Blood-derived human osteoclast resorption activity is impaired by Hyaluronan-CD44 engagement via a p38-dependent mechanism

Journal of Cellular Physiology

Volumn 226, Issue 3, 2011, Pages 769-779

  Pivetta, Eliana ^a   Scapolan, Martina ^a   Wassermann, Bruna ^a   Steffan, Agostino ^a   Colombatti, Alfonso ^a,b   Spessotto, Paola ^a  

^a CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^b UNIVERSITY OF UDINE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN K; COLLAGEN; FOCAL ADHESION KINASE 2; GELATINASE B; HERMES ANTIGEN; HYALURONIC ACID; PHOSPHATASE; SERINE; SYNAPTOPHYSIN; TARTRATE RESISTANT ACID PHOSPHATASE POSITIVE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG;

ARTICLE; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MONOCYTE; OSTEOCLAST ACTIVITY; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACID PHOSPHATASE; ANTIGENS, CD44; BONE RESORPTION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SHAPE; CELL SURVIVAL; DOWN-REGULATION; HUMANS; HYALURONIC ACID; ISOENZYMES; MODELS, BIOLOGICAL; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING;

EID: 78650637999     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22398     Document Type: Article

References (47)

1. Andersen TL, del Carmen Ovejero M, Kirkegaard T, Lenhard T, Foged NT, Delaisse JM. 2004. A scrutiny of matrix metalloproteinases in osteoclasts: Evidence for heterogeneity and for the presence of MMPs synthesized by other cells. Bone 35: 1107-1119.
2. Arai F, Miyamoto T, Ohneda O, Inada T, Sudo T, Brasel K, Miyata T, Anderson DM, Suda T. 1999. Commitment and differentiation of OC precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappa B (RANK) receptors. J Exp Med 190: 1741-1754.
3. Avnet S, Lamolinara A, Zini N, Solimando L, Quacquaruccio G, Granchi D, Maraldi NM, Giunti A, Baldini N. 2006. Effects of antisense mediated inhibition of cathepsin K on human osteoclasts obtained from peripheral blood. J Orthop Res 24: 1699-1708.
4. Bastow ER, Byers S, Golub SB, Clarkin CE, Pitsillides AA, Fosang AJ. 2008. Hyaluronan synthesis and degradation in cartilage and bone. Cell Mol Life Sci 65: 395-413.
5. Chang EJ, Kim HJ, Ha J, Kim HJ, Ryu J, Park KH, Kim UH, Lee ZH, Kim HM, Fisher DE, Kim HH. 2007. Hyaluronan inhibits osteoclast differentiation via Toll-like receptor 4. J Cell Sci 120: 166-176.
6. Chellaiah MA, Kizer N, Biswas R, Alvarez U, Strauss-Schoenberger J, Rifas L, Rittling SR, Denhardt DT, Hruska KA. 2003. Osteopontin deficiency produces osteoclast dysfunction due to reduced CD44 surface expression. Mol Biol Cell 14: 173-189.
7. de Vries TJ, Schoenmaker T, Beertsen W, van der Neut R, Everts V. 2005. Effect of CD44 deficiency on in vitro and in vivo OC formation. J Cell Biochem 94: 954-966.
8. Delaisse JM, Engsig MT, Everts V, Ovejero MC, Ferreras M, Lund L, Vu TH, Werb Z, Winding B, Lochter A, Karsdal MA, Troen T, Kirkegaard T, Lenhard T, Heegaard AM, Neff L, Baron R, Foged NT. 2000. Proteinases in bone resorption: Obvious and less obvious roles. Clinica Chimica Acta 291: 223-234.
9. Delaisse JM, Andersen T, Engsig MT, Henriksen K, Troen T, Blavier L. 2003. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to OC activities. Microsc Res Tec 61: 504-513.
10. Denning SM, Telen MJ, Hale LP, Liao HX, Haynes BF. 1995. CD44 and CD44R cluster report. In: Schlossman SF, Boumsell L, Gilks W, Harlan JM, Kishimoto T, Morimoto C, Ritz J, Shaw S, Silverstein R, Springer T, Tedder TF, Todd RF, editors. Leucocyte typing V. Oxford: Oxford University Press. pp. 1713-1719.
11. Everts V, Korper W, Hoeben KA, Jansen ID, Bromme D, Cleutjens KB, Heeneman S, Peters C, Reinheckel T, Saftig P, Beertsen W. 2006. Osteoclastic bone degradation and the role of different cysteine proteinases and matrix metalloproteinases: Differences between calvaria and long bone. J Bone Miner Res 21: 1399-1408.
12. Fraser JRE, Laurent TC, Laurent UBG. 1997. Hyaluronan: Its nature, distribution, functions and turnover. J Inter Med 242: 27-33.
13. Ghosh P, Guidolin D. 2002. Potential mechanism of action of intra-articluar hyaluronan therapy in osteoarthritis: Are the effects molecular weight dependent? Semin Arthritis Rheum 32: 10-37.
14. Ikeda F, Nishimura R, Matsubara T, Hata K, Reddy SV, Yoneda T. 2006. Activation of NFAT signal in vivo leads to osteopenia associated with increased osteoclastogenesis and bone-resorbing activity. J Immunol 177: 2384-2390.
15. Julovi SM, Yasuda T, Shimizu M, Hiramitsu T, Nakamura T. 2004. Inhibition of interleukin-1beta-stimulated production of matrix metalloproteinases by hyaluronan via CD44 in human articular cartilage. Arthritis Rheum 50: 516-525.
16. Kania JR, Kehat-Stadler T, Kupfer SR. 1997. CD44 antibodies inhibit OC formation. J Bone Miner Res 12: 1155-1164.
17. Komarova SV, Pereverzev A, Shum JW, Sims SM, Dixon SJ. 2005. Convergent signaling by acidosis and receptor activator of NF-kappaB ligand (RANKL) on the calcium/calcineurin/NFAT pathway in osteoclasts. Proc Natl Acad Sci USA 102: 2643-2648.
18. Kothapalli D, Flowers J, Xu T, Puré E, Assoian RK. 2008. Differential activation of ERK and Rac mediates the proliferative and anti-proliferative effects of hyaluronan and CD44. J Biol Chem 283: 31823-31829.
19. Lee ZH, Kim HH. 2003. Signal transduction by receptor activator of nuclear factor kappa B in osteoclast. Biochem Biophys Res Commun 305: 211-214.
20. Lee JY, Spicer AP. 2000. Hyaluronan: A multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol 12: 581-586.
21. Lesley J, Hyman R. 1998. CD44 structure and function. Front Biosci 3: D616-D630.
22. Lewis CA, Townsend PA, Isacke CM. 2001. Ca2+/calmodulin-dependent protein kinase mediates the phosphorylation of CD44 required for cell migration on hyaluronan. Biochem J 357: 843-850.
23. Li X, Udagawa N, Itoh K, Suda K, Murase Y, Nishihara T, Suda T, Takahashi N. 2002. p38 MAPK-mediated signals are required for inducing osteoclast differentiation but not for osteoclast function. Endocrinology 143: 3105-3115.
24. Logar DB, Komadina R, Ostanek JPB, Trost Z, Marc J. 2007. Expression of bone resorption genes in osteoarthritis and osteoporosis. J Bone Miner Metab 25: 219-225.
25. Mangeat P, Roy C, Martin M. 2009. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol 9: 187-192.
26. Nakamura H, Ozawa H. 1996. Immunolocalization of CD44 and the ERM family in bone cells of mouse tibiae. J Bone Miner Res 11: 1715-1722.
27. Negishi-Koga T, Takayanagi H. 2009. Ca2+-NFATc1 signaling is an essential axis of osteoclast differentiation. Immunol Rev 231: 241-256.
28. Noble PW. 2002. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol 21: 25-29.
29. Pandey P, Avraham S, Kumar S, Nakazawa A, Place A, Ghanem L, Rana A, Kumar V, Majumder PK, Avraham H, Davis RJ, Kharbanda S. 1999. Activation of p38 mitogen-activated protein kinase by PYK2/related adhesion focal tyrosine kinase-dependent mechanism. J Biol Chem 274: 10140-10144.
30. Ross FP, Teitelbaum SL. 2005. Alphavbeta3 and macrophage colony-stimulating factor: Patners in osteoclast biology. Immunol Rev 208: 88-105.
31. Samanna V, Ma T, Rogers M, Chellaiah MA. 2007. Actin polymerization modulates CD44 surface expression, MMP-9 activation, and OC function. J Cell Physiol 213: 710-720.
32. Sato T, del Carmen Ovejero M, Hou P, Heegaard AM, Kumegawa M, Foged NT, Delaisse JM. 1997. Identification of the membrane-type matrix metalloproteinase MT1-MMP in OCs. J Cell Sci 110: 589-596.
33. Shalhoub V, Elliott G, Chiu L, Manoukian R, Kelley M, Hawkins N, Davy E, Shimamoto G, Beck J, Kaufman SA, Van G, Scully S, Qi M, Grisanti M, Dunstan C, Boyle WJ, Lacey DL. 2000. Characterization of osteoclast precursors in human blood. Br J Haematol 111: 501-512.
34. Song I, Kim JH, Kim K, Jin HM, Youn BU, Kim N. 2009. Regulatory mechanism of NFATc1 in RANKL-induced osteoclast activation. FEBS Lett 583: 2435-2440.
35. Spessotto P, Rossi FM, Degan M, Di Francia R, Perris R, Colombatti A, Gattei V. 2002. Hyaluronan-CD44 interaction hampers migration of OC-like cells by downregulating MMP-9. J Cell Biol 158: 1133-1144.
36. Spessotto P, Lacrima K, Nicolosi PA, Pivetta E, Scapolan M, Perris R. 2009. Fluorescence-based assays for in vitro analysis of cell adhesion and migration. Methods Mol Biol 522: 221-250.
37. Stancíková M, Svík K, Istok R, Rovenskỳ J, Velebnỳ V. 2004. The effects of hyaluronan on bone resorption and bone mineral density in a rat model of estrogen deficiency-induced osteopenia. Int J Tissue React 26: 9-16.
38. Stern R, Asari AA, Sugahara KN. 2006. Hyaluronan fragments: An information-rich system. Eur J Cell Biol 85: 699-715.
39. Suter A, Everts V, Boyde A, Jones SJ, Lullmann-Rauch R, Hartmann D, Hayman AR, CoX TM, Evans MJ, Meister T, von Figura K, Saftig P. 2001. Overlapping functions of lysosomal acid phosphatase (LAP) and tartrateresistant acid phosphatase (Acp5) revealed by doubly deficient mice. Development 128: 4899-4910.
40. 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 RANK signaling in terminal differentiation of osteoclasts. Dev Cell 3: 889-901.
41. Teitelbaum SL, Ross P. 2003. Genetic regulation of osteoclast development and function. Nat Rev Genet 4: 638-649.
42. Tezuka K, Nemoto K, Tezuka Y, Sato T, Ikeda Y, Kobori M, Kawashima H, Eguchi H, Hakeda Y, Kumegawa M. 1994. Identification of matrix metalloproteinase 9 in rabbit OCs. J Biol Chem 269: 15006-15009.
43. Thorne RF, Legg JW, Isacke CM. 2004. The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J Cell Sci 117: 373-380.
44. Wittrant Y, Theoleyre S, Couillaud S, Dunstan C, Heymann D, Rédini F. 2003. Regulation of osteoclast protease expression by RANKL. Biochem Biophys Res Commun 310: 774-778.
45. Yasui T, Akatsuk M, Tobetto K, Hayaishi M, Ando T. 1992. The effect of hyaluronan on interleukin-1 alpha-induced prostaglandin E2 production in human osteoarthritic synovial cells. Agents Actions 37: 155-156.
46. Yu X, Huang Y, Collin-Osdoby P, Osdoby P. 2003. Stromal cell-derived factor I (SDF-I) recruits osteoclast precursors by inducing chemotaxis, matrix metalloproteinase-9 (MMP-9) activity, and collagen transmigration. J Bone Miner Res 18: 1404-1418.
47. Zaidi M. 2007. Skeletal remodeling in health and disease. Nat Med 13: 791-801.