Heparanase expression and activity influences chondrogenic and osteogenic processes during endochondral bone formation

Bone

Volumn 43, Issue 4, 2008, Pages 689-699

  Brown, A J ^a   Alicknavitch, M ^a   D'Souza, S S ^a   Daikoku, T ^b   Kirn Safran, C B ^a   Marchetti, D ^c   Carson, D D ^a   Farach Carson, M C ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Bone; Chondrogenesis; Heparanase; Migration; Osteogenesis; PI 88

Indexed keywords

GROWTH FACTOR; HEPARANASE; HEPARANASE ANTIBODY; HEPARANASE INHIBITOR; OSTEOCALCIN; PERLECAN; PI 88; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; BONE REMODELING; CARTILAGE CELL; CELL GROWTH; CELL INTERACTION; CHONDROGENESIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; EX VIVO STUDY; EXTRACELLULAR MATRIX; IMMUNOLOCALIZATION; IN SITU HYBRIDIZATION; IN VITRO STUDY; MOUSE; NONHUMAN; PATTERN STIMULATION; PERICHONDRIUM; PROTEIN EXPRESSION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CHONDROCYTES; CHONDROGENESIS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONIDASE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; OLIGOSACCHARIDES; ORGAN CULTURE TECHNIQUES; OSTEOGENESIS;

EID: 51149092044     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.05.022     Document Type: Article

References (85)

1. DeLise A.M., Fischer L., and Tuan R.S. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8 (2000) 309-334
2. Olsen B.R., Reginato A.M., and Wang W. Bone development. Annu Rev Cell Dev Biol 16 (2000) 191-220
3. Ohta S., Muramatsu H., Senda T., Zou K., Iwata H., and Muramatsu T. Midkine is expressed during repair of bone fracture and promotes chondrogenesis. J Bone Miner Res 14 (1999) 1132-1144
4. Gritli-Linde A., Lewis P., McMahon A.P., and Linde A. The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev Biol 236 (2001) 364-386
5. Murakami S., Kan M., McKeehan W.L., and de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 97 (2000) 1113-1118
6. Pizette S., and Niswander L. BMPs are required at two steps of limb chondrogenesis: formation of prechondrogenic condensations and their differentiation into chondrocytes. Dev Biol 219 (2000) 237-249
7. Tapp H., Hernandez D.J., Neame P.J., and Koob T.J. Pleiotrophin inhibits chondrocyte proliferation and stimulates proteoglycan synthesis in mature bovine cartilage. Matrix Biol 18 (1999) 543-556
8. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., and Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273 (1996) 613-622
9. Yano F., Kugimiya F., Ohba S., Ikeda T., Chikuda H., Ogasawara T., Ogata N., Takato T., Nakamura K., Kawaguchi H., and Chung U.I. The canonical Wnt signaling pathway promotes chondrocyte differentiation in a Sox9-dependent manner. Biochem Biophys Res Commun 333 (2005) 1300-1308
10. Mukherjee A., Dong S.S., Clemens T., Alvarez J., and Serra R. Co-ordination of TGF-beta and FGF signaling pathways in bone organ cultures. Mech Dev 122 (2005) 557-571
11. Lee K., Lanske B., Karaplis A.C., Deeds J.D., Kohno H., Nissenson R.A., Kronenberg H.M., and Segre G.V. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 137 (1996) 5109-5118
12. Gomes Jr. R.R., Van Kuppevelt T.H., Farach-Carson M.C., and Carson D.D. Spatiotemporal distribution of heparan sulfate epitopes during murine cartilage growth plate development. Histochem Cell Biol 126 (2006) 713-722
13. Atha D.H., Stephens A.W., Rimon A., and Rosenberg R.D. Sequence variation in heparin octasaccharides with high affinity for antithrombin III. Biochemistry 23 (1984) 5801-5812
14. Chiao E., Fisher P., Crisponi L., Deiana M., Dragatsis I., Schlessinger D., Pilia G., and Efstratiadis A. Overgrowth of a mouse model of the Simpson-Golabi-Behmel syndrome is independent of IGF signaling. Dev Biol 243 (2002) 185-206
15. Esko J.D., and Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71 (2002) 435-471
16. Nicole S., Davoine C.S., Topaloglu H., Cattolico L., Barral D., Beighton P., Hamida C.B., Hammouda H., Cruaud C., White P.S., Samson D., Urtizberea J.A., Lehmann-Horn F., Weissenbach J., Hentati F., and Fontaine B. Perlecan, the major proteoglycan of basement membranes, is altered in patients with Schwartz-Jampel syndrome (chondrodystrophic myotonia). Nat Genet 26 (2000) 480-483
17. Ashikari S., Habuchi H., and Kimata K. Characterization of heparan sulfate oligosaccharides that bind to hepatocyte growth factor. J Biol Chem 270 (1995) 29586-29593
18. Faham S., Hileman R.E., Fromm J.R., Linhardt R.J., and Rees D.C. Heparin structure and interactions with basic fibroblast growth factor. Science 271 (1996) 1116-1120
19. Lindahl U., Thunberg L., Backstrom G., Riesenfeld J., Nordling K., and Bjork I. Extension and structural variability of the antithrombin-binding sequence in heparin. J Biol Chem 259 (1984) 12368-12376
20. So C.L., Kaluarachchi K., Tam P.P., and Cheah K.S. Impact of mutations of cartilage matrix genes on matrix structure, gene activity and chondrogenesis. Osteoarthritis Cartilage 9 Suppl A (2001) S160-173
21. Pacicca D.M., Patel N., Lee C., Salisbury K., Lehmann W., Carvalho R., Gerstenfeld L.C., and Einhorn T.A. Expression of angiogenic factors during distraction osteogenesis. Bone 33 (2003) 889-898
22. Gomes Jr. R.R., Joshi S.S., Farach-Carson M.C., and Carson D.D. Ribozyme-mediated perlecan knockdown impairs chondrogenic differentiation of C3H10T1/2 fibroblasts. Differentiation 74 (2006) 53-63
23. Gomes Jr. R.R., Farach Carson M.C., and Carson D.D. Perlecan-stimulated nodules undergo chondrogenic maturation in response to rhBMP-2 treatment in vitro. Connect Tissue Res 44 Suppl 1 (2003) 196-201
24. French M.M., Gomes Jr. R.R., Timpl R., Hook M., Czymmek K., Farach-Carson M.C., and Carson D.D. Chondrogenic activity of the heparan sulfate proteoglycan perlecan maps to the N-terminal domain I. J Bone Miner Res 17 (2002) 48-55
25. French M.M., Smith S.E., Akanbi K., Sanford T., Hecht J., Farach-Carson M.C., and Carson D.D. Expression of the heparan sulfate proteoglycan, perlecan, during mouse embryogenesis and perlecan chondrogenic activity in vitro. J Cell Biol 145 (1999) 1103-1115
26. Kirn-Safran C.B., Gomes R.R., Brown A.J., and Carson D.D. Heparan sulfate proteoglycans: coordinators of multiple signaling pathways during chondrogenesis. Birth Defects Res C Embryo Today 72 (2004) 69-88
27. Zcharia E., Zilka R., Yaar A., Yacoby-Zeevi O., Zetser A., Metzger S., Sarid R., Naggi A., Casu B., Ilan N., Vlodavsky I., and Abramovitch R. Heparanase accelerates wound angiogenesis and wound healing in mouse and rat models. Faseb J 19 (2005) 211-221
28. Miao H.Q., Navarro E., Patel S., Sargent D., Koo H., Wan H., Plata A., Zhou Q., Ludwig D., Bohlen P., and Kussie P. Cloning, expression, and purification of mouse heparanase. Protein Expr Purif 26 (2002) 425-431
29. Podyma-Inoue K.A., Yokote H., Sakaguchi K., Ikuta M., and Yanagishita M. Characterization of heparanase from a rat parathyroid cell line. J Biol Chem 277 (2002) 32459-32465
30. Levy-Adam F., Miao H.Q., Heinrikson R.L., Vlodavsky I., and Ilan N. Heterodimer formation is essential for heparanase enzymatic activity. Biochem Biophys Res Commun 308 (2003) 885-891
31. D'Souza S.S., Daikoku T., Farach-Carson M.C., and Carson D.D. Heparanase Expression and Function During Early Pregnancy in Mice. Biol Reprod 77 (2007) 433-441
32. Vlodavsky I., Ilan N., Naggi A., and Casu B. Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate. Curr Pharm Des 13 (2007) 2057-2073
33. Bame K.J. Heparanases: endoglycosidases that degrade heparan sulfate proteoglycans. Glycobiology 11 (2001) 91R-98R
34. Freeman C., Browne A.M., and Parish C.R. Evidence that platelet and tumour heparanases are similar enzymes. Biochem J 342 Pt 2 (1999) 361-368
35. Sewell R.F., Brenchley P.E., and Mallick N.P. Human mononuclear cells contain an endoglycosidase specific for heparan sulphate glycosaminoglycan demonstrable with the use of a specific solid-phase metabolically radiolabelled substrate. Biochem J 264 (1989) 777-783
36. Laskov R., Michaeli R.I., Sharir H., Yefenof E., and Vlodavsky I. Production of heparanase by normal and neoplastic murine B-lymphocytes. Int J Cancer 47 (1991) 92-98
37. Matzner Y., Bar-Ner M., Yahalom J., Ishai-Michaeli R., Fuks Z., and Vlodavsky I. Degradation of heparan sulfate in the subendothelial extracellular matrix by a readily released heparanase from human neutrophils. Possible role in invasion through basement membranes. J Clin Invest 76 (1985) 1306-1313
38. Mollinedo F., Nakajima M., Llorens A., Barbosa E., Callejo S., Gajate C., and Fabra A. Major co-localization of the extracellular-matrix degradative enzymes heparanase and gelatinase in tertiary granules of human neutrophils. Biochem J 327 Pt 3 (1997) 917-923
39. Vlodavsky I., Goldshmidt O., Zcharia E., Metzger S., Chajek-Shaul T., Atzmon R., Guatta-Rangini Z., and Friedmann Y. Molecular properties and involvement of heparanase in cancer progression and normal development. Biochimie 83 (2001) 831-839
40. Elkin M., Ilan N., Ishai-Michaeli R., Friedmann Y., Papo O., Pecker I., and Vlodavsky I. Heparanase as mediator of angiogenesis: mode of action. Faseb J 15 (2001) 1661-1663
41. Parish C.R., Freeman C., and Hulett M.D. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta 1471 (2001) M99-108
42. Zcharia E., Metzger S., Chajek-Shaul T., Aingorn H., Elkin M., Friedmann Y., Weinstein T., Li J.P., Lindahl U., and Vlodavsky I. Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. Faseb J 18 (2004) 252-263
43. Kram V., Zcharia E., Yacoby-Zeevi O., Metzger S., Chajek-Shaul T., Gabet Y., Muller R., Vlodavsky I., and Bab I. Heparanase is expressed in osteoblastic cells and stimulates bone formation and bone mass. J Cell Physiol 207 (2006) 784-792
44. Shukunami C., Ishizeki K., Atsumi T., Ohta Y., Suzuki F., and Hiraki Y. Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J Bone Miner Res 12 (1997) 1174-1188
45. Das S.K., Wang X.N., Paria B.C., Damm D., Abraham J.A., Klagsbrun M., Andrews G.K., and Dey S.K. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120 (1994) 1071-1083
46. Addison W.N., Azari F., Sorensen E.S., Kaartinen M.T., and McKee M.D. Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. J Biol Chem 282 (2007) 15872-15883
47. MacRae V.E., Farquharson C., and Ahmed S.F. The restricted potential for recovery of growth plate chondrogenesis and longitudinal bone growth following exposure to pro-inflammatory cytokines. J Endocrinol 189 (2006) 319-328
48. McKee M.D., Addison W.N., and Kaartinen M.T. Hierarchies of extracellular matrix and mineral organization in bone of the craniofacial complex and skeleton. Cells Tissues Organs 181 (2005) 176-188
49. Ueda K., Yamanaka Y., Harada D., Yamagami E., Tanaka H., and Seino Y. PTH has the potential to rescue disturbed bone growth in achondroplasia. Bone 41 (2007) 13-18
50. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
51. Porzio M.A., and Pearson A.M. Improved resolution of myofibrillar proteins with sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Biochim Biophys Acta 490 (1977) 27-34
52. Reiland J., Sanderson R.D., Waguespack M., Barker S.A., Long R., Carson D.D., and Marchetti D. Heparanase degrades syndecan-1 and perlecan heparan sulfate: functional implications for tumor cell invasion. J Biol Chem 279 (2004) 8047-8055
53. Denker A.E., Haas A.R., Nicoll S.B., and Tuan R.S. Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64 (1999) 67-76
54. Atkinson B.L., Fantle K.S., Benedict J.J., Huffer W.E., and Gutierrez-Hartmann A. Combination of osteoinductive bone proteins differentiates mesenchymal C3H/10T1/2 cells specifically to the cartilage lineage. J Cell Biochem 65 (1997) 325-339
55. Izzo M.W., Pucci B., Tuan R.S., and Hall D.J. Gene expression profiling following BMP-2 induction of mesenchymal chondrogenesis in vitro. Osteoarthritis Cartilage 10 (2002) 23-33
56. Miller S.A., Brown A.J., Farach-Carson M.C., and Kirn-Safran C.B. HIP/RPL29 down-regulation accompanies terminal chondrocyte differentiation. Differentiation 71 (2003) 322-336
57. Seghatoleslami M.R., and Tuan R.S. Cell density dependent regulation of AP-1 activity is important for chondrogenic differentiation of C3H10T1/2 mesenchymal cells. J Cell Biochem 84 (2002) 237-248
58. Naik M.U., and Naik U.P. Calcium- and integrin-binding protein regulates focal adhesion kinase activity during platelet spreading on immobilized fibrinogen. Blood 102 (2003) 3629-3636
59. Lazarus J.E., Hegde A., Andrade A.C., Nilsson O., and Baron J. Fibroblast growth factor expression in the postnatal growth plate. Bone 40 (2007) 577-586
60. Colnot C., Lu C., Hu D., and Helms J.A. Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Dev Biol 269 (2004) 55-69
61. Akiyama H., Shigeno C., Iyama K., Ito H., Hiraki Y., Konishi J., and Nakamura T. Indian hedgehog in the late-phase differentiation in mouse chondrogenic EC cells, ATDC5: upregulation of type X collagen and osteoprotegerin ligand mRNAs. Biochem Biophys Res Commun 257 (1999) 814-820
62. Colnot C., de la Fuente L., Huang S., Hu D., Lu C., St-Jacques B., and Helms J.A. Indian hedgehog synchronizes skeletal angiogenesis and perichondrial maturation with cartilage development. Development 132 (2005) 1057-1067
63. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15 (2001) 3059-3087
64. Datta M.W., Hernandez A.M., Schlicht M.J., Kahler A.J., DeGueme A.M., Dhir R., Shah R.B., Farach-Carson C., Barrett A., and Datta S. Perlecan, a candidate gene for the CAPB locus, regulates prostate cancer cell growth via the Sonic Hedgehog pathway. Mol Cancer 5 (2006) 9
65. Strigini M. Mechanisms of morphogen movement. J Neurobiol 64 (2005) 324-333
66. Arikawa-Hirasawa E., Watanabe H., Takami H., Hassell J.R., and Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat Genet 23 (1999) 354-358
67. Cano-Gauci D.F., Song H.H., Yang H., McKerlie C., Choo B., Shi W., Pullano R., Piscione T.D., Grisaru S., Soon S., Sedlackova L., Tanswell A.K., Mak T.W., Yeger H., Lockwood G.A., Rosenblum N.D., and Filmus J. Glypican-3-deficient mice exhibit developmental overgrowth and some of the abnormalities typical of Simpson-Golabi-Behmel syndrome. J Cell Biol 146 (1999) 255-264
68. Costell M., Gustafsson E., Aszodi A., Morgelin M., Bloch W., Hunziker E., Addicks K., Timpl R., and Fassler R. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147 (1999) 1109-1122
69. Koyama E., Leatherman J.L., Shimazu A., Nah H.D., and Pacifici M. Syndecan-3, tenascin-C, and the development of cartilaginous skeletal elements and joints in chick limbs. Dev Dyn 203 (1995) 152-162
70. Seghatoleslami M.R., and Kosher R.A. Inhibition of in vitro limb cartilage differentiation by syndecan-3 antibodies. Dev Dyn 207 (1996) 114-119
71. Wu Z.L., Zhang L., Yabe T., Kuberan B., Beeler D.L., Love A., and Rosenberg R.D. The involvement of heparan sulfate (HS) in FGF1/HS/FGFR1 signaling complex. J Biol Chem 278 (2003) 17121-17129
72. Ortega N., Behonick D., Stickens D., and Werb Z. How proteases regulate bone morphogenesis. Ann N Y Acad Sci 995 (2003) 109-116
73. Liu Z., Lavine K.J., Hung I.H., and Ornitz D.M. FGF18 is required for early chondrocyte proliferation, hypertrophy and vascular invasion of the growth plate. Dev Biol 302 (2007) 80-91
74. Hansen N.M., Felix R., Bisaz S., and Fleisch H. Aggregation of hydroxyapatite crystals. Biochim Biophys Acta 451 (1976) 549-559
75. Levidiotis V., Freeman C., Punler M., Martinello P., Creese B., Ferro V., van der Vlag J., Berden J.H., Parish C.R., and Power D.A. A synthetic heparanase inhibitor reduces proteinuria in passive Heymann nephritis. J Am Soc Nephrol 15 (2004) 2882-2892
76. Mushtaq T., Farquharson C., Seawright E., and Ahmed S.F. Glucocorticoid effects on chondrogenesis, differentiation and apoptosis in the murine ATDC5 chondrocyte cell line. J Endocrinol 175 (2002) 705-713
77. Guicheux J., Palmer G., Shukunami C., Hiraki Y., Bonjour J.P., and Caverzasio J. A novel in vitro culture system for analysis of functional role of phosphate transport in endochondral ossification. Bone 27 (2000) 69-74
78. Patel V.N., Knox S.M., Likar K.M., Lathrop C.A., Hossain R., Eftekhari S., Whitelock J.M., Elkin M., Vlodavsky I., and Hoffman M.P. Heparanase cleavage of perlecan heparan sulfate modulates FGF10 activity during ex vivo submandibular gland branching morphogenesis. Development 134 (2007) 4177-4186
79. Thomas D.M., Johnson S.A., Sims N.A., Trivett M.K., Slavin J.L., Rubin B.P., Waring P., McArthur G.A., Walkley C.R., Holloway A.J., Diyagama D., Grim J.E., Clurman B.E., Bowtell D.D., Lee J.S., Gutierrez G.M., Piscopo D.M., Carty S.A., and Hinds P.W. Terminal osteoblast differentiation, mediated by runx2 and p27KIP1, is disrupted in osteosarcoma. J Cell Biol 167 (2004) 925-934
80. Lian J.B., McKee M.D., Todd A.M., and Gerstenfeld L.C. Induction of bone-related proteins, osteocalcin and osteopontin, and their matrix ultrastructural localization with development of chondrocyte hypertrophy in vitro. J Cell Biochem 52 (1993) 206-219
81. Miao H.Q., Liu H., Navarro E., Kussie P., and Zhu Z. Development of heparanase inhibitors for anti-cancer therapy. Curr Med Chem 13 (2006) 2101-2111
82. Morales T.I. Chondrocyte moves: clever strategies. Osteoarthritis Cartilage (2007)
83. Farach-Carson M.C., Hecht J.T., and Carson D.D. Heparan sulfate proteoglycans: key players in cartilage biology. Crit Rev Eukaryot Gene Expr 15 (2005) 29-48
84. Yang W., Gomes R.R., Brown A.J., Burdett A.R., Alicknavitch M., Farach-Carson M.C., and Carson D.D. Chondrogenic differentiation on perlecan domain I, collagen II, and bone morphogenetic protein-2-based matrices. Tissue Eng 12 (2006) 2009-2024
85. Boudreaux J.M., and Towler D.A. Synergistic induction of osteocalcin gene expression: identification of a bipartite element conferring fibroblast growth factor 2 and cyclic AMP responsiveness in the rat osteocalcin promoter. J Biol Chem 271 (1996) 7508-7515