Fibroblast growth factor-2 isoform (low molecular weight/18 kDa) overexpression in preosteoblast cells promotes bone regeneration in critical size calvarial defects in male mice

Endocrinology

Volumn 155, Issue 3, 2014, Pages 965-974

  Xiao, Liping ^a   Ueno, Daisuke ^b   Catros, Sylvain ^c   Homer Bouthiette, Collin ^a   Charles, Lyndon ^a   Kuhn, Liisa ^a   Hurley, Marja M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b TSURUMI UNIVERSITY   (Japan)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; LOW MOLECULAR WEIGHT FIBROBLAST GROWTH FACTOR 2; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEFECT; BONE RADIOGRAPHY; BONE REGENERATION; CALVARIAL DEFECT; COMPUTED TOMOGRAPHY SCANNER; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FRACTURE HEALING; GENETIC ANALYSIS; MALE; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL DIFFERENTIATION; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; OSTEOBLASTS; OSTEOGENESIS; PHOSPHORYLATION; PROTEIN ISOFORMS; SKULL; TOMOGRAPHY, X-RAY COMPUTED; WNT SIGNALING PATHWAY; X-RAY MICROTOMOGRAPHY;

EID: 84896899403     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1919     Document Type: Article

References (44)

1. Fei Y, Gronowicz G, Hurley MM. Fibroblast growth factor-2, bone homeostasis and fracture repair. Curr Pharm Des. 2013;19:3354-3363.
2. Einhorn TA. The cell and molecular biology of fracture healing. Clin Orthop Relat Res. 1998;355:S7-S21.
3. Gospodarowicz D. Fibroblast growth factor. Chemical structure and biologic function. Clin Orthop Relat Res. 1990;257:231-248. (Pubitemid 20246747)
4. Florkiewicz RZ, Sommer A. Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc Natl Acad Sci USA. 1989;86:3978-3981. (Pubitemid 19154728)
5. Arese M, Chen Y, Florkiewicz RZ, Gualandris A, Shen B, Rifkin DB. Nuclear activities of basic fibroblast growth factor: potentiation of low-serum growth mediated by natural or chimeric nuclear localization signals. Mol Biol Cell. 1999;10:1429-1444. (Pubitemid 29230900)
6. Delrieu I. The high molecular weight isoforms of basic fibroblast growth factor (FGF-2): an insight into an intracrine mechanism. FEBS Lett. 2000;468:6-10. (Pubitemid 30101671)
7. Touriol C, Bornes S, Bonnal S, et al. Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol Cell. 2003;95:169-178. (Pubitemid 36889219)
8. Coffin JD, Florkiewicz RZ, Neumann J, et al. Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. MolBiol Cell. 1995;6:1861-1873.
9. Sobue T, Naganawa T, Xiao L, et al. Over-expression of fibroblast growth factor-2 causes defective bone mineralization and osteopenia in transgenic mice. J Cell Biochem. 2005;95:83-94. (Pubitemid 41420218)
10. Xiao L, Liu P, Li X, et al. Exported 18-kDa isoform of fibroblast growth factor-2 is a critical determinant of bone mass in mice. J Biol Chem. 2009;284:3170-3182.
11. Xiao L, Naganawa T, Lorenzo J, Carpenter TO, Coffin JD, Hurley MM. Nuclear isoforms of fibroblast growth factor 2 are novel inducers of hypophosphatemia via modulation of FGF23 and KLOTHO. J Biol Chem. 2010;285:2834-2846.
12. Naganawa T, Xiao L, Abogunde E, et al. In vivo and in vitro comparison of the effects of FGF-2 null and haplo-insufficiency on bone formation in mice. Biochem Biophys ResCommun. 2006;339:490-498. (Pubitemid 41739694)
13. Chen WJ, Jingushi S, Aoyama I, et al. Effects of FGF-2 on metaphyseal fracture repair in rabbit tibiae. J Bone Miner Metab. 2004;22:303-309. (Pubitemid 38980946)
14. Kwan MD, Sellmyer MA, Quarto N, Ho AM, Wandless TJ, Longaker MT. Chemical control of FGF-2 release for promoting calvarial healing with adipose stem cells. J Biol Chem. 2011;286:11307-11313.
15. Behr B, Panetta NJ, Longaker MT, Quarto N. Different endogenous threshold levels of fibroblast growth factor-ligands determine the healing potential of frontal and parietal bones. Bone. 2010;47:281-294.
16. Santana RB, Trackman PC. Controlled release of fibroblast growth factor 2 stimulates bone healing in an animal model of diabetes mellitus. Int J Oral Maxillofac Implants. 2006;21:711-718. (Pubitemid 44671934)
17. Sabbieti M, Agas D, Marchetti L, Coffin JD, Xiao L, Hurley MM. BMP-2 differentially modulates FGF-2 isoform effects in osteoblasts from newborn transgenic mice. Endocrinology. 2013;154:2723-2733.
18. Church VL, Francis-West P. Wnt signalling during limb development. Int J Dev Biol. 2002;46:927-936. (Pubitemid 35364641)
19. Patel MS, Karsenty G. Regulation of bone formation and vision by LRP5. N Engl J Med. 2002;346:1572-1574. (Pubitemid 34755698)
20. Goltzman D. Discoveries, drugs and skeletal disorders. Nat Rev Drug Discov. 2002;1:784-796. (Pubitemid 37361562)
21. Zhang R, Oyajobi BO, Harris SE, et al. Wnt/β-catenin signaling activates bone morphogenetic protein 2 expression in osteoblasts. Bone. 2013;52:145-156.
22. Dacic S, Kalajzic I, Visnjic D, Lichtler AC, Rowe DW. Col1a1-driven transgenic markers of osteoblast lineage progression. J Bone Miner Res. 2001;16:1228-1236. (Pubitemid 32574651)
23. Sachse A, Wagner A, Keller M, et al. Osteointegration of hydroxy-apatite-titanium implants coated with nonglycosylated recombinant human bone morphogenetic protein-2 (BMP-2) in aged sheep. Bone. 2005;37:699-710. (Pubitemid 41476393)
24. Dempster DW, Compston JE, Drezner MK, et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 2013;28:2-17.
25. Nakajima A, Nakajima F, Shimizu S, et al. Spatial and temporal gene expression for fibroblast growth factor type I receptor (FGFR1) during fracture healing in the rat. Bone. 2001;29:458-466. (Pubitemid 33026467)
26. Stavri GT, Zachary IC, Baskerville PA, Martin JF, Erusalimsky JD. Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. Circulation. 1995;92:11-14.
27. Hurley MM, Naski, M, Marie PJ. Fibroblast growth factor and fibroblast growth factor receptor families in bone. In: Bilezikian J, Raisz LG, and Martin TJ, eds. Principles of Bone Biology. San Diego, CA: Academic Press; 2008:1103-1132.
28. Stein GS, Lian JB, Stein JL, Van Wijnen AJ, Montecino M. Transcriptional control of osteoblast growth and differentiation. Physiol Rev. 1996;76:593-629. (Pubitemid 26163716)
29. Xie J, Baumann MJ, McCabe LR. Osteoblasts respond to hydroxyapatite surfaces with immediate changes in gene expression. J Biomed Mater Res A. 2004;71:108-117. (Pubitemid 39244401)
30. Tcacencu I, Wendel M. Collagen-hydroxyapatite composite enhances regeneration of calvaria bone defects in young rats but postpones the regeneration of calvaria bone in aged rats. J Mater Sci Mater Med. 2008;19:2015-2021. (Pubitemid 351436306)
31. Kobayashi N, Miyaji H, Sugaya T, Kawanami M. Bone augmentation by implantation of FGF2-loaded collagen gel-sponge composite scaffold. J Oral Tissue Eng. 2010;8:91-101.
32. Kawaguchi H, Oka H, Jingushi S, et al. A local application of recombinant human fibroblast growth factor 2 for tibial shaft fractures: a randomized, placebo-controlled trial. J Bone Miner Res. 2010;25:2735-2743.
33. Tanaka E, Ishino Y, Sasaki A, et al. Fibroblast growth factor-2 augments recombinant human bone morphogenetic protein-2-induced osteoinductive activity. Ann Biomed Eng. 2006;34:717-725. (Pubitemid 43824021)
34. Xiao G, Jiang D, Gopalakrishnan R, Franceschi RT. Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J Biol Chem. 2002;277:36181-36187.
35. Colin S, Jeanny JC, Mascarelli F, et al. In vivo involvement of heparan sulfate proteoglycan in the bioavailability, internalization, and catabolism of exogenous basic fibroblast growth factor. Mol Pharmacol. 1999;55:74-82. (Pubitemid 29042524)
36. Kan M, Wang F, To B, Gabriel JL, McKeehan WL. Divalent cations and heparin/heparan sulfate cooperate to control assembly and activity of the fibroblast growth factor receptor complex. J Biol Chem. 1996;271:26143-26148. (Pubitemid 26347458)
37. Ruppert R, Hoffmann E, Sebald W. Human bone morphogenetic protein 2 contains a heparin-binding site which modifies its biological activity. Eur J Biochem. 1996;237:295-302. (Pubitemid 26110301)
38. Blanquaert F, Barritault D, Caruelle JP. Effects of heparan-like polymers associated with growth factors on osteoblast proliferation and phenotype expression. J Biomed Mater Res. 1999;44:63-72. (Pubitemid 28544086)
39. Naganawa T, Xiao L, Coffin JD, et al. Reduced expression and function of bone morphogenetic protein-2 in bones of Fgf2 null mice. J Cell Biochem. 2008;103:1975-1988. (Pubitemid 351501926)
40. Agas D, Sabbieti MG, Marchetti L, Xiao L, Hurley MM. FGF-2 enhances Runx-2/Smads nuclear localization in BMP-2 canonical signaling in osteoblasts. J Cell Physiol. 2013;228:2149-2158.
41. Krishnan V, Bryant HU, Macdougald OA. Regulation of bone mass by Wnt signaling. J Clin Invest. 2006;116:1202-1209.
42. Sato MM, Nakashima A, Nashimoto M, Yawaka Y, Tamura M. Bone morphogenetic protein-2 enhances Wnt/β-catenin signaling-induced osteoprotegerin expression. Genes Cells. 2009;14:141-153.
43. Zhang R, Oyajobi BO, Harris SE, et al. Wnt/β-catenin signaling activates bone morphogenetic protein 2 expression in osteoblasts. Bone. 2013;52:145-146.
44. Fakhry A, Ratisoontorn C, Vedhachalam C, et al. Effects of FGF-2/-9 in calvarial bone cell cultures: differentiation stage-dependent mitogenic effect, inverse regulation of BMP-2 and noggin, and enhancement of osteogenic potential. Bone. 2005;36:254-266. (Pubitemid 40283582)