Glycosaminoglycans modulate RANKL-induced osteoclastogenesis

Journal of Cellular Biochemistry

Volumn 109, Issue 6, 2010, Pages 1222-1231

  Ling, Ling ^a   Murali, Sadasivam ^a   Stein, Gary S ^b   Van Wijnen, Andre J ^b   Cool, Simon M ^a,c  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

ERK; Glycosaminoglycans; Osteoclastogenesis; RANKL

Indexed keywords

GLYCOSAMINOGLYCAN; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCLAST DIFFERENTIATION FACTOR;

ANIMAL CELL; ARTICLE; BONE; CELL CULTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; OSTEOCLAST; OSTEOPENIA; PRIORITY JOURNAL; SWINE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CHROMATOGRAPHY, ION EXCHANGE; GLYCOSAMINOGLYCANS; IMMUNOBLOTTING; MICE; MICROSCOPY, CONFOCAL; OSTEOCLASTS; RANK LIGAND; SWINE;

EID: 77951756269     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22506     Document Type: Article

References (55)

1. Ariyoshi W, Takahashi T, Kanno T, Ichimiya H, Takano H, Koseki T, Nishihara T. 2005. Mechanisms involved in enhancement of osteoclast formation and function by low molecular weight hyaluronic acid. J Biol Chem 280:18967-18972. (Pubitemid 41379600)
2. Ariyoshi W, Takahashi T, Kanno T, Ichimiya H, Shinmyouzu K, Takano H, Koseki T, Nishihara T. 2008. Heparin inhibits osteoclastic differentiation and function. J Cell Biochem 103:1707-1717. (Pubitemid 351501904)
3. Braunsteiner H, Thumb N. 1963. Mast cells, basophils and heparin liberation. Bibl Haematol 15:9-15.
4. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS. 1998. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev 12:1260-1268. (Pubitemid 28213402)
5. Burgess TL, Qian Y, Kaufman S, Ring BD, Van G, Capparelli C, Kelley M, Hsu H, Boyle WJ, Dunstan CR, Hu S, Lacey DL. 1999. The ligand for osteoprotegerin (OPGL) directly activates mature osteoclasts. J Cell Biol 145:527-538. (Pubitemid 29215717)
6. Collin-Osdoby P, Yu X, Zheng H, Osdoby P. 2003. RANKL-mediated osteoclast formation from murine RAW 264.7 cells. Methods Mol Med 80:153-166.
7. Cool SM, Nurcombe V. 2006. Heparan sulfate regulation of progenitor cell fate. J Cell Biochem 99:1040-1051. (Pubitemid 44673962)
8. Cool SM, Kenny B, Wu A, Nurcombe V, Trau M, Cassady AI, Grondahl L. 2007. Poly(3-hydroxybutyrate-co-3-hydroxyvalerate) composite biomaterials for bone tissue regeneration: In vitro performance assessed by osteoblast proliferation, osteoclast adhesion and resorption, and macrophage proinflammatory response. J Biomed Mater Res A 82:599-610.
9. Dougall WC, Glaccum M, Charrier K, Rohrbach K, Brasel K, De Smedt T, Daro E, Smith J, Tometsko ME, Maliszewski CR, Armstrong A, Shen V, Bain S, Cosman D, Anderson D, Morrissey PJ, Peschon JJ, Schuh J. 1999. RANK is essential for osteoclast and lymph node development. Genes Dev 13:2412-2424. (Pubitemid 29453612)
10. Ecarot-Charrier B, Broekhuyse H. 1987. Proteoglycans synthesized by cultured mouse osteoblasts. J Biol Chem 262:5345-5351.
11. Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. 2003. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest 111:1221-1230. (Pubitemid 36519939)
12. Fuller K, Wong B, Fox S, Choi Y, Chambers TJ. 1998. TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J Exp Med 188:997-1001. (Pubitemid 28433427)
13. Gandhi NS, Mancera RL. 2008. The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des 72:455-482.
14. Haupt LM, Murali S, Mun FK, Teplyuk N, Mei LF, Stein GS, van Wijnen AJ, Nurcombe V, Cool SM. 2009. The heparan sulfate proteoglycan (HSPG) glypican-3 mediates commitment of MC3T3-E1 cells toward osteogenesis. J Cell Physiol 220:780-791.
15. Henriksen K, Neutzsky-Wulff AV, Bonewald LF, Karsdal MA. 2009. Local communication on and within bone controls bone remodeling. Bone 44:1026-1033.
16. Hotokezaka H, Sakai E, Kanaoka K, Saito K, Matsuo K, Kitaura H, Yoshida N, Nakayama K. 2002. U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J Biol Chem 277:47366-47372. (Pubitemid 36159251)
17. Hsu H, Lacey DL, Dunstan CR, Solovyev I, Colombero A, Timms E, Tan HL, Elliott G, Kelley MJ, Sarosi I, Wang L, Xia XZ, Elliott R, Chiu L, Black T, Scully S, Capparelli C, Morony S, Shimamoto G, Bass MB, Boyle WJ. 1999. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci USA 96:3540-3545. (Pubitemid 29168945)
18. Hughes AE, Ralston SH, Marken J, Bell C, MacPherson H, Wallace RG, van Hul W, Whyte MP, Nakatsuka K, Hovy L, Anderson DM. 2000. Mutations in TNFRSF11A, affecting the signal peptide of RANK, cause familial expansile osteolysis. Nat Genet 24:45-48. (Pubitemid 30041418)
19. Hunter GK, Heersche JN, Aubin JE. 1983. Isolation of three species of proteoglycan synthesized by cloned bone cells. Biochemistry 22:831-837.
20. Iozzo RV. 1998. Matrix proteoglycans: From molecular design to cellular function. Annu Rev Biochem 67:609-652.
21. Irie A, Takami M, Kubo H, Sekino-Suzuki N, Kasahara K, Sanai Y. 2007. Heparin enhances osteoclastic bone resorption by inhibiting osteoprotegerin activity. Bone 41:165-174. (Pubitemid 47001824)
22. Jackson RA, Nurcombe V, Cool SM. 2006. Coordinated fibroblast growth factor and heparan sulfate regulation of osteogenesis. Gene 379:79-91. (Pubitemid 44262446)
23. Jackson RA, Murali S, van Wijnen AJ, Stein GS, Nurcombe V, Cool SM. 2007. Heparan sulfate regulates the anabolic activity of MC3T3-E1 preosteoblast cells by induction of Runx2. J Cell Physiol 210:38-50. (Pubitemid 44904699)
24. Katagiri T, Takahashi N. 2002. Regulatory mechanisms of osteoblast and osteoclast differentiation. Oral Dis 8:147-159. (Pubitemid 34535063)
25. Khosla S. 2001. Minireview: The OPG/RANKL/RANK system. Endocrinology 142:5050-5055.
26. Kim N, Odgren PR, Kim DK, Marks SC, Jr., Choi Y. 2000. Diverse roles of the tumor necrosis factor family member TRANCE in skeletal physiology revealed by TRANCE deficiency and partial rescue by a lymphocyte-expressed TRANCE transgene. Proc Natl Acad Sci USA 97:10905-10910.
27. Kumarasuriyar A, Lee I, Nurcombe V, Cool SM. 2009. De-sulfation of MG-63 cell glycosaminoglycans delays in vitro osteogenesis, up-regulates cholesterol synthesis and disrupts cell cycle and the actin cytoskeleton. J Cell Physiol 219:572-583.
28. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176. (Pubitemid 28180851)
29. Lamoureux F, Baud'huin M, Duplomb L, Heymann D, Redini F. 2007. Proteoglycans: Key partners in bone cell biology. Bioessays 29:758-771.
30. Lee SE, Woo KM, Kim SY, Kim HM, Kwack K, Lee ZH, Kim HH. 2002. The phosphatidylinositol 3-kinase, p38, and extracellular signal-regulated kinase pathways are involved in osteoclast differentiation. Bone 30:71-77. (Pubitemid 34044303)
31. Ling L, Murali S, Dombrowski C, Haupt LM, Stein GS, van Wijnen AJ, Nurcombe V, Cool SM. 2006. Sulfated glycosaminoglycans mediate the effects of FGF2 on the osteogenic potential of rat calvarial osteoprogenitor cells. J Cell Physiol 209:811-825. (Pubitemid 44665703)
32. Manton KJ, Sadasivam M, Cool SM, Nurcombe V. 2006. Bone-specific heparan sulfates induce osteoblast growth arrest and downregulation of retinoblastoma protein. J Cell Physiol 209:219-229. (Pubitemid 44318682)
33. Matsumoto M, Sudo T, Saito T, Osada H, Tsujimoto M. 2000. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J Biol Chem 275:31155-31161.
34. Mizuno A, Amizuka N, Irie K, Murakami A, Fujise N, Kanno T, Sato Y, Nakagawa N, Yasuda H, Mochizuki S, Gomibuchi T, Yano K, Shima N, Washida N, Tsuda E, Morinaga T, Higashio K, Ozawa H. 1998. Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem Biophys Res Commun 247:610-615. (Pubitemid 28418439)
35. Nakamura H, Hirata A, Tsuji T, Yamamoto T. 2001. Immunolocalization of keratan sulfate proteoglycan in rat calvaria. Arch Histol Cytol 64:109-118. (Pubitemid 32230343)
36. Nakatsuka K, Nishizawa Y, Ralston SH. 2003. Phenotypic characterization of early onset Paget's disease of bone caused by a 27-bp duplication in the TNFRSF11A gene. J Bone Miner Res 18:1381-1385. (Pubitemid 41070792)
37. Nicolin V, Bareggi R, Baldini G, Bortul R, Martinelli B, Narducci P. 2007. Effects of neridronic acid on osteoclasts derived by physiological dual-cell cultures. Acta Histochem 109:397-402. (Pubitemid 47496173)
38. Nurcombe V, Goh FJ, Haupt LM, Murali S, Cool SM. 2007. Temporal and functional changes in glycosaminoglycan expression during osteogenesis. J Mol Histol 38:469-481. (Pubitemid 350056775)
39. Pearse RN, Sordillo EM, Yaccoby S, Wong BR, Liau DF, Colman N, Michaeli J, Epstein J, Choi Y. 2001. Multiple myeloma disrupts the TRANCE/osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proc Natl Acad Sci USA 98:11581-11586. (Pubitemid 32928771)
40. Perrimon N, Bernfield M. 2000. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725-728. (Pubitemid 30212391)
41. Roodman GD. 1999. Cell biology of the osteoclast. Exp Hematol 27:1229-1241.
42. Sasaki N, Kusano E, Ando Y, Nemoto J, Iimura O, Ito C, Takeda S, Yano K, Tsuda E, Asano Y. 2002. Changes in osteoprotegerin and markers of bone metabolism during glucocorticoid treatment in patients with chronic glomerulonephritis. Bone 30:853-858. (Pubitemid 34616013)
43. Schoppet M, Al-Fakhri N, Franke FE, Katz N, Barth PJ, Maisch B, Preissner KT, Hofbauer LC. 2004. Localization of osteoprotegerin, tumor necrosis factor-related apoptosis-inducing ligand, and receptor activator of nuclear factor-kappaB ligand in Monckeberg's sclerosis and atherosclerosis. J Clin Endocrinol Metab 89:4104-4112. (Pubitemid 39071519)
44. Seibel MJ, Robins SP, Bilezikian JP. 2006. Dynamics of bone and cartilage metabolism (2nd edition). Academic Press. p. 85.
45. Shinmyouzu K, Takahashi T, Ariyoshi W, Ichimiya H, Kanzaki S, Nishihara T. 2007. Dermatan sulfate inhibits osteoclast formation by binding to receptor activator of NF-kappa B ligand. Biochem Biophys Res Commun 354:447-452. (Pubitemid 46164840)
46. Sims NA, Gooi JH. 2008. Bone remodeling: Multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 19:444-451.
47. Suda T, Takahashi N, Martin TJ. 1992. Modulation of osteoclast differentiation. Endocr Rev 13:66-80.
48. Takada T, Katagiri T, Ifuku M, Morimura N, Kobayashi M, Hasegawa K, Ogamo A, Kamijo R. 2003. Sulfated polysaccharides enhance the biological activities of bone morphogenetic proteins. J Biol Chem 278:43229-43235. (Pubitemid 37345942)
49. Takahashi N, Udagawa N, Suda T. 1999. A new member of tumor necrosis factor ligand family, ODF/OPGL/TRANCE/RANKL, regulates osteoclast differentiation and function. Biochem Biophys Res Commun 256:449-455. (Pubitemid 29301126)
50. Takayanagi H, Kim S, Koga T, Nishina H, Isshiki M, Yoshida H, Saiura A, Isobe M, Yokochi T, Inoue J, Wagner EF, Mak TW, Kodama T, Taniguchi T. 2002. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 3:889-901. (Pubitemid 35460788)
51. Teplyuk NM, Haupt LM, Ling L, Dombrowski C, Mun FK, Nathan SS, Lian JB, Stein JL, Stein GS, Cool SM, van Wijnen AJ. 2009. The osteogenic transcription factor Runx2 regulates components of the fibroblast growth factor/ proteoglycan signaling axis in osteoblasts. J Cell Biochem 107:144-154.
52. Theoleyre S, Kwan Tat S, Vusio P, Blanchard F, Gallagher J, Ricard-Blum S, Fortun Y, Padrines M, Redini F, Heymann D. 2006. Characterization of osteoprotegerin binding to glycosaminoglycans by surface plasmon resonance: Role in the interactions with receptor activator of nuclear factor kappaB ligand (RANKL) and RANK. Biochem Biophys Res Commun 347:460-467. (Pubitemid 44063559)
53. Watts NB, Harris ST, Genant HK, Wasnich RD, Miller PD, Jackson RD, Licata AA, Ross P, Woodson GC III, Yanover MJ, Mysiw WJ, Kohse L, Rao MB, Steiger P, Richmond B, Chesnut CH. 1990. Intermittent cyclical etidronate treatment of postmenopausal osteoporosis. N Engl J Med 323:73-79. (Pubitemid 20221642)
54. Whyte MP, Hughes AE. 2002. Expansile skeletal hyperphosphatasia is caused by a 15-base pair tandem duplication in TNFRSF11A encoding RANK and is allelic to familial expansile osteolysis. J Bone Miner Res 17:26-29.
55. Whyte MP, Obrecht SE, Finnegan PM, Jones JL, Podgornik MN, McAlister WH, Mumm S. 2002. Osteoprotegerin deficiency and juvenile Paget's disease. N Engl J Med 347:175-184. (Pubitemid 34764821)