Two sides of MGP null arterial disease: chondrogenic lesions dependent on transglutaminase 2 and elastin fragmentation associated with induction of adipsin

J Biol Chem. 2013 Oct 25;288(43):31400-8. doi: 10.1074/jbc.M113.495556. Epub 2013 Sep 13.

Abstract

Mutations in matrix Gla protein (MGP) have been correlated with vascular calcification. In the mouse model, MGP null vascular disease presents as calcifying cartilaginous lesions and mineral deposition along elastin lamellae (elastocalcinosis). Here we examined the mechanisms underlying both of these manifestations. Genetic ablation of enzyme transglutaminase 2 (TG2) in Mgp(-/-) mice dramatically reduced the size of cartilaginous lesions in the aortic media, attenuated calcium accrual more than 2-fold, and doubled longevity as compared with control Mgp(-/-) animals. Nonetheless, the Mgp(-/-);Tgm2(-/-) mice still died prematurely as compared with wild-type and retained the elastocalcinosis phenotype. This pathology in Mgp(-/-) animals was developmentally preceded by extensive fragmentation of elastic lamellae and associated with elevated serine elastase activity in aortic tissue and vascular smooth muscle cells. Systematic gene expression analysis followed by an immunoprecipitation study identified adipsin as the major elastase that is induced in the Mgp(-/-) vascular smooth muscle even in the TG2 null background. These results reveal a central role for TG2 in chondrogenic transformation of vascular smooth muscle and implicate adipsin in elastin fragmentation and ensuing elastocalcinosis. The importance of elastin calcification in MGP null vascular disease is highlighted by significant residual vascular calcification and mortality in Mgp(-/-);Tgm2(-/-) mice with reduced cartilaginous lesions. Our studies identify two potential therapeutic targets in vascular calcification associated with MGP dysfunction and emphasize the need for a comprehensive approach to this multifaceted disorder.

Keywords: Adipsin; Calcification; Cardiovascular Disease; Elastin; Matrix Gla Protein; Transgenic Mice; Transglutaminase 2; Vascular Smooth Muscle Cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Aortic Diseases / genetics
  • Aortic Diseases / metabolism*
  • Aortic Diseases / pathology
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism*
  • Complement Factor D / genetics
  • Complement Factor D / metabolism
  • Elastin / genetics
  • Elastin / metabolism*
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism*
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism*
  • Matrix Gla Protein
  • Mice
  • Mice, Knockout
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Protein Glutamine gamma Glutamyltransferase 2
  • Transglutaminases / genetics
  • Transglutaminases / metabolism*
  • Vascular Calcification / genetics
  • Vascular Calcification / metabolism*
  • Vascular Calcification / pathology

Substances

  • Calcium-Binding Proteins
  • Extracellular Matrix Proteins
  • Elastin
  • Protein Glutamine gamma Glutamyltransferase 2
  • Transglutaminases
  • Complement Factor D
  • complement factor D, mouse
  • GTP-Binding Proteins