Secreted frizzled-related protein-1 inhibits RANKL-dependent osteoclast formation

Journal of Bone and Mineral Research

Volumn 19, Issue 11, 2004, Pages 1873-1881

  Häusler, Karl D ^a   Horwood, Nicole J ^a   Chuman, Yoshiro ^b   Fisher, Jane L ^a   Ellis, Jennifer ^b   Martin, T John ^a   Rubin, Jeffrey S ^b   Gillespie, Matthew T ^a  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Osteoclast; RANKL; Secreted Frizzled related protein; Wnt

Indexed keywords

CALCITRIOL; CALCITRIOL DERIVATIVE; COLONY STIMULATING FACTOR 1; INTERLEUKIN 1; INTERLEUKIN 11; INTERLEUKIN 6; MESSENGER RNA; NEUTRALIZING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; PROSTAGLANDIN E2; PROTEIN; RECOMBINANT PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WNT PROTEIN; CARRIER PROTEIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MEMBRANE PROTEIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SFRP1 PROTEIN, MOUSE; SIGNAL PEPTIDE; TNFRSF11A PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BONE REMODELING; CARTILAGE CELL; CELL LINEAGE; COCULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IN SITU HYBRIDIZATION; NONHUMAN; OSTEOBLAST; OSTEOCLAST; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SPLEEN CELL; STROMA CELL; ANIMAL; BONE; BONE MARROW CELL; C57BL MOUSE; CELL LINE; CHEMISTRY; DOSE RESPONSE; DRUG ANTAGONISM; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; METABOLISM; MOUSE; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; BONE AND BONES; BONE MARROW CELLS; CALCITRIOL; CARRIER PROTEINS; CELL LINE; CHONDROCYTES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUTATHIONE TRANSFERASE; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-11; INTERLEUKIN-6; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOCLASTS; PARATHYROID HORMONE; POLYMERASE CHAIN REACTION; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 16644399496     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/JBMR.040807     Document Type: Article

References (50)

1. 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.
2. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, Tomoyasu A, Yano K, Goto M, Murakami A, Tsuda E, Morinaga T, Higashio K, Udagawa N, Takahashi N, Suda T 1998 Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA 95:3597-3602.
3. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Boyle WJ 1997 Osteoprotegerin: A novel secreted protein involved in the regulation of bone density. Cell 89:309-319.
4. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ 1999 Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:345-357.
5. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM 1999 OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397:315-323.
6. Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D, Galibert L 1997 A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature 390:175-179.
7. Smalley MJ, Dale TC 1999 Wnt signalling in mammalian development and cancer. Cancer Metastasis Rev 18:215-230.
8. Wodarz A, Nusse R 1998 Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14:59-88.
9. Dale TC 1998 Signal transduction by the Wnt family of ligands. Biochem J 329:209-223.
10. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA II, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L 2002 Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157:303-314.
11. Little RD, Recker RR, Johnson ML 2002 High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 347:943-944.
12. Little RD, Carulli JP, Del Mastro RG, Dupuis J, Osbome M, Folz C, Manning SP, Swain PM, Zhao SC, Eustace B, Lappe MM, Spitzer L, Zweier S, Braunschweiger K, Benchekroun Y, Hu X, Adair R, Chee L, FitzGerald MG, Tulig C, Caruso A, Tzellas N, Bawa A, Franklin B, McGuire S, Nogues X, Gong G, Allen KM, Anisowicz A, Morales AJ, Lomedico PT, Recker SM, Van Eerdewegh P, Recker RR, Johnson ML 2002 A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am J Hum Genet 70:11-19.
13. Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG, Jenkins NA, Nathans J 1997 A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci USA 94:2859-2863.
14. Jones SE, Jomary C 2002 Secreted Frizzled-related proteins: Searching for relationships and patterns. Bioessays 24:811-820.
15. Leyns L, Bouwmeester T, Kim SH, Piccolo S, De Robertis EM 1997 Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88:747-756.
16. Wang S, Krinks M, Lin K, Luyten FP, Moos M Jr 1997 Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88:757-766.
17. Bafico A, Gazit A, Pramila T, Finch PW, Yaniv A, Aaronson SA 1999 Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J Biol Chem 274:16180-16187.
18. Uren A, Reichsman F, Anest V, Taylor WG, Muraiso K, Bottaro DP, Cumberledge S, Rubin JS 2000 Secreted frizzled-related protein-1 binds directly to Wingless and is a biphasic modulator of Wnt signaling. J Biol Chem 275:4374-4382.
19. Hoang B, Moos M Jr, Vukicevic S, Luyten FP 1996 Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J Biol Chem 271:26131-26137.
20. James IE, Kumar S, Barnes MR, Gress CJ, Hand AT, Dodds RA, Connor JR, Bradley BR, Campbell DA, Grabill SE, Williams K, Blake SM, Gowen M, Lark MW 2000 FrzB-2: A human secreted frizzled-related protein with a potential role in chondrocyte apoptosis. Osteoarthritis Cartilage 8:452-463.
21. Baranski M, Berdougo E, Sandler JS, Darnell DK, Burrus LW 2000 The dynamic expression pattern of frzb-1 suggests multiple roles in chick development. Dev Biol 217:25-41.
22. Udagawa N, Horwood NJ, Elliott J, Mackay A, Owens J, Okamura H, Kurimoto M, Chambers TJ, Martin TJ, Gillespie MT 1997 Interleukin-18 (interferon-gamma- inducing factor) is produced by osteoblasts and acts via granulocyte/macrophage colony-stimulating factor and not via interferon-gamma to inhibit osteoclast formation. J Exp Med 185:1005-1012.
23. Chambers TJ, Owens JM, Hattersley G, Jat PS, Noble MD 1993 Generation of osteoclast-inductive and osteoclastogenic cell lines from the H-2KbtsA58 transgenic mouse. Proc Natl Acad Sci USA 90:5578-5582.
24. Owens JM, Gallagher AC, Chambers TJ 1996 Bone cells required for osteoclastic resorption but not for osteoclastic differentiation. Biochem Biophys Res Commun 222:225-229.
25. Udagawa N, Takahashi N, Akatsu T, Sasaki T, Yamaguchi A, Kodama H, Martin TJ, Suda T 1989 The bone marrow-derived stromal cell lines MC3T3-G2/PA6 and ST2 support osteoclast-like cell differentiation in cocultures with mouse spleen cells. Endocrinology 125:1805-1813.
26. Umezawa A, Maruyama T, Segawa K, Shadduck RK, Waheed A, Hata J 1992 Multipotent marrow stromal cell line is able to induce hematopoiesis in vivo. J Cell Physiol 151:197-205.
27. Horwood NJ, Elliott J, Martin TJ, Gillespie MT 2001 IL-12 alone and in synergy with IL-18 inhibits osteoclast formation in vitro. J Immunol 166:4915-4921.
28. Lam J, Nelson CA, Ross FP, Teitelbaum SL, Fremont DH 2001 Crystal structure of the TRANCE/RANKL cytokine reveals determinants of receptor-ligand specificity. J Clin Invest 108:971-979.
29. Southby J, Murphy LM, Martin TJ, Gillespie MT 1996 Cell-specific and regulator-induced promoter usage and messenger ribonucleic acid splicing for parathyroid hormone-related protein. Endocrinology 137:1349-1357.
30. Traianedes K, Findlay DM, Martin TJ, Gillespie MT 1995 Modulation of the signal recognition particle 54-kDa subunit (SRP54) in rat preosteoblasts by the extracellular matrix. J Biol Chem 270:20891-20894.
31. Takahashi N, Yamana H, Yoshiki S, Roodman GD, Mundy GR, Jones SJ, Boyde A, Suda T 1988 Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology 122:1373-1382.
32. Horwood NJ, Udagawa N, Elliott J, Grail D, Okamura H, Kurimoto M, Dunn AR, Martin T, Gillespie MT 1998 Interleukin 18 inhibits osteoclast formation via T cell production of granulocyte macrophage colony-stimulating factor. J Clin Invest 101:595-603.
33. Udagawa N, Takahashi N, Katagiri T, Tamura T, Wada S, Findlay DM, Martin TJ, Hirota H, Taga T, Kishimoto T 1995Interleukin (IL)-6 induction of osteoclast differentiation depends on IL-6 receptors expressed on osteoblastic cells but not on osteoclast progenitors. J Exp Med 182:1461-1468.
34. Han X, Amar S 2004 Secreted frizzled-related protein 1 (SFRP1) protects fibroblasts from ceramide-induced apoptosis. J Biol Chem 279:2832-2840.
35. Kartsogiannis V, Zhou H, Horwood NJ, Thomas RJ, Hards DK, Quinn JM, Niforas P, Ng KW, Martin TJ, Gillespie MT 1999 Localization of RANKL (receptor activator of NF kappa B ligand) mRNA and protein in skeletal and extraskeletal tissues. Bone 25:525-534.
36. Horwood NJ, Elliott J, Martin TJ, Gillespie MT 1998 Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 139:4743-4746.
37. Khosla S 2001 Minireview: The OPG/RANKL/RANK system. Endocrinology 142:5050-5055.
38. Kawano Y, Kypta R 2003 Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116:2627-2634.
39. Zhou H, Kartsogiannis V, Quinn JM, Ly C, Gange C, Elliott J, Ng KW, Gillespie MT 2002 Osteoclast inhibitory lectin, a family of new osteoclast inhibitors. J Biol Chem 277:48808-48815.
40. Bodine PV, Zhao W, Kharode YP, Bex FJ, Lambert AJ, Goad MB, Gaur T, Stein GS, Lian JB, Komm BS 2004 The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol Endocrinol 18:1222-1237.
41. Xu L, Tan L, Goldring MB, Olsen BR, Li Y 2001 Expression of frizzled genes in mouse costochondral chondrocytes. Matrix Biol 20:147-151.
42. Fischer L, Boland G, Tuan RS 2002 Wnt signaling during BMP-2 stimulation of mesenchymal chondrogenesis. J Cell Biochem 84:816-831.
43. Stott NS, Jiang TX, Chuong CM 1999 Successive formative stages of precartilaginous mesenchymal condensations in vitro: Modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 180:314-324.
44. Bergwitz C, Wendlandt T, Kispert A, Brabant G 2001 Wnts differentially regulate colony growth and differentiation of chondrogenic rat calvaria cells. Biochim Biophys Acta 1538:129-140.
45. Hartmann C, Tabin CJ 2000 Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development 127:3141-3159.
46. Fischer L, Boland G, Tuan RS 2002 Wnt-3A enhances bone morphogenetic protein-2-mediated chondrogenesis of murine C3H10T1/2 mesenchymal cells. J Biol Chem 277:30870-30878.
47. Kawakami Y, Capdevila J, Buscher D, Itoh T, Rodriguez Esteban C, Izpisua Belmonte JC 2001 WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104:891-900.
48. Hartmann C, Tabin CJ 2001 Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104:341-351.
49. Saneyoshi T, Kume S, Amasaki Y, Mikoshiba K 2002 The Wnt/calcium pathway activates NF-AT and promotes ventral cell fate in Xenopus embryos. Nature 417:295-299.
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.