PDGF-AA promotes osteogenic differentiation and migration of mesenchymal stem cell by down-Regulating PDGFRa and derepressing BMP-Smad1/5/8 signaling

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Li, Anna ^a,b   Xia, Xuechun ^b   Yeh, James ^b   Kua, Huiyi ^c   Liu, Huijuan ^b   Mishina, Yuji ^d   Hao, Aijun ^a   Li, Baojie ^b  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR ALPHA; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG; BMP2 PROTEIN, MOUSE; BMPR1A PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET-DERIVED GROWTH FACTOR A; PROTEIN BINDING; SMAD PROTEIN;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL ACTIVATION; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; LYSOSOME; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; DEFICIENCY; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; MESENCHYMAL STROMA CELL; METABOLISM; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; DOWN-REGULATION; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOGENESIS; PLATELET-DERIVED GROWTH FACTOR; PROTEIN BINDING; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

EID: 84942206220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113785     Document Type: Article

References (58)

1. Andrae J, Gallini R, Betsholtz C (2008) Role of platelet-derived growth factors in physiology and medicine. Genes Dev 22: 1276-1312.
2. Hoch RV, Soriano P (2003) Roles of PDGF in animal development. Development 130: 4769-4784.
3. Donovan J, Abraham D, Norman J (2013) Platelet-derived growth factor signaling in mesenchymal cells. Front Biosci (Landmark Ed) 18: 106-119.
4. Joly M, Kazlauskas A, Fay FS, Corvera S (1994) Disruption of PDGF receptor trafficking by mutation of its PI-3 kinase binding sites. Science 263: 684-687.
5. Wang Y, Pennock SD, Chen X, Kazlauskas A, Wang Z (2004) Platelet-derived growth factor receptormediated signal transduction from endosomes. J Biol Chem 279: 8038-8046.
6. Karlsson S, Kowanetz K, Sandin A, Persson C, Ostman A, et al. (2006) Loss of T-cell protein tyrosine phosphatase induces recycling of the platelet-derived growth factor (PDGF) beta-receptor but not the PDGF alpha-receptor. Mol Biol Cell 17: 4846-4855.
7. Caplan AI, Correa D (2011) PDGF in bone formation and regeneration: new insights into a novel mechanism involving MSCs. J Orthop Res 29: 1795-1803.
8. Caverzasio J, Biver E, Thouverey C (2013) Predominant role of PDGF receptor transactivation in Wnt3a-nduced osteoblastic cell proliferation. J Bone Miner Res 28: 260-270.
9. Fantauzzo KA, Soriano P (2014) PI3K-mediated PDGFRalpha signaling regulates survival and proliferation in skeletal development through p53-dependent intracellular pathways. Genes Dev 28: 1005-1017.
10. Soriano P (1997) The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124: 2691-2700.
11. Tallquist MD, Weismann KE, Hellstrom M, Soriano P (2000) Early myotome specification regulates PDGFA expression and axial skeleton development. Development 127: 5059-5070.
12. Fierro FA, Kalomoiris S, Sondergaard CS, Nolta JA (2011) Effects on proliferation and differentiation of multipotent bone marrow stromal cells engineered to express growth factors for combined cell and gene therapy. Stem Cells 29: 1727-1737.
13. Graham S, Leonidou A, Lester M, Heliotis M, Mantalaris A, et al. (2009) Investigating the role of PDGF as a potential drug therapy in bone formation and fracture healing. Expert Opin Investig Drugs 18: 1633-1654.
14. Caverzasio J, Biver E, Thouverey C (2013) Predominant role of PDGF receptor transactivation in Wnt3a-induced osteoblastic cell proliferation. J Bone Miner Res 28: 260-270.
15. Yang D, Chen J, Jing Z, Jin D (2000) Platelet-derived growth factor (PDGF)-AA: A self-imposed cytokine in the proliferation of human fetal osteoblasts. Cytokine 12: 1271-1274.
16. Huang W, Fridman Y, Bonfil RD, Ustach CV, Conley-LaComb MK, et al. (2012) A novel function for platelet-derived growth factor D: induction of osteoclastic differentiation for intraosseous tumor growth. Oncogene 31: 4527-4535.
17. Tokunaga A, Oya T, Ishii Y, Motomura H, Nakamura C, et al. (2008) PDGF receptor beta is a potent regulator of mesenchymal stromal cell function. J Bone Miner Res 23: 1519-1528.
18. O'Sullivan S, Naot D, Callon K, Porteous F, Horne A, et al. (2007) Imatinib promotes osteoblast differentiation by inhibiting PDGFR signaling and inhibits osteoclastogenesis by both direct and stromal cell-dependent mechanisms. J Bone Miner Res 22: 1679-1689.
19. Zhang YY, Cui YZ, Luan J, Zhou XY, Zhang GL, et al. (2012) Platelet-derived growth factor receptor kinase inhibitor AG-1295 promotes osteoblast differentiation in MC3T3-E1 cells via the Erk pathway. Biosci Trends 6: 130-135.
20. Yu X, Hsieh SC, Bao W, Graves DT (1997) Temporal expression of PDGF receptors and PDGF regulatory effects on osteoblastic cells in mineralizing cultures. Am J Physiol 272: C1709-C1716.
21. Li B (2008) Bone morphogenetic protein-Smad pathway as drug targets for osteoporosis and cancer therapy. Endocr Metab Immune Disord Drug Targets 8: 208-219.
22. Massague J (2012) TGFbeta signalling in context. Nat Rev Mol Cell Biol 13: 616-630.
23. Canalis E (2009) Growth factor control of bone mass. J Cell Biochem 108: 769-777.
24. Mishina Y, Starbuck MW, Gentile MA, Fukuda T, Kasparcova V, et al. (2004) Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling. J Biol Chem 279: 27560-27566.
25. Kua H-Y, Liu H, Leong WF, Li L, Jia D, et al. (2012) c-Abl promotes osteoblast expansion by differentially regulating canonical and non-canonical BMP pathways and p16INK4a expression. Nat Cell Biol 14: 727-737.
26. Wang X, Goh CH, Li B (2007) p38 mitogen-Activated protein kinase regulates osteoblast differentiation through osterix. Endocrinology 148: 1629-1637.
27. Ball SG, Shuttleworth A, Kielty CM (2012) Inhibition of platelet-derived growth factor receptor signaling regulates Oct4 and Nanog expression, cell shape, and mesenchymal stem cell potency. Stem Cells 30: 548-560.
28. Shah P, Keppler L, Rutkowski J (2012) A review of Platelet Derived Growth Factor playing pivotal role in bone regeneration. J Oral Implantol.
29. Cao X, Chen D (2005) The BMP signaling and in vivo bone formation. Gene 357: 1-8.
30. Zhang J, Li L (2005) BMP signaling and stem cell regulation. Dev Biol 284: 1-11.
31. Chen G, Deng C, Li Y-P, Chen G, Deng C, et al. (2012) TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 8: 272.
32. Huang JS, Huang SS, Deuel TF (1983) Human platelet-derived growth factor: Radioimmunoassay and discovery of a specific plasma-binding protein. J Cell Biol 97: 383-388.
33. Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J (2006) The serum levels of growth factors: PDGF, TGF-beta and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol 57: 189-197.
34. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, et al. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4: 33-41.
35. Ma G, Li L, Hu Y, Chau JFL, Au BJ, et al. (2012) Atypical Atm-p53 genetic interaction in osteogenesis is mediated by Smad1 signaling. J Mol Cell Biol 4: 118-120.
36. Hock JM, Canalis E (1994) Platelet-derived growth factor enhances bone cell replication, but not differentiated function of osteoblasts. Endocrinology 134: 1423-1428.
37. Inai K, Norris RA, Hoffman S, Markwald RR, Sugi Y (2008) BMP-2 induces cell migration and periostin expression during atrioventricular valvulogenesis. Dev Biol 315: 383-396.
38. Darby S, Cross SS, Brown NJ, Hamdy FC, Robson CN (2008) BMP-6 over-expression in prostate cancer is associated with increased Id-1 protein and a more invasive phenotype. J Pathol 214: 394-404.
39. Sanchez-Fernandez MA, Gallois A, Riedl T, Jurdic P, Hoflack B (2008) Osteoclasts control osteoblast chemotaxis via PDGF-BB/PDGF receptor beta signaling. PLoS One 3: e3537.
40. Malabanan KP, Sheahan AV, Khachigian LM (2012) Platelet-derived growth factor-BB mediates cell migration through induction of activating transcription factor 4 and tenascin-C. Am J Pathol 180: 2590- 2597.
41. Pickett EA, Olsen GS, Tallquist MD (2008) Disruption of PDGFRalpha-initiated PI3K activation and migration of somite derivatives leads to spina bifida. Development 135: 589-598.
42. Bordei P (2011) Locally applied platelet-derived growth factor accelerates fracture healing. J Bone Joint Surg Br 93: 1653-1659.
43. Chaudhary LR, Hofmeister AM, Hruska KA (2004) Differential growth factor control of bone formation through osteoprogenitor differentiation. Bone 34: 402-411.
44. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
45. Chen PH, Chen X, He X (2013) Platelet-derived growth factors and their receptors: structural and functional perspectives. Biochim Biophys Acta 1834: 2176-2186.
46. Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, et al. (1994) Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8: 1875-1887.
47. Kubota K, Sakikawa C, Katsumata M, Nakamura T, Wakabayashi K (2002) Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor. J Bone Miner Res 17: 257-265.
48. Rydziel S, Shaikh S, Canalis E (1994) Platelet-derived growth factor-AA and -BB (PDGF-AA and -BB) enhance the synthesis of PDGF-AA in bone cell cultures. Endocrinology 134: 2541-2546.
49. Centrella M, McCarthy TL, Kusmik WF, Canalis E (1992) Isoform-specific regulation of platelet-derived growth factor activity and binding in osteoblast-enriched cultures from fetal rat bone. J Clin Invest 89: 1076-1084.
50. Caplan AI, Correa D (2011) PDGF in bone formation and regeneration: new insights into a novel mechanism involving MSCs. J Orthop Res 29: 1795-1803.
51. Massague J (2003) Integration of Smad and MAPK pathways: A link and a linker revisited. Genes Dev 17: 2993-2997.
52. Pera EM, Ikeda A, Eivers E, De Robertis EM (2003) Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev 17: 3023-3028.
53. Chau JFL, Jia D, Wang Z, Liu Z, Hu Y, et al. (2012) A crucial role for bone morphogenetic protein- Smad1 signalling in the DNA damage response. Nat Commun 3: 836.
54. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, et al. (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131: 980-993.
55. Verheyen EM (2007) Opposing effects of Wnt and MAPK on BMP/Smad signal duration. Dev Cell 13: 755-756.
56. Eivers E, Demagny H, De Robertis EM (2009) Integration of BMP and Wnt signaling via vertebrate Smad1/5/8 and Drosophila Mad. Cytokine Growth Factor Rev 20: 357-365.
57. Sieber C, Kopf J, Hiepen C, Knaus P (2009) Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev 20: 343-355.
58. Karlsson L, Lindahl P, Heath JK, Betsholtz C (2000) Abnormal gastrointestinal development in PDGFA and PDGFR-(alpha) deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis. Development 127: 3457-3466.