Transcriptome Analysis of Ullrich Congenital Muscular Dystrophy Fibroblasts Reveals a Disease Extracellular Matrix Signature and Key Molecular Regulators

PLoS One. 2015 Dec 15;10(12):e0145107. doi: 10.1371/journal.pone.0145107. eCollection 2015.

Abstract

Background: Collagen VI related myopathies encompass a range of phenotypes with involvement of skeletal muscle, skin and other connective tissues. They represent a severe and relatively common form of congenital disease for which there is no treatment. Collagen VI in skeletal muscle and skin is produced by fibroblasts.

Aims & methods: In order to gain insight into the consequences of collagen VI mutations and identify key disease pathways we performed global gene expression analysis of dermal fibroblasts from patients with Ullrich Congenital Muscular Dystrophy with and without vitamin C treatment. The expression data were integrated using a range of systems biology tools. Results were validated by real-time PCR, western blotting and functional assays.

Findings: We found significant changes in the expression levels of almost 600 genes between collagen VI deficient and control fibroblasts. Highly regulated genes included extracellular matrix components and surface receptors, including integrins, indicating a shift in the interaction between the cell and its environment. This was accompanied by a significant increase in fibroblasts adhesion to laminin. The observed changes in gene expression profiling may be under the control of two miRNAs, miR-30c and miR-181a, which we found elevated in tissue and serum from patients and which could represent novel biomarkers for muscular dystrophy. Finally, the response to vitamin C of collagen VI mutated fibroblasts significantly differed from healthy fibroblasts. Vitamin C treatment was able to revert the expression of some key genes to levels found in control cells raising the possibility of a beneficial effect of vitamin C as a modulator of some of the pathological aspects of collagen VI related diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ascorbic Acid / pharmacology
  • Cell Adhesion / drug effects
  • Cell Adhesion / genetics
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Extracellular Matrix / drug effects
  • Extracellular Matrix / metabolism*
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Gene Expression Profiling*
  • Gene Regulatory Networks / drug effects
  • Humans
  • Integrin alpha3 / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Muscular Dystrophies / genetics*
  • Muscular Dystrophies / pathology
  • Sclerosis / genetics*
  • Sclerosis / pathology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Up-Regulation / drug effects
  • Up-Regulation / genetics
  • Wound Healing / drug effects
  • Wound Healing / genetics

Substances

  • Integrin alpha3
  • MicroRNAs
  • Ascorbic Acid

Supplementary concepts

  • Scleroatonic muscular dystrophy

Associated data

  • GEO/GSE56741

Grants and funding

This work was funded by the " Plan Nacional de I+D+I and Instituto de Salud Carlos III- Subdirección General de Evaluación y Fomento de la Investigación Sanitaria, http://www.isciii.es/", projects PI10/00177 (CJM), and PI13/00837 (CJM) and PI15/01822 (JDM), and the European Regional Development Fund (FEDER) (CJM). MAR is sponsored by the Hospital Sant Joan de Déu Reserch Grants. CJM is funded by the Instituto de Salud Carlos III grant CP09/00011.