Substrate stiffness and oxygen as regulators of stem cell differentiation during skeletal tissue regeneration: A mechanobiological model

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Burke, Darren Paul ^a   Kelly, Daniel John ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

ADIPOGENESIS; ANGIOGENESIS; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; BONE TISSUE; CARTILAGE; CELL DIFFERENTIATION; CELL FATE; CHONDROGENESIS; COMPUTATIONAL MODEL; ENDOSTEUM; ENVIRONMENTAL FACTOR; FRACTURE; FRACTURE HEALING; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL MODEL; MECHANOBIOLOGICAL MODEL; MESENCHYMAL STEM CELL; MODEL; OXYGEN TENSION; PERIOSTEUM; PHYSICAL PARAMETERS; PREDICTION; SIMULATION; SUBSTRATE STIFFNESS; TISSUE DIFFERENTIATION;

BIOMECHANICS; CELL DIFFERENTIATION; COMPUTER SIMULATION; MESENCHYMAL STROMAL CELLS; MODELS, THEORETICAL; NEOVASCULARIZATION, PHYSIOLOGIC; ORGANOGENESIS; OXYGEN CONSUMPTION; REGENERATION;

EID: 84864269916     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040737     Document Type: Article

References (79)

1. Pauwels F, (1960) [A new theory on the influence of mechanical stimuli on the differentiation of supporting tissue. The tenth contribution to the functional anatomy and causal morphology of the supporting structure]. Z Anat Entwicklungsgesch 121: 478-515.
2. Carter DR, Beaupre GS, Giori NJ, Helms JA, (1998) Mechanobiology of skeletal regeneration. Clin Orthop Relat Res pp. S41-55.
3. Carter DR, Blenman PR, Beaupre GS, (1988) Correlations between mechanical stress history and tissue differentiation in initial fracture healing. J Orthop Res 6: 736-748.
4. Claes LE, Heigele CA, (1999) Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J Biomech 32: 255-266.
5. Prendergast PJ, Huiskes R, Soballe K, (1997) ESB Research Award 1996. Biophysical stimuli on cells during tissue differentiation at implant interfaces. J Biomech 30: 539-548.
6. Isaksson H, Wilson W, van Donkelaar CC, Huiskes R, Ito K, (2006) Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing. J Biomech 39: 1507-1516.
7. Lacroix D, Prendergast PJ, (2002) A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 35: 1163-1171.
8. Kelly DJ, Prendergast PJ, (2005) Mechano-regulation of stem cell differentiation and tissue regeneration in osteochondral defects. Journal of Biomechanics 38: 1413-1422.
9. Kelly DJ, Prendergast PJ, (2006) Prediction of the optimal mechanical properties for a scaffold used in osteochondral defect repair. Tissue Engineering 12: 2509-2519.
10. Boccaccio A, Kelly DJ, Pappalettere C, (2011) A mechano-regulation model of fracture repair in vertebral bodies. J Orthop Res 29: 433-443.
11. Isaksson H, Comas O, van Donkelaar CC, Mediavilla J, Wilson W, et al. (2007) Bone regeneration during distraction osteogenesis: Mechano-regulation by shear strain and fluid velocity. Journal of Biomechanics 40: 2002-2011.
12. Boccaccio A, Prendergast PJ, Pappalettere C, Kelly DJ, (2008) Tissue differentiation and bone regeneration in an osteotomized mandible: A computational analysis of the latency period. Medical and Biological Engineering and Computing 46: 283-298.
13. Boccaccio A, Pappalettere C, Kelly D, (2007) The Influence of Expansion Rates on Mandibular Distraction Osteogenesis: A Computational Analysis. Annals of Biomedical Engineering 35: 1940-1960.
14. Khayyeri H, Checa S, Tagil M, Prendergast PJ, (2009) Corroboration of mechanobiological simulations of tissue differentiation in an in vivo bone chamber using a lattice-modeling approach. J Orthop Res 27: 1659-1666.
15. Nagel T, Kelly DJ, (2010) Mechano-regulation of mesenchymal stem cell differentiation and collagen organisation during skeletal tissue repair. Biomech Model Mechanobiol 9: 359-372.
16. Hayward LN, Morgan EF, (2009) Assessment of a mechano-regulation theory of skeletal tissue differentiation in an in vivo model of mechanically induced cartilage formation. Biomech Model Mechanobiol.
17. Vetter A, Witt F, Sander O, Duda GN, Weinkamer R, (2011) The spatio-temporal arrangement of different tissues during bone healing as a result of simple mechanobiological rules. Biomech Model Mechanobiol.
18. Holzwarth C, Vaegler M, Gieseke F, Pfister SM, Handgretinger R, et al. (2010) Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol 11: 11.
19. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, et al. (2007) Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 6: 745-757.
20. Yun Z, Maecker HL, Johnson RS, Giaccia AJ, (2002) Inhibition of PPAR [gamma]2 Gene Expression by the HIF-1-Regulated Gene DEC1/Stra13: A Mechanism for Regulation of Adipogenesis by Hypoxia. Developmental Cell 2: 331-341.
21. Merceron C, Vinatier C, Portron S, Masson M, Amiaud J, et al. (2010) Differential effects of hypoxia on osteochondrogenic potential of human adipose-derived stem cells. American Journal of Physiology - Cell Physiology 298: C355-C364.
22. Hausman MR, Schaffler MB, Majeska RJ, (2001) Prevention of fracture healing in rats by an inhibitor of angiogenesis. Bone 29: 560-564.
23. Claes L, Eckert-Hubner K, Augat P, (2002) The effect of mechanical stability on local vascularization and tissue differentiation in callus healing. J Orthop Res 20: 1099-1105.
24. Checa S, Prendergast PJ, (2009) A mechanobiological model for tissue differentiation that includes angiogenesis: a lattice-based modeling approach. Ann Biomed Eng 37: 129-145.
25. Chen G, Niemeyer F, Wehner T, Simon U, Schuetz MA, et al. (2009) Simulation of the nutrient supply in fracture healing. J Biomech 42: 2575-2583.
26. Geris L, Gerisch A, Sloten JV, Weiner R, Oosterwyck HV, (2008) Angiogenesis in bone fracture healing: a bioregulatory model. J Theor Biol 251: 137-158.
27. Geris L, Vandamme K, Naert I, Vander Sloten J, Van Oosterwyck H, et al. (2010) Mechanical loading affects angiogenesis and osteogenesis in an in vivo bone chamber: a modeling study. Tissue Eng Part A 16: 3353-3361.
28. Peiffer V, Gerisch A, Vandepitte D, Van Oosterwyck H, Geris L, (2011) A hybrid bioregulatory model of angiogenesis during bone fracture healing. Biomech Model Mechanobiol 10: 383-395.
29. Hirao M, Tamai N, Tsumaki N, Yoshikawa H, Myoui A, (2006) Oxygen tension regulates chondrocyte differentiation and function during endochondral ossification. J Biol Chem 281: 31079-31092.
30. Kanichai M, Ferguson D, Prendergast PJ, Campbell VA, (2008) Hypoxia promotes chondrogenesis in rat mesenchymal stem cells: a role for AKT and hypoxia-inducible factor (HIF)-1alpha. J Cell Physiol 216: 708-715.
31. Meyer EG, Buckley CT, Thorpe SD, Kelly DJ, (2010) Low oxygen tension is a more potent promoter of chondrogenic differentiation than dynamic compression. J Biomech 43: 2516-2523.
32. Buckley CT, Vinardell T, Kelly DJ, (2010) Oxygen tension differentially regulates the functional properties of cartilaginous tissues engineered from infrapatellar fat pad derived MSCs and articular chondrocytes. Osteoarthritis and Cartilage 18: 1345-1354.
33. Taylor DK, Meganck JA, Terkhorn S, Rajani R, Naik A, et al. (2009) Thrombospondin-2 influences the proportion of cartilage and bone during fracture healing. J Bone Miner Res 24: 1043-1054.
34. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix Elasticity Directs Stem Cell Lineage Specification. Cell 126: 677-689.
35. Pek YS, Wan AC, Ying JY, (2010) The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31: 385-391.
36. Park JS, Chu JS, Tsou AD, Diop R, Tang Z, et al. (2011) The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-beta. Biomaterials 32: 3921-3930.
37. Vetter A, Epari DR, Seidel R, Schell H, Fratzl P, et al. (2010) Temporal tissue patterns in bone healing of sheep. J Orthop Res 28: 1440-1447.
38. Cenni E, (2005) ANGIOGENESIS AND BONE REGENERATION. J Bone Joint Surg Br 87-B: 58-.
39. Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, et al. (2002) Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A 99: 9656-9661.
40. Cao Y, (2007) Angiogenesis modulates adipogenesis and obesity. The Journal of Clinical Investigation 117: 2362-2368.
41. Gomillion CT, Burg KJ, (2006) Stem cells and adipose tissue engineering. Biomaterials 27: 6052-6063.
42. Hausman GJ, Richardson RL, (2004) Adipose tissue angiogenesis. J Anim Sci 82: 925-934.
43. Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M, (2008) Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40: 46-62.
44. Roach HI, Erenpreisa J, Aigner T, (1995) Osteogenic differentiation of hypertrophic chondrocytes involves asymmetric cell divisions and apoptosis. J Cell Biol 131: 483-494.
45. Kronenberg HM, (2003) Developmental regulation of the growth plate. Nature 423: 332-336.
46. Mente PL, Lewis JL, (1994) Elastic modulus of calcified cartilage is an order of magnitude less than that of subchondral bone. J Orthop Res 12: 637-647.
47. Frost HM, (1990) Skeletal structural adaptations to mechanical usage (SATMU): 1. Redefining Wolff's law: the bone modeling problem. Anat Rec 226: 403-413.
48. Rubin C, Lanyon L, (1985) Regulation of bone mass by mechanical strain magnitude. Calcified Tissue International 37: 411-417.
49. Brueton RN, Brookes M, Heatley FW, (1990) The vascular repair of an experimental osteotomy held in an external fixator. Clinical Orthopaedics and Related Research pp. 286-304.
50. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA, (2003) Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 88: 873-884.
51. Simon U, Augat P, Utz M, Claes L, (2011) A numerical model of the fracture healing process that describes tissue development and revascularisation. Comput Methods Biomech Biomed Engin 14: 79-93.
52. Krinner A, Zscharnack M, Bader A, Drasdo D, Galle J, (2009) Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif 42: 471-484.
53. Pattappa G, Heywood HK, de Bruijn JD, Lee DA, (2010) The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol.
54. Hershey D, Karhan T, (1968) Diffusion coefficients for oxygen transport in whole blood. AIChE Journal 14: 969-972.
55. Epari DR, Lienau J, Schell H, Witt F, Duda GN, (2008) Pressure, oxygen tension and temperature in the periosteal callus during bone healing - an in vivo study in sheep. Bone 43: 734-739.
56. Lacroix D, Prendergast PJ, Li G, Marsh D, (2002) Biomechanical model to simulate tissue differentiation and bone regeneration: application to fracture healing. Med Biol Eng Comput 40: 14-21.
57. Lacroix D, (2000) Simulation of tissue differentiation during fracture healing. Dublin: Trinity College Dublin.
58. Prendergast PJ, (1997) Finite element models in tissue mechanics and orthopaedic implant design. Clin Biomech (Bristol, Avon) 12: 343-366.
59. Gómez-Benito MJ, García-Aznar JM, Kuiper JH, Doblaré M, (2005) Influence of fracture gap size on the pattern of long bone healing: A computational study. Journal of Theoretical Biology 235: 105-119.
60. Byrne DP, Lacroix D, Prendergast PJ, (2011) Simulation of fracture healing in the tibia: Mechanoregulation of cell activity using a lattice modeling approach. J Orthop Res.
61. Sheehy EJ, Buckley CT, Kelly DJ, (2012) Oxygen tension regulates the osteogenic, chondrogenic and endochondral phenotype of bone marrow derived mesenchymal stem cells. Biochem Biophys Res Commun 417: 305-310.
62. Yin M, Gentili C, Koyama E, Zasloff M, Pacifici M, (2002) Antiangiogenic treatment delays chondrocyte maturation and bone formation during limb skeletogenesis. J Bone Miner Res 17: 56-65.
63. Vinardell T, Rolfe RA, Buckley CT, Meyer EG, Ahearne M, et al. (2012) Hydrostatic pressure acts to stabilise a chondrogenic phenotype in porcine joint tissue derived stem cells. Eur Cell Mater 23: 121-134.
64. Bian L, Zhai DY, Zhang EC, Mauck RL, Burdick JA, (2012) Dynamic Compressive Loading Enhances Cartilage Matrix Synthesis and Distribution and Suppresses Hypertrophy in hMSC-Laden Hyaluronic Acid Hydrogels. Tissue Eng Part A 18: 715-724.
65. Steward AJ, Thorpe SD, Vinardell T, Buckley CT, Wagner DR, et al. (2012) Cell-matrix interactions regulate mesenchymal stem cell response to hydrostatic pressure. Acta Biomater 8: 2153-2159.
66. Boerckel JD, Uhrig BA, Willett NJ, Huebsch N, Guldberg RE, (2011) Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc Natl Acad Sci U S A 108: E674-680.
67. Lienau J, Schell H, Duda GN, Seebeck P, Muchow S, et al. (2005) Initial vascularization and tissue differentiation are influenced by fixation stability. J Orthop Res 23: 639-645.
68. Gomez-Benito MJ, Garcia-Aznar JM, Kuiper JH, Doblare M, (2005) Influence of fracture gap size on the pattern of long bone healing: a computational study. J Theor Biol 235: 105-119.
69. Garcia-Aznar JM, Kuiper JH, Gomez-Benito MJ, Doblare M, Richardson JB, (2007) Computational simulation of fracture healing: influence of interfragmentary movement on the callus growth. J Biomech 40: 1467-1476.
70. Bailon-Plaza A, van der Meulen MC, (2001) A mathematical framework to study the effects of growth factor influences on fracture healing. J Theor Biol 212: 191-209.
71. Garcia P, Pieruschka A, Klein M, Tami A, Histing T, et al. (2012) Temporal and spatial vascularization patterns of unions and nonunions: role of vascular endothelial growth factor and bone morphogenetic proteins. J Bone Joint Surg Am 94: 49-58.
72. Geris L, Reed AA, Vander Sloten J, Simpson AH, Van Oosterwyck H, (2010) Occurrence and treatment of bone atrophic non-unions investigated by an integrative approach. PLoS Comput Biol 6: e1000915.
73. Kelly DJ, Jacobs CR, (2010) The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defects Research Part C - Embryo Today: Reviews 90: 75-85.
74. Ma T, Grayson WL, Frohlich M, Vunjak-Novakovic G, (2009) Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol Prog 25: 32-42.
75. Hori RY, Lewis JL, (1982) Mechanical properties of the fibrous tissue found at the bone-cement interface following total joint replacement. J Biomed Mater Res 16: 911-927.
76. Armstrong CG, Mow VC, (1982) Variations in the Intrinsic Mechanical Proterties of Human Articular-Cartilage with Age, Degeneration, and Water-Content. Journal of Bone and Joint Surgery-American Volume 64: 88-94.
77. Ochoa JA, Hillberry BM, (1992) Permeability of bovine cancellous bone. Trans of the 38th ORS.
78. Cowin SC, (1999) Bone poroelasticity. J Biomech 32: 217-238.
79. Schaffler MB, Burr DB, (1988) Stiffness of compact bone: effects of porosity and density. J Biomech 21: 13-16.