Orchestrating osteogenic differentiation of mesenchymal stem cells - Identification of placental growth factor as a mechanosensitive gene with a pro-osteogenic role

Stem Cells

Volumn 31, Issue 11, 2013, Pages 2420-2431

  McCoy, Ryan J ^a,b   Widaa, Amro ^a,b   Watters, Karen M ^a   Wuerstle, Maximilian ^a   Stallings, Ray L ^a   Duffy, Garry P ^a,b   O'Brien, Fergal J ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Bioreactors; Cellular mechanotransduction; Fracture healing; Osteogenesis; Placental growth factor

Indexed keywords

GLYCOSAMINOGLYCAN; PLACENTAL GROWTH FACTOR;

ACTIN POLYMERIZATION; ANGIOGENESIS; ANIMAL CELL; ARTICLE; BIOREACTOR; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE CONTROL; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; RAT; STEM CELL CULTURE; UMBILICAL VEIN ENDOTHELIAL CELL;

BIOREACTORS; CELLULAR MECHANOTRANSDUCTION; FRACTURE HEALING; OSTEOGENESIS; PLACENTAL GROWTH FACTOR;

ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; FRACTURE HEALING; GENE EXPRESSION; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICE; OSTEOGENESIS; PREGNANCY PROTEINS; RATS; RATS, WISTAR;

EID: 84887884772     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1482     Document Type: Article

References (94)

1. Ferguson C, Alpern E, Miclau T et al. Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev 1999; 87: 57-66. (Pubitemid 29428086)
2. Vortkamp A, Pathi S, Peretti GM et al. Recapitulation of signals regulating embryonic bone formation during postnatal growth and in fracture repair. Mech Dev 1998; 71: 65-76. (Pubitemid 28153519)
3. Morey E, Baylink D. Inhibition of bone formation during space flight. Science 1978; 201: 1138-1141. (Pubitemid 9044853)
4. Zerwekh JE, Ruml LA, Gottschalk F et al. The effects of twelve weeks of bed rest on bone histology, biochemical markers of bone turnover, and calcium homeostasis in eleven normal subjects. J Bone Miner Res 1998; 13: 1594-1601. (Pubitemid 28465300)
5. Bikle DD, Halloran BP. The response of bone to unloading. J Bone Miner Metab 1999; 17: 233-244.
6. Lanyon LE. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. J Biomech 1987; 20: 1083-1093. (Pubitemid 18010108)
7. Buckwalter JA. Effects of early motion on healing of musculoskeletal tissues. Hand Clin 1996; 12: 13-24. (Pubitemid 26073206)
8. Goodship AE, Kenwright J. The influence of induced micromovement upon the healing of experimental tibial fractures. J Bone Joint Surg Br 1985; 67B: 650-655. (Pubitemid 16228160)
9. Goodship AE, Cunningham JL, Kenwright J. Strain rate and timing of stimulation in mechanical modulation of fracture healing. Clin Orthop Relat Res 1998; (355 suppl):S105-S115.
10. Goodship AE, Lawes TJ, Rubin CT. Low-magnitude high-frequency mechanical signals accelerate and augment endochondral bone repair: Preliminary evidence of efficacy. J Orthop Res 2009; 27: 922-930.
11. Kenwright J, Goodship AE. Controlled mechanical stimulation in the treatment of tibial fractures. Clin Orthop Relat Res 1989: 36-47. (Pubitemid 19101241)
12. Kenwright J, Richardson JB, Cunningham JL et al. Axial movement and tibial fractures. A controlled randomised trial of treatment. J Bone Joint Surg Br 1991; 73B: 654-659.
13. Klein P, Schell H, Streitparth F et al. The initial phase of fracture healing is specifically sensitive to mechanical conditions. J Orthop Res 2003; 21: 662-669. (Pubitemid 36758210)
14. Le AX, Miclau T, Hu D et al. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res 2001; 19: 78-84. (Pubitemid 32288639)
15. Thompson Z, Miclau T, Hu D et al. A model for intramembranous ossification during fracture healing. J Orthop Res 2002; 20: 1091-1098.
16. Bancroft GN, Sikavitsas VI, van den Dolder J et al. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 2002; 99: 12600-12605.
17. Cartmell S, Porter BD, Garcia AJ et al. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng 2003; 9: 1197.
18. Datta N, Holtorf HL, Sikavitsas VI et al. Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 2005; 26: 971-977. (Pubitemid 39208984)
19. van den Dolder J, Bancroft GN, Sikavitsas VI et al. Flow perfusion culture of marrow stromal osteoblasts in titanium fiber mesh. J Biomed Mater Res 2003; 64A: 235-241. (Pubitemid 37521442)
20. Gomes ME, Sikavitsas VI, Behravesh E et al. Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J Biomed Mater Res A 2003; 67: 87-95. (Pubitemid 37517158)
21. Gomes ME, Holtorf HL, Reis RL et al. Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng 2006; 12: 801-809. (Pubitemid 43726522)
22. Holtorf HL, Datta N, Jansen JA et al. Scaffold mesh size affects the osteoblastic differentiation of seeded marrow stromal cells cultured in a flow perfusion bioreactor. J Biomed Mater Res A 2005; 74: 171-180. (Pubitemid 40995531)
23. Holtorf HL, Jansen JA, Mikos AG. Flow perfusion culture induces the osteoblastic differentiation of marrow stromal cell-scaffold constructs in the absence of dexamethasone. J Biomed Mater Res A 2005; 72: 326-334. (Pubitemid 40271003)
24. Holtorf HL, Sheffield TL, Ambrose CG et al. Flow perfusion culture of marrow stromal cells seeded on porous biphasic calcium phosphate ceramics. Ann Biomed Eng 2005; 33: 1238-1248. (Pubitemid 41240017)
25. Mueller SM, Mizuno S, Gerstenfeld LC et al. Medium perfusion enhances osteogenesis by murine osteosarcoma cells in three-dimensional collagen sponges. J Bone Miner Res 1999; 14: 2118-2126. (Pubitemid 30026961)
26. Sikavitsas VI, Bancroft GN, Holtorf HL et al. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci USA 2003; 100: 14683-14688. (Pubitemid 37517951)
27. Sikavitsas V, Bancroft G, Lemoine J et al. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann Biomed Eng 2005; 33: 63-70. (Pubitemid 40496060)
28. Vance J, Galley S, Liu DF et al. Mechanical stimulation of MC3T3 osteoblastic cells in a bone tissue-engineering bioreactor enhances prostaglandin E2 release. Tissue Eng 2005; 11: 1832-1839. (Pubitemid 43120195)
29. Keogh MB, Partap S, Daly JS et al. Three hours of perfusion culture prior to 28 days of static culture, enhances osteogenesis by human cells in a collagen GAG scaffold. Biotechnol Bioeng 2011; 108: 1203-1210.
30. Braccini A, Wendt D, Jaquiery C et al. Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells 2005; 23: 1066-1072. (Pubitemid 41377722)
31. Hofmann S, Hagenmuller H, Koch AM et al. Control of in vitro tissue-engineered bone-like structures using human mesenchymal stem cells and porous silk scaffolds. Biomaterials 2007; 28: 1152-1162. (Pubitemid 44822565)
32. Stiehler M, Bunger C, Baatrup A et al. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J Biomed Mater Res A 2009; 89: 96-107.
33. Jungreuthmayer C, Jaasma MJ, Al-Munajjed AA et al. Deformation simulation of cells seeded on a collagen-GAG scaffold in a flow perfusion bioreactor using a sequential 3D CFD-elastostatics model. Med Eng Phys 2009; 31: 420-427.
34. Stamenoviac D, Ingber DE. Models of cytoskeletal mechanics of adherent cells. Biomech Model Mechanobiol 2002; 1: 95-108.
35. Arnsdorf EJ, Tummala P, Kwon RY et al. Mechanically induced osteogenic differentiation - The role of Rho A, ROCKII and cytoskeletal dynamics. J Cell Sci 2009; 122: 546-553.
36. Ingber DE. Tensegrity: The architectural basis of cellular mechanotransduction. Annu Rev Physiol 1997; 59: 575-599. (Pubitemid 27142456)
37. McBeath R, Pirone DM, Nelson CM et al. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004; 6: 483-495. (Pubitemid 38456178)
38. Ruiz SA, Chen CS. Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells 2008; 26: 2921-2927.
39. Wang N, Naruse K, Stamenoviac D et al. Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci USA 2001; 98: 7765-7770. (Pubitemid 32642635)
40. Sen B, Guilluy C, Xie Z et al. Mechanically induced focal adhesion assembly amplifies anti-adipogenic pathways in mesenchymal stem cells. Stem Cells 2011; 29: 1829-1836.
41. Hoey DA, Tormey S, Ramcharan S et al. Primary cilia mediated mechanotransduction in human mesenchymal stem cells. Stem Cells 2012; 30: 2561-2570.
42. Sun Y, Chen CS, Fu J. Forcing stem cells to behave: A biophysical perspective of the cellular microenvironment. Ann Rev Biophys 2012; 41: 519-542.
43. Thompson WR, Rubin CT, Rubin J. Mechanical regulation of signaling pathways in bone. Gene 2012; 503: 179-193.
44. O'Brien F.J., Harley BA, Yannas IV et al. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials 2004; 25: 1077-1086. (Pubitemid 37393297)
45. Haugh MG, Murphy CM, O'Brien FJ. Novel freeze-drying methods to produce a range of collagen-glycosaminoglycan scaffolds with tailored mean pore sizes. Tissue Eng Part C: Methods 2010; 16: 887-894.
46. Murphy CM, Matsiko A, Haugh MG et al. Mesenchymal stem cell fate is regulated by the composition and mechanical properties of col-lagen- glycosaminoglycan scaffolds. J Mech Behav Biomed Mater 2012; 1: 53-62.
47. Jaasma MJ, Plunkett NA, O'Brien FJ. Design and validation of a dynamic flow perfusion bioreactor for use with compliant tissue engineering scaffolds. J Biotechnol 2008; 133: 490-496.
48. Murphy CM, Haugh MG, O'Brien FJ. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010; 31: 461-466.
49. Jaasma MJ, O'Brien FJ. Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng Part A 2008; 14: 1213-1223. (Pubitemid 351931508)
50. McCoy RJ, Jungreuthmayer C, O'Brien FJ. Influence of flow rate and scaffold pore size on cell behavior during mechanical stimulation in a flow perfusion bioreactor. Biotechnol Bioeng 2012; 109: 1583-1594.
51. McCoy RJ, O'Brien FJ. Influence of shear stress in perfusion bioreac-tor cultures for the development of 3D bone tissue constructs: A review. Tissue Eng Part B: Rev 2010; 16: 587-601.
52. Street J, Lenehan B. Vascular endothelial growth factor regulates osteoblast survival - Evidence for an autocrine feedback mechanism. J Orthop Surg Res 2009; 4: 19.
53. Abramoff M, Magelhaes P, Ram S. Image processing with ImageJ. Biophotonics Int 2004; 11: 36-42.
54. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT Method. Methods 2001; 25: 402-408. (Pubitemid 34164012)
55. Bolstad BM, Irizarry RA, Astrand M et al. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003; 19: 185-193. (Pubitemid 36181903)
56. Irizarry RA, Hobbs B, Collin F et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Bio-statistics 2003; 4: 249-264.
57. Maes C, Coenegrachts L, Stockmans I et al. Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest 2006; 116: 1230-1242.
58. Fiedler J, Leucht F, Waltenberger J et al. VEGF - A and PlGF-1 stimulate chemotactic migration of human mesenchymal progenitor cells. Biochem Biophys Res Commun 2005; 334: 561-568. (Pubitemid 40982403)
59. Jacobsen KA, Al-Aql ZS, Wan C et al. Bone formation during distraction osteogenesis is dependent on both VEGFR1 and VEGFR2 signaling. J Bone Miner Res 2008; 23: 596-609. (Pubitemid 351575014)
60. Otomo H, Sakai A, Uchida S et al. Flt-1 tyrosine kinase-deficient homozygous mice result in decreased trabecular bone volume with reduced osteogenic potential. Bone 2007; 40: 1494-1501. (Pubitemid 46756416)
61. Aldridge SE, Lennard TWJ, Williams JR et al. Vascular endothelial growth factor receptors in osteoclast differentiation and function. Bio-chem Biophys Res Commun 2005; 335: 793-798. (Pubitemid 41188268)
62. Niida S, Kondo T, Hiratsuka S et al. VEGF receptor 1 signaling is essential for osteoclast development and bone marrow formation in colony-stimulating factor 1-deficient mice. PNAS 2005; 102: 14016-14021. (Pubitemid 41377695)
63. Henriksen K, Karsdal M, Delaisse J-M et al. RANKL and vascular endothelial growth factor (VEGF) induce osteoclast chemotaxis through an ERK1/2-dependent mechanism. J Biol Chem 2003; 278: 48745-48753. (Pubitemid 41079516)
64. Hattori K, Heissig B, Wu Y et al. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1+ stem cells from bone-marrow microenvironment. Nat Med 2002; 8: 841-849.
65. Maes C, Carmeliet G, Schipani E. Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol 2012; 8: 358-366.
66. Miralles F, Visa N. Actin in transcription and transcription regulation. Curr Opin Cell Biol 2006; 18: 261-266.
67. Selvakumar, B. Hess DT, Goldschmidt-Clermont PJ et al. Co-regulation of constitutive nitric oxide synthases and NADPH oxidase by the small GTPase Rac. FEBS Lett 2008; 582: 2195-2202.
68. Ushio-Fukai M., Urao N. Novel role of NADPH oxidase in angiogene-sis and stem/progenitor cell function. Antioxid Redox Signal 2009; 11: 2517-2533.
69. Wang FS, Wang CJ, Sheen-Chen SM et al. Superoxide mediates shock wave induction of ERK-dependent osteogenic transcription factor (cBFA1) and mesenchymal cell differentiation toward osteoprogenitors. J Biol Chem 2002; 277: 10931-10937.
70. Wang FS, Wang CJ, Chen YJ et al. Ras induction of superoxide activates ERK-dependent angiogenic transcription factor HIF-1a and VEGF - A expression in shock wave-stimulated osteoblasts. J Biol Chem 2004; 279: 10331-10337.
71. Van Lent P.L., Nabbe KC, Blom AB et al NADPH-oxidase-driven oxygen radical production determines chondrocyte death and partly regulates metalloproteinase-mediated cartilage matrix degradation during interferon-gamma-stimulated immune complex arthritis. Arthritis Res Ther 2005; 7:R885-R895.
72. Mandal CC, Ganapathy S, Gorin, Y et al. Reactive oxygen species derived from Nox4 mediate BMP2 gene transcription and osteoblast differentiation. Biochem J 2011; 433: 393-402.
73. Marrony S, Bassilana F, Seuwen K et al. Bone morphogenetic protein 2 induces placental growth factor in mesenchymal stem cells. Bone 2003; 33: 426-433. (Pubitemid 37103259)
74. Hassan MQ, Tare RS, Lee SH et al BMP2 commitment to the osteo-genic lineage involves activation of Runx2 by DLX3 and a homeodo-main transcriptional network. J Biol Chem 2006; 29: 281: 40515-40526. (Pubitemid 46041853)
75. Fang TD, Salim A, Xia W et al. Angiogenesis is required for successful bone induction during distraction osteogenesis. J Bone Miner Res 2005; 20: 1114-1124. (Pubitemid 40863799)
76. Klein-Nulend J., Sterck JG, Semeins CM et al. Donor age and mecha-nosensitivity of human bone cells. Osteoporosis Int 2002; 13: 137-146. (Pubitemid 34241034)
77. Sterck JG, Klein-Nulend J, Lips P et al. Response of normal and osteoporotic human bone cells to mechanical stress in vitro. Am J Physiol 1998; 274(6 Pt 1):E1113-E1120.
78. Mulvihill BM, McNamara LM, Prendergast PJ. Loss of trabeculae by mechano-biological means may explain rapid bone loss in osteoporosis. J R Soc Interface 2008; 5: 1243-1253.
79. Van Rietbergen B., Huiskes R, Eckstein F et al. Trabecular bone tissue strains in the healthy and osteoporotic human femur. J Bone Miner Res 2003; 18: 1781-1788. (Pubitemid 37322555)
80. Rubin CT, Bain SD, McLeod KJ. Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 1992; 50: 306-313.
81. Lill CA, Hesseln J, Schlegel U et al. Biomechanical evaluation of healing in a non-critical defect in a large animal model of osteoporosis. J Orthop Res 2003; 21: 836-842. (Pubitemid 37045561)
82. Kubo T, Shiga T, Hashimoto J et al. Osteoporosis influences the late period of fracture healing in a rat model prepared by ovariectomy and low calcium diet. J Steroid Biochem Mol Biol 1999; 68: 197-202. (Pubitemid 29290655)
83. Duffy GP, Ahsan T, O'Brien T et al. Bone marrow-derived mesenchy-mal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro. Tissue Eng Part A 2009; 15: 2459-2470.
84. Goodwin A. In vitro assays of angiogenesis for assessment of angio-genic and anti-angiogenic agents. Microvasc Res 2007; 74: 172-183. (Pubitemid 350064283)
85. Kubota Y, Kleinman HK, Martin GR et al. Role of laminin and basement membrane in the morphological differentiation of human endo-thelial cells into capillary-like structures. J Cell Biol 1988; 107: 1589-1598.
86. Autiero M, Waltenberger J, Communi D et al. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med 2003; 9: 936-943. (Pubitemid 36889938)
87. Cao Y, Chen H, Zhou L et al. Heterodimers of Placenta growth factor/vascular endothelial growth factor endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J Biol Chem 1996; 271: 3154-3162. (Pubitemid 26060529)
88. DiSalvo J, Bayne ML, Conn G et al. Purification and characterization of a naturally occurring vascular endothelial growth factor placenta growth factor heterodimer. J Biol Chem 1995; 270: 7717-7723.
89. Street J, Bao M, de Guzman L et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. PNAS 2002; 99: 9656-9661. (Pubitemid 34831103)
90. Maes C, Carmeliet P, Moermans K et al. Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 2002; 111: 61-73. (Pubitemid 34136979)
91. Lee K, Silva EA, Mooney DJ. Growth factor delivery-based tissue engineering: General approaches and a review of recent developments. J R Soc Interface 2011; 8: 153-170.
92. Patil SD, Rhodes DG, Burgess DJ. DNA-based therapeutics and DNA delivery systems: A comprehensive review. AAPS J 2005; 7:E61-E77. (Pubitemid 41554297)
93. Curtin CM, Cunniffe GM, Lyons FG et al. Innovative collagen nano-hydroxyapatite scaffolds offer a highly efficient non-viral gene delivery platform for stem cell-mediated bone formation. Adv Mater 2012; 24: 749-754.
94. Tierney EG, Duffy GP, Hibbitts AJ et al. The development of non-viral gene-activated matrices for bone regeneration using polyethyle-neimine (PEI) and collagen-based scaffolds. J Control Release 2012; 158: 304-311.