Ablation of Perlecan Domain 1 Heparan Sulfate Reduces Progressive Cartilage Degradation, Synovitis, and Osteophyte Size in a Preclinical Model of Posttraumatic Osteoarthritis

Arthritis and Rheumatology

Volumn 68, Issue 4, 2016, Pages 868-879

  Shu, Cindy C ^a   Jackson, Miriam T ^a   Smith, Margaret M ^a   Smith, Susan M ^a   Penm, Steven ^b   Lord, Megan S ^b   Whitelock, John M ^b   Little, Christopher B ^a   Melrose, James ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GELATINASE A; GLYCOSAMINOGLYCAN; INTERLEUKIN 1ALPHA; MESSENGER RNA; PERLECAN; STROMELYSIN; FGFR1 PROTEIN, MOUSE; FGFR3 PROTEIN, MOUSE; MMP2 PROTEIN, MOUSE; MMP3 PROTEIN, MOUSE; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; BONE MATURATION; CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CHONDROPROTECTION; CONTROLLED STUDY; DISEASE COURSE; FEMUR HEAD; GENE DELETION; GENE EXPRESSION; GROWTH PLATE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; KNOCKOUT GENE; MALE; MOUSE; NONHUMAN; OSTEOARTHRITIS; OSTEOPHYTE; POSTTRAUMATIC ARTHROPATHY; POSTTRAUMATIC OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SYNOVITIS; WESTERN BLOTTING; ANIMAL; ARTICULAR CARTILAGE; COMPLICATION; GENE EXPRESSION PROFILING; GENETICS; KNEE INJURY; KNOCKOUT MOUSE; METABOLISM; ORGAN SIZE; OSTEOARTHRITIS, KNEE; OSTEOSCLEROSIS; PATHOLOGY;

ANIMALS; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; DISEASE PROGRESSION; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION PROFILING; GLYCOSAMINOGLYCANS; HEPARAN SULFATE PROTEOGLYCANS; IMMUNOHISTOCHEMISTRY; KNEE INJURIES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 3; MICE; MICE, KNOCKOUT; ORGAN SIZE; OSTEOARTHRITIS, KNEE; OSTEOPHYTE; OSTEOSCLEROSIS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; RNA, MESSENGER; SYNOVITIS;

EID: 84962090409     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39529     Document Type: Article

References (47)

1. Melrose J, Hayes AJ, Whitelock JM, Little CB., Perlecan, the "jack of all trades" proteoglycan of cartilaginous weight-bearing connective tissues. Bioessays 2008; 30: 457-69.
2. Kvist AJ, Nystrom A, Hultenby K, Sasaki T, Talts JF, Aspberg A., The major basement membrane components localize to the chondrocyte pericellular matrix-a cartilage basement membrane equivalent? Matrix Biol 2008; 27: 22-33.
3. Vincent TL, McLean CJ, Full LE, Peston D, Saklatvala J., FGF-2 is bound to perlecan in the pericellular matrix of articular cartilage, where it acts as a chondrocyte mechanotransducer. Osteoarthritis Cartilage 2007; 15: 752-63.
4. Wilusz RE, Defrate LE, Guilak F., A biomechanical role for perlecan in the pericellular matrix of articular cartilage. Matrix Biol 2012; 31: 320-7.
5. Smith SM, Shu C, Melrose J., Comparative immunolocalisation of perlecan with collagen II and aggrecan in human foetal, newborn and adult ovine joint tissues demonstrates perlecan as an early developmental chondrogenic marker. Histochem Cell Biol 2010; 134: 251-63.
6. Whitelock JM, Melrose J, Iozzo RV., Diverse cell signaling events modulated by perlecan. Biochemistry 2008; 47: 11174-83.
7. Knox S, Fosang AJ, Last K, Melrose J, Whitelock J., Perlecan from human epithelial cells is a hybrid heparan/chondroitin/keratan sulfate proteoglycan. FEBS Lett 2005; 579: 5019-23.
8. Lord MS, Chuang CY, Melrose J, Davies MJ, Iozzo RV, Whitelock JM., The role of vascular-derived perlecan in modulating cell adhesion, proliferation and growth factor signaling. Matrix Biol 2014; 35: 112-22.
9. Chuang CY, Lord MS, Melrose J, Rees MD, Knox SM, Freeman C, et al., Heparan sulfate-dependent signaling of fibroblast growth factor 18 by chondrocyte-derived perlecan. Biochemistry 2010; 49: 5524-32.
10. Ornitz DM, Itoh N., The fibroblast growth factor signaling pathway. Wiley Interdiscip Rev Dev Biol 2015; 4: 215-66.
11. Ellman MB, Yan D, Ahmadinia K, Chen D, An HS, Im HJ., Fibroblast growth factor control of cartilage homeostasis. J Cell Biochem 2013; 114: 735-42.
12. Vincent TL., Fibroblast growth factor 2: good or bad guy in the joint? Arthritis Res Ther 2011; 13: 127.
13. Davidson D, Blanc A, Filion D, Wang H, Plut P, Pfeffer G, et al., Fibroblast growth factor (FGF) 18 signals through FGF receptor 3 to promote chondrogenesis. J Biol Chem 2005; 280: 20509-15.
14. Liu Z, Lavine KJ, Hung IH, Ornitz DM., FGF18 is required for early chondrocyte proliferation, hypertrophy and vascular invasion of the growth plate. Dev Biol 2007; 302: 80-91.
15. Yan D, Chen D, Im HJ., Fibroblast growth factor-2 promotes catabolism via FGFR1-Ras-Raf-MEK1/2-ERK1/2 axis that coordinates with the PKCδ pathway in human articular chondrocytes. J Cell Biochem 2012; 113: 2856-65.
16. Yan D, Chen D, Cool SM, van Wijnen AJ, Mikecz K, Murphy G, et al., Fibroblast growth factor receptor 1 is principally responsible for fibroblast growth factor 2-induced catabolic activities in human articular chondrocytes. Arthritis Res Ther 2011; 13: R130.
17. Chong KW, Chanalaris A, Burleigh A, Jin H, Watt FE, Saklatvala J, et al., Fibroblast growth factor 2 drives changes in gene expression following injury to murine cartilage in vitro and in vivo. Arthritis Rheum 2013; 65: 2346-55.
18. Vincent T, Hermansson M, Bolton M, Wait R, Saklatvala J., Basic FGF mediates an immediate response of articular cartilage to mechanical injury. Proc Natl Acad Sci U S A 2002; 99: 8259-64.
19. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y., Perlecan is essential for cartilage and cephalic development. Nat Genet 1999; 23: 354-8.
20. Lowe DA, Lepori-Bui N, Fomin PV, Sloofman LG, Zhou X, Farach-Carson MC, et al., Deficiency in perlecan/HSPG2 during bone development enhances osteogenesis and decreases quality of adult bone in mice. Calcif Tissue Int 2014; 95: 29-38.
21. Liu Z, Xu J, Colvin JS, Ornitz DM., Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev 2002; 16: 859-69.
22. Valverde-Franco G, Binette JS, Li W, Wang H, Chai S, Laflamme F, et al., Defects in articular cartilage metabolism and early arthritis in fibroblast growth factor receptor 3 deficient mice. Hum Mol Genet 2006; 15: 1783-92.
23. Jacob AL, Smith C, Partanen J, Ornitz DM., Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev Biol 2006; 296: 315-28.
24. Chia SL, Sawaji Y, Burleigh A, McLean C, Inglis J, Saklatvala J, et al., Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis. Arthritis Rheum 2009; 60: 2019-27.
25. Weng T, Yi L, Huang J, Luo F, Wen X, Du X, et al., Genetic inhibition of fibroblast growth factor receptor 1 in knee cartilage attenuates the degeneration of articular cartilage in adult mice. Arthritis Rheum 2012; 64: 3982-92.
26. Rossi M, Morita H, Sormunen R, Airenne S, Kreivi M, Wang L, et al., Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J 2003; 22: 236-45.
27. Zhou Z, Wang J, Cao R, Morita H, Soininen R, Chan KM, et al., Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res 2004; 64: 4699-702.
28. Whitelock JM, Graham LD, Melrose J, Murdoch AD, Iozzo RV, Underwood PA., Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol 1999; 18: 163-78.
29. Glasson SS, Blanchet TJ, Morris EA., The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage 2007; 15: 1061-9.
30. Jackson MT, Moradi B, Zaki S, Smith MM, McCracken S, Smith SM, et al., Depletion of protease-activated receptor 2 but not protease-activated receptor 1 may confer protection against osteoarthritis in mice through extracartilaginous mechanisms. Arthritis Rheumatol 2014; 66: 3337-48.
31. Farndale RW, Buttle DJ, Barrett AJ., Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986; 883: 173-7.
32. Morita H, Yoshimura A, Inui K, Ideura T, Watanabe H, Wang L, et al., Heparan sulfate of perlecan is involved in glomerular filtration. J Am Soc Nephrol 2005; 16: 1703-10.
33. Melrose J, Isaacs MD, Smith SM, Hughes CE, Little CB, Caterson B, et al., Chondroitin sulphate and heparan sulphate sulphation motifs and their proteoglycans are involved in articular cartilage formation during human foetal knee joint development. Histochem Cell Biol 2012; 138: 461-75.
34. Little CB, Hunter DJ., Post-traumatic osteoarthritis: from mouse models to clinical trials. Nat Rev Rheumatol 2013; 9: 485-97.
35. Celie JW, Rutjes NW, Keuning ED, Soininen R, Heljasvaara R, Pihlajaniemi T, et al., Subendothelial heparan sulfate proteoglycans become major L-selectin and monocyte chemoattractant protein-1 ligands upon renal ischemia/reperfusion. Am J Pathol 2007; 170: 1865-78.
36. Kaneko H, Ishijima M, Futami I, Tomikawa-Ichikawa N, Kosaki K, Sadatsuki R, et al., Synovial perlecan is required for osteophyte formation in knee osteoarthritis. Matrix Biol 2013; 32: 178-87.
37. Naganawa T, Xiao L, Coffin JD, Doetschman T, Sabbieti MG, Agas D, et al., Reduced expression and function of bone morphogenetic protein-2 in bones of Fgf2 null mice. J Cell Biochem 2008; 103: 1975-88.
38. Xiao L, Sobue T, Esliger A, Kronenberg MS, Coffin JD, Doetschman T, et al., Disruption of the Fgf2 gene activates the adipogenic and suppresses the osteogenic program in mesenchymal marrow stromal stem cells. Bone 2010; 47: 360-70.
39. Echtermeyer F, Bertrand J, Dreier R, Meinecke I, Neugebauer K, Fuerst M, et al., Syndecan-4 regulates ADAMTS-5 activation and cartilage breakdown in osteoarthritis. Nat Med 2009; 15: 1072-6.
40. Honsawek S, Yuktanandana P, Tanavalee A, Saetan N, Anomasiri W, Parkpian V., Correlation between plasma and synovial fluid basic fibroblast growth factor with radiographic severity in primary knee osteoarthritis. Int Orthop 2012; 36: 981-5.
41. Im HJ, Muddasani P, Natarajan V, Schmid TM, Block JA, Davis F, et al., Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cδ pathways in human adult articular chondrocytes. J Biol Chem 2007; 282: 11110-21.
42. Hoshiyama Y, Otsuki S, Oda S, Kurokawa Y, Nakajima M, Jotoku T, et al., Chondrocyte clusters adjacent to sites of cartilage degeneration have characteristics of progenitor cells. J Orthop Res 2015; 33: 548-55.
43. Tchetina EV, Squires G, Poole AR., Increased type II collagen degradation and very early focal cartilage degeneration is associated with upregulation of chondrocyte differentiation related genes in early human articular cartilage lesions. J Rheumatol 2005; 32: 876-86.
44. Uchino M, Izumi T, Tominaga T, Wakita R, Minehara H, Sekiguchi M, et al., Growth factor expression in the osteophytes of the human femoral head in osteoarthritis. Clin Orthop Relat Res 2000; 377: 119-25.
45. Tesche F, Miosge N., Perlecan in late stages of osteoarthritis of the human knee joint. Osteoarthritis Cartilage 2004; 12: 852-62.
46. Li X, Ellman MB, Kroin JS, Chen D, Yan D, Mikecz K, et al., Species-specific biological effects of FGF-2 in articular cartilage: implication for distinct roles within the FGF receptor family. J Cell Biochem 2012; 113: 2532-42.
47. Lohmander LS, Hellot S, Dreher D, Krantz EF, Kruger DS, Guermazi A, et al., Intraarticular sprifermin (recombinant human fibroblast growth factor 18) in knee osteoarthritis: a randomized, double-blind, placebo-controlled trial. Arthritis Rheumatol 2014; 66: 1820-31.