Osteogenic response of human adipose-derived stem cells to BMP-6, VEGF, and combined VEGF plus BMP-6 in vitro

Growth Factors

Volumn 30, Issue 5, 2012, Pages 333-343

  Zhang, Yi ^a,b   Madhu, Vedavathi ^a   Dighe, Abhijit S ^a   Irvine, James N ^a   Cui, Quanjun ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

Author keywords

BMP 6; Bone repair; Mesenchymal stem cells; Osteogenesis; VEGF

Indexed keywords

BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR; CANCER GROWTH FACTOR; COL1A1 PROTEIN; MESSENGER RNA; PROTEIN; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR OSTERIX; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADIPOSE DERIVED STEM CELL; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRUCTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MOLECULAR INTERACTION; OSTEOBLAST; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALIA;

EID: 84866944598     PISSN: 08977194     EISSN: 10292292     Source Type: Journal    
DOI: 10.3109/08977194.2012.720574     Document Type: Article

References (46)

1. Boden SD, Liu Y, Hair GA, Helms JA, HuD, Racine M, Nanes MS, Titus L. 1998. LMP-1, a LIM-domain protein, mediates BMP-6effects on bone formation. Endocrinology 139(12):5125-5134.
2. Chen SJ, Artlett CM, Jimenez SA, Varga J. 1998. Modulation ofhuman alpha1(I) procollagen gene activity by interaction withSp1 and Sp3 transcription factors in vitro. Gene 215:101-110.
3. Chen HT, Lee MJ, Chen CH, Chuang SC, Chang LF, Ho ML, Hung SH, Fu YC, Wang YH, Wang HI, Wang GJ, Kang L, Chang JK. 2011. Proliferation and differentiation potential ofhuman adipose-derived mesenchymal stem cells isolated fromelderly patients with osteoporotic fractures. J Cell Mol Med16(3):582-593.
4. Cui F, Wang X, Liu X, Dighe AS, Balian G, Cui Q. 2010. VEGFand BMP-6 enhance bone formation mediated by cloned mouseosteoprogenitor cells. Growth Factors 28(5):306-317.
5. Diefenderfer DL, Osyczka AM, Garino JP, Leboy PS. 2003a. Regulation of BMP-induced transcription in cultured humanbone marrow stromal cells. J Bone Joint Surg Am 85:19-28.
6. Diefenderfer DL, Osyczka AM, Reilly GC, Leboy PS. 2003b. BMPresponsiveness in human mesenchymal stem cells. ConnectTissue Res 44:305-311.
7. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop DJ, Horwitz E. 2006. Minimal criteria for defining multipotent mesenchymal stromalcells. The International Society for Cellular Therapy positionstatement. Cytotherapy 8:315-317.
8. Estes BT, Wu AW, Guilak F. 2006. Potent induction of chondrocyticdifferentiation of human adipose-derived adult stem cells bybone morphogenetic protein 6. Arthritis Rheum 54(4):1222-1232.
9. Gabbay JS, Heller JB, Mitchell SA, Zuk PA, Spoon DB, Wasson KL, Jarrahy R, Benhaim P, Bradley JP. 2006. Osteogenic potentiationof human adipose-derived stem cells in a 3-dimensional matrix. Ann Plast Surg 57(1):89-93.
10. Garcia P, Pieruschka A, Klein M, Tami A, Histing T, Holstein JH, Scheuer C, Pohlemann T, Menger MD. 2012. Temporal andspatial vascularization patterns of unions and nonunions: Role ofvascular endothelial growth factor and bone morphogeneticproteins. J Bone Joint Surg Am 94:49-58.
11. Geiger F, Bertram H, Berger I, Lorenz H, Wall O, Eckhardt C, Simank HG, Richter W. 2005. Vascular endothelial growthfactor gene-activated matrix (VEGF165-GAM) enhancesosteogenesis and angiogenesis in large segmental bone defects. J Bone Miner Res 20(11):2028-2035, Epub 2005 Jul 5.
12. Gregory CA, Gunn WG, Peister A, Prockop DJ. 2004. An Alizarinred-based assay of mineralization by adherent cells in culture:Comparison with cetylpyridinium chloride extraction. AnalBiochem 329(1):77-84.
13. Hanada K, Dennis JE, Caplan AI. 1997. Stimulatory effects of basicfibroblast growth factor and bone morphogenetic protein-2 onosteogenic differentiation of rat bone marrow-derived mesenchymalstem cells. J Bone Miner Res 12:1606-1614.
14. Hanada K, Solchaga LA, Caplan AI, Hering TM, Goldberg VM, Yoo JU, Johnstone B. 2001. BMP-2 induction and TGF-beta 1modulation of rat periosteal cell chondrogenesis. J Cell Biochem81(2):284-294.
15. Hou H, Zhang X, Tang T, Dai K, Ge R. 2009. Enhancement ofbone formation by genetically-engineered bone marrow stromalcells expressing BMP-2, VEGF and angiopoietin-1. BiotechnolLett 31(8):1183-1189, Epub 2009 Apr 24.
16. Huang YC, Kaigler D, Rice KG, Krebsbach PH, Mooney DJ. 2005. Combined angiogenic and osteogenic factor delivery enhancesbone marrow stromal cell-driven bone regeneration. J BoneMiner Res 20(5):848-857, Epub 2004 Dec 20.
17. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, Jiang W, Luu HH, Luo J, Luo J, Szatkowski JP, Vanichakarn P, Park JY, Li Y, Haydon RC, He TC. 2004. Characterization of thedistinct orthotopic bone-forming activity of 14 BMPs usingrecombinant adenovirus-mediated gene delivery. Gene Ther 11:1312-1320.
18. Kempen DH, Lu L, Heijink A, Hefferan TE, Creemers LB, Maran A, Yaszemski MJ, Dhert WJ. 2009. Effect of localsequential VEGF and BMP-2 delivery on ectopic and orthotopicbone regeneration. Biomaterials 30(14):2816-2825, Epub2009 Feb 20.
19. Kern B, Shen J, Starbuck M, Karsenty G. 2001. Cbfa1 contributesto the osteoblast-specific expression of type I collagen genes. J Biol Chem 276:7101-7107.
20. Krause U, Seckinger A, Gregory CA. 2011. Assays of osteogenicdifferentiation by cultured human mesenchymal stem cells. Methods Mol Biol 698:215-230.
21. Kubo S, CooperGM, MatsumotoT, Phillippi JA, Corsi KA, Usas A, Li G, Fu FH, Huard J. 2009. Blocking vascular endothelialgrowth factor with soluble Flt-1 improves the chondrogenicpotential of mouse skeletal muscle-derived stem cells. ArthritisRheum 60(1):155-165.
22. Lee MH, Kwon TG, Park HS, Wozney JM, Ryoo HM. 2003. BMP-2-induced Osterix expression is mediated by Dlx5 but isindependent of Runx2. Biochem Biophys Res Commun 309:689-694.
23. Li X, Cui Q, Kao C, Wang GJ, Balian G, 2003a. Lovastatin inhibitsadipogenic and stimulates osteogenic differentiation by suppressingPPARgamma2 and increasing Cbfa1/Runx2 expression inbone marrow mesenchymal cell cultures. Bone 33:652-659.
24. Li JZ, Li H, Sasaki T, Holman D, Beres B, Dumont RJ, PittmanDD, Hankins GR, Helm GA. 2003b. Osteogenic potential offive different recombinant human bone morphogenetic proteinadenoviral vectors in the rat. Gene Ther 10:1735-1743.
25. Li G, Corsi-Payne K, Zheng B, Usas A, Peng H, Huard J. 2009. Thedose of growth factors influences the synergistic effect of vascularendothelial growth factor on bone morphogenetic protein4-induced ectopic bone formation. Tissue Eng Part A 15(8):2123-2133.
26. Matsubara T, Kida K, Yamaguchi A, Hata K, Ichida F, Meguro H, Aburatani H, Nishimura R, Yoneda T. 2008. BMP2 regulatesOsterix through Msx2 and Runx2 during osteoblast differentiation. J Biol Chem 283:29119-29125.
27. Matsumoto T, Cooper GM, Gharaibeh B, Meszaros LB, Li G, Usas A, Fu FH, Huard J. 2009. Cartilage repair in a rat model ofosteoarthritis through intraarticular transplantation of musclederivedstem cells expressing bone morphogenetic protein 4 andsoluble Flt-1. Arthritis Rheum 60(5):1390-1405.
28. Mizuno D, Agata H, Furue H, Kimura A, Narita Y, Watanabe N, Ishii Y, Ueda M, Tojo A, Kagami H. 2010. Limited butheterogeneous osteogenic response of human bone marrowmesenchymal stem cells to bone morphogenetic protein-2 andserum. Growth Factors 28:34-43.
29. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B. 2002. The novel zincfinger-containing transcription factor osterix is required forosteoblast differentiation and bone formation. Cell 108:17-29.
30. Osyczka AM, Diefenderfer DL, Bhargave G, Leboy PS. 2004. Different effects of BMP-2 on marrow stromal cells from humanand rat bone. Cells Tissues Organs 176:109-119.
31. Patel ZS, Young S, Tabata Y, Jansen JA, Wong ME, Mikos AG. 2008. Dual delivery of an angiogenic and an osteogenic growthfactor for bone regeneration in a critical size defect model. Bone43(5):931-940, Epub 2008 Jul 14.
32. Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, Huard J. 2002. Synergistic enhancement of bone formation andhealing by stem cell-expressed VEGF and bone morphogeneticprotein-4. J Clin Invest 110(6):751-759.
33. Peng H, Usas A, Olshanski A, Ho AM, Gearhart B, Cooper GM, Huard J. 2005. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulationof angiogenesis. J Bone Miner Res 20(11):2017-2027, Epub2005 Jul 18.
34. Puleo DA. 1997. Dependence of mesenchymal cell responses onduration of exposure to bone morphogenetic protein-2 in vitro. J Cell Physiol 173:93-101.
35. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, SaggioI, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P. 2007. Self-renewing osteoprogenitors in bone marrow sinusoidscan organize a hematopoietic microenvironment. Cell 131:324-336.
36. Saito M, Marumo K. 2010. Collagen cross-links as a determinant ofbone quality: A possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195-214.
37. Samee M, Kasugai S, Kondo H, Ohya K, Shimokawa H, Kuroda S. 2008. Bone morphogenetic protein-2 (BMP-2) and vascularendothelial growth factor (VEGF) transfection to humanperiosteal cells enhances osteoblast differentiation and boneformation. J Pharmacol Sci 108(1):18-31, Epub 2008 Sep 6.
38. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, ZhaoQ, Pukac L, Löwik CW, ten Dijke P. 2007. BMP-9 signals viaALK1 and inhibits bFGF-induced endothelial cell proliferationand VEGF-stimulated angiogenesis. J Cell Sci 120(Pt 6):964-972, Epub 2007 Feb 20.
39. Tallone T, Realini C, Böhmler A, Kornfeld C, Vassalli G, MoccettiT, Bardelli S, Soldati G. 2011. Adult human adipose tissuecontains several types of multipotent cells. J Cardiovasc TranslRes 4:200-210.
40. Turner CH. 2006. Bone strength: Current concepts. Ann NY AcadSci 1068:429-446.
41. Verrecchia F, Rossert J, Mauviel A. 2001. Blocking Sp1 transcriptionfactor broadly inhibits extracellular matrix gene expressionin vitro and in vivo: Implications for the treatment of tissuefibrosis. J Invest Dermatol 116:755-763.
42. Wang X, Cui F, Madhu V, Dighe AS, Balian G, Cui Q. 2011. Combined VEGF and LMP-1 delivery enhances osteoprogenitorcell differentiation and ectopic bone formation. GrowthFactors 29(1):36-48.
43. Weinand C, Nabili A, Khumar M, Dunn JR, Ramella-Roman J, JengJC, Jordan MH, Tabata Y. 2011. Factors of osteogenesisinfluencing various human stem cells on third-generationgelatin/B-tricalcium phosphate scaffold material. RejuvenationRes 14(2):185-194, Epub 2011 Jan 16.
44. Young S, Patel ZS, Kretlow JD, Murphy MB, Mountziaris PM, Baggett LS, Ueda H, Tabata Y, Jansen JA, Wong M, Mikos AG. 2009. Dose effect of dual delivery of vascular endothelial growthfactor and bone morphogenetic protein-2 on bone regenerationin a rat critical-size defect model. Tissue Eng Part A 15(9):2347-2362.
45. Zhang X, Yang M, Lin L, Chen P, Ma KT, Zhou CY, Ao YF. 2006. Epub 2006 Sep 11 Runx2 overexpression enhances osteoblasticdifferentiation and mineralization in adipose-derived stem cellsin vitro and in vivo. Calcif Tissue Int 79(3):169-178.
46. Zuk P, Chou YF, Mussano F, Benhaim P, Wu BM. 2011. Adiposederivedstem cells and BMP2: Part 2. BMP2 may not influencethe osteogenic fate of human adipose-derived stem cells. Connect Tissue Res 52:119-132.