Sequential exposure to fibroblast growth factors (FGF) 2, 9 and 18 enhances hMSC chondrogenic differentiation

Osteoarthritis and Cartilage

Volumn 23, Issue 3, 2015, Pages 443-453

  Correa, D ^a   Somoza, R A ^a   Lin, P ^a   Greenberg, S ^a   Rom, E ^b   Duesler, L ^a   Welter, J F ^a   Yayon, A ^b   Caplan, A I ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ProCore BioMed Ltd   (Israel)

Author keywords

Cartilage repair; Chondrogenesis; FGFR; Fibroblast growth factor (FGF); Hypertrophy; Mesenchymal stem cells

Indexed keywords

FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 3; NEUTRALIZING ANTIBODY; TRANSCRIPTION FACTOR SOX9; FGFR1 PROTEIN, HUMAN; FGFR3 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR;

ARTICLE; CELL AGGREGATION; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CHEMICAL ANALYSIS; CHONDROGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; CARTILAGE CELL; DRUG EFFECTS; GENETICS; HYPERTROPHY; MESENCHYMAL STROMA CELL; METABOLISM;

CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTORS; HUMANS; HYPERTROPHY; IN VITRO TECHNIQUES; MESENCHYMAL STROMAL CELLS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3;

EID: 84925198518     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2014.11.013     Document Type: Article

References (42)

1. Barry F. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res 2001, 268(2):189-200.
2. Caplan A.I. Why are MSCs therapeutic? new data: new insight. JPathol 2009, 217(2):318-324.
3. Richardson S.M., Hoyland J.A., Mobasheri R., Csaki C., Shakibaei M., Mobasheri A. Mesenchymal stem cells in regenerative medicine: opportunities and challenges for articular cartilage and intervertebral disc tissue engineering. JCell Physiol 2010, 222(1):23-32.
4. Solchaga L.A., Penick K., Goldberg V.M., Caplan A.I., Welter J.F. Fibroblast growth factor-2 enhances proliferation and delays loss of chondrogenic potential in human adult bone-marrow-derived mesenchymal stem cells. Tissue Eng Part A 2010, 16(3):1009-1019.
5. Solchaga L.A., Penick K., Porter J.D., Goldberg V.M., Caplan A.I., Welter J.F. FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells. JCell Physiol 2005, 203(2):398-409.
6. Mueller M.B., Fischer M., Zellner J., Berner A., Dienstknecht T., Prantl L., et al. Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning. Cells Tissues Organs 2010, 192(3):158-166.
7. Mueller M.B., Tuan R.S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 2008, 58(5):1377-1388.
8. Pelttari K., Winter A., Steck E., Goetzke K., Hennig T., Ochs B.G., et al. Premature induction of hypertrophy during invitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 2006, 54(10):3254-3266.
9. Steinert A.F., Proffen B., Kunz M., Hendrich C., Ghivizzani S.C., Nöth U., et al. Hypertrophy is induced during the invitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther 2009, 11(5):R148.
10. Gadjanski I., Spiller K., Vunjak-Novakovic G. Time-dependent processes in stem cell-based tissue engineering of articular cartilage. Stem Cell Rev 2012, 8(3):863-881.
11. Oldershaw R.A., Baxter M.A., Lowe E.T., Bates N., Grady L.M., Soncin F., et al. Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 2010, 28(11):1187-1194.
12. Hellingman C.A., Koevoet W., Kops N., Farrell E., Jahr H., Liu W., et al. Fibroblast growth factor receptors in invitro and invivo chondrogenesis: relating tissue engineering using adult mesenchymal stem cells to embryonic development. Tissue Eng Part A 2010, 16(2):545-556.
13. Weiss S., Hennig T., Bock R., Steck E., Richter W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. JCell Physiol 2010, 223(1):84-93.
14. Ellman M.B., Yan D., Ahmadinia K., Chen D., An H.S., Im H.J. Fibroblast growth factor control of cartilage homeostasis. JCell Biochem 2013, 114(4):735-742.
15. Davidson D., Blanc A., Filion D., Wang H., Plut P., Pfeffer G., et al. Fibroblast growth factor (FGF) 18 signals through FGF receptor 3 to promote chondrogenesis. JBiol Chem 2005, 280(21):20509-20515.
16. Ellsworth J.L., Berry J., Bukowski T., Claus J., Feldhaus A., Holderman S., et al. Fibroblast growth factor-18 is a trophic factor for mature chondrocytes and their progenitors. Osteoarthritis Cartilage 2002, 10(4):308-320.
17. Moore E.E., Bendele A.M., Thompson D.L., Littau A., Waggie K.S., Reardon B., et al. Fibroblast growth factor-18 stimulates chondrogenesis and cartilage repair in a rat model of injury-induced osteoarthritis. Osteoarthritis Cartilage 2005, 13(7):623-631.
18. Beenken A., Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 2009, 8(3):235-253.
19. Hung I.H., Yu K., Lavine K.J., Ornitz D.M. FGF9 regulates early hypertrophic chondrocyte differentiation and skeletal vascularization in the developing stylopod. Dev Biol 2007, 307(2):300-313.
20. Govindarajan V., Overbeek P.A. FGF9 can induce endochondral ossification in cranial mesenchyme. BMC Dev Biol 2006, 6:7.
21. Vincent T.L. Explaining the fibroblast growth factor paradox on osteoarthritis: lessons from conditional knockout mice. Arthritis Rheum 2012, 64(12):3835-3838.
22. Hidaka C., Goldring M.B. Regulatory mechanisms of chondrogenesis and implications for understanding articular cartilage homeostasis. Curr Rheumatol Rev 2008, 4(3):136-147.
23. Zhang X., Ibrahimi O.A., Olsen S.K., Umemori H., Mohammadi M., Ornitz D.M. Receptor specificity of the fibroblast growth factor family. the complete mammalian FGF family. JBiol Chem 2006, 281(23):15694-15700.
24. Haynesworth S.E., Goshima J., Goldberg V.M., Caplan A.I. Characterization of cells with osteogenic potential from human marrow. Bone 1992, 13(1):81-88.
25. Vunjak-Novakovic G., Freshney R.I. Culture of Cells for Tissue Engineering 2006, John Wiley & Sons.
26. Carrino D.A., Arias J.L., Caplan A.I. Aspectrophotometric modification of a sensitive densitometric Safranin O assay for glycosaminoglycans. Biochem Int 1991, 24(3):485-495.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
28. Puetzer J.L., Petitte J.N., Loboa E.G. Comparative review of growth factors for induction of three-dimensional invitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B, Rev 2010, 16(4):435-444.
29. Martin I., Jakob M., Schäfer D., Dick W., Spagnoli G., Heberer M. Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritic joints. Osteoarthritis Cartilage 2001, 9(2):112-118.
30. Pei M., Seidel J., Vunjak-Novakovic G., Freed L.E. Growth factors for sequential cellular de- and re-differentiation in tissue engineering. Biochem Biophys Res Commun 2002, 294(1):149-154.
31. Worster A.A., Brower-Toland B.D., Fortier L.A., Bent S.J., Williams J., Nixon A.J. Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix. JOrthop Res 2001, 19(4):738-749.
32. Aaron R.K., Wang S., Ciombor D.M. Upregulation of basal TGFbeta1 levels by EMF coincident with chondrogenesis-implications for skeletal repair and tissue engineering. JOrthop Res 2002, 20(2):233-240.
33. Handorf A.M., Li W.J. Fibroblast growth factor-2 primes human mesenchymal stem cells for enhanced chondrogenesis. PLoS One 2011, 6(7):e22887.
34. de Crombrugghe B., Lefebvre V., Behringer R.R., Bi W., Murakami S., Huang W. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 2000, 19(5):389-394.
35. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., de Crombrugghe B. Sox9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 1997, 17(4):2336-2346.
36. Coutu D.L., François M., Galipeau J. Inhibition of cellular senescence by developmentally regulated FGF receptors in mesenchymal stem cells. Blood 2011, 117(25):6801-6812.
37. Coutu D.L., Galipeau J. Roles of FGF signaling in stem cell self-renewal, senescence and aging. Aging 2011, 3(10):920-933.
38. Yan D., Chen D., Cool S.M., van Wijnen A.J., Mikecz K., Murphy G., et al. Fibroblast growth factor receptor 1 is principally responsible for fibroblast growth factor 2-induced catabolic activities in human articular chondrocytes. Arthritis Res Ther 2011, 13(4):R130.
39. Robinson D., Hasharoni A., Cohen N., Yayon A., Moskowitz R.M., Nevo Z. Fibroblast growth factor receptor-3 as a marker for precartilaginous stem cells. Clin Orthop Relat Res 1999, 367(Suppl l):S163-S175.
40. Gadjanski I., Spiller K., Vunjak-Novakovic G. Time-dependent processes in stem cell-based tissue engineering of articular cartilage. Stem Cell Rev 2011, 8(3):863-881.
41. Vincent T.L. Fibroblast growth factor 2: good or bad guy in the joint?. Arthritis Res Ther 2011, 13(5):127.
42. Hanada K., Solchaga L.A., Caplan A.I., Hering T.M., Goldberg V.M., Yoo J.U., et al. BMP-2 induction and TGF-beta 1 modulation of rat periosteal cell chondrogenesis. JCell Biochem 2001, 81(2):284-294.