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Tenascin-C expression by fibroblasts is elevated in stressed collagen gels

Chiquet-Ehrismann, R ; Tannheimer, M ; Koch, M ; Brunner, A ; Spring, J ; Martin, D ; Baumgartner, S LU orcid and Chiquet, M (1994) In Journal of Cell Biology 127(6 Pt 2). p.2093-2101
Abstract

Chick embryo fibroblasts cultured on a collagen matrix exert tractional forces leading to the contraction of unrestrained, floating collagen gels and to the development of tension in attached, restrained gels. On a restrained, attached collagen gel the fibroblasts synthesize large quantities of tenascin-C, whereas in a floating, contracting gel tenascin-C synthesis is decreased. This regulation of tenascin-C synthesis can be observed by the secretion of metabolically labeled tenascin-C into the conditioned medium, as well as by the deposition of tenascin-C into the collagen matrix as judged by immunofluorescence. Regulation appears to occur at the transcriptional level, because when cells on attached or floating collagen gels are... (More)

Chick embryo fibroblasts cultured on a collagen matrix exert tractional forces leading to the contraction of unrestrained, floating collagen gels and to the development of tension in attached, restrained gels. On a restrained, attached collagen gel the fibroblasts synthesize large quantities of tenascin-C, whereas in a floating, contracting gel tenascin-C synthesis is decreased. This regulation of tenascin-C synthesis can be observed by the secretion of metabolically labeled tenascin-C into the conditioned medium, as well as by the deposition of tenascin-C into the collagen matrix as judged by immunofluorescence. Regulation appears to occur at the transcriptional level, because when cells on attached or floating collagen gels are transfected with promoter constructs of the tenascin-C gene, luciferase expression driven by the tenascin-C promoter parallels the effects measured for endogenous tenascin-C synthesis, whereas luciferase expression under the control of the SV40 promoter does not depend on the state of the collagen gel. The promoter region responsible for tenascin-C induction on attached collagen gels is distinct from the region important for the induction of tenascin-C by serum, and may define a novel kind of response element. By joining this tenascin-C sequence to the SV40 promoter of a reporter plasmid, its activity can be transferred to the heterologous promoter. We propose that the tenascin-C promoter is directly or indirectly activated in fibroblasts generating and experiencing mechanical stress within a restrained collagen matrix. This may be an important aspect of the regulation of tenascin-C expression during embryogenesis as well as during wound healing and other regenerative and morphogenetic processes.

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author
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publishing date
type
Contribution to journal
publication status
published
keywords
Animals, Base Sequence, Cell Adhesion Molecules, Neuronal/biosynthesis, Cells, Cultured, Chick Embryo, Collagen, DNA Mutational Analysis, Extracellular Matrix Proteins/biosynthesis, Fibroblasts/metabolism, Friction, Gels, Gene Expression Regulation, Molecular Sequence Data, Physical Stimulation, Promoter Regions, Genetic/genetics, Recombinant Proteins, Sequence Deletion, Tenascin, Transcription, Genetic, Transfection
in
Journal of Cell Biology
volume
127
issue
6 Pt 2
pages
2093 - 2101
publisher
Rockefeller University Press
external identifiers
  • scopus:0028566512
  • pmid:7528751
ISSN
0021-9525
DOI
10.1083/jcb.127.6.2093
language
English
LU publication?
no
id
67b83502-da68-49f8-a08b-3dc8d7ca477a
date added to LUP
2019-05-21 14:24:42
date last changed
2024-01-01 05:57:57
@article{67b83502-da68-49f8-a08b-3dc8d7ca477a,
  abstract     = {{<p>Chick embryo fibroblasts cultured on a collagen matrix exert tractional forces leading to the contraction of unrestrained, floating collagen gels and to the development of tension in attached, restrained gels. On a restrained, attached collagen gel the fibroblasts synthesize large quantities of tenascin-C, whereas in a floating, contracting gel tenascin-C synthesis is decreased. This regulation of tenascin-C synthesis can be observed by the secretion of metabolically labeled tenascin-C into the conditioned medium, as well as by the deposition of tenascin-C into the collagen matrix as judged by immunofluorescence. Regulation appears to occur at the transcriptional level, because when cells on attached or floating collagen gels are transfected with promoter constructs of the tenascin-C gene, luciferase expression driven by the tenascin-C promoter parallels the effects measured for endogenous tenascin-C synthesis, whereas luciferase expression under the control of the SV40 promoter does not depend on the state of the collagen gel. The promoter region responsible for tenascin-C induction on attached collagen gels is distinct from the region important for the induction of tenascin-C by serum, and may define a novel kind of response element. By joining this tenascin-C sequence to the SV40 promoter of a reporter plasmid, its activity can be transferred to the heterologous promoter. We propose that the tenascin-C promoter is directly or indirectly activated in fibroblasts generating and experiencing mechanical stress within a restrained collagen matrix. This may be an important aspect of the regulation of tenascin-C expression during embryogenesis as well as during wound healing and other regenerative and morphogenetic processes.</p>}},
  author       = {{Chiquet-Ehrismann, R and Tannheimer, M and Koch, M and Brunner, A and Spring, J and Martin, D and Baumgartner, S and Chiquet, M}},
  issn         = {{0021-9525}},
  keywords     = {{Animals; Base Sequence; Cell Adhesion Molecules, Neuronal/biosynthesis; Cells, Cultured; Chick Embryo; Collagen; DNA Mutational Analysis; Extracellular Matrix Proteins/biosynthesis; Fibroblasts/metabolism; Friction; Gels; Gene Expression Regulation; Molecular Sequence Data; Physical Stimulation; Promoter Regions, Genetic/genetics; Recombinant Proteins; Sequence Deletion; Tenascin; Transcription, Genetic; Transfection}},
  language     = {{eng}},
  number       = {{6 Pt 2}},
  pages        = {{2093--2101}},
  publisher    = {{Rockefeller University Press}},
  series       = {{Journal of Cell Biology}},
  title        = {{Tenascin-C expression by fibroblasts is elevated in stressed collagen gels}},
  url          = {{http://dx.doi.org/10.1083/jcb.127.6.2093}},
  doi          = {{10.1083/jcb.127.6.2093}},
  volume       = {{127}},
  year         = {{1994}},
}