Fibroblast growth factor 2 inhibits bone morphogenetic protein9-induced osteogenic differentiation of mesenchymal stem cells byrepressing Smads signaling and subsequently reducing Smadsdependent up-regulation of ALK1 and ALK2

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 8, 2013, Pages 1639-1646

  Song, Tao ^a   Wang, Wenjuan ^a   Xu, Jing ^a   Zhao, Dan ^a   Dong, Qian ^a   Li, Li ^a   Yang, Xue ^a   Duan, Xinglian ^a   Liang, Yiwen ^a   Xiao, Yan ^a   Wang, Jin ^a   He, Juanwen ^a   Tang, Ming ^a   Wang, Jian ^a   Luo, Jinyong ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Bone morphogenic proteins 9; Fibroblast growth factor 2; Mesenchymal stem cells; Osteogenic differentiation; Smads

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ACTIVIN RECEPTOR LIKE KINASE 2; BONE MORPHOGENETIC PROTEIN 9; FIBROBLAST GROWTH FACTOR 2; PROTEIN KINASE; SMAD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; ENZYME INDUCTION; GENE REPRESSION; GENETIC TRANSFECTION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOBLAST; SIGNAL TRANSDUCTION;

EID: 84884891747     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.05.005     Document Type: Article

References (44)

1. Arthur A, Zannettino A, Gronthos S. The therapeutic applications of multipotentialmesenchymal/stromal stem cells in skeletal tissue repair. Journal of Cellular Physiology 2009;218:237-45..
2. Bilican B, Fiore-Heriche C, Compston A, Allen ND, Chandran S. Induction of Olig2precursors by FGF involves BMP signalling blockade at the Smad level. PLoS ONE2008;3:e2863..
3. Biver E, Soubrier AS, Thouverey C, Cortet B, Broux O, Caverzasio J, et al. ibroblastgrowth factor 2 inhibits up-regulation of bone morphogenic proteins and theirreceptors during osteoblastic differentiation of human mesenchymal stem cells. Biochemical and Biophysical Research Communications 2012;427:737-42..
4. Bolander ME. Regulation of fracture repair by growth factors. Proceedings of theSociety for Experimental Biology and Medicine 1992;200:165-70..
5. Boraiah S, Paul O, Hawkes D, Wickham M, Lorich DG. Complications of recombinanthuman BMP-2 for treating complex tibial plateau fractures: a preliminary report. Clinical Orthopaedics and Related Research 2009;467:3257-62..
6. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded withautologous mesenchymal stem cells on the healing of canine segmental bonedefects. Journal of Bone and Joint Surgery 1998;80:985-96.. (Pubitemid 28355669)
7. Canalis E, Centrella M, McCarthy T. Effects of basic fibroblast growth factor on boneformation in vitro. Journal of Clinical Investigation 1988;81:1572-7..
8. Chen C, Grzegorzewski KJ, Barash S, Zhao Q, Schneider H, Wang Q, et al. An integratedfunctional genomics screening program reveals a role for BMP-9 in glucosehomeostasis. Nature Biotechnology 2003;21:294-301.. (Pubitemid 36314814)
9. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins. Growth Factors 2004;22:233-41.. (Pubitemid 40136452)
10. Cushing MC, Mariner PD, Liao JT, Sims EA, Anseth KS. Fibroblast growth factorrepresses Smad-mediated myofibroblast activation in aortic valvular interstitialcells. FASEB Journal 2008;22:1769-77.. (Pubitemid 351811454)
11. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S. Identification of BMP9 and BMP10as functional activators of the orphan activin receptor-like kinase 1 (ALK1) inendothelial cells. Blood 2007;109(March (5)):1953-61 [Epub 2006 October 26].. (Pubitemid 46348192)
12. Deng ZL, Sharff KA, Tang N, Song WX, Luo J, Luo X, et al. Regulation ofosteogenic differentiation during skeletal development. Frontiers in Bioscience 2008;13:2001-21.. (Pubitemid 351589231)
13. Ducy P, Karsenty G. Two distinct osteoblast-specific cis-acting elements con-trol expression of a mouse osteocalcin gene. Molecular and Cellular Biology 1995;15:1858-69..
14. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptionalactivator of osteoblast differentiation. Cell 1997;89:747-54..
15. Estrela C, Alencar AH, Kitten GT, Vencio EF, Gava E. Mesenchymal stem cells inthe dental tissues: perspectives for tissue regeneration. Brazilian Dental Journal 2011;22:91-8..
16. Hanada K, Dennis JE, Caplan AI. Stimulatory effects of basic fibroblast growth factorand bone morphogenetic protein-2 on osteogenic differentiation of rat bonemarrow-derived mesenchymal stem cells. Journal of Bone and Mineral Research 1997;12:1606-14.. (Pubitemid 27422361)
17. He BC, Chen L, Zuo GW, Zhang W, Bi Y, Huang J, et al. Synergistic antitumor effectof the activated PPARgamma and retinoid receptors on human osteosarcoma. Clinical Cancer Research 2010;16:2235-45..
18. Herrera B, van Dinther M, Ten Dijke P, Inman GJ. Autocrine bone morphogeneticprotein-9 signals through activin receptor-like kinase-2/Smad1/Smad4 to pro-mote ovarian cancer cell proliferation. Cancer Research 2009;69:9254-62..
19. Hogan BL. Bone morphogenetic proteins: multifunctional regulators of vertebratedevelopment. Genes and Development 1996;10:1580-94.. (Pubitemid 26268864)
20. House SL, House BE, Glascock B, Kimball T, Nusayr E, Schultz JE, et al. Fibroblastgrowth factor 2 mediates isoproterenol-induced cardiac hypertrophy throughactivation of the extracellular regulated kinase. Molecular and Cellular Pharma-cology 2010;2:143-54..
21. Huang Z, Nelson ER, Smith RL, Goodman SB. The sequential expression profilesof growth factors from osteoprogenitors [correction of osteroprogenitors] toosteoblasts in vitro. Tissue Engineering 2007;13:2311-20.. (Pubitemid 47404446)
22. Kaewsrichan J, Wongwitwichot P, Chandarajoti K, Chua KH, Ruszymah BH. Sequen-tial induction of marrow stromal cells by FGF2 and BMP2 improves their growthand differentiation potential in vivo. Archives of Oral Biology 2010;56:90-101..
23. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, et al. Characterizationof the distinct orthotopic bone-forming activity of 14 BMPs using recombinantadenovirus-mediated gene delivery. Gene Therapy 2004;11:1312-20.. (Pubitemid 39213996)
24. Kizhner T, Ben-David D, Rom E, Yayon A, Livne E. Effects of FGF2 and FGF9 onosteogenic differentiation of bone marrow-derived progenitors. In Vitro Cellularand Developmental Biology Animal 2011;47:294-301..
25. Kørbling M, Estrov Z. Adult stem cells for tissue repair - a new therapeutic concept?New England Journal of Medicine 2003;349:570-82.. (Pubitemid 36951370)
26. López-Coviella I, Berse B, Krauss R, Thies RS, Blusztajn JK. Induction and maintenanceof the neuronal cholinergic phenotype in the central nervous system by BMP9. Science 2000;289:313-6.. (Pubitemid 30469912)
27. Luo J, Tang M, Huang J, He BC, Gao JL, Chen L, et al. TGFbeta/BMP type I receptors ALK1and ALK2 are essential for BMP9-induced osteogenic signaling in mesenchymalstem cells. Journal of Biological Chemistry 2010;285:29588-98..
28. Luther G, Wagner ER, Zhu G, Kang Q, Luo Q, Lamplot J, et al. BMP-9 inducedosteogenic differentiation of mesenchymal stem cells: molecular mechanismand therapeutic potential. Current Gene Therapy 2011;11:229-40..
29. Luu HH, Song WX, Luo X, Manning D, Luo J, Deng ZL, et al. Distinct roles of bone mor-phogenetic proteins in osteogenic differentiation of mesenchymal stem cells. Journal of Orthopaedic Research 2007;25:665-77.. (Pubitemid 46730519)
30. Marcacci M, Kon E, Moukhachev V, Lavroukov A, Kutepov S, Quarto R, et al. Stemcells associated with macroporous bioceramics for long bone repair: 6- to 7-yearoutcome of a pilot clinical study. Tissue Engineering 2007;13:947-55.. (Pubitemid 46870419)
31. Mayahara H, Ito T, Nagai H, Miyajima H, Tsukuda R, Taketomi S, et al. In vivo stim-ulation of endosteal bone formation by basic fibroblast growth factor in rats. Growth Factors 1993;9:73-80.. (Pubitemid 23241843)
32. McCarthy TL, Centrella M, Canalis E. Effects of fibroblast growth factors on deoxyri-bonucleic acid and collagen synthesis in rat parietal bone cells. Endocrinology 1989;125:2118-26.. (Pubitemid 19258650)
33. Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biology 2001;2[REVIEWS3005, Epub 2001]..
34. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.. (Pubitemid 29282067)
35. Ploemacher RE, Engels LJ, Mayer AE, Thies S, Neben S. Bone morphogenetic pro-tein 9 is a potent synergistic factor for murine hemopoietic progenitor cellgeneration and colony formation in serum-free cultures. Leukemia 1999;13:428-37.. (Pubitemid 29108082)
36. Rodan SB, Wesolowski G, Yoon K, Rodan GA. Opposing effects of fibroblast growthfactor and pertussis toxin on alkaline phosphatase, osteopontin, osteocalcin and type I collagen mRNA levels in ROS 17/2.8 Cells. Journal of Biological Chemistry 1989;264:19934-41.. (Pubitemid 20008108)
37. Rutherford RB, Nussenbaum B, Krebsbach PH. Bone morphogenetic protein 7 exvivo gene therapy. Drug News & Perspectives 2003;16:5-10.. (Pubitemid 36527829)
38. Song JJ, Celeste AJ, Kong FM, Jirtle RL, Rosen V, Thies RS. Bone morphogeneticprotein-9 binds to liver cells and stimulates proliferation. Endocrinology 1995;136:4293-7..
39. Tang W, Wei Y, Le K, Li Z, Bao Y, Gao J, et al. Mitogen-activated proteinkinases ERK 1/2- and p38-GATA4 pathways mediate the Ang II-induced acti-vation of FGF2 gene in neonatal rat cardiomyocytes. Biochemical Pharmacology 2011;81:518-25..
40. Truksa J, Peng H, Lee P, Beutler E. Bone morphogenetic proteins 2, 4, and 9 stimu-late murine hepcidin 1 expression independently of Hfe, transferring receptor 2(Tfr2), and IL-6. Proceedings of the National Academy of Sciences of the United States of America 2006;103:10289-91..
41. Visser R, Arrabal PM, Santos-Ruiz L, Becerra J, Cifuentes M. Basic fibroblast growthfactor enhances the osteogenic differentiation induced by bone morphogeneticprotein-6 in vitro and in vivo. Cytokine 2012;58:27-33..
42. Xiao L, Sobue T, Esliger A, Kronenberg MS, Coffin JD, Doetschman T, et al. Disruptionof the Fgf2 gene activates the adipogenic and suppresses the osteogenic programin mesenchymal marrow stromal stem cells. Bone 2010;47:360-70..
43. Xu DJ, Zhao YZ, Wang J, He JW, Weng YG, Luo JY. Smads, p38 and ERK1/2 are involvedin BMP9-induced osteogenic differentiation of C3H10T1/2 mesenchymal stemcells. BMB Reports 2011;45:247-52..
44. Zhao Y, Song T, Wang W, Wang J, He J, Wu N, et al. P38 and ERK1/2 MAPKs act inopposition to regulate BMP9-induced osteogenic differentiation of mesenchy-mal progenitor cells. PLoS ONE 2012;7:e43383..