An integrative systems approach identifies novel candidates in Marfan syndrome-related pathophysiology

J Cell Mol Med. 2019 Apr;23(4):2526-2535. doi: 10.1111/jcmm.14137. Epub 2019 Jan 24.

Abstract

Marfan syndrome (MFS) is an autosomal dominant genetic disorder caused by mutations in the FBN1 gene. Although many peripheral tissues are affected, aortic complications, such as dilation, dissection and rupture, are the leading causes of MFS-related mortality. Aberrant TGF-beta signalling plays a major role in the pathophysiology of MFS. However, the contributing mechanisms are still poorly understood. Here, we aimed at identifying novel aorta-specific pathways involved in the pathophysiology of MFS. For this purpose, we employed the Fbn1 under-expressing mgR/mgR mouse model of MFS. We performed RNA-sequencing of aortic tissues of 9-week-old mgR/mgR mice compared with wild-type (WT) mice. With a false discovery rate <5%, our analysis revealed 248 genes to be differentially regulated including 20 genes previously unrelated with MFS-related pathology. Among these, we identified Igfbp2, Ccl8, Spp1, Mylk2, Mfap4, Dsp and H19. We confirmed the expression of regulated genes by quantitative real-time PCR. Pathway classification revealed transcript signatures involved in chemokine signalling, cardiac muscle contraction, dilated and hypertrophic cardiomyopathy. Furthermore, our immunoblot analysis of aortic tissues revealed altered regulation of pSmad2 signalling, Perk1/2, Igfbp2, Mfap4, Ccl8 and Mylk2 protein levels in mgR/mgR vs WT mice. Together, our integrative systems approach identified several novel factors associated with MFS-aortic-specific pathophysiology that might offer potential novel therapeutic targets for MFS.

Keywords: Chemokine signalling; Igfbp2 signalling; Marfan syndrome; Mfap4; RNA-sequencing; Spp1; TGF-beta signalling; Transcriptomics; mgR/mgR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta, Thoracic / metabolism*
  • Aorta, Thoracic / physiopathology
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Chemokine CCL8 / genetics
  • Chemokine CCL8 / metabolism
  • Desmoplakins / genetics
  • Desmoplakins / metabolism
  • Disease Models, Animal
  • Extracellular Matrix Proteins / genetics*
  • Extracellular Matrix Proteins / metabolism
  • Fibrillin-1 / deficiency
  • Fibrillin-1 / genetics*
  • Gene Expression Regulation
  • Gene Ontology
  • Glycoproteins / genetics*
  • Glycoproteins / metabolism
  • Humans
  • Insulin-Like Growth Factor Binding Protein 2 / genetics*
  • Insulin-Like Growth Factor Binding Protein 2 / metabolism
  • Marfan Syndrome / genetics*
  • Marfan Syndrome / metabolism
  • Marfan Syndrome / physiopathology
  • Mice
  • Mice, Transgenic
  • Molecular Sequence Annotation
  • Myosin-Light-Chain Kinase / genetics
  • Myosin-Light-Chain Kinase / metabolism
  • Osteopontin / genetics*
  • Osteopontin / metabolism
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism
  • Signal Transduction
  • Smad2 Protein / genetics
  • Smad2 Protein / metabolism
  • Systems Biology / methods
  • eIF-2 Kinase / genetics
  • eIF-2 Kinase / metabolism

Substances

  • Carrier Proteins
  • Ccl8 protein, mouse
  • Chemokine CCL8
  • Desmoplakins
  • Dsp protein, mouse
  • Extracellular Matrix Proteins
  • Fbn1 protein, mouse
  • Fibrillin-1
  • Glycoproteins
  • H19 long non-coding RNA
  • Insulin-Like Growth Factor Binding Protein 2
  • MFAP4 protein, mouse
  • MYLK protein, mouse
  • RNA, Long Noncoding
  • Smad2 Protein
  • Smad2 protein, mouse
  • Spp1 protein, mouse
  • Osteopontin
  • PERK kinase
  • eIF-2 Kinase
  • Myosin-Light-Chain Kinase