Iduronic Acid in Chondroitin/dermatan Sulfate Affects Directional Migration of Aortic Smooth Muscle Cells

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Jul 12

PMID 23843960

Citations 16

Authors

Barbara Bartolini

Martin A Thelin

Lena Svensson

Giancarlo Ghiselli

Toin H van Kuppevelt

Anders Malmstrom

Marco Maccarana

Affiliations

Soon will be listed here.

Abstract

Aortic smooth muscle cells produce chondroitin/dermatan sulfate (CS/DS) proteoglycans that regulate extracellular matrix organization and cell behavior in normal and pathological conditions. A unique feature of CS/DS proteoglycans is the presence of iduronic acid (IdoA), catalyzed by two DS epimerases. Functional ablation of DS-epi1, the main epimerase in these cells, resulted in a major reduction of IdoA both on cell surface and in secreted CS/DS proteoglycans. Downregulation of IdoA led to delayed ability to re-populate wounded areas due to loss of directional persistence of migration. DS-epi1-/- aortic smooth muscle cells, however, had not lost the general property of migration showing even increased speed of movement compared to wild type cells. Where the cell membrane adheres to the substratum, stress fibers were denser whereas focal adhesion sites were fewer. Total cellular expression of focal adhesion kinase (FAK) and phospho-FAK (pFAK) was decreased in mutant cells compared to control cells. As many pathological conditions are dependent on migration, modulation of IdoA content may point to therapeutic strategies for diseases such as cancer and atherosclerosis.

Citing Articles

Ventral body wall closure: Mechanistic insights from mouse models and translation to human pathology.

Formstone C, Aldeiri B, Davenport M, Francis-West P Dev Dyn. 2024; 254(2):102-141.

PMID: 39319771 PMC: 11809137. DOI: 10.1002/dvdy.735.

Histories of Dermatan Sulfate Epimerase and Dermatan 4--Sulfotransferase from Discovery of Their Enzymes and Genes to Musculocontractural Ehlers-Danlos Syndrome.

Mizumoto S, Yamada S Genes (Basel). 2023; 14(2).

PMID: 36833436 PMC: 9957132. DOI: 10.3390/genes14020509.

An Overview of Functions of Chondroitin Sulfate and Dermatan Sulfate Revealed by Their Deficient Mice.

Mizumoto S, Yamada S Front Cell Dev Biol. 2021; 9:764781.

PMID: 34901009 PMC: 8652114. DOI: 10.3389/fcell.2021.764781.

Fabrication of Injectable Chitosan-Chondroitin Sulfate Hydrogel Embedding Kartogenin-Loaded Microspheres as an Ultrasound-Triggered Drug Delivery System for Cartilage Tissue Engineering.

Yuan F, Wang H, Guan J, Fu J, Yang M, Zhang J Pharmaceutics. 2021; 13(9).

PMID: 34575563 PMC: 8472453. DOI: 10.3390/pharmaceutics13091487.

Inhibition of iduronic acid biosynthesis by ebselen reduces glycosaminoglycan accumulation in mucopolysaccharidosis type I fibroblasts.

Maccarana M, Tykesson E, Pera E, Gouignard N, Fang J, Malmstrom A Glycobiology. 2021; 31(10):1319-1329.

PMID: 34192316 PMC: 8600295. DOI: 10.1093/glycob/cwab066.

References

Deepa S, Yamada S, Zako M, Goldberger O, Sugahara K . Chondroitin sulfate chains on syndecan-1 and syndecan-4 from normal murine mammary gland epithelial cells are structurally and functionally distinct and cooperate with heparan sulfate chains to bind growth factors. A novel function to control.... J Biol Chem. 2004; 279(36):37368-76. DOI: 10.1074/jbc.M403031200. View

Schober M, Raghavan S, Nikolova M, Polak L, Pasolli H, Beggs H . Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol. 2007; 176(5):667-80. PMC: 2064024. DOI: 10.1083/jcb.200608010. View

Tufvesson E, Malmstrom J, Marko-Varga G, Westergren-Thorsson G . Biglycan isoforms with differences in polysaccharide substitution and core protein in human lung fibroblasts. Eur J Biochem. 2002; 269(15):3688-96. DOI: 10.1046/j.1432-1033.2002.03058.x. View

Doran A, Meller N, McNamara C . Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol. 2008; 28(5):812-9. PMC: 2734458. DOI: 10.1161/ATVBAHA.107.159327. View

Clark R, Lin F, Greiling D, An J, Couchman J . Fibroblast invasive migration into fibronectin/fibrin gels requires a previously uncharacterized dermatan sulfate-CD44 proteoglycan. J Invest Dermatol. 2004; 122(2):266-77. DOI: 10.1046/j.0022-202X.2004.22205.x. View

Bartolini B, Thelin M, Rauch U, Feinstein R, Oldberg A, Malmstrom A . Mouse development is not obviously affected by the absence of dermatan sulfate epimerase 2 in spite of a modified brain dermatan sulfate composition. Glycobiology. 2012; 22(7):1007-16. DOI: 10.1093/glycob/cws065. View

Ten Dam G, Yamada S, Kobayashi F, Purushothaman A, van de Westerlo E, Bulten J . Dermatan sulfate domains defined by the novel antibody GD3A12, in normal tissues and ovarian adenocarcinomas. Histochem Cell Biol. 2009; 132(1):117-27. DOI: 10.1007/s00418-009-0592-2. View

Couchman J . Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol. 2010; 26:89-114. DOI: 10.1146/annurev-cellbio-100109-104126. View

Kim S, Turnbull J, Guimond S . Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol. 2011; 209(2):139-51. DOI: 10.1530/JOE-10-0377. View

10.

Bolte S, Cordelieres F . A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2007; 224(Pt 3):213-32. DOI: 10.1111/j.1365-2818.2006.01706.x. View

11.

Kalmes A, Daum G, Clowes A . EGFR transactivation in the regulation of SMC function. Ann N Y Acad Sci. 2002; 947:42-54; discussion 54-5. DOI: 10.1111/j.1749-6632.2001.tb03929.x. View

12.

Kozma E, Wisowski G, Olczyk K . Platelet derived growth factor BB is a ligand for dermatan sulfate chain(s) of small matrix proteoglycans from normal and fibrosis affected fascia. Biochimie. 2009; 91(11-12):1394-404. DOI: 10.1016/j.biochi.2009.07.010. View

13.

Schaller M, Hildebrand J, Shannon J, Fox J, Vines R, Parsons J . Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol Cell Biol. 1994; 14(3):1680-8. PMC: 358526. DOI: 10.1128/mcb.14.3.1680-1688.1994. View

14.

Ferro D, Provasoli A, Ragazzi M, Casu B, Torri G, Bossennec V . Conformer populations of L-iduronic acid residues in glycosaminoglycan sequences. Carbohydr Res. 1990; 195(2):157-67. DOI: 10.1016/0008-6215(90)84164-p. View

15.

Fager G, Camejo G, Olsson U, LUSTIG F, Bondjers G . Binding of platelet-derived growth factor and low density lipoproteins to glycosaminoglycan species produced by human arterial smooth muscle cells. J Cell Physiol. 1995; 163(2):380-92. DOI: 10.1002/jcp.1041630218. View

16.

Bao X, Nishimura S, Mikami T, Yamada S, Itoh N, Sugahara K . Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of L-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities. J Biol Chem. 2003; 279(11):9765-76. DOI: 10.1074/jbc.M310877200. View

17.

Rasente R, Egitto P, Calabrese G . Low molecular mass dermatan sulfate modulates endothelial cells proliferation and migration. Carbohydr Res. 2012; 356:233-7. DOI: 10.1016/j.carres.2012.03.036. View

18.

Mitsunaga C, Mikami T, Mizumoto S, Fukuda J, Sugahara K . Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum. Spatiotemporal regulation of the expression of critical disulfated disaccharides by specific sulfotransferases. J Biol Chem. 2006; 281(28):18942-52. DOI: 10.1074/jbc.M510870200. View

19.

Ilarraza Lomeli H, Herrera Franco R, Lomeli Rivas A, Zavala Ramirez J, Martinez Ramirez L, Ramos Becerril F . [National Registry of Cardiac Rehabilitation Programs in México]. Arch Cardiol Mex. 2009; 79(1):63-72. View

20.

Li H, Yuan X, Tang J, Zhang Y . Lipopolysaccharide disrupts the directional persistence of alveolar myofibroblast migration through EGF receptor. Am J Physiol Lung Cell Mol Physiol. 2012; 302(6):L569-79. DOI: 10.1152/ajplung.00217.2011. View