Dermatan Sulfate-Free Mice Display Embryological Defects and Are Neonatal Lethal Despite Normal Lymphoid and Non-Lymphoid Organogenesis

PLoS One. 2015 Oct 21;10(10):e0140279. doi: 10.1371/journal.pone.0140279. eCollection 2015.

Abstract

The epimerization of glucuronic acid into iduronic acid adds structural variability to chondroitin/dermatan sulfate polysaccharides. Iduronic acid-containing domains play essential roles in processes such as coagulation, chemokine and morphogen modulation, collagen maturation, and neurite sprouting. Therefore, we generated and characterized, for the first time, mice deficient in dermatan sulfate epimerase 1 and 2, two enzymes uniquely involved in dermatan sulfate biosynthesis. The resulting mice, termed DKO mice, were completely devoid of iduronic acid, and the resulting chondroitin sulfate chains were structurally different from the wild type chains, from which a different protein binding specificity can be expected. As a consequence, a vast majority of the DKO mice died perinatally, with greatly variable phenotypes at birth or late embryological stages such as umbilical hernia, exencephaly and a kinked tail. However, a minority of embryos were histologically unaffected, with apparently normal lung and bone/cartilage features. Interestingly, the binding of the chemokine CXCL13, an important modulator of lymphoid organogenesis, to mouse DKO embryonic fibroblasts was impaired. Nevertheless, the development of the secondary lymphoid organs, including the lymph nodes and spleen, was normal. Altogether, our results indicate an important role of dermatan sulfate in embryological development and perinatal survival.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Carbohydrate Epimerases / deficiency*
  • Carbohydrate Epimerases / genetics
  • Cells, Cultured
  • Chemokine CXCL13 / metabolism
  • Chondroitin Sulfates / metabolism
  • Dermatan Sulfate / metabolism*
  • Disaccharides / metabolism
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / embryology
  • Embryo, Mammalian / metabolism*
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Lymphoid Tissue / growth & development*
  • Lymphoid Tissue / metabolism
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Fluorescence
  • Organogenesis*
  • Protein Binding

Substances

  • Chemokine CXCL13
  • Disaccharides
  • Dermatan Sulfate
  • Chondroitin Sulfates
  • Carbohydrate Epimerases
  • dermatan sulfate epimerase 1, mouse

Grants and funding

This work was supported by Netherlands Organization for Scientific Research (916.13.011 to RR) http://www.nwo.nl; Medical Faculty Lund University to AM; http://www.med.lu.se; Swedish Research Council to AM; http://www.vr.se/; Cancerfonden (grant 14 0530 to MM) https://www.cancerfonden.se; Anna-Greta Crafoord to XS http://www.annagretacrafoord.se/; Mizutani (grant 120115 to MM) http://www.mizutanifdn.or.jp/; Greta and Johan Kock to ET http://www.kockskastiftelsen.se/; and FLAK research school to AM http://www.flak.lu.se/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.