Extracellular matrix disruption is an early event in the pathogenesis of skeletal disease in mucopolysaccharidosis I

Molecular Genetics and Metabolism

Volumn 114, Issue 2, 2015, Pages 146-155

  Heppner, Jonathan M ^a,b   Zaucke, Frank ^c   Clarke, Lorne A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Arthritis; Extracellular matrix structural integrity; ITRAQ; MPS I; MRM; SLRPs

Indexed keywords

ADAMTS12 PROTEIN; AGGRECAN; ALKALINE PHOSPHATASE; ASPORIN; BETA N ACETYLHEXOSAMINIDASE A; BIGLYCAN; CATALASE; CHAD PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 9; DECORIN; FIBROMODULIN; FIBRONECTIN 1; GLYCOSAMINOGLYCAN; HAPLN4 PROTEIN; LACTOFERRIN; LACTOYLGLUTATHIONE LYASE; LAMIN A; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MATN1 PROTEIN; MESSENGER RNA; PRELP PROTEIN; PROTEOGLYCAN; RAB32 PROTEIN; SCLEROPROTEIN; SERPINF1 PROTEIN; STROMELYSIN; THROMBOSPONDIN 1; THROMBOSPONDIN 3; UNCLASSIFIED DRUG; BGN PROTEIN, MOUSE; EYE PROTEIN; GLYCOPROTEIN; NERVE GROWTH FACTOR; PIGMENT EPITHELIUM-DERIVED FACTOR; PRELP PROTEIN, MOUSE; SERINE PROTEINASE INHIBITOR;

ARTICLE; BONE DISEASE; EXTRACELLULAR MATRIX; FEMUR HEAD; GENE EXPRESSION; HUMAN; HUMAN TISSUE; HURLER SYNDROME; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEOMICS; TANDEM MASS SPECTROMETRY; TRABECULAR BONE; WESTERN BLOTTING; ANIMAL; BONE DISEASES; DISEASE MODEL; GENE EXPRESSION PROFILING; KNOCKOUT MOUSE; MASS SPECTROMETRY; METABOLISM; MOUSE;

MURINAE; MUS;

ANIMALS; BIGLYCAN; BONE DISEASES; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; EYE PROTEINS; GENE EXPRESSION PROFILING; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; IMMUNOHISTOCHEMISTRY; LACTOFERRIN; MASS SPECTROMETRY; MICE; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS I; NERVE GROWTH FACTORS; OSTEOARTHRITIS; PROTEOGLYCANS; PROTEOMICS; SERPINS;

EID: 84921725803     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2014.09.012     Document Type: Article

References (56)

1. Clarke L.A. Pathogenesis of skeletal and connective tissue involvement in the mucopolysaccharidoses: glycosaminoglycan storage is merely the instigator. Rheumatology 2011, 50:13-18.
2. Gatto F., Redaelli D., Salvadè A., Marzorati S., Sacchetti B., Ferina C., Roobrouck V.D., Bertola F., Romano M., Villani G., Antolini L., Rovelli A., Verfaillie C.M., Biondi A., Riminucci M., Bianco P., Serafini M. Hurler disease bone marrow stromal cells exhibit altered ability to support osteoclast formation. Stem Cells Dev. 2012, 21:1466-1477.
3. Metcalf J.A., Zhang Y., Hilton M.J., Long F., Ponder K.P. Mechanism of shortened bones in mucopolysaccharidosis VII. Mol. Genet. Metab. 2009, 97:202-211.
4. Opoka-Winiarska V., Jurecka A., Emeryk A., Tylki-Szymańska A. Osteoimmunology in mucopolysaccharidoses type I, II, VI and VII. Immunological regulation of the osteoarticular system in the course of metabolic inflammation. Osteoarthr. Cartil. 2013, 21:1813-1823.
5. Simonaro C.M., D'Angelo M., He X., Eliyahu E., Shtraizent N., Haskins M.E., et al. Mechanism of glycosaminoglycan-mediated bone and joint disease: implications for the mucopolysaccharidoses and other connective tissue diseases. Am. J. Pathol. 2008, 172:112-122.
6. Simonaro C.M. Cartilage and chondrocyte pathology in the mucopolysaccharidoses: the role of glycosaminoglycan-mediated inflammation. J. Pediatr. Rehabil. Med. 2010, 3:112-122.
7. Simonaro C.M., Haskins M.E., Schuchman E.H. Articular chondrocytes from animals with a dermatan sulfate storage disease undergo a high rate of apoptosis and release nitric oxide and inflammatory cytokines: a possible mechanism underlying degenerative joint disease in the mucopolysaccharidoses. Lab. Investig. 2001, 81:1319-1328.
8. Homan E.P., Rauch F., Grafe I., Lietman C., Doll J.A., Dawson B., Bertin T., Napierala D., Morello R., Gibbs R., White L., Miki R., Cohn D.H., Crawford S., Travers R., Glorieux F.H., Lee B. Mutations in SERPINF1 cause osteogenesis imperfecta type VI. J. Bone Miner. Res. 2011, 26:2798-27803.
9. Russell C., Hendson G., Jevon G., Matlock T., Yu J., Aklujkar M., Ng K.Y., Clarke L.A. Murine MPS I: insights into the pathogenesis of Hurler syndrome. Clin. Genet. 1998, 53:349-361.
10. Jiang X., Ye M., Jiang X., Liu G., Feng S., Cui L., Zou H. Method development of efficient protein extraction in bone tissue for proteome analysis. J. Proteome Res. 2007, 66:2287-2294.
11. Craig R., Cortens J.P., Beavis R.C. An open source system for analyzing, validating and storing protein identification data. J. Proteome Res. 2004, 3:1234-1242.
12. Illumina Whole-Genome Gene Expression Direct Hybridization Assay Guide Revision A 2010, 9-75. Illumina Inc.
13. Smyth G.K., Ritchie M., Thorne N., Wettenhall J., Shi W., Hu Y. Linear Models for Microarray Data User Guide 2002, 1-71. Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia. first edition.
14. SABiosciences RT2 Profiler PCR Array Handbook 2013, 1-56. Qiagen Inc.
15. Hua C.T., Hopwood J.J., Carlsson S.R., Harris R.J., Meikle P.J. Evaluation of the lysosome-associated membrane protein LAMP-2 as a marker for lysosomal storage disorders. Clin. Chem. 1998, 44:2094-2102.
16. Zheng Y., Rozengurt N., Ryazantsev S., Kohn D.B., Satake N., Neufeld E.F. Treatment of the mouse model of mucopolysaccharidosis I with retrovirally transduced bone marrow. Mol. Genet. Metab. 2003, 79:233-244.
17. Bhaumik M., Muller V.J., Rozaklis T., Johnson L., Dobrenis K., Bhattacharyya R., Wurzelmann S., Finamore P., Hopwood J.J., Walkley S.U., Stanley P. A mouse model for mucopolysaccharidosis type III A (Sanfilippo syndrome). Glycobiology 1999, 9:1389-1396.
18. Li H.H., Yu W.H., Rozengurt N., Zhao H.Z., Lyons K.M., Anagnostaras S., Fanselow M.S., Suzuki K., Vanier M.T., Neufeld E.F. Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N-acetylglucosaminidase. PNAS 1999, 96:14505-14510.
19. Birkenmeier E.H., Barker J.E., Vogler C.A., Kyle J.W., Sly W.S., Gwynn B., Levy B., Pegors C. Increased life span and correction of metabolic defects in murine mucopolysaccharidosis type VII after syngeneic bone marrow transplantation. Blood 1991, 78:3081-3092.
20. Martin D.C., Atmuri V., Hemming R.J., Farley J., Mort J.S., Byers S., Hombach-Klonisch S., Csoka A.B., Stern R., Triggs-Raine B.L. A mouse model of human mucopolysaccharidosis IX exhibits osteoarthritis. Hum. Mol. Genet. 2008, 17:1904-1915.
21. Chen J., Gupta T., Barasz J.A., Kalajzic Z., Yeh W.C., Drissi H., Hand A.R., Wadhwa S. Analysis of microarchitectural changes in a mouse temporomandibular joint osteoarthritis model. Arch. Oral Biol. 2009, 54:1091-1098.
22. 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.
23. Young M.F., Bi Y., Ameye L., Chen X.D. Biglycan knockout mice: new models for musculoskeletal diseases. Glycoconj. J. 2002, 19:257-262.
24. Posey K.L., Coustry F., Veerisetty A.C., Liu P., Alcorn J.L., Hecht J.T. Chondrocyte-specific pathology during skeletal growth and therapeutics in a murine model of pseudoachondroplasia. J. Bone Miner. Res. 2013, 29:1258-1268.
25. Matsui Y., Iwasaki N., Kon S., Takahashi D., Morimoto J., Matsui Y., Denhardt D.T., Rittling S., Minami A., Uede T. Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum. 2009, 60:2362-2371.
26. Echtermeyer F., Bertrand J., Dreier R., Meinecke I., Neugebauer K., Fuerst M., Lee Y.J., Song Y.W., Herzog C., Theilmeier G., Pap T. Syndecan-4 regulates ADAMTS-5 activation and cartilage breakdown in osteoarthritis. Nat. Med. 2009, 15:1072-1076.
27. Osteoarthritis Beasley J., Arthritis Rheumatoid Conservative therapeutic management. J. Hand Ther. 2012, 25:163-171.
28. Schuchman E.H., Ge Y., Lai A., Borisov Y., Faillace M., Eliyahu E., He X., Iatridis J., Vlassara H., Striker G., Simonaro C.M. Pentosan polysulfate: a novel therapy for the mucopolysaccharidoses. PLoS One 2013, 8:e54459.
29. Simonaro C.M., Ge Y., Eliyahu E., He X., Jepsen K.J., Schuchman E.H. Involvement of the Toll-like receptor 4 pathway and use of TNF-alpha antagonists for treatment of the mucopolysaccharidoses. PNAS 2010, 107:222-227.
30. Eliyahu E., Wolfson T., Ge Y., Jepsen K.J., Schuchman E.H., Simonaro C.M. Anti-TNF-alpha therapy enhances the effects of enzyme replacement therapy in rats with mucopolysaccharidosis type V. PLoS One 2011, 6:e22447.
31. Bornstein P., Sage E.H. Matricellular proteins: extracellular modulators of cell function. Curr. Opin. Cell Biol. 2002, 14:608-616.
32. Miguez P.A., Terajima M., Nagaoka H., Ferreira J.A., Braswell K., Ko C.C., Yamauchi M. Recombinant biglycan promotes bone morphogenetic protein-induced osteogenesis. J. Dent. Res. 2014, 93:406-411.
33. Halper J. Proteoglycans and diseases of soft tissues, progress in heritable soft connective tissue diseases. Adv. Exp. Med. Biol. 2014, 802:49-58.
34. Genovese F., Barascuk N., Larsen L., Larsen M.R., Nawrocki A., Li Y., Zheng Q., Wang J., Veidal S.S., Leeming D.J., Karsdal M.A. Biglycan fragmentation in pathologies associated with extracellular matrix remodeling by matrix metalloproteinases. Fibrogenesis Tissue Repair 2013, 6:9.
35. Berendsen A.D., Fisher L.W., Kilts T.M., Owens R.T., Robey P.G., Gutkind J.S., Young M.F. Modulation of canonical Wnt signaling by the extracellular matrix component biglycan. PNAS 2011, 108:17022-17027.
36. Burton-Wurster N., Liu W., Matthews G.L., Lust G., Roughley P.J., Glant T.T., Cs-Szabó G. TGF beta 1 and biglycan, decorin, and fibromodulin metabolism in canine cartilage. Osteoarthr. Cartil. 2003, 11:167-176.
37. 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.
38. Merline R., Schaefer R.M., Schaefer L. The matricellular functions of small leucine-rich proteoglycans (SLRPs). J. Cell Commun. Signal. 2009, 3:323-335.
39. Song R., Zeng Q., Ao L., Yu J.A., Cleveland J.C., Zhao K.S., Fullerton D.A., Meng X. Biglycan induces the expression of osteogenic factors in human aortic valve interstitial cells via Toll-like receptor-2. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2711-2720.
40. Chen S., Young M.F., Chakravarti S., Birk D.E. Interclass small leucine-rich repeat proteoglycan interactions regulate collagen fibrillogenesis and corneal stromal assembly. Matrix Biol. 2014, 35:103-111.
41. Juneja S.C., Veillette C. Defects in tendon, ligament, and enthesis in response to genetic alterations in key proteoglycans and glycoproteins: a review. Arthritis 2013, e154812.
42. Young M.F., Fallon J.R. Biglycan: a promising new therapeutic for neuromuscular and musculoskeletal diseases. Curr. Opin. Genet. Dev. 2012, 22:398-400.
43. Bengtsson E., Mörgelin M., Sasaki T., Timpl R., Heinegård D., Aspberg A. The leucine-rich repeat protein PRELP binds perlecan and collagens and may function as a basement membrane anchor. J. Biol. Chem. 2002, 277:15061-15068.
44. Tillgren V., Onnerfjord 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. Biol. Chem. 2009, 284:28543-28553.
45. Happonen K.E., Fürst C.M., Saxne T., Heinegård D., Blom A.M. PRELP protein inhibits the formation of the complement membrane attack complex. J. Biol. Chem. 2012, 287:8092-8100.
46. Suphapeetiporn K., Tongkobpetch S., Mahayosnond A., Shotelersuk V. Expanding the phenotypic spectrum of Caffey disease. Clin. Genet. 2007, 71:280-284.
47. Beighton P., De Paepe A., Steinmann B., Tsipouras P., Wenstrup R.J. Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). Am. J. Med. Genet. 1998, 77:31-37.
48. Van Dijk F.S., Sillence D.O. Osteogenesis imperfecta: clinical, biochemical and molecular findings. Am. J. Med. Genet. 2014, 70:131-139.
49. Tortorella M.D., Malfait A.M., Deccico C., Arner E. The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation. Osteoarthr. Cartil. 2001, 9:539-552.
50. Fosang A.J., Last K., Maciewicz R.A. Aggrecan is degraded by matrix metalloproteinases in human arthritis. Evidence that matrix metalloproteinase and aggrecanase activities can be independent. J. Clin. Invest. 1996, 98:2292-2299.
51. McCawley L.J., Matrisian L.M. Matrix metalloproteinases: they're not just for matrix anymore. Curr. Opin. Cell Biol. 2001, 13:534-540.
52. Posthumus M.D., Limburg P.C., Westra J., Cats H.A., Stewart R.E., van Leeuwen M.A., van Rijswijk M.H. Serum levels of matrix metalloproteinase-3 in relation to the development of radiological damage in patients with early rheumatoid arthritis. Rheumatology 1999, 38:1081-1087.
53. Lee A., Choi S.J., Park K., Park J.W., Kim K., Choi K., Yoon S.Y., Youn I. Detection of active matrix metalloproteinase-3 in serum and fibroblast-like synoviocytes of collagen-induced arthritis mice. Bioconjug. Chem. 2013, 24:1068-1074.
54. Fässler R., Schnegelsberg P.N., Dausman J., Shinya T., Muragaki Y., McCarthy M.T., Olsen B.R., Jaenisch R. Mice lacking alpha 1 (IX) collagen develop noninflammatory degenerative joint disease. PNAS 1994, 91:5070-5074.
55. Alizadeh B.Z., Njajou O.T., Bijkerk C., Meulenbelt I., Wildt S.C., Hofman A., Pols H.A., Slagboom P.E., Duijn C.M. Evidence for a role of the genomic region of the gene encoding for the alpha1 chain of type IX collagen (COL9A1) in hip osteoarthritis: a population-based study. Arthritis Rhuem. 2005, 52:1437-1442.
56. Loughlin J., Mustafa Z., Dowling B., Southam L., Marcelline L., Räinä S.S., Ala-Kokko L., Chapman K. Finer linkage mapping of a primary hip osteoarthritis susceptibility locus on chromosome 6. Eur. J. Hum. Genet. 2002, 10:562-568.