dependent ECM modifications regulate the transition of trunk neural crest cells from a non-segmental sheet like migration mode to a segmental stream migration mode.
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    • Grant Information:
      R01 HD037975 United States HD NICHD NIH HHS; HD037975 United States HD NICHD NIH HHS
    • Accession Number:
      0 (Collagen Type XVIII)
      0 (Zebrafish Proteins)
      0 (plod3 protein, zebrafish)
      EC 1.14.11.4 (Procollagen-Lysine, 2-Oxoglutarate 5-Dioxygenase)
      EC 2.4.- (Glycosyltransferases)
    • Publication Date:
      Date Created: 20130126 Date Completed: 20130719 Latest Revision: 20211021
    • Publication Date:
      20221213
    • Accession Number:
      PMC3548841
    • Accession Number:
      10.1371/journal.pone.0054609
    • Accession Number:
      23349938