Prostaglandin F2α involves heparan sulphate sugar chains and FGFRs to modulate osteoblast growth and differentiation

Journal of Cellular Physiology

Volumn 217, Issue 1, 2008, Pages 48-59

  Sabbieti, Maria Giovanna ^a   Agas, Dimitrios ^a   Materazzi, Stefano ^b   Capacchietti, Mariolina ^a   Materazzi, Giovanni ^a   Hurley, Marja M ^c   Menghi, Giovanna ^a   Marchetti, Luigi ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; HEPARIN LYASE; HEPARINASE III; MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN F2 ALPHA; PROTEIN P42; PROTEIN P44; PROTEOHEPARAN SULFATE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL METABOLISM; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNTHESIS; ANIMAL; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DINOPROST; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 2; FLUORESCENT ANTIBODY TECHNIQUE; HEPARAN SULFATE PROTEOGLYCANS; MALE; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; OSTEOBLASTS; RECEPTORS, FIBROBLAST GROWTH FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 49649096644     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21471     Document Type: Article

References (53)

1. Agas D, Marchetti L, Menghi G, Materazzi S, Materazzi G, Capacchietti M, Hurley MM, Sabbieti MG. 2008. Antiapoptotic Bcl-2 enhancing requires FGF-2/FGF receptor-1 binding in mouse osteoblasts. J Cell Physiol 214:145-152.
2. Cheng F, Petersson P, Arroyo-Yanguas Y, Westergren-Thorsson G. 2001. Differences in the uptake and nuclear localization of anti-proliferative heparan sulfate between human lung fibroblasts and human lung carcinoma cells. J Cell Biochem 83:597-606.
3. Chua CC, Rahimi N, Forsten-Williams K, Nugent MA. 2004. Heparan sulfate proteoglycans function as receptors for fibroblast growth factor-2 activation of extracellular signal-regulated kinases 1 and 2. Circ Res 94:316-323.
4. David G, Van der Bai XMSB, Cassiman JJ, Van den BH. 1992. Developmental changes in heparan sulfate expression: In situ detection with mAbs. J Cell Biol 119:961-975.
5. Debiais F, Lemonnier J, Hay E, Delannoy P, Caverzasio J, Marie PJ. 2001. Fibroblast growth factor-2 (FGF-2) increases N-cadherin expression through protein kinase C and Src-kinase pathways in human calvaria osteoblasts. J Cell Biochem 81:68-81.
6. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:677-680.
7. Galindo M, Pratap J, Young DW, Hovhannisyan H, Im HJ, Choi JY, Lian JB, Stein JL, Stein GS, van Wijnen AJ. 2005. The bone-specific expression of Runx2 oscillates during the cell cycle to support a G1-related antiproliferative function in osteoblasts. J Biol Chem 280:20274-20285.
8. Globus RK, Plouet J, Gospodarowicz D. 1989. Cultured bovine bone cells synthesize basic fibroblast growth factor and store it in their extracellular matrix. Endocrinology 124:1539-1547.
9. Horowitz A, Tkachenko E, Simons M. 2002. Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol 157:715-725.
10. Hurley MM, Marie P, Florkiewicz R. 2002. Fibroblast growth factor and fibroblast growth factor receptor families. In: Bilezikian JP, Raisz LG, Rodan G, editors. Principles of bone biology. San Diego: Academic Press. pp 825-852.
11. Hurley MM, Okada Y, Xiao L, Tanaka Y, Ito M, Okimoto N, Nakamura T, Rosen CJ, Doetschman T, Coffin JD. 2006. Impaired bone anabolic response to parathyroid hormone in Fgf2-/- and Fgf2+/- mice. Biochem Biophys Res Commun 341:989-994.
12. Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y. 2003. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 302:1044-1046.
13. Ishihara M, Fedarko NS, Conrad HE. 1986. Transport of heparan sulfate into the nuclei of hepatocytes. J Biol Chem 261:13575-13580.
14. 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.
15. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
16. Lai CF, Chaudhary L, Fausto A, Halstead LR, Ory DS, Avioli LV, Cheng SL. 2001. Erk is essential for growth, differentiation, integrin expression, and cell function in human osteoblastic cells. J Biol Chem 276:14443-14450.
17. Leadbeater WE, Gonzalez AM, Logaras N, Berry M, Turnbull JE, Logan A. 2006. Intracellular trafficking in neurones and glia of fibroblast growth factor-2, fibroblast growth factor receptor 1 and heparan sulphate proteoglycans in the injured adult rat cerebral cortex. J Neurochem 96:1189-1200.
18. Lin X. 2004. Functions of heparan sulfate proteoglycans in cell signalling during development. Development 131:6009-6021.
19. Lin X, Buff EM, Perrimon N, Michelson AM. 1999. Heparan sulfate proteoglycans are essential for FGF receptor signalling during Drosophila embryonic development. Development 126:3715-3723.
20. Liu D, Shriver Z, Venkataraman G, El Shabrawi Y, Sasisekharan R. 2002. Tumor cell surface heparan sulfate as cryptic promoters or inhibitors of tumor growth and metastasis. Proc Natl Acad Sci USA 99:568-573.
21. Mani K, Cheng F, Sandgren S, Van Den Born J, Havsmark B, Ding K, Fransson LA. 2004. The heparan sulfate-specific epitope 10E4 is NO-sensitive and partly inaccessible in glypican-1. Glycobiology 14:599-607.
22. Mansukhani A, Bellosta P, Sahni M, Basilico C. 2000. Signalling by fibroblast growth factors (FGF) and fibroblast growth factor receptor 2 (FGFR2)-activating mutations blocks mineralization and induces apoptosis in osteoblasts. J Cell Biol 149:1297-1308.
23. Marchetti L, Sabbieti MG, Agas D, Menghi M, Materazzi G, Menghi G, Hurley MM. 2006. PGF2alpha increases FGF-2 and FGFR2 trafficking in Py1a rat osteoblasts via clathrin independent and importin beta dependent pathway. J Cell Biochem 97:1379-1392.
24. Marie PJ. 2003. Fibroblast growth factor signalling controlling osteoblast differentiation. Gene 316:23-32.
25. Montero A, Okada Y, Tomita M, Ito M, Tsurukami H, Nakamura T, Doetschman T, Coffin JD, Hurley MM. 2000. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest 105:1085-1093.
26. Moscatelli D. 1988. Metabolism of receptor-bound and matrix-bound basic fibroblast growth factor by bovine capillary endothelial cells. J Cell Biol 107:753-759.
27. Mundhenke C, Meyer K, Drew S, Friedl A. 2002. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 receptor binding in breast carcinoma. Am J Pathol 160:185-194.
28. Naganawa T, Xiao L, Abogunde E, Sobue T, Kalajzic I, Sabbieti M, Agas D, Hurley MM. 2006. In vivo and in vitro comparison of the effects of FGF-2 null and haplo-insufficiency on bone formation in mice. Biochem Biophys Res Commun 339:490-498.
29. Newberry EP, Willis D, Latifi T, Boudreaux JM, Towler DA. 1997. Fibroblast growth factor receptor signalling activates the human interstitial collagenase promoter via the bipartite Ets-AP1 element. Mol Endocrinol 1:1129-1144.
30. Nugent MA, Iozzo RV. 2000. Fibroblast growth factor-2. Int J Biochem Cell Biol 32:115-120.
31. Ornitz DM. 2000. FGFs, heparan sulfate and FGFRs: Complex interactions essential for development. Bioessays 22:108-112.
32. Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E, Leder P. 1992. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol 12:240-247.
33. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen DR, Selby PB, Ownen MG. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
34. Partanen J, Vainikka S, Alitalo K. 1993. Structural and functional specificity of FGF receptors. Philos Trans R Soc Lond B Biol Sci 340:297-303.
35. Pawley J. 1995. Fundamental limits in confocal microscopy. In: Pawley JB, editor. Handbook of biological confocal microscopy. 2nd edition. New York and London: Plenum Press. pp 19-37.
36. Pellegrini L. 2001. Role of heparan sulfate in fibroblast growth factor signalling: A structural view. Curr Opin Struct Biol 11:629-634.
37. Perrimon N, Bernfield M. 2000. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725-728.
38. Rapraeger AC, Krufka A, Olwin BB. 1991. Requirement of heparin sulphate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252:1705-1708.
39. Reiland J, Kempf D, Roy M, Denkins Y, Marchetti D. 2006. FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia 8:596-606.
40. Reilly JF, Mizukoshi E, Maher PA. 2004. Ligand dependent and independent internalization and nuclear translocation of fibroblast growth factor (FGF) receptor 1. DNA Cell Biol 23:538-548.
41. Richardson TP, Trinkaus-Randall V, Nugent MA. 2001. Regulation of heparan sulfate proteoglycan nuclear localization by fibronectin. J Cell Sci 114:1613-1623.
42. Sabbieti MG, Marchetti L, Abreu C, Montero A, Hand AR, Raisz LG, Hurley MM. 1999. Prostaglandins regulate the expression of fibroblast growth factor-2 in bone. Endocrinology 140:434-444.
43. Sabbieti MG, Marchetti L, Gabrielli MG, Menghi M, Materazzi S, Menghi G, Raisz LG, Hurley MM. 2005. Prostaglandins differently regulate FGF-2 and FGF receptor expression and induce nuclear translocation in osteoblasts via MAPK kinase. Cell Tissue Res 319:267-278.
44. Sanderson RD. 2001. Heparan sulfate proteoglycans in invasion and metastasis. Semin Cell Dev Biol 12:89-98.
45. Sanderson RD, Yang Y, Kelly T, MacLeod V, Dai Y, Theus A. 2005. Enzymatic remodeling of heparan sulfate proteoglycans within the tumor microenvironment: Growth regulation and the prospect of new cancer therapies. J Cell Biochem 96:897-905.
46. Shotton DM. 1989. Confocal scanning optical microscopy and its applications for biological specimens. J Cell Sci 94:175-206.
47. Sudo H, Kodama HA, Amagai Y, Yamamoto S, Kasai S. 1983. In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J Cell Biol 96:191-198.
48. Szebenyi G, Fallon JF. 1999. Fibroblast growth factors as multifunctional signaling factors. Int Rev Cytol 185:45-106.
49. Turnbull J, Powell A, Guimond S. 2001. Heparan sulfate: Decoding a dynamic multifunctional cell regulator. Trends Cell Biol 11:75-82.
50. Venkataraman G, Shriver Z, Raman R, Sasisekharan R. 1999. Sequencing complex polysaccharides. Science 286:537-542.
51. Vlodavsky I, Folkman J, Sullivan R, Fridman R, Ishai-Michaeli R, Sasse J, Klagsbrun M. 1987. Endothelial cell-derived basic fibroblast growth factor: Synthesis and deposition into subendothelial extracellular matrix. Proc Natl Acad Sci USA 84:2292-2296.
52. Yayon A, Ma YS, Safran M, Klagsbrun M, Halaban R. 1997. Suppression of autocrine cell proliferation and tumorigenesis of human melanoma cells and fibroblast growth factor transformed fibroblasts by a kinase-deficient FGF receptor 1: Evidence for the involvement of Src-family kinases. Oncogene 14:2999-3009.
53. Zaidi SK, Sullivan AJ, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2002. Integration of Runx and Smad regulatory signals at transcriptionally active subnuclear sites. Proc Natl Acad Sci USA 12:8048-8053.