Skip to main content

Small Leucine-Rich Proteoglycans

  • Chapter
  • First Online:
The Extracellular Matrix: an Overview

Part of the book series: Biology of Extracellular Matrix ((BEM))

Abstract

The small leucine-rich proteoglycans (SLRPs) comprise an expanding family of proteoglycans and glycoproteins that now encompass five distinct groups including three canonical and two noncanonical classes based on shared structural and functional parameters. SLRPs are tissue organizers by orienting and ordering various collagenous matrices during ontogeny, wound repair, and cancer and interact with a number of surface receptors and growth factors, thereby regulating cell behavior. The focus of this chapter is on novel conceptual and functional advances in our understanding of SLRP biology with special emphasis on genetic diseases, cancer growth, fibrosis, osteoporosis, and other biological processes where these proteoglycans play a central role.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adany R, Iozzo RV (1990) Altered methylation of versican proteoglycan gene in human colon carcinoma. Biochem Biophys Res Commun 171:1402–1413

    Article  CAS  PubMed  Google Scholar 

  • Adany R, Heimer R, Caterson B, Sorrell JM, Iozzo RV (1990) Altered expression of chondroitin sulfate proteoglycan in the stroma of human colon carcinoma. Hypomethylation of PG-40 gene correlates with increased PG-40 content and mRNA levels. J Biol Chem 265:11389–11396

    CAS  PubMed  Google Scholar 

  • Ameye L, Young MF (2002) Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers–Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12:107R–116R

    Article  CAS  PubMed  Google Scholar 

  • Ameye L, Aria D, Jepsen K, Oldberg A, Xu T, Young MF (2002) Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB J 16:673–680

    Article  CAS  PubMed  Google Scholar 

  • Araki K, Wakabayashi H, Shintani K, Morikawa J, Matsumine A, Kusuzaki K, Sudo A, Uchida A (2009) Decorin suppresses bone metastasis in a breast cancer cell line. Oncology 77:92–99

    Article  CAS  PubMed  Google Scholar 

  • Babelova A, Moreth K, Tsalastra-Greul W, Zeng-Brouwers J, Eickelberg O, Young MF, Bruckner P, Pfeilschifter J, Schaefer RM, Gröne H-J, Schaefer L (2009) Biglycan, a danger signal that activates the NLRP3 inflammasome via Toll-like and P2X receptors. J Biol Chem 284:24035–24048

    Article  CAS  PubMed  Google Scholar 

  • Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B, Birch DG, Bergen AAB, Prinsen CFM, Polomeno RC, Gal A, Drack AV, Musarella MA, Jacobson SG, Young RSL, Weleber RG (2000) Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat Genet 26:319–323

    Article  CAS  PubMed  Google Scholar 

  • Bi Y, Stueltens CH, Kilts T, Wadhwa S, Iozzo RV, Robey PG, Chen X-D, Young MF (2005) Extracellular matrix proteoglycans control the fate of bone marrow stromal cells. J Biol Chem 280:30481–30489

    Article  CAS  PubMed  Google Scholar 

  • Bi Y, Ehirchiou D, Kilts TM, Inkson CA, Embree MC, Sonoyama W, Li L, Leet AI, Seo B-M, Zhang L, Shi S, Young MF (2007) Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13:1219–1227

    Article  CAS  PubMed  Google Scholar 

  • Bi X, Tong C, Dokendorff A, Banroft L, Gallagher L, Guzman-Hartman G, Iozzo RV, Augenlicht LH, Yang W (2008) Genetic deficiency of decorin causes intestinal tumor formation through disruption of intestinal cell maturation. Carcinogenesis 29:1435–1440

    Article  CAS  PubMed  Google Scholar 

  • Bianco P, Fisher LW, Young MF, Termine JD, Robey PG (1990) Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J Histochem Cytochem 38:1549–1563

    CAS  PubMed  Google Scholar 

  • Biglari A, Bataille D, Naumann U, Weller M, Zirger J, Castro MG, Lowenstein PR (2004) Effects of ectopic decorin in modulating intracranial glioma progression in vivo, in a rat syngeneic model. Cancer Gene Ther 11:721–732

    Article  CAS  PubMed  Google Scholar 

  • Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF (2003) MET, metastasis, motility and more. Nat Rev Mol Cell Biol 4:915–925

    Article  CAS  PubMed  Google Scholar 

  • Brandan E, Retamal C, Cabello-Verrugio C, Marzolo M-P (2006) The low density lipoprotein receptor-related protein functions as an endocytic receptor for decorin. J Biol Chem 281:31562–31571

    Article  CAS  PubMed  Google Scholar 

  • Brandan E, Cabello-Verrugio C, Vial C (2008) Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol 27:700–708

    Article  CAS  PubMed  Google Scholar 

  • Bredrup C, Knappskog PM, Majewski J, Rodahl E, Boman H (2005a) Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Invest Ophthalmol Vis Sci 46:420–426

    Article  PubMed  Google Scholar 

  • Bredrup C, Knappskog PM, Majewski J, Rødahl E, Boman H (2005b) Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Invest Ophthalmol Vis Sci 46:420–426

    Article  PubMed  Google Scholar 

  • Brézillon S, Radwanska A, Zeltz C, Malkowski A, Ploton D, Bobichon H, Perreau C, Malicka-Blaszkiewicz M, Maquart F-X, Wegrowski Y (2009) Lumican core protein inhibits melanoma cell migration via alterations of focal adhesion complexes. Cancer Lett 283:92–100

    Article  PubMed  CAS  Google Scholar 

  • Brown EL, Wooten RM, Johnson BJB, Iozzo RV, Smith A, Dolan MC, Guo BP, Weis JJ, Höök M (2001) Resistance to Lyme disease in decorin-deficient mice. J Clin Invest 107:845–852

    Article  CAS  PubMed  Google Scholar 

  • Bussolino F, Di Renzo MF, Ziche M, Bocchietto E, Olivero M, Naldini L, Gaudino G, Tamagnone L, Coffer A, Comoglio PM (1992) Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol 119:629–641

    Article  CAS  PubMed  Google Scholar 

  • Cao R, Björndahl MA, Gallego MI, Chen S, Religa P, Hansen AJ, Cao Y (2006) Hepatocyte growth factor is a lymphangiogenic factor with an indirect mechanism of action. Blood 107:3531–3536

    Article  CAS  PubMed  Google Scholar 

  • Carlson EC, Lin M, Liu C-Y, Kao WWY, Perez VL, Pearlman E (2007) Keratocan and lumican regulate neutrophil infiltration and corneal clarity in lipopolysaccharide-induced keratitis by direct interaction with CXCL1. J Biol Chem 282:33502–33509

    Google Scholar 

  • Chakravarti S (2003) Functions of lumican and fibromodulin: lessons from knockout mice. Glycoconj J 19:287–293

    Article  Google Scholar 

  • Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141:1277–1286

    Article  CAS  PubMed  Google Scholar 

  • Chakravarti S, Paul J, Roberts L, Chervoneva I, Oldberg A, Birk DE (2003) Ocular and scleral alterations in gene-targeted lumican-fibromodulin double-null mice. Invest Ophthalmol Vis Sci 44:2422–2432

    Article  PubMed  Google Scholar 

  • Chen X-D, Allen MR, Bloomfield S, Xu T, Young M (2003) Biglycan-deficient mice have delayed osteogenesis after marrow ablation. Calcif Tissue Int 72:577–582

    Article  CAS  PubMed  Google Scholar 

  • Chen X-D, Fisher LW, Robey PG, Young MF (2004) The small leucine-rich proteoglycan biglycan modulates BMP-4-induced osteoblast differentiation. FASEB J 18:948–958

    Article  CAS  PubMed  Google Scholar 

  • Chen ZTY, Wang I-J, Shih Y-F, Lin LLK (2009) The association of haplotype at the lumican gene with high myopia susceptibilty in Taiwanese patients. Ophthalmology 116:1920–1927

    Article  PubMed  Google Scholar 

  • Corsi A, Xu T, Chen X-D, Boyde A, Liang J, Mankani M, Sommer B, Iozzo RV, Eichstetter I, Robey PG, Bianco P, Young MF (2002) Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers–Danlos-like changes in bone and other connective tissues. J Bone Miner Res 17:1180–1189

    Article  CAS  PubMed  Google Scholar 

  • Csordás G, Santra M, Reed CC, Eichstetter I, McQuillan DJ, Gross D, Nugent MA, Hajnóczky G, Iozzo RV (2000) Sustained down-regulation of the epidermal growth factor receptor by decorin. A mechanism for controlling tumor growth in vivo. J Biol Chem 275:32879–32887

    Article  PubMed  Google Scholar 

  • Danielson KG, Fazzio A, Cohen I, Cannizzaro LA, Eichstetter I, Iozzo RV (1993) The human decorin gene: intron–exon organization, discovery of two alternatively spliced exons in the 5′ untranslated region, and mapping of the gene to chromosome 12q23. Genomics 15:146–160

    Article  CAS  PubMed  Google Scholar 

  • Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136:729–743

    Article  CAS  PubMed  Google Scholar 

  • Day AA, McQuillan CI, Termine JD, Young MR (1987) Molecular cloning and sequence analysis of the cDNA for small proteoglycan II of bovine bone. Biochem J 248:801–805

    CAS  PubMed  Google Scholar 

  • de Lange DC, Melder RJ, Munn LL, Mouta-Carreira C, Jain RK, Boucher Y (2001) Decorin inhibits endothelial migration and tube-like structure formation: role of thrombospondin-1. Microvasc Res 62:26–42

    Article  CAS  Google Scholar 

  • De Luca A, Santra M, Baldi A, Giordano A, Iozzo RV (1996) Decorin-induced growth suppression is associated with upregulation of p21, an inhibitor of cyclin-dependent kinases. J Biol Chem 271:18961–18965

    Article  PubMed  Google Scholar 

  • Du Y, Carlson EC, Funderburgh ML, Birk DE, Pearlman E, Guo N, Kao WW-Y, Funderburgh JL (2009) Stem cell therapy restores transparency to defective murine corneas. Stem Cells 27:1635–1642

    Article  CAS  PubMed  Google Scholar 

  • Dugan TA, Yang VWC, McQuillan DJ, Höök M (2003) Decorin binds fibrinogen in a Zn2+-dependent interaction. J Biol Chem 278:13655–13662

    Article  CAS  PubMed  Google Scholar 

  • Elliott DM, Robinson PS, Gimbel JA, Sarver JJ, Abboud JA, Iozzo RV, Soslowsky LJ (2003) Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann Biomed Eng 31:599–605

    Article  PubMed  Google Scholar 

  • Embree MC, Kilts TM, Ono M, Inkson CA, Seyed-Picard F, Karsdal MA, Oldberd Ã…, Bi Y, Young MF (2010) Biglycan and fibromodulin have essential roles in regulating chondrogenesis and extracellular matrix turnover in temporomandibular joint osteoarthritis. Am J Pathol 176:812–826

    Article  CAS  PubMed  Google Scholar 

  • Ezura Y, Chakravarti S, Oldberg Ã…, Chervoneva I, Birk DE (2000) Differential expression of lumican and fibromodulin regulate collagen fibrillogenesis in developing mouse tendons. J Cell Biol 151:779–787

    Article  CAS  PubMed  Google Scholar 

  • Fadic R, Mezzano V, Alvarez K, Cabrera D, Holmgren J, Brandan E (2006) Increase in decorin and biglycan in Duchenne muscular dystrophy: role of fibroblasts as cell source of these proteoglycans in the disease. J Cell Mol Med 10:758–769

    Article  CAS  PubMed  Google Scholar 

  • Ferdous Z, Wei VM, Iozzo RV, Höök M, Grande-Allen KJ (2007) Decorin-transforming growth factor-β interaction regulates matrix organization and mechanical characteristics of three-dimensional collagen matrices. J Biol Chem 282:35887–35898

    Article  CAS  PubMed  Google Scholar 

  • Ferdous Z, Lazaro LD, Iozzo RV, Höök M, Grande-Allen KJ (2008) Influence of cyclic strain and decorin deficiency on 3D cellularized collagen matrices. Biomaterials 29:2740–2748

    Article  CAS  PubMed  Google Scholar 

  • Ferdous Z, Peterson SB, Tseng H, Anderson DK, Iozzo RV, Grande-Allen KJ (2010) A role for decorin in controlling proliferation, adhesion, and migration of murine embryonic fibroblasts. J Biomed Mater Res A 93:419–428

    CAS  PubMed  Google Scholar 

  • Fischer JW, Kinsella MG, Levkau B, Clowes AW, Wight TN (2001) Retroviral overexpression of decorin differentially affects the response of arterial smooth muscle cells to growth factors. Arterioscler Thromb Vasc Biol 21:777–784

    CAS  PubMed  Google Scholar 

  • Friedl A (2010) Proteoglycans: master modulators of paracrine fibroblast-carcinoma interactions. Semin Cell Dev Biol 21:66–71

    Article  CAS  PubMed  Google Scholar 

  • Fust A, LeBellego F, Iozzo RV, Roughley PJ, Ludwig MS (2005) Alterations in lung mechanics in decorin deficient mice. Am J Physiol Lung Cell Mol Physiol 288:L159–L166

    Article  CAS  PubMed  Google Scholar 

  • Geng Y, McQuillan D, Roughley PJ (2006) SLRP interaction can protect collagen fibrils from cleavage by collagenases. Matrix Biol 25:484–491

    Article  CAS  PubMed  Google Scholar 

  • Gill MR, Oldberd Ã…, Reinholt FP (2002) Fibromodulin-null murine knee joints display increased incidences of osteoarthritis and alterations in tissue biochemistry. Osteoarthritis Cartilage 10:751–757

    Article  CAS  PubMed  Google Scholar 

  • Goldberg M, Septier D, Rapoport O, Iozzo RV, Young MF, Ameye LG (2005) Targeted disruption of two small leucine-rich proteoglycans, biglycan and decorin, exerts divergent effects on enamel and dentin formation. Calcif Tissue Int 77:297–310

    Article  CAS  PubMed  Google Scholar 

  • Goldberg M, Septier D, Oldberd Ã…, Young MF, Ameye LG (2006) Fibromodulin-deficient mice display impaired collagen fibrillogenesis in predentin as well as altered dentin mineralization and enamel formation. J Histochem Cytochem 54:525–537

    Article  CAS  PubMed  Google Scholar 

  • Goldoni S, Iozzo RV (2008) Tumor microenvironment: modulation by decorin and related molecules harboring leucine-rich tandem motifs. Int J Cancer 123:2473–2479

    Article  CAS  PubMed  Google Scholar 

  • Goldoni S, Owens RT, McQuillan DJ, Shriver Z, Sasisekharan R, Birk DE, Campbell S, Iozzo RV (2004) Biologically active decorin is a monomer in solution. J Biol Chem 279:6606–6612

    Article  CAS  PubMed  Google Scholar 

  • Goldoni S, Seidler DG, Heath J, Fassan M, Baffa R, Thakur ML, Owens RA, McQuillan DJ, Iozzo RV (2008) An anti-metastatic role for decorin in breast cancer. Am J Pathol 173:844–855

    Article  CAS  PubMed  Google Scholar 

  • Goldoni S, Hunphries A, Nyström A, Sattar S, Owens RT, McQuillan DJ, Ireton K, Iozzo RV (2009) Decorin is a novel antagonistic ligand of the Met receptor. J Cell Biol 185:743–754

    Article  CAS  PubMed  Google Scholar 

  • Grant DS, Kleinman HK, Goldberg ID, Bhargava MM, Nickoloff BJ, Kinsella JL, Polverini P, Rosen EM (1993) Scatter factor induces blood vessel formation in vivo. Proc Natl Acad Sci USA 90:1937–1941

    Article  CAS  PubMed  Google Scholar 

  • Grant DS, Yenisey C, Rose RW, Tootell M, Santra M, Iozzo RV (2002) Decorin suppresses tumor cell-mediated angiogenesis. Oncogene 21:4765–4777

    Article  CAS  PubMed  Google Scholar 

  • Groeneveld TWL, Oroszlán M, Owens RT, Faber-Krol MC, Bakker AC, Arlaud GJ, McQuillan DJ, Kishore U, Daha MR, Roos A (2005) Interactions of the extracellular matrix proteoglycans decorin and biglycan with C1q and collectins. J Immunol 175:4715–4723

    CAS  PubMed  Google Scholar 

  • Gu Y, Zhang S, Wu Q, Xu S, Cui Y, Yang Z, Zhao X (2010) Differential expression of decorin, EGFR and cyclin D1 during mammary gland carcinogenesis in TA2 mice with spontaneous breast cancers. J Exp Clin Cancer Res 29:6

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez J, Osses N, Brandan E (2006) Changes in secreted and cell associated proteoglycan synthesis during conversion of myoblasts to osteoblasts in response to bone morphogenetic protein-2: role of decorin in cell response to BMP-2. J Cell Physiol 206:58–67

    Article  CAS  PubMed  Google Scholar 

  • Häkkinen L, Strassburger S, Kahari VM, Scott PG, Eichstetter I, Iozzo RV, Larjava H (2000) A role for decorin in the structural organization of periodontal ligament. Lab Invest 80:1869–1880

    Article  PubMed  Google Scholar 

  • Haruyama N, Sreenath TL, Suzuki S, Yao X, Wang Z, Wang Y, Honeycutt C, Iozzo RV, Young MF, Kulkarni AB (2009) Genetic evidence for key roles of decorin and biglycan in dentin mineralization. Matrix Biol 28:129–136

    Article  CAS  PubMed  Google Scholar 

  • Heegaard A-M, Corsi A, Danielsen CC, Nielsen KL, Jorgensen HL, Riminucci M, Young MF, Bianco P (2007) Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation 115:2731–2738

    Article  CAS  PubMed  Google Scholar 

  • HeinegÃ¥rd D (2009) Proteoglycans and more – from molecules to biology. Int J Exp Pathol 90:575–586

    Article  PubMed  CAS  Google Scholar 

  • Henninger HB, Maas SA, Underwood CJ, Whitaker RT, Weiss JA (2006) Spatial distribution and orientation of dermatan sulfate in human medial collateral ligament. J Struct Biol 158:33–45

    Article  PubMed  CAS  Google Scholar 

  • Hu Y, Sun H, Owens RT, Wu J, Chen YQ, Berquin IM, Perry D, O’Flaherty JT, Edwards IJ (2009) Decorin suppresses prostate tumor growth through inhibition of epidermal growth factor and androgen receptor pathways. Neoplasia 11:1042–1053

    CAS  PubMed  Google Scholar 

  • Hwang J-Y, Johnson PY, Braun KR, Hinek A, Fischer JW, O’Brien KD, Starcher B, Clowes AW, Merrilees MJ, Wight TN (2008) Retrovirally mediated overexpression of glycosaminoglycan-deficient biglycan in arterial smooth muscle cells induces tropoelastin synthesis and elastic fiber formation in vitro and in neointimae after vascular injury. Am J Pathol 173:1919–1928

    Article  CAS  PubMed  Google Scholar 

  • Iacob D, Cai J, Tsonis M, Babwah A, Chakraborty RN, Lala PK (2008) Decorin-mediated inhibition of proliferation and migration of the human trophoblast via different tyrosine kinase receptors. Endocrinology 149:6187–6197

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV (1995) Tumor stroma as a regulator of neoplastic behavior. Agonistic and antagonistic elements embedded in the same connective tissue. Lab Invest 73:157–160

    CAS  PubMed  Google Scholar 

  • Iozzo RV (1997) The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth. Crit Rev Biochem Mol Biol 32:141–174

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609–652

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV (1999) The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J Biol Chem 274:18843–18846

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Cohen I (1993) Altered proteoglycan gene expression and the tumor stroma. Experientia 49:447–455

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Danielson KG (1999) Transcriptional and post-transcriptional control of proteoglycan gene expression. Prog Nucleic Acid Res Mol Biol 62:19–53

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Murdoch AD (1996) Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J 10:598–614

    CAS  PubMed  Google Scholar 

  • Iozzo RV, Schaefer L (2010) Proteoglycan roles in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 277:3864–3875

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Chakrani F, Perrotti D, McQuillan DJ, Skorski T, Calabretta B, Eichstetter I (1999a) Cooperative action of germline mutations in decorin and p53 accelerates lymphoma tumorigenesis. Proc Natl Acad Sci USA 96:3092–3097

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Moscatello D, McQuillan DJ, Eichstetter I (1999b) Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274:4489–4492

    Article  CAS  PubMed  Google Scholar 

  • Järveläinen HT, Iruela-Arispe ML, Kinsella MG, Sandell LJ, Sage EH, Wight TN (1992) Expression of decorin by sprouting bovine aortic endothelial cells exhibiting angiogenesis in vitro. Exp Cell Res 203:395–401

    Article  PubMed  Google Scholar 

  • Järveläinen H, Puolakkainen P, Pakkanen S, Brown EL, Höök M, Iozzo RV, Sage H, Wight TN (2006) A role for decorin in cutaneous wound healing and angiogenesis. Wound Rep Reg 14:443–452

    Article  Google Scholar 

  • Jepsen KE, Wu F, Peragallo JH, Paul J, Roberts L, Ezura Y, Oldberg Ä, Birk DE, Chakravarti S (2002) A syndrome of joint laxity and impaired tendon integrity in lumican- and fibromodulin-deficient mice. J Biol Chem 277:35532–35540

    Article  CAS  PubMed  Google Scholar 

  • Kajiya K, Hirakawa S, Ma B, Drinnenberg I, Detmar M (2005) Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 24:2885–2895

    Article  CAS  PubMed  Google Scholar 

  • Kalamajski S, Oldberd Ã… (2010) The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 29:248–253

    Article  CAS  PubMed  Google Scholar 

  • Kalamajski S, Oldberg Ã… (2009) Homologous sequence in lumican and fibromodulin leucine-rich repeat 5–7 competes for collagen binding. J Biol Chem 284:534–539

    Article  CAS  PubMed  Google Scholar 

  • Kalamajski S, Aspberg A, Lindblom K, HeinegÃ¥rd D, Oldberd Ã… (2009) Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization. Biochem J 423:53–59

    Article  CAS  PubMed  Google Scholar 

  • Keene DR, San Antonio JD, Mayne R, McQuillan DJ, Sarris G, Santoro SA, Iozzo RV (2000) Decorin binds near the C terminus of type I collagen. J Biol Chem 275:21801–21804

    Article  CAS  PubMed  Google Scholar 

  • Kilts T, Ameye L, Syed-Picard F, Ono M, Berendsen AD, Oldberg A, Heegaard A-M, Young MF (2009) Potential roles for the small leucine-rich proteoglycans biglycan and fibromodulin in ectopic ossification of tendon induced by exercise and in modulating rotarod performance. Scand J Med Sci Sports 19:536–546

    Article  CAS  PubMed  Google Scholar 

  • King VL, Hatch NW, Chan H-W, de Beer MC, de Beer FC, Tannock LR (2009) A murine model of obesity with accelerated atherosclerosis. Obesity 18:35–41

    Article  PubMed  CAS  Google Scholar 

  • Kinsella MG, Fischer JW, Mason DP, Wight TN (2000) Retrovirally mediated expression of decorin by macrovascular endothelial cells. Effects on cellular migration and fibronectin fibrillogenesis in vitro. J Biol Chem 275:13924–13932

    Article  CAS  PubMed  Google Scholar 

  • Kishioka Y, Thomas M, Wakamatsu J-I, Hattori A, Sharma M, Kambadur R, Nishimura T (2008) Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J Cell Physiol 215:856–867

    Article  CAS  PubMed  Google Scholar 

  • Kitaya K, Yasuo T (2009) Dermatan sulfate proteoglycan biglycan as a potential selectin L/CD44 ligand involved in selective recruitment of peripheral blood CD16(−) natural killer cells into human endometrium. J Leukoc Biol 85:391–400

    Article  CAS  PubMed  Google Scholar 

  • Kizawa H, Kou I, Iida A, Sudo A, Miyamoto Y, Fukuda A, Mabuchi A, Kotani A, Kawakami A, Yamamoto S, Uchida A, Nakamura K, Notoya K, Nakamura Y, Ikegawa S (2005) An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat Genet 37:138–144

    Article  CAS  PubMed  Google Scholar 

  • Kozma EM, Wisowski G, Olczyk K (2009) Platelet derived growth bactor BB is a ligand for dermatan sulfate chain(s) of small matrix proteoglycans from normal and fibrosis affected fascia. Biochimie 91:1394–1404

    Article  CAS  PubMed  Google Scholar 

  • Krusius T, Ruoslahti E (1986) Primary structure of an extracellular matrix proteoglycan core protein deduced from cloned cDNA. Proc Natl Acad Sci USA 83:7683–7687

    Article  CAS  PubMed  Google Scholar 

  • Kuriyama S, Lupo G, Ohta K, Ohnuma SI, Harris WA, Tanaka H (2005) Tsukushi controls extodermal patterning and neural crest specification in Xenopus by direct regulation of BMP4 and X-delta-1 activity. Development 133:75–88

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Bowrin K, Hamad AR, Chakravarti S (2009) Extracellular matrix lumican deposited on the surface of neutrophils promotes migration by binding to β2 integrin. J Biol Chem 284:23662–23669

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Aoki T, Mori Y, Ahmad M, Miyamori H, Takino T, Sato H (2004) Cleavage of lumican by membrane-type matrix metalloprotease-1 abrogates this proteoglycan-mediated suppression of tumor cell colony formation in soft agar. Cancer Res 64:7058–7064

    Article  CAS  PubMed  Google Scholar 

  • Li L, Okada H, Takemura G, Kosai K-I, Kanamori H, Esaki M, Takahashi T, Goto K, Tsujimoto A, Maruyama R, Kawamura I, Kawaguchi T, Takeyama T, Fujiwara T, Fujiwara H, Minatoguchi S (2009) Postinfarction gene therapy with adenoviral vector expressing decorin mitigates cardiac remodeling and dysfunction. Am J Physiol Heart Circ Physiol 297:H1504–H1513

    Article  CAS  PubMed  Google Scholar 

  • Liang FT, Wang T, Brown EL, Iozzo RV, Fikrig E (2004) Protective niche for Borrelia burgdorferi to evade humoral immunity. Am J Pathol 165:977–985

    Article  PubMed  Google Scholar 

  • Little PJ, Osman N, O’Brien KD (2008) Hyperelongated biglycan: the surreptitious initiator of atherosclerosis. Curr Opin Lipidol 19:448–454

    Article  CAS  PubMed  Google Scholar 

  • Liu C-Y, Birk D, Hassell JR, Kane B, Kao W-Y (2003) Keratocan-deficient mice display alterations in corneal structure. J Biol Chem 278:21672–21677

    Article  CAS  PubMed  Google Scholar 

  • Maccarana M, Kalamajski S, Kongsgaard M, Magnusson SP, Oldberg Ã…, Malmström A (2009) Dermatan sulfate epimerase 1-deficient mice have reduced content and changed distribution of iduronic acids in dermatan sulfate and an altered collagen structure in skin. Mol Cell Biol 29:5517–5528

    Article  CAS  PubMed  Google Scholar 

  • Majava M, Bishop PN, Hägg P, Scott PG, Rice A, Inglehearn C, Hammond CJ, Spector TD, Ala-Kokko L, Männikkö M (2007) Novel mutations in small leucine-rich repeat protein/proteoglycan (SLRP) genes in high myopia. Hum Mutat 28:336–344

    Article  CAS  PubMed  Google Scholar 

  • Matsumine A, Shintani K, Kusuzaki K, Matsubara T, Satonaka H, Wakabayashi T, Iino T, Uchida A (2007) Expression of decorin, a small leucine-rich proteoglycan, as a prognostic factor in soft tissue tumors. J Surg Oncol 96:411–418

    Article  CAS  PubMed  Google Scholar 

  • Mauviel A, Santra M, Chen YQ, Uitto J, Iozzo RV (1995) Transcriptional regulation of decorin gene expression. Induction by quiescence and repression by tumor necrosis factor-α. J Biol Chem 270:11692–11700

    Article  CAS  PubMed  Google Scholar 

  • Mercado ML, Amenta AR, Hagiwara H, Rafii MS, Lechner BE, Owens RT, McQuillan DJ, Froehner SC, Fallon JR (2006) Biglycan regulates the expression and sarcolemmal localization of dystrobrevin, syntrophin and nNOS. FASEB J 20:1724–1726

    Article  CAS  PubMed  Google Scholar 

  • Merline R, Lazaroski S, Babelova A, Tsalastra-Greul W, Pfeilschifter J, Schluter KD, Gunther A, Iozzo RV, Schaefer RM, Schaefer L (2009) Decorin deficiency in diabetic mice: aggravation of nephropathy due to overexpression of profibrotic factors, enhanced apoptosis and mononuclear cell infiltration. J Physiol Pharmacol 60(suppl 4):5–13

    PubMed  Google Scholar 

  • Mimura T, Han KY, Onguchi T, Chang J-H, Kim T-I, Kojima T, Zhou Z, Azar DT (2008) MT1-MMP-mediated cleavage of decorin in corneal angiogenesis. J Vasc Res 46:541–550

    Article  CAS  Google Scholar 

  • Miura T, Kishioka Y, Wakamatsu J, Hattori A, Hennebry A, Berry CJ, Sharma M, Kambadur R, Nishimura T (2006) Decorin binds myostatin and modulates its activity to muscle cells. Biochem Biophys Res Commun 340:675–680

    Article  CAS  PubMed  Google Scholar 

  • Moreno M, Muñoz R, Aroca F, Labarca M, Brandan E, Larraín J (2005) Biglycan is a new extracellular component of the chordin-BMP4 signaling pathway. EMBO J 24:1397–1405

    Article  CAS  PubMed  Google Scholar 

  • Moscatello DK, Santra M, Mann DM, McQuillan DJ, Wong AJ, Iozzo RV (1998) Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J Clin Invest 101:406–412

    Article  CAS  PubMed  Google Scholar 

  • Nagy N, Melchior-Becker A, Fischer JW (2010) Long-term treatment with AT1-receptor antagonist telmisartan inhibits biglycan accumulation in murine atherosclerosis. Basic Res Cardiol 105:29–38

    Article  CAS  PubMed  Google Scholar 

  • Nakashima Y, Fujii H, Sumiyoshi S, Wight TN, Sueishi K (2007) Early human atherosclerosis; accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 27:1159–1165

    Article  CAS  PubMed  Google Scholar 

  • Nash MA, Loercher AE, Freedman RS (1999) In vitro growth inhibition of ovarian cancer cells by decorin: synergism of action between decorin and carboplatin. Cancer Res 59:6192–6196

    CAS  PubMed  Google Scholar 

  • Nelimarkka L, Kainulainen V, Schönherr E, Moisander S, Jortikka M, Lammi M, Elenius K, Jalkanen M, Järveläinen HT (1997) Expression of small extracellular chondroitin/dermatan sulfate proteoglycans is differentially regulated in human endothelial cells. J Biol Chem 272:12730–12737

    Article  CAS  PubMed  Google Scholar 

  • Nelimarkka L, Salminen H, Kuopio T, Nikkari S, Ekfors T, Laine J, Pelliniemi L, Järveläinen H (2001) Decorin is produced by capillary endothelial cells in inflammation-associated angiogenesis. Am J Pathol 158:345–353

    Article  CAS  PubMed  Google Scholar 

  • Nikitovic D, Berdiaki A, Zfiropoulos A, Katonis P, Tsatsakis A, Karamanos N, Tzanakakis GN (2008a) Lumican expression is positively correlated with the differentiation and negatively with the growth of human osteosarcoma cells. FEBS J 275:350–361

    Article  CAS  PubMed  Google Scholar 

  • Nikitovic D, Berdiaki K, Chalkiadaki G, Karamanos N, Tzanakakis G (2008b) The role of SLRP-proteoglycans in osteosarcoma pathogenesis. Connect Tissue Res 49:235–238

    Article  CAS  PubMed  Google Scholar 

  • Nili N, Cheema AN, Giordano FJ, Barolet AW, Babaei S, Hickey R, Eskandarian MR, Smeets M, Butany J, Pasterkamp G, Strauss BH (2003) Decorin inhibition of PDGF-stimulated vascular smooth muscle cell function. Potential mechanism for inhibition of intimal hyperplasia after balloon angioplasty. Am J Pathol 163:869–878

    Article  CAS  PubMed  Google Scholar 

  • Nuka S, Zhou W, Henry SP, Gendron CMSJB, Shinomura T, Johnson J, Wang Y, Keene DR, Ramírez-Solis R, Behringer RR, Young MF, Höök M (2010) Phenotypic characterization of epiphycan-deficient and epiphycan/biglycan double-deficient mice. Osteoarthritis Cartilage 18:88–96

    Article  CAS  PubMed  Google Scholar 

  • O’Connor E, Eisenhaber B, Dalley J, Wang T, Missen C, Bulleid N, Bishop PN, Trump D (2005) Species specific membrane anchoring of nyctalopin, a small leucine-rich repeat protein. Hum Mol Genet 14:1877–1887

    Article  PubMed  CAS  Google Scholar 

  • Ohta K, Lupo G, Kuriyama S, Keynes R, Holt CE, Harris WA, Tanaka H, Ohnuma S-I (2004) Tsukushi functions as an organizer inducer by inhibition of BMP activity in cooperation with chordin. Dev Cell 7:347–358

    Article  CAS  PubMed  Google Scholar 

  • Ohta K, Kuriyama S, Okafuji T, Gejima R, Ohnuma S-I, Tanaka H (2006) Tsukushi cooperates with VG1 to induce primitive streak and Hensen’s node formation in the chick embryo. Development 133:3777–3786

    Article  CAS  PubMed  Google Scholar 

  • Park H, Huxley-Jones J, Boot-Handford RP, Bishop PN, Attwood TK, Bella J (2008) LRRCE: a leucine-rich repeat cysteine capping motif unique to the chordate lineage. BMC Genomics 9:599

    Article  PubMed  CAS  Google Scholar 

  • Patel S, Santra M, McQuillan DJ, Iozzo RV, Thomas AP (1998) Decorin activates the epidermal growth factor receptor and elevates cytosolic Ca2+ in A431 cells. J Biol Chem 273:3121–3124

    Article  CAS  PubMed  Google Scholar 

  • Pellegata NS, Dieguez-Lucena JL, Joensuu T, Lau S, Montgomery KT, Krahe R, Kivela T, Kucherlapati R, Forsius H, de la Chapelle A (2000) Mutations in KERA, encoding keratocan, cause cornea plana. Nat Genet 25:91–95

    Article  CAS  PubMed  Google Scholar 

  • Petit AMV, Rak J, Hung M-C, Rockwell P, Goldstein N, Fendly B, Kerbel RS (1997) Neutralizing antibodies against epidermal growth factor and Erb-2/neu receptor tyrosine kinases down-regulated vascular endothelial growth factor production by tumor cells in vitro and in vivo. Angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 151:1523–1530

    CAS  PubMed  Google Scholar 

  • Phung TL, Ziv K, Dabydeen D, Eyah-Mensah G, Riveros M, Peruzzi C, Sun J, Monahan-Early RA, Shiojima I, Nagy JALMI, Walsh K, Dvorak AM, Briscoe DM, Neeman M, Sessa WC, Dvorak HF, Benjamin LE (2006) Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10:159–170

    Article  CAS  PubMed  Google Scholar 

  • Pusch CM, Zeitz C, Brandau O, Pesch K, Achatz H, Feil S, Scharfe C, Maurer J, Jacobi FK, Pinckers A, Andreasson S, Hardcastle A, Wissinger B, Berger W, Meindl A (2000) The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat Genet 26:324–327

    Article  CAS  PubMed  Google Scholar 

  • Rafii MS, Hagiwara H, Mercado ML, Seo NS, Xu T, Dugan T, Owens RT, Höök M, McQuillan DJ, Young MF, Fallon JR (2006) Biglycan binds to α- and γ-sarcoglycan and regulates their expression during development. J Cell Physiol 209:439–447

    Article  CAS  PubMed  Google Scholar 

  • Raspanti M, Violoa M, Forlino A, Tenni R, Gruppi C, Tira ME (2008) Glycosaminoglycans show a specific periodic interaction with type I collagen fibrils. J Struct Biol 164:134–139

    Article  CAS  PubMed  Google Scholar 

  • Reed CC, Iozzo RV (2002) The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 19:249–255

    Article  CAS  PubMed  Google Scholar 

  • Reed CC, Gauldie J, Iozzo RV (2002) Suppression of tumorigenicity by adenovirus-mediated gene transfer of decorin. Oncogene 21:3688–3695

    Article  CAS  PubMed  Google Scholar 

  • Reed CC, Waterhouse A, Kirby S, Kay P, Owens RA, McQuillan DJ, Iozzo RV (2005) Decorin prevents metastatic spreading of breast cancer. Oncogene 24:1104–1110

    Article  CAS  PubMed  Google Scholar 

  • Reinboth BJ, Finnis ML, Gibson MA, Sandberg LB, Cleary EG (2000) Developmental expression of dermatan sulfate proteoglycans in the elastic bovine nuchal ligament. Matrix Biol 19:149–162

    Article  CAS  PubMed  Google Scholar 

  • Reinboth B, Hanssen E, Cleary EG, Gibson MA (2002) Molecular interactions of biglycan and decorin with elastic fiber components: biglycan forms a ternary complex with tropoelastin and micrfibril-associated glycoprotein 1. J Biol Chem 277:3950–3957

    Article  CAS  PubMed  Google Scholar 

  • Robinson PS, Huang TF, Kazam E, Iozzo RV, Birk DE, Soslowsky LJ (2005) Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J Biomech Eng 127:181–185

    Article  PubMed  Google Scholar 

  • Rødahl E, Van Ginderdeuren R, Knappskog PM, Bredrup C, Boman H (2006) A second decorin frame shift mutation in a family with congenital stromal corneal dystrophy. Am J Ophthalmol 142:520–521

    Article  PubMed  CAS  Google Scholar 

  • Rucci N, Rufo A, Alamanou M, Capulli M, Del Fattore A, Ã…hrman E, Capece D, Iansante V, Zazzeroni F, Alesse E, HeinegÃ¥rd D, Teti A (2009) The glycosaminoglycan-binding domain of PRELP acts as a cell type-specific NF-κB inhibitor that impairs osteoclastogenesis. J Cell Biol 187:669–683

    Article  CAS  PubMed  Google Scholar 

  • Rühland C, Schönherr E, Robenek H, Hansen U, Iozzo RV, Bruckner P, Seidler DG (2007) The glycosaminoglycan chain of decorin plays an important role in collagen fibril formation at the early stages of fibrillogenesis. FEBS J 274:4246–4255

    Article  PubMed  CAS  Google Scholar 

  • Salomäki HH, Sainio AO, Söderström M, Pakkanen S, Laine J, Järveläinen HT (2008) Differential expression of decorin by human malignant and benign vascular tumors. J Histochem Cytochem 56:639–646

    Article  PubMed  CAS  Google Scholar 

  • Sanches JCT, Jones CJP, Aplin JD, Iozzo RV, Zorn TMT, Oliveira SF (2010) Collagen fibril organization in the pregnant endometrium of decorin-deficient mice. J Anat 216:144–155

    Article  PubMed  Google Scholar 

  • Santra M, Danielson KG, Iozzo RV (1994) Structural and functional characterization of the human decorin gene promoter. J Biol Chem 269:579–587

    CAS  PubMed  Google Scholar 

  • Santra M, Skorski T, Calabretta B, Lattime EC, Iozzo RV (1995) De novo decorin gene expression suppresses the malignant phenotype in human colon cancer cells. Proc Natl Acad Sci USA 92:7016–7020

    Article  CAS  PubMed  Google Scholar 

  • Santra M, Mann DM, Mercer EW, Skorski T, Calabretta B, Iozzo RV (1997) Ectopic expression of decorin protein core causes a generalized growth suppression in neoplastic cells of various histogenetic origin and requires endogenous p21, an inhibitor of cyclin-dependent kinases. J Clin Invest 100:149–157

    Article  CAS  PubMed  Google Scholar 

  • Santra M, Eichstetter I, Iozzo RV (2000) An anti-oncogenic role for decorin: downregulation of ErbB2 leads to growth suppression and cytodifferentiation of mammary carcinoma cells. J Biol Chem 275:35153–35161

    Article  CAS  PubMed  Google Scholar 

  • Santra M, Reed CC, Iozzo RV (2002) Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping with but distinct from the EGF-binding epitope. J Biol Chem 277:35671–35681

    Article  CAS  PubMed  Google Scholar 

  • Saucier C, Khoury H, Lai K-M V, Peschard P, Dankort D, Naujokas MA, Holash J, Yancopoulos GD, Muller WJ, Pawson T, Park M (2004) The Shc adaptor protein is critical for VEGF induction by Met/HGF and ErbB2 receptors and for early onset of tumor angiogenesis. Proc Natl Acad Sci USA 101:2345–2350

    Article  CAS  PubMed  Google Scholar 

  • Schaefer L (2010) Extracellular matrix molecules: endogenous danger signals as new drug targets in kidney diseases. Curr Opin Pharmacol 10:185–190

    Article  CAS  PubMed  Google Scholar 

  • Schaefer L, Iozzo RV (2008) Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem 283:21305–21309

    Article  CAS  Google Scholar 

  • Schaefer L, Macakova K, Raslik I, Micegova M, Gröne H-J, Schönherr E, Robenek H, Echtermeyer FG, Grässel S, Bruckner P, Schaefer RM, Iozzo RV, Kresse H (2002) Absence of decorin adversely influences tubulointerstitial fibrosis of the obstructed kidney by enhanced apoptosis and increased inflammatory reaction. Am J Pathol 160:1181–1191

    Article  CAS  PubMed  Google Scholar 

  • Schaefer L, Mihalik D, Babelova A, Krzyzankova M, Grone HJ, Iozzo RV, Young MF, Seidler DG, Lin G, Reinhardt D, Schaefer RM (2004) Regulation of fibrillin-1 by biglycan and decorin is important for tissue preservation in the kidney during pressure-induced injury. Am J Pathol 165:383–396

    Article  CAS  PubMed  Google Scholar 

  • Schaefer L, Babelova A, Kiss E, Hausser H-J, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Götte M, Malle E, Schaefer RM, Gröne H-J (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115:2223–2233

    Article  CAS  PubMed  Google Scholar 

  • Schaefer L, Tsalastra W, Babelova A, Baliova M, Minnerup J, Sorokin L, Gröne H-J, Reinhardt DP, Pfeilschifter J, Iozzo RV, Schaefer RM (2007) Decorin-mediated regulation of fibrillin-1 in the kidney involves the insulin-like growth factor-1 receptor and mammalian target of rapamycin. Am J Pathol 170:301–315

    Article  CAS  PubMed  Google Scholar 

  • Scholzen T, Solursh M, Suzuki S, Reiter R, Morgan JL, Buchberg AM, Siracusa LD, Iozzo RV (1994) The murine decorin. Complete cDNA cloning, genomic organization, chromosomal assignment and expression during organogenesis and tissue differentiation. J Biol Chem 269:28270–28281

    CAS  PubMed  Google Scholar 

  • Schönherr E, Levkau B, Schaefer L, Kresse H, Walsh K (2001) Decorin-mediated signal transduction in endothelial cells. Involvement of Akt/protein kinase B in up-regulation of p21WAF1/CIP1 but not p27KIP1. J Biol Chem 276:40687–40692

    Article  PubMed  Google Scholar 

  • Schönherr E, Sunderkotter C, Schaefer L, Thanos S, Grässel S, Oldberg Ã…, Iozzo RV, Young MF, Kresse H (2004) Decorin deficiency leads to impaired angiogenesis in injured mouse cornea. J Vasc Res 41:499–508

    Article  PubMed  CAS  Google Scholar 

  • Schönherr E, Sunderkötter C, Iozzo RV, Schaefer L (2005) Decorin, a novel player in the insulin-like growth factor system. J Biol Chem 280:15767–15772

    Article  PubMed  CAS  Google Scholar 

  • Scott JE (1988) Proteoglycan-fibrillar collagen interactions. Biochem J 252:313–323

    CAS  PubMed  Google Scholar 

  • Seidler DG, Schaefer L, Robenek H, Iozzo RV, Kresse H, Schönherr E (2005) A physiologic three-dimensional cell culture system to investigate the role of decorin in matrix organisation and cell survival. Biochem Biophys Res Commun 332:1162–1170

    Article  CAS  PubMed  Google Scholar 

  • Seidler DG, Goldoni S, Agnew C, Cardi C, Thakur ML, Owens RA, McQuillan DJ, Iozzo RV (2006) Decorin protein core inhibits in vivo cancer growth and metabolism by hindering epidermal growth factor receptor function and triggering apoptosis via caspase-3 activation. J Biol Chem 281:26408–26418

    Article  CAS  PubMed  Google Scholar 

  • Shintani K, Matsumine A, Kusuzaki K, Morikawa J, Matsubara T, Wakabayashi T, Araki K, Satonaka H, Wakabayashi H, Lino T, Uchida A (2008) Decorin suppresses lung metastases of murine osteosarcoma. Oncol Rep 19:1533–1539

    CAS  PubMed  Google Scholar 

  • Sini P, Wyder L, Schnell C, O’Reilly T, Littlewood A, Brandt R, Hynes NE, Wood J (2005) The antitumor and antiangiogenic activity of vascular endothelial growth factor receptor inhibition is potentiated by ErbB1 blockade. Clin Cancer Res 11:4521–4532

    Article  CAS  PubMed  Google Scholar 

  • Ständer M, Naumann U, Dumitrescu L, Heneka M, Löschmann P, Gulbins E, Dichgans J, Weller M (1998) Decorin gene transfer-mediated suppression of TGF-β synthesis abrogates experimental malignant glioma growth in vivo. Gene Ther 5:1187–1194

    Article  PubMed  Google Scholar 

  • Ständer M, Naumann U, Wick W, Weller M (1999) Transforming growth factor-β and p-21: multiple molecular targets of decorin-mediated suppression of neoplastic growth. Cell Tissue Res 296:221–227

    Article  PubMed  Google Scholar 

  • Sulochana KN, Fan H, Jois S, Subramanian V, Sun F, Kini RM, Ge R (2005) Peptides derived from human decorin leucine-rich repeat 5 inhibit angiogenesis. J Biol Chem 280:27935–27948

    Article  CAS  PubMed  Google Scholar 

  • Svensson L, Aszódi A, Reinholt FP, Fässler R, HeinegÃ¥rd D, Oldberg Ã… (1999) Fibromodulin-null mice have abnormal collagen fibrils, tissue organization and altered lumican deposition in tendon. J Biol Chem 274:9636–9647

    Article  CAS  PubMed  Google Scholar 

  • Theocharis AD, Karamanos NK (2002) Decreased biglycan expression and differential decorin localization in human abdominal aortic aneurysms. Atherosclerosis 165:221–230

    Article  CAS  PubMed  Google Scholar 

  • Tomoeda M, Yamada S, Shirai H, Ozawa Y, Yanagita M, Murakami S (2008) PLAP-1/asporin inhibits activation of BMP receptor via its leucine-rich repeat motif. Biochem Biophys Res Commun 371:191–196

    Article  CAS  PubMed  Google Scholar 

  • Tralhão JG, Schaefer L, Micegova M, Evaristo C, Schönherr E, Kayal S, Veiga-Fernandes H, Danel C, Iozzo RV, Kresse H, Lemarchand P (2003) In vivo selective and distant killing of cancer cells using adenovirus-mediated decorin gene transfer. FASEB J 17:464–466

    PubMed  Google Scholar 

  • Trask BC, Trask TM, Broekelmann T, Mecham RP (2000) The microfibrillar proteins MAGP-1 and fibrillin-1form a ternary complex with the chondroitin sulfate proteoglycan decorin. Mol Biol Cell 11:1499–1507

    CAS  PubMed  Google Scholar 

  • Troup S, Njue C, Kliewer EV, Parisien M, Roskelley C, Chakravarti S, Roughley PJ, Murphy LC, Watson PH (2003) Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin Cancer Res 9:207–214

    CAS  PubMed  Google Scholar 

  • Tufvesson E, Westergren-Thorsson G (2002) Tumor necrosis factor-α interacts with biglycan and decorin. FEBS Lett 530:124–128

    Article  CAS  PubMed  Google Scholar 

  • van Cruijsen H, Giaccone G, Hoekman K (2006) Epidermal growth factor receptor and angiogenesis:opportunities for combined anticancer strategies. Int J Cancer 118:883–888

    Google Scholar 

  • Vesentini S, Redaelli A, Montevecchi FM (2005) Estimation of the binding force of the collagen molecule-decorin core protein complex in collagen fibril. J Biomech 38:433–443

    Article  PubMed  Google Scholar 

  • Vij N, Roberts L, Joyce S, Chakravarti S (2004) Lumican suppresses cell proliferation and aids Fas–Fas ligand mediated apoptosis: implications in the cornea. Exp Eye Res 78:957–971

    Article  CAS  PubMed  Google Scholar 

  • Vogel KG, Paulsson M, HeinegÃ¥rd D (1984) Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem J 223:587–597

    CAS  PubMed  Google Scholar 

  • Vuillermoz B, Khoruzhenko A, D’Onofrio MF, Ramont L, Venteo L, Perreau C, Antonicelli F, Maquart FX, Wegrowski Y (2004) The small leucine-rich proteoglycan lumican inhibits melanoma progression. Exp Cell Res 296:294–306

    Article  CAS  PubMed  Google Scholar 

  • Wadhwa S, Bi Y, Ortiz AT, Embree MC, Kilts T, Iozzo R, Opperman LA, Young MF (2007) Impaired posterior frontal sutural fusion in the biglycan/decorin double deficient mice. Bone 40:861–866

    Article  CAS  PubMed  Google Scholar 

  • Wallace JM, Rajachar RM, Chen X-D, Shi S, Allen MR, Bloomfield SA, Les CM, Robey PG, Young MF, Khon DH (2006) The mechanical phenotype of biglycan-deficient mice is bone- and gender-specific. Bone 39:106–116

    Article  CAS  PubMed  Google Scholar 

  • Wang I-J, Chiang T-H, Shih Y-F, Hsiao CK, Lu S-C, Hou Y-C, Lin LLK (2006) The association of single nucleotide polymorphisms in the 5′-regulatory region of the lumican gene with susceptibility to high myopia in Taiwan. Mol Vis 12:852–857

    CAS  PubMed  Google Scholar 

  • Wegrowski Y, Pillarisetti J, Danielson KG, Suzuki S, Iozzo RV (1995) The murine biglycan: complete cDNA cloning, genomic organization, promoter function and expression. Genomics 30:8–17

    Article  CAS  PubMed  Google Scholar 

  • Weis SM, Zimmerman SD, Shah M, Covell JW, Omens JH, Ross J Jr, Dalton N, Jones Y, Reed CC, Iozzo RV, McCulloch AD (2005) A role for decorin in the remodeling of myocardial infarction. Matrix Biol 24:313–324

    Article  CAS  PubMed  Google Scholar 

  • Westermann D, Mersmann J, Melchior A, Freudenberger T, Petrik C, Schaefer L, Lüllmann-Rauch R, Lettau O, Jacoby C, Schrader J, Brand-Herrmann S-M, Young MF, Schultheiss HP, Levkau B, Baba HA, Unger T, Zacharowski K, Tschöpe C, Fischer JW (2008) Biglycan is required for adaptive remodeling after myocardial infarction. Circulation 117:1269–1276

    Article  CAS  PubMed  Google Scholar 

  • Williams KJ, Qiu G, Usui HK, Dunn SR, McCue P, Bottinger E, Iozzo RV, Sharma K (2007) Decorin deficiency enhances progressive nephropathy in diabetic mice. Am J Pathol 171:1441–1450

    Article  CAS  PubMed  Google Scholar 

  • Wilson PG, Thompson JC, Webb NR, deBeer FC, King VL, Tannock LR (2008) Serum amyloid A, but not C-reactive protein, stimulates vascular proteoglycan synthesis in a pro-atherogenic manner. Am J Pathol 173:1902–1910

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Vij N, Roberts L, Lopez-Briones S, Joyce S, Chakravarti S (2007) A novel role of the lumican core protein in bacterial lipopolysaccharide-induced innate immune response. J Biol Chem 282:26409–26417

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Wang S, Xue A, Liu Y, Liu Y, Liu Y, Wang H, Chen Q, Guo M, Zhang Z (2008) Overexpression of decorin induces apoptosis and cell growth arrest in cultured rat mesangial cells in vitro. Nephrology 13:607–615

    Article  CAS  PubMed  Google Scholar 

  • Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, Bonadio J, Boskey A, Heegaard A-M, Sommer B, Satomura K, Dominguez P, Zhao C, Kulkarni AB, Robey PG, Young MF (1998) Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet 20:78–82

    Article  CAS  PubMed  Google Scholar 

  • Yamada S, Tomoeda M, Ozawa Y, Yoneda S, Terashima Y, Ikezawa K, Ikegawa S, Saito M, Toyosawa S, Murakami S (2007) PLAP-1/asporin, a novel negative regulator of periodontal ligament mineralization. J Biol Chem 282:23070–23080

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi Y, Mann DM, Ruoslahti E (1990) Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature 346:281–284

    Article  CAS  PubMed  Google Scholar 

  • Yan W, Wank P, Zhao CX, Tang J, Xiao X, Wang DW (2009) Decorin gene delivery inhibits cardiac fibrosis in spontaneously hypertensive rats by modulation of transforming growth factor-β/Smad and p38 mitogen-activated protein kinase signaling pathways. Hum Gene Ther 20:1190–1199

    Article  CAS  PubMed  Google Scholar 

  • Yang VWC, LaBrenz SR, Rosenberg LC, McQuillan D, Höök M (1999) Decorin is a Zn2+ metalloprotein. J Biol Chem 274:12454–12460

    Article  CAS  PubMed  Google Scholar 

  • Zafiropoulos A, Nikitovic D, Katonis P, Tsatsakis A, Karamanos NK, Tzanakakis GN (2008) Decorin-induced growth inhibition is overcome through protracted expression and activation of epidermal growth factor receptors in osteosarcoma cells. Mol Cancer Res 6:785–794

    Article  CAS  PubMed  Google Scholar 

  • Zeltz C, Brézillon S, Perreau C, Ramont L, Maquart F-X, Wegrowski Y (2009) Lumcorin: a leucine-rich repeat 9-derived peptide from human lumican inhibiting melanoma cell migration. FEBS Lett 583:3027–3032

    Article  CAS  PubMed  Google Scholar 

  • Zeng X, Chen J, Miller YI, Javaherian K, Moulton KS (2005) Endostatin binds biglycan and LDL and interferes with LDL retention to the subendothelial matrix during atherosclerosis. J Lipid Res 46:1849–1859

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y-W, Su Y, Volpert OV, Vande Woude GF (2003) Hepatocyte growth factor/scatter factor mediates angiogenesis through positive VEGF and negative thrombospondin 1 regulation. Proc Natl Acad Sci USA 100:12718–12723

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Ezura Y, Chervoneva I, Robinson PS, Beason DP, Carine ET, Soslowsky LJ, Iozzo RV, Birk DE (2006) Decorin regulates assembly of collagen fibrils and acquisition of biomechanical properties during tendon development. J Cell Biochem 98:1436–1449

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Chen S, Goldoni S, Calder BW, Simpson HC, Owens RT, McQuillan DJ, Young MF, Iozzo RV, Birk DE (2009) Genetic evidence for the coordinated regulation of collagen fibrillogenesis in the cornea by decorin and biglycan. J Biol Chem 284:8888–8897

    Article  CAS  PubMed  Google Scholar 

  • Zhu J-X, Goldoni S, Bix G, Owens RA, McQuillan D, Reed CC, Iozzo RV (2005) Decorin evokes protracted internalization and degradation of the EGF receptor via caveolar endocytosis. J Biol Chem 280:32468–32479

    Article  CAS  PubMed  Google Scholar 

  • Zoeller JJ, Pimtong W, Corby H, Goldoni S, Iozzo AE, Owens RT, Ho S-Y, Iozzo RV (2009) A central role for decorin during vertebrate convergent extension. J Biol Chem 284:11728–11737

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We like to thank all the past and present members of our laboratories for their invaluable contribution to this field of research. We are indebted to Angela McQuillan for her outstanding help with the illustrations. The original work in Iozzo’s laboratory was supported in part by NIH grants RO1 CA39481, RO1 CA47282, and RO1 CA120975, and in the Young’s laboratory by the Intramural Program of the NIDCR, NIH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Renato V. Iozzo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Berlin Heidelberg

About this chapter

Cite this chapter

Iozzo, R.V., Goldoni, S., Berendsen, A.D., Young, M.F. (2011). Small Leucine-Rich Proteoglycans. In: Mecham, R. (eds) The Extracellular Matrix: an Overview. Biology of Extracellular Matrix. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-16555-9_6

Download citation

Publish with us

Policies and ethics