PUBLICATION

Gene profile of zebrafish fin regeneration offers clues to kinetics, organization and biomechanics of basement membrane

Authors
Nauroy, P., Guiraud, A., Chlasta, J., Malbouyres, M., Gillet, B., Hughes, S., Lambert, E., Ruggiero, F.
ID
ZDB-PUB-180722-23
Date
2018
Source
Matrix biology : journal of the International Society for Matrix Biology   75-76: 82-101 (Journal)
Registered Authors
Keywords
Basement membrane, Collagen XIV, Extracellular matrix, Regeneration, Transcriptome, Zebrafish
Datasets
GEO:GSE112498
MeSH Terms
  • Animal Fins/growth & development*
  • Animal Fins/ultrastructure
  • Animals
  • Basement Membrane/growth & development*
  • Basement Membrane/ultrastructure
  • CRISPR-Cas Systems
  • Collagen/genetics*
  • Extracellular Matrix/genetics
  • Extracellular Matrix/ultrastructure
  • Extracellular Matrix Proteins/genetics
  • Gene Expression Regulation, Developmental/genetics
  • Kinetics
  • Regeneration/genetics*
  • Transcriptome/genetics
  • Wound Healing/genetics
  • Zebrafish/genetics
  • Zebrafish/growth & development
  • Zebrafish Proteins/genetics*
PubMed
30031067 Full text @ Matrix Biol.
Abstract
How some animals regenerate missing body parts is not well understood. Taking advantage of the zebrafish caudal fin model, we performed a global unbiased time-course transcriptomic analysis of fin regeneration. Biostatistics analyses identified extracellular matrix (ECM) as the most enriched gene sets. Basement membranes (BMs) are specialized ECM structures that provide tissues with structural cohesion and serve as a major extracellular signaling platform. While the embryonic formation of BM has been extensively investigated, its regeneration in adults remains poorly studied. We therefore focused on BM gene expression kinetics and showed that it recapitulates many aspects of development. As such, the re-expression of the embryonic col14a1a gene indicated that col14a1a is part of the regeneration-specific program. We showed that laminins and col14a1a genes display similar kinetics and that the corresponding proteins are spatially and temporally controlled during regeneration. Analysis of our CRISPR/Cas9-mediated col14a1a knockout fish showed that collagen XIV-A contributes to timely deposition of laminins. As changes in ECM organization can affect tissue mechanical properties, we analyzed the biomechanics of col14a1a-/- regenerative BM using atomic force microscopy (AFM). Our data revealed a thinner BM accompanied by a substantial increase of the stiffness when compared to controls. Further AFM 3D-reconstructions showed that BM is organized as a checkerboard made of alternation of soft and rigid regions that is compromised in mutants leading to a more compact structure. We conclude that collagen XIV-A transiently acts as a molecular spacer responsible for BM structure and biomechanics possibly by helping laminins integration within regenerative BM.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping