d‐BRU - Dental Biomaterials Research Unit - ULiège [BE]
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Zappia, Jérémie ; Université de Liège - ULiège > Département des sciences de la motricité > Path. générale et physiopath./Tech. part. de kinésithérapie
Joiret, Marc ; Université de Liège - ULiège > In silico medecine-Biomechanics Research Unit
Sanchez, Christelle ; Université de Liège - ULiège > Département des sciences de la motricité > Unité de recherche sur l'os et le cartilage (U.R.O.C.)
Lambert, Cécile ; Université de Liège - ULiège > Département des sciences de la motricité > Unité de recherche sur l'os et le cartilage (U.R.O.C.)
Geris, Liesbet ; Université de Liège - ULiège > Département d'aérospatiale et mécanique > Génie biomécanique
Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > I3-Laboratory for Organogenesis and Regeneration
Henrotin, Yves ; Université de Liège - ULiège > Département des sciences de la motricité > Unité de recherche sur l'os et le cartilage (U.R.O.C.)
Language :
English
Title :
From translation to protein degradation as mechanisms for regulating biological functions: A review on the SLRP family in skeletal tissues.
Publication date :
2020
Journal title :
Biomolecules
eISSN :
2218-273X
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
Hynes, R.O.; Naba, A. Overview of the matrisome-An inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol. 2012, 4, 4903.
Bonnans, C.; Chou, J.; Werb, Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Boil. 2014, 15, 786–801.
Naba, A.; Clauser, K.R.; Ding, H.; Whittaker, C.A.; Carr, S.A.; Hynes, R.O. The extracellular matrix: Tools and insights for the “omics” era. Matrix Biol. 2016, 49, 10–24.
Kalamajski, S.; Oldberg, A. The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Boil. 2010, 29, 248–253.
Nikitovic, A.; Aggelidakis, J.; Young, M.F.; Iozzo, R.V.; Karamanos, N.K.; Tzanakakis, G.N. The Biology of Small Leucine-rich Proteoglycans in Bone Pathophysiology. J. Boil. Chem. 2012, 287, 33926–33933.
Chen, S.; Birk, D.E. The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J. 2013, 280, 2120–2137.
Chen, X.-D.; Fisher, L.W.; Robey, P.G.; Young, M.F. The small leucine-rich proteoglycan biglycan modulates BMP-4-induced osteoblast differentiation. FASEB J. 2004, 18, 948–958.
Bi, Y.; Stuelten, C.H.; Kilts, T.; Wadhwa, S.; Iozzo, R.V.; Robey, P.G.; Chen, X.-D.; Young, M.F. Extracellular Matrix Proteoglycans Control the Fate of Bone Marrow Stromal Cells. J. Boil. Chem. 2005, 280, 30481–30489.
Schaefer, L.; Iozzo, R. V Biological Functions of the Small Leucine-rich Proteoglycans: From Genetics to Signal Transduction. J. Biol. Chem. 2008, 283, 21305–21309.
Kram, V.; Kilts, T.M.; Bhattacharyya, N.; Li, L.; Young, M.F. Small leucine rich proteoglycans, a novel link to osteoclastogenesis. Sci. Rep. 2017, 7, 12627.
Marín, M. Folding at the rhythm of the rare codon beat. Biotechnol. J. 2008, 3, 1047–1057.
Plotkin, J.B.; Kudla, G. Synonymous but not the same: The causes and consequences of codon bias. Nat. Rev. Genet. 2011, 12, 32–42.
Sherman, M.Y.; Qian, S.-B. Less is more: Improving proteostasis by translation slow down. Trends Biochem. Sci. 2013, 38, 585–591.
Chan, C.; Pham, P.; Dedon, P.C.; Begley, T.J. Lifestyle modifications: Coordinating the tRNA epitranscriptome with codon bias to adapt translation during stress responses. Genome Boil. 2018, 19, 228.
Duan, G.; Walther, D. The Roles of Post-translational Modifications in the Context of Protein Interaction Networks. PLoS Comput. Boil. 2015, 11, e1004049.
Schaefer, L.; Schaefer, R.M. Proteoglycans: From structural compounds to signaling molecules. Cell Tissue Res. 2010, 339, 237–246.
Iozzo, R.V.; Goldoni, S.; Berendsen, A.D.; Young, M.F. Small Leucine-Rich Proteoglycans. In The Extracellular Matrix: An Overview; Springer: Berlin/Heidelberg, Germany, 2011; pp. 197–231.
McEwan, P.A.; Scott, P.G.; Bishop, P.N.; Bella, J. Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans. J. Struct. Boil. 2006, 155, 294–305.
Kobe, B. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Boil. 2001, 11, 725–732.
Chen, S.; Sun, M.; Iozzo, R.V.; Kao, W.W.-Y.; Birk, D.E. Intracellularly-retained decorin lacking the C- terminal ear repeat causes ER stress: A cell-based etiological mechanism for congenital stromal corneal dystrophy. Am. J. Pathol. 2013, 183, 247–256.
Prydz, K.; Dalen, K.T. Synthesis and sorting of proteoglycans. J. Cell Sci. 2000, 113, 193–205.
Funderburgh, J.L. Keratan Sulfate Biosynthesis. IUBMB Life 2002, 54, 187–194.
Fuller, M.; Meikle, P.J.; Hopwood, J.J. Glycosaminoglycan degradation fragments in mucopolysaccharidosis I. Glycobiology 2004, 14, 443–450.
Ernst, S.; Langer, R.; Cooney, C.L.; Sasisekharan, R. Enzymatic Degradation of GlycosaminogIycans. Crit. Rev. Biochem. Mol. Boil. 1995, 30, 387–444.
Krishnan, P.; Hocking, A.M.; Scholtz, J.M.; Pace, C.N.; Holik, K.K.; McQuillan, D.J. Distinct secondary structures of the leucine-rich repeat proteoglycans decorin and biglycan. Glycosylation-dependent conformational stability. J. Boil. Chem. 1999, 274, 10945–10950.
Seo, N.-S.; Hocking, A.M.; Höök, M.; McQuillan, D.J. Decorin Core Protein Secretion Is Regulated byN- Linked Oligosaccharide and Glycosaminoglycan Additions. J. Boil. Chem. 2005, 280, 42774–42784.
Bateman, A. UniProt: A worldwide hub of protein knowledge. Nucleic Acids Res. 2019, 28, 32.
Fisher, L.W.; Termine, J.D.; Young, M.F. Deduced protein sequence of bone small proteoglycan I (biglycan) shows homology with proteoglycan II (decorin) and several nonconnective tissue proteins in a variety of species. J. Boil. Chem. 1989, 264, 4571–4576.
Johnson, H.J.; Rosenberg, L.; Choi, H.U.; Garza, S.; Höök, M.; Neame, P.J. Characterization of epiphycan, a small proteoglycan with a leucine-rich repeat core protein. J. Boil. Chem. 1997, 272, 18709–18717.
Iozzo, R.V.; Schaefer, L. Proteoglycan form and function: A comprehensive nomenclature of proteoglycans. Matrix Boil. 2015, 42, 11–55.
Roughley, P.J.; White, R.J. Dermatan sulphate proteoglycans of human articular cartilage. The properties of dermatan sulphate proteoglycans I and II. Biochem. J. 1989, 262, 823–827.
Krusius, T.; Ruoslahti, E. Primary structure of an extracellular matrix proteoglycan core protein deduced from cloned cDNA. Proc. Natl. Acad. Sci. USA 1986, 83, 7683–7687.
Klein, J.A.; Meng, L.; Zaia, J. Deep sequencing of complex proteoglycans: A novel strategy for high coverage and sitespecific identification of glycosaminoglycanlinked peptides. Mol. Cell. Proteom. 2018, 17, 1578–1590.
Lorenzo, P.; Aspberg, A.; Önnerfjord, P.; Bayliss, M.T.; Neame, P.J.; Heinegård, D. Identification and Characterization of Asporin. J. Boil. Chem. 2001, 276, 12201–12211.
Blochberger, T.C.; Vergnes, J.P.; Hempel, J.; Hassell, J.R. cDNA to chick lumican (corneal keratan sulfate proteoglycan) reveals homology to the small interstitial proteoglycan gene family and expression in muscle and intestine. J. Boil. Chem. 1992, 267, 347–352.
Cornuet, P.K.; Blochberger, T.C.; Hassell, J.R. Molecular polymorphism of lumican during corneal development. Investig. Ophthalmol. Vis. Sci. 1994, 35, 870–877.
Önnerfjord, P.; Heathfield, T.F.; Heinegård, D. Identification of Tyrosine Sulfation in Extracellular Leucine-rich Repeat Proteins Using Mass Spectrometry. J. Biol. Chem. 2004, 279, 26–33.
Corpuz, L.M.; Funderburgh, J.L.; Funderburgh, M.L.; Bottomley, G.S.; Prakash, S.; Conrad, G.W. Molecular cloning and tissue distribution of keratocan. Bovine corneal keratan sulfate proteoglycan 37A. J. Boil. Chem. 1996, 271, 9759–9763.
Oldberg, A.; Antonsson, P.; Lindblom, K.; Heinegård, D. A collagen-binding 59-kd protein (fibromodulin) is structurally related to the small interstitial proteoglycans PG-S1 and PG-S2 (decorin). EMBO J. 1989, 8, 2601–2604.
Antonsson, P.; Heinegird, D.; Oldberg, A. Posttranslational Modifications of Fibromodulin. J. Biol. Chem. 1991, 267, 6132–6136.
Plaas, A.H.; Wong-Palms, S. Biosynthetic mechanisms for the addition of polylactosamine to chondrocyte fibromodulin. J. Boil. Chem. 1993, 268, 26634–26644.
Wendel, M.; Sommarin, Y.; Heinegård, D. Characterization of osteoadherin—a novel, cell binding keratan sulfate proteoglycan from bone. Acta Orthop. Scand. 1995, 66, 77.
Wendel, M.; Sommarin, Y.; Heinegård, D. Bone Matrix Proteins: Isolation and Characterization of a Novel Cell-binding Keratan Sulfate Proteoglycan (Osteoadherin) from Bovine Bone. J. Cell Boil. 1998, 141, 839– 847.
Sommarin, Y. Osteoadherin, a Cell-binding Keratan Sulfate Proteoglycan in Bone, Belongs to the Family of Leucine-rich Repeat Proteins of the Extracellular Matrix. J. Boil. Chem. 1998, 273, 16723–16729.
Bengtsson, E.; Neame, P.J.; Heinegård, D.; Sommarin, Y. The Primary Structure of a Basic Leucine-rich Repeat Protein, PRELP, Found in Connective Tissues. J. Biol. Chem. 1995, 270, 25639–25644.
Bengtsson, E.; Aspberg, A.; Heinegãrd, D.; Sommarin, Y.; Spillmann, D. The Amino-terminal Part of PRELP Binds to Heparin and Heparan Sulfate. J. Boil. Chem. 2000, 275, 40695–40702.
Bentz, H.; Nathan, R.M.; Rosen, D.M.; Armstrong, R.M.; Thompson, A.Y.; Segarini, P.R.; Mathews, M.C.; Dasch, J.R.; Piez, K.A.; Seyedin, S.M. Purification and characterization of a unique osteoinductive factor from bovine bone. J. Boil. Chem. 1989, 264, 20805–20810.
Funderburgh, J.L.; Corpuz, L.M.; Roth, M.R.; Funderburgh, M.L.; Tasheva, E.S.; Conrad, G.W. Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J. Boil. Chem. 1997, 272, 28089–28095.
Kampmann, A.; Fernández, B.; Deindl, E.; Kubin, T.; Pipp, F.; Eitenmüller, I.; Hoefer, I.E.; Schaper, W.; Zimmermann, R. The proteoglycan osteoglycin/mimecan is correlated with arteriogenesis. Mol. Cell. Biochem. 2009, 322, 15–23.
Rienks, M.; Papageorgiou, A.; Wouters, K.; Verhesen, W.; Leeuwen, R. van; Carai, P.; Summer, G.; Westermann, D.; Heymans, S. A novel 72-kDa leukocyte-derived osteoglycin enhances the activation of toll-like receptor 4 and exacerbates cardiac inflammation during viral myocarditis. Cell. Mol. Life Sci. 2017, 74, 1511–1525.
Madisen, L.; Neubauer, M.; Plowman, G.; Rosen, D.; Segarini, P.; Dasch, J.; Thompson, A.; Ziman, J.; Bentz, H.; Purchio, A. Molecular Cloning of a Novel Bone-Forming Compound: Osteoinductive Factor. DNA Cell Boil. 1990, 9, 303–309.
Reardon, A.J.; Le Goff, M.; Briggs, M.D.; McLeod, D.; Sheehan, J.K.; Thornton, D.J.; Bishop, P.N. Identification in vitreous and molecular cloning of opticin, a novel member of the family of leucine-rich repeat proteins of the extracellular matrix. J. Boil. Chem. 2000, 275, 2123–2129.
Hobby, P.; Wyatt, M.K.; Gan, W.; Bernstein, S.; Tomarev, S.; Slingsby, C.; Wistow, G. Cloning, modeling, and chromosomal localization for a small leucine-rich repeat proteoglycan (SLRP) family member expressed in human eye. Mol. Vis. 2000, 6, 72–78.
Neame, P.J.; Sommarin, Y.; Boynton, R.E.; Heinegård, D. The structure of a 38-kDa leucine-rich protein (chondroadherin) isolated from bovine cartilage. J. Boil. Chem. 1994, 269, 21547–21554.
ShimizuHirota, R.; Sasamura, H.; Kuroda, M.; Kobayashi, E.; Saruta, T. Functional characterization of podocan, a member of a new class in the small leucine-rich repeat protein family. FEBS Lett. 2004, 563, 69–74.
Ross, M.D.; Bruggeman, L.A.; Hanss, B.; Marras, D.; Klotman, M.E.; Sunamoto, M.; Klotman, P.E. Podocan, a Novel Small Leucine-rich Repeat Protein Expressed in the Sclerotic Glomerular Lesion of Experimental HIV-associated Nephropathy. J. Boil. Chem. 2003, 278, 33248–33255.
Mochida, Y.; Kaku, M.; Yoshida, K.; Katafuchi, M.; Atsawasuwan, P.; Yamauchi, M. Podocan-like protein: A novel small leucine-rich repeat matrix protein in bone. Biochem. Biophys. Res. Commun. 2011, 410, 333– 338.
Endres, L.; Dedon, P.C.; Begley, T.J. Codon-biased translation can be regulated by wobble-base tRNA modification systems during cellular stress responses. RNA Biol. 2015, 12, 603–614.
Rapino, F.; Delaunay, S.; Zhou, Z.; Chariot, A.; Close, P. tRNA Modification: Is Cancer Having a Wobble? Trends Cancer 2017, 3, 249–252.
Hou, Y.-M.; Gamper, H.; Yang, W. Post-transcriptional modifications to tRNA--a response to the genetic code degeneracy. RNA 2015, 21, 642–644.
Rapino, F.; Delaunay, S.; Rambow, F.; Zhou, Z.; Tharun, L.; De Tullio, P.; Sin, O.; Shostak, K.; Schmitz, S.; Piepers, J.; et al. Codon-specific translation reprogramming promotes resistance to targeted therapy. Nat. 2018, 558, 605–609.
James, G.; Witten, D.; Hastie, T.; Tibshirani, R. An Introduction to Statistical Learning; Springer: New York, NY, USA, 2013; Volume 112, p. 18.
Raspanti, M.; Viola, M.; Forlino, A.; Tenni, R.; Gruppi, C.; Tira, M.E. Glycosaminoglycans show a specific periodic interaction with type I collagen fibrils. J. Struct. Boil. 2008, 164, 134–139.
Tatara, Y.; Kakizaki, I.; Suto, S.; Ishioka, H.; Negishi, M.; Endo, M. Chondroitin sulfate cluster of epiphycan from salmon nasal cartilage defines binding specificity to collagens. Glycobiology 2015, 25, 557–569.
Lewis, P.N.; Pinali, C.; Young, R.D.; Meek, K.M.; Quantock, A.J.; Knupp, C. Structural Interactions between Collagen and Proteoglycans Are Elucidated by Three-Dimensional Electron Tomography of Bovine Cornea. Structure 2010, 18, 239–245.
Parfitt, G.J.; Pinali, C.; Young, R.D.; Quantock, A.J.; Knupp, C. Three-dimensional reconstruction of collagen–proteoglycan interactions in the mouse corneal stroma by electron tomography. J. Struct. Boil. 2010, 170, 392–397.
Stamov, D.R.; Müller, A.; Wegrowski, Y.; Brezillon, S.; Franz, C.M.; Müller, A. Quantitative analysis of type I collagen fibril regulation by lumican and decorin using AFM. J. Struct. Boil. 2013, 183, 394–403.
Scott, J.E. Extracellular matrix, supramolecular organisation and shape. J. Anat. 1995, 187, 259–269.
Scott, J.E.; Thomlinson, A.M. The structure of interfibrillar proteoglycan bridges (‘shape modules’) in extracellular matrix of fibrous connective tissues and their stability in various chemical environments. J. Anat. 1998, 192, 391–405.
Lujan, T.J.; Underwood, C.J.; Henninger, H.B.; Thompson, B.M.; Weiss, J.A. Effect of dermatan sulfate glycosaminoglycans on the quasi-static material properties of the human medial collateral ligament. J. Orthop. Res. 2007, 25, 894–903.
Seidler, D.G.; Faiyaz-Ul-Haque, M.; Hansen, U.; Yip, G.W.; Zaidi, S.H.E.; Teebi, A.S.; Kiesel, L.; Götte, M. Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers–Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I (β4GalT-7). J. Mol. Med. 2006, 84, 583–594.
Rühland, C.; Schönherr, E.; Robenek, H.; Hansen, U.; Iozzo, R.V.; Bruckner, P.; Seidler, D.G. The glycosaminoglycan chain of decorin plays an important role in collagen fibril formation at the early stages of fibrillogenesis. FEBS J. 2007, 274, 4246–4255.
Malfait, F.; Kariminejad, A.; Van Damme, T.; Gauche, C.; Syx, D.; Merhi-Soussi, F.; Gulberti, S.; Symoens, S.; Vanhauwaert, S.; Willaert, A.; et al. Defective initiation of glycosaminoglycan synthesis due to B3GALT6 mutations causes a pleiotropic Ehlers-Danlos-syndrome-like connective tissue disorder. Am. J. Hum. Genet. 2013, 92, 935–945, doi:10.1016/j.ajhg.2013.04.016.
Moffatt, P.; Geng, Y.; Lamplugh, L.; Nanci, A.; Roughley, P.J. Absence of the dermatan sulfate chain of decorin does not affect mouse development. J. Negat. Results Biomed. 2017, 16, 7.
Reese, S.P.; Underwood, C.J.; Weiss, J.A. Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Boil. 2013, 32, 414–423.
Scott, J.E. Elasticity in extracellular matrix ‘shape modules’ of tendon, cartilage, etc. A sliding proteoglycan-filament model. J. Physiol. 2003, 553, 335–343.
Redaelli, A.; Vesentini, S.; Soncini, M.; Vena, P.; Mantero, S.; Montevecchi, F. Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons—A computational study from molecular to microstructural level. J. Biomech. 2003, 36, 1555–1569.
Vesentini, S.; Redaelli, A.; Montevecchi, F.M. Estimation of the binding force of the collagen molecule-decorin core protein complex in collagen fibril. J. Biomech. 2005, 38, 433–443.
Liao, J.; Vesely, I. Skewness angle of interfibrillar proteoglycans increases with applied load on mitral valve chordae tendineae. J. Biomech. 2007, 40, 390–398.
Lujan, T.J.; Underwood, C.J.; Jacobs, N.T.; Weiss, J.A. Contribution of glycosaminoglycans to viscoelastic tensile behavior of human ligament. J. Appl. Physiol. 2009, 106, 423–431.
Fessel, G.; Snedeker, J.G. Equivalent stiffness after glycosaminoglycan depletion in tendon—An ultrastructural finite element model and corresponding experiments. J. Theor. Boil. 2011, 268, 77–83.
Svensson, R.B.; Hassenkam, T.; Hansen, P.; Kjaer, M.; Magnusson, S.P. Tensile Force Transmission in Human Patellar Tendon Fascicles Is Not Mediated by Glycosaminoglycans. Connect. Tissue Res. 2011, 52, 415–421.
Choi, R.K.; Smith, M.M.; Martin, J.H.; Clarke, J.L.; Dart, A.J.; Little, C.B.; Clarke, E.C. Chondroitin sulphate glycosaminoglycans contribute to widespread inferior biomechanics in tendon after focal injury. J. Biomech. 2016, 49, 2694–2701.
Rigozzi, S.; Müller, R.; Stemmer, A.; Snedeker, J. Tendon glycosaminoglycan proteoglycan sidechains promote collagen fibril sliding—AFM observations at the nanoscale. J. Biomech. 2013, 46, 813–818.
Tatara, Y.; Suto, S.; Itoh, K. Novel roles of glycosaminoglycans in the degradation of type I collagen by cathepsin K. Glycobiology 2017, 27, 1089–1098.
Johnstone, B.; Markopoulos, M.; Neame, P.; Caterson, B. Identification and characterization of glycanated and non-glycanated forms of biglycan and decorin in the human intervertebral disc. Biochem. J. 1993, 292, 661–666.
Roughley, P.J.; White, R.J.; Magny, M.C.; Liu, J.; Pearce, R.H.; Mort, J.S. Non-proteoglycan forms of biglycan increase with age in human articular cartilage. Biochem. J. 1993, 295, 421–426.
Waddington, R.; Hall, R.; Embery, G.; Lloyd, D. Changing profiles of proteoglycans in the transition of predentine to dentine. Matrix Boil. 2003, 22, 153–161.
Chan, W.L.; Steiner, M.; Witkos, T.; Egerer, J.; Busse, B.; Mizumoto, S.; Pestka, J.M.; Zhang, H.; Hausser, I.; Khayal, L.A.; et al. Impaired proteoglycan glycosylation, elevated TGF-β signaling, and abnormal osteoblast differentiation as the basis for bone fragility in a mouse model for gerodermia osteodysplastica. PLoS Genet. 2018, 14, e1007242.
Derwin, K.A.; Soslowsky, L.J.; Kimura, J.H.; Plaas, A.H. Proteoglycans and glycosaminoglycan fine structure in the mouse tail tendon fascicle. J. Orthop. Res. 2001, 19, 269–277.
Roughley, P.J.; White, R.J.; Cs-Szabó, G.; Mort, J.S. Changes with age in the structure of fibromodulin in human articular cartilage. Osteoarthr. Cartil. 1996, 4, 153–161.
Santer, V.; White, R.J.; Roughley, P.J. O-linked oligosaccharides of human articular cartilage proteoglycan. BBA Gen. Subj. 1982, 716, 277–282.
Grover, J.; Chen, X.N.; Korenberg, J.R.; Roughley, P.J. The human lumican gene. Organization, chromosomal location, and expression in articular cartilage. J. Boil. Chem. 1995, 270, 21942–21949.
Melching, L.I.; Roughley, P.J. Modulation of keratan sulfate synthesis on lumican by the action of cytokines on human articular chondrocytes. Matrix Boil. 1999, 18, 381–390.
Sugars, R.V.; Olsson, M.L.; Marchner, S.; Hultenby, K.; Wendel, M. The glycosylation profile of osteoadherin alters during endochondral bone formation. Bone 2013, 53, 459–467.
Waddington, R.J.; Roberts, H.C.; Sugars, R.V.; Schönherr, E. Differential roles for small leucine-rich proteoglycans in bone formation. Eur Cell Mater 2003, 6, 12–21.
Goldberg, M.; Rapoport, O.; Septier, D.; Palmier, K.; Hall, R.; Embery, G.; Young, M.; Ameye, L. Proteoglycans in predentin: The last 15 micrometers before mineralization. Connect. Tissue Res. 2003, 44, 184–188.
Ho, S.P.; Sulyanto, R.M.; Marshall, S.J.; Marshall, G.W. The cementum–dentin junction also contains glycosaminoglycans and collagen fibrils. J. Struct. Boil. 2005, 151, 69–78.
Bertassoni, L.E.; Stankoska, K.; Swain, M.V. Insights into the structure and composition of the peritubular dentin organic matrix and the lamina limitans. Micron 2012, 43, 229–236.
Bertassoni, L.E.; Kury, M.; Rathsam, C.; Little, C.B.; Swain, M.V. The role of proteoglycans in the nanoindentation creep behavior of human dentin. J. Mech. Behav. Biomed. Mater. 2015, 55, 264–270.
Dorvee, J.R.; Gerkowicz, L.; Bahmanyar, S.; Deymier-Black, A.; Veis, A. Chondroitin sulfate is involved in the hypercalcification of the organic matrix of bovine peritubular dentin. Arch. Oral Biol. 2016, 62, 93–100.
Farina, A.P.; Vidal, C.M.P.; Cecchin, D.; Aguiar, T.R.; Bedran-Russo, A.K. Structural and biomechanical changes to dentin extracellular matrix following chemical removal of proteoglycans. Odontology 2019, 107, 316–323.
Gutierrez, J.; Osses, N.; Brandan, E. 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. 2006, 206, 58–67.
Halper, J.; Kim, B.; Khan, A.; Yoon, J.H.; Mueller, P.O.E. Degenerative suspensory ligament desmitis as a systemic disorder characterized by proteoglycan accumulation. BMC Vet. Res. 2006, 2, 12.
Kim, B.; Yoon, J.H.; Zhang, J.; Mueller, P.E.; Halper, J. Glycan profiling of a defect in decorin glycosylation in equine systemic proteoglycan accumulation, a potential model of progeroid form of Ehlers-Danlos syndrome. Arch. Biochem. Biophys. 2010, 501, 221–231.
Young, M.; Moshood, O.; Zhang, J.; Sarbacher, C.A.; Mueller, P.O.E.; Halper, J. Does BMP2 play a role in the pathogenesis of equine degenerative suspensory ligament desmitis? BMC Res. Notes 2018, 11, 672.
Ye, Y.; Hu, W.; Guo, F.; Zhang, W.; Wang, J.; Chen, A. Glycosaminoglycan chains of biglycan promote bone morphogenetic protein-4-induced osteoblast differentiation. Int. J. Mol. Med. 2012, 30, 1075–1080.
Wang, X.; Harimoto, K.; Xie, S.; Cheng, H.; Liu, J.; Wang, Z. Matrix protein biglycan induces osteoblast differentiation through extracellular signal-regulated kinase and Smad pathways. Boil. Pharm. Bull. 2010, 33, 1891–1897.
Miguez, P.; Terajima, M.; Nagaoka, H.; Mochida, Y.; Yamauchi, M. Role of Glycosaminoglycans of Biglycan in BMP-2 Signaling. Biochem. Biophys. Res. Commun. 2011, 405, 262–266.
Miguez, P.; Terajima, M.; Nagaoka, H.; Ferreira, J.; Braswell, K.; Ko, C.; Yamauchi, M. Recombinant Biglycan Promotes Bone Morphogenetic Protein-induced Osteogenesis. J. Dent. Res. 2014, 93, 406–411.
Kanan, Y., Siefert, J.C., Kinter, M. and Al-Ubaidi, M.R. Complement factor H, vitronectin, and opticin are tyrosine-sulfated proteins of the retinal pigment epithelium. PLoS ONE 2014, 9, e105409.
Heathfield, T.F.; Önnerfjord, P.; Dahlberg, L.; Heinegård, D. Cleavage of Fibromodulin in Cartilage Explants Involves Removal of the N-terminal Tyrosine Sulfate-rich Region by Proteolysis at a Site That Is Sensitive to Matrix Metalloproteinase-13. J. Biol. Chem. 2004, 279, 6286–6295.
Tillgren, V.; Önnerfjord, P.; Haglund, L.; Heinegård, D. The Tyrosine Sulfate-rich Domains of the LRR Proteins Fibromodulin and Osteoadherin Bind Motifs of Basic Clusters in a Variety of Heparin-binding Proteins, Including Bioactive Factors. J. Boil. Chem. 2009, 284, 28543–28553.
Tillgren, V.; Mörgelin, M.; Önnerfjord, P.; Kalamajski, S.; Aspberg, A. The Tyrosine Sulfate Domain of Fibromodulin Binds Collagen and Enhances Fibril Formation. J. Boil. Chem. 2016, 291, 23744–23755.
Imai, K.; Hiramatsu, A.; Fukushima, D.; Pierschbacher, M.D.; Okada, Y. Degradation of decorin by matrix metalloproteinases: Identification of the cleavage sites, kinetic analyses and transforming growth factor-β1 release. Biochem. J. 1997, 322, 809–814.
Li, Y.; Aoki, T.; Mori, Y.; Ahmad, M.; Miyamori, H.; Takino, T.; Sato, H. Cleavage of Lumican by Membrane- Type Matrix Metalloproteinase-1 Abrogates This Proteoglycan-Mediated Suppression of Tumor Cell Colony Formation in Soft Agar. Cancer Res. 2004, 64, 7058–7064.
Geng, Y.; McQuillan, D.; Roughley, P.J. SLRP interaction can protect collagen fibrils from cleavage by collagenases. Matrix Boil. 2006, 25, 484–491.
Monfort, J.; Tardif, G.; Reboul, P.; Mineau, F.; Roughley, P.; Pelletier, J.-P.; Martel-Pelletier, J. Degradation of small leucine-rich repeat proteoglycans by matrix metalloprotease-13: Identification of a new biglycan cleavage site. Arthritis Res. Ther. 2006, 8, 26.
Monfort, J.; Tardif, G.; Roughley, P.; Reboul, P.; Boileau, C.; Bishop, P.; Pelletier, J.-P.; Martel-Pelletier, J. Identification of opticin, a member of the small leucine-rich repeat proteoglycan family, in human articular tissues: A novel target for MMP-13 in osteoarthritis. Osteoarthr. Cartil. 2008, 16, 749–755.
Zhang, L.; Yang, M.; Yang, N.; Cavey, G.; Davidson, P.; Gibson, G. Molecular Interactions of MMP-13 C- Terminal Domain with Chondrocyte Proteins. Connect. Tissue Res. 2010, 51, 230–239.
Tío, L.; Martel-Pelletier, J.; Pelletier, J.-P.; Bishop, P.N.; Roughley, P.; Farran, A.; Benito, P.; Monfort, J. Characterization of opticin digestion by proteases involved in osteoarthritis development. Jt. Bone Spine 2014, 81, 137–141.
Genovese, F.; Barascuk, N.; Larsen, L.; Larsen, M.R.; Nawrocki, A.; Li, Y.; Zheng, Q.; Wang, J.; Veidal, S.S.; Leeming, D.J.; et al. Biglycan fragmentation in pathologies associated with extracellular matrix remodeling by matrix metalloproteinases. Fibrogenesis Tissue Repair 2013, 6, 9.
Melching, L.; Fisher, W.; Lee, E.; Mort, J.; Roughley, P. The cleavage of biglycan by aggrecanases. Osteoarthr. Cartil. 2006, 14, 1147–1154.
Boivin, W.A.; Shackleford, M.; Vanden Hoek, A.; Zhao, H.; Hackett, T.L.; Knight, D.A.; Granville, D.J. Granzyme B Cleaves Decorin, Biglycan and Soluble Betaglycan, Releasing Active Transforming Growth Factor-β1. PLoS ONE 2012, 7, 33163.
Fuller, E.; Little, C.B.; Melrose, J. Interleukin-1α induces focal degradation of biglycan and tissue degeneration in an in-vitro ovine meniscal model. Exp. Mol. Pathol. 2016, 101, 214–220.
Akhatib, B.; Onnerfjord, P.; Gawri, R.; Ouellet, J.; Jarzem, P.; Heinegård, D.; Mort, J.; Roughley, P.; Haglund, L. Chondroadherin Fragmentation Mediated by the Protease HTRA1 Distinguishes Human Intervertebral Disc Degeneration from Normal Aging. J. Boil. Chem. 2013, 288, 19280–19287.
Samiric, T.; Ilic, M.Z.; Handley, C.J. Characterisation of proteoglycans and their catabolic products in tendon and explant cultures of tendon. Matrix Biol. 2004, 23, 127–140.
Rees, S.G.; Flannery, C.R.; Little, C.B.; Hughes, C.E.; Caterson, B.; Dent, C.M. Catabolism of aggrecan, decorin and biglycan in tendon. Biochem. J. 2000, 350, 181–188.
Melrose, J.; Smith, S.M.; Fuller, E.S.; Young, A.A.; Roughley, P.J.; Dart, A.; Little, C.B. Biglycan and fibromodulin fragmentation correlates with temporal and spatial annular remodelling in experimentally injured ovine intervertebral discs. Eur. Spine J. 2007, 16, 2193–2205.
Zhen, E.Y.; Brittain, I.J.; Laska, D.A.; Mitchell, P.G.; Sumer, E.U.; Karsdal, M.A.; Duffin, K.L. Characterization of metalloprotease cleavage products of human articular cartilage. Arthritis Rheum. 2008, 58, 2420–2431.
Melrose, J.; Fuller, E.S.; Roughley, P.J.; Smith, M.M.; Kerr, B.; Hughes, C.E.; Caterson, B.; Little, C.B. Fragmentation of decorin, biglycan, lumican and keratocan is elevated in degenerate human meniscus, knee and hip articular cartilages compared with age-matched macroscopically normal and control tissues. Arthritis Res. Ther. 2008, 10, 79.
Shu, C.C.; Flannery, C.R.; Little, C.B.; Melrose, J. Catabolism of Fibromodulin in Developmental Rudiment and Pathologic Articular Cartilage Demonstrates Novel Roles for MMP-13 and ADAMTS-4 in C-terminal Processing of SLRPs. Int. J. Mol. Sci. 2019, 20, 579.
Cs-Szabo, G.; Roughley, P.J.; Plaas, A.H.K.; Glant, T.T. Large and small proteoglycans of osteoarthritic and rheumatoid articular cartilage. Arthritis Rheum. 1995, 38, 660–668.
Young, A.A.; Smith, M.M.; Smith, S.M.; Cake, M.A.; Ghosh, P.; Read, R.A.; Melrose, J.; Sonnabend, D.H.; Roughley, P.J.; Little, C.B. Regional assessment of articular cartilage gene expression and small proteoglycan metabolism in an animal model of osteoarthritis. Arthritis Res. Ther. 2005, 7, 852–861.
Haglund, L.; Ouellet, J.; Roughley, P. Variation in Chondroadherin Abundance and Fragmentation in the Human Scoliotic Disc. Spine 2009, 34, 1513–1518.
Brown, S., Melrose, J., Caterson, B., Roughley, P., Eisenstein, S.M. and Roberts, S. A comparative evaluation of the small leucine-rich proteoglycans of pathological human intervertebral discs. Spine J. 2012, 21, 154– 159.
Erwin, W.M.; DeSouza, L.; Funabashi, M.; Kawchuk, G.; Karim, M.Z.; Kim, S.; Mӓdler S.; Matta, A.; Wang, X.; Mehrkens, K.A. The biological basis of degenerative disc disease: Proteomic and biomechanical analysis of the canine intervertebral disc. Arthritis Res. 2015, 17, 240.
Bock, H.; Michaeli, P.; Bode, C.; Schultz, W.; Kresse, H.; Herken, R.; Miosge, N. The small proteoglycans decorin and biglycan in human articular cartilage of late-stage osteoarthritis. Osteoarthr. Cartil. 2001, 9, 654– 663.
Goldring, M.B., Otero, M., Plumb, D.A., Dragomir, C., Favero, M., El Hachem, K., Hashimoto, K., Roach, H.I., Olivotto, E., Borzì, R.M; et al. Roles of inflammatory and anabolic cytokines in cartilage metabolism: Signals and multiple effectors converge upon MMP-13 regulation in osteoarthritis. Cells Mater. 2011, 21, 202.
Fuller, E.; Smith, M.; Little, C.; Melrose, J. Zonal differences in meniscus matrix turnover and cytokine response. Osteoarthr. Cartil. 2012, 20, 49–59.
Billinghurst, R.C.; Dahlberg, L.; Ionescu, M.; Reiner, A.; Bourne, R.; Rorabeck, C.; Mitchell, P.; Hambor, J.; Diekmann, O.; Tschesche, H.; et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J. Clin. Investig. 1997, 99, 1534–1545.
Frey, H.; Schroeder, N.; Manon-Jensen, T.; Iozzo, R.V.; Schaefer, L. Biological interplay between proteoglycans and their innate immune receptors in inflammation. FEBS J. 2013, 280, 2165–2179.
Barreto, G.; Soininen, A.; Ylinen, P.; Sandelin, J.; Konttinen, Y.T.; Nordström, D.C.; Eklund, K.K. Soluble biglycan: A potential mediator of cartilage degradation in osteoarthritis. Arthritis Res. 2015, 17, 379.
Avenoso, A.; D’Ascola, A.; Scuruchi, M.; Mandraffino, G.; Calatroni, A.; Saitta, A.; Campo, S.; Campo, G.M. The proteoglycan biglycan mediates inflammatory response by activating TLR-4 in human chondrocytes: Inhibition by specific siRNA and high polymerized Hyaluronan. Arch. Biochem. Biophys. 2018, 640, 75–82.
Le Goff, M.M.; Sutton, M.J.; Slevin, M.; Latif, A.; Humphries, M.J.; Bishop, P.N. Opticin exerts its anti-angiogenic activity by regulating extracellular matrix adhesiveness. J. Boil. Chem. 2012, 287, 28027–28036.
Merline, R.; Schaefer, R.M.; Schaefer, L. The matricellular functions of small leucine-rich proteoglycans (SLRPs). J. Cell Commun. Signal. 2009, 3, 323–335.
Hildebrand, A.; Romaris, M.; Rasmussen, L.M.; Heinegård, D.; Twardzik, D.R.; Border, W.A.; Ruoslahti, E. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor β. Biochem. J. 1994, 302, 527–534.
Kizawa, H.; Kou, I.; Iida, A.; Sudo, A.; Miyamoto, Y.; Fukuda, A.; Mabuchi, A.; Kotani, A.; Kawakami, A.; Yamamoto, S.; et al. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat. Genet. 2005, 37, 138–144.
Embree, M.C.; Kilts, T.M.; Ono, M.; Inkson, C.A.; Syed-Picard, F.; Karsdal, M.A.; Oldberg, A.; Bi, Y.; Young, M.F. Biglycan and Fibromodulin Have Essential Roles in Regulating Chondrogenesis and Extracellular Matrix Turnover in Temporomandibular Joint Osteoarthritis. Am. J. Pathol. 2010, 176, 812–826.
Campbell, M.A.; Handley, C.J.; Hascall, V.C.; Campbell, R.A.; Lowther, D.A. Turnover of proteoglycans in cultures of bovine articular cartilage. Arch. Biochem. Biophys. 1984, 234, 275–289.
Campbell, M.A.; Winter, A.D.; Ilic, M.Z.; Handley, C.J. Catabolism and Loss of Proteoglycans from Cultures of Bovine Collateral Ligament. Arch. Biochem. Biophys. 1996, 328, 64–72.
Winter, A.D.; Campbell, M.A.; Robinson, H.; Handley, C.J. Catabolism of newly synthesized decorin by explant cultures of bovine ligament. Matrix Boil. 2000, 19, 129–138.
Samiric, T.; Ilic, M.Z.; Handley, C.J. Large aggregating and small leucine-rich proteoglycans are degraded by different pathways and at different rates in tendon. JBIC J. Boil. Inorg. Chem. 2004, 271, 3612–3620.
Ilic, M.Z.; Carter, P.; Tyndall, A.; Dudhia, J.; Handley, C.J. Proteoglycans and catabolic products of proteoglycans present in ligament. Biochem. J. 2005, 385, 381–388.
Hausser, H.; Hoppe, W.; Rauch, U.; Kresse, H. Endocytosis of a small dermatan sulphate proteoglycan. Identification of binding proteins. Biochem. J. 1989, 263, 137–142.
Hausser, H. Binding of heparin and of the small proteoglycan decorin to the same endocytosis receptor proteins leads to different metabolic consequences. J. Cell Boil. 1991, 114, 45–52.
Hausser, H.; Ober, B.; Quentin-Hoffmann, E.; Schmidt, B.; Kresse, H. Endocytosis of Different Members of the Small Chondroitin/Dermatan Sulfate Proteoglycan Family. J. Biol. Chem. 1992, 267, 11559–11564.
Hausser, H.; Schönherr, E.; Müller, M.; Liszio, C.; Bin, Z.; Fisher, L.W.; Kresse, H. Receptor-Mediated Endocytosis of Decorin: Involvement of Leucine-Rich Repeat Structures. Arch. Biochem. Biophys. 1998, 349, 363–370.
Hausser, H.; Kresse, H. Decorin endocytosis: Structural features of heparin and heparan sulphate oligosaccharides interfering with receptor binding and endocytosis. Biochem. J. 1999, 344, 827–835.
Schmidt, G.; Hausser, H.; Kresse, H. Extracellular accumulation of small dermatan sulphate proteoglycan II by interference with the secretion-recapture pathway. Biochem. J. 1990, 266, 591–595.
Feugaing, D.D.S.; Kresse, H.; Greb, R.R.; Götte, M. A Novel 110-kDa Receptor Protein is Involved in Endocytic Uptake of Decorin by Human Skin Fibroblasts. Sci. World J. 2006, 6, 35–52.
Schönherr, E.; Sunderkotter, C.; Iozzo, R.; Schaefer, L. Decorin, a Novel Player in the Insulin-like Growth Factor System. J. Boil. Chem. 2005, 280, 15767–15772.
Santiago-García, J.; Kodama, T.; Pitas, R.E. The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix. J. Biol. Chem. 2003, 278, 6942–6946.
Feugaing, D.; Tammi, R.; Echtermeyer, F.; Stenmark, H.; Kresse, H.; Smollich, M.; Schönherr, E.; Kiesel, L.; Götte, M. Endocytosis of the dermatan sulfate proteoglycan decorin utilizes multiple pathways and is modulated by epidermal growth factor receptor signaling. Biochimie 2007, 89, 637–657.
Wang, M.; Xue, S.; Fang, Q.; Zhang, M.; He, Y.; Zhang, Y.; Lammi, M.J.; Cao, J.; Chen, J. Expression and localization of the small proteoglycans decorin and biglycan in articular cartilage of Kashin-Beck disease and rats induced by T-2 toxin and selenium deficiency. Glycoconj. J. 2019, 36, 1–9.
Cillero-Pastor, B.; Eijkel, G.B.; Kiss, A.; Blanco, F.J.; Heeren, R.M.A.; Garcia, F.J.B. Matrix-assisted laser desorption ionization-imaging mass spectrometry: A new methodology to study human osteoarthritic cartilage. Arthritis Rheum. 2013, 65, 710–720.
Balakrishnan, L.; Nirujogi, R.S.; Ahmad, S.; Bhattacharjee, M.; Manda, S.S.; Renuse, S.; Kelkar, D.S.; Subbannayya, Y.; Raju, R.; Goel, R.; et al. Poteomic analysis of human osteoarthritis synovial fluid. Clin. Proteom. 2014, 11, 6.
Peffers, M.; McDermott, B.; Clegg, P.; Riggs, C. Comprehensive protein profiling of synovial fluid in osteoarthritis following protein equalization. Osteoarthr. Cartil. 2015, 23, 1204–1213.
Peffers, M.J.; Thornton, D.J.; Clegg, P.D. Characterization of neopeptides in equine articular cartilage degradation. J. Orthop. Res. 2016, 34, 106–120.
