Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 11, Issue , 2012, Pages 53-62

  Murphy, Ciara M ^a,b   Matsiko, Amos ^a,b   Haugh, Matthew G ^a,b   Gleeson, John P ^a,b   O'Brien, Fergal J ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Collagen GAG scaffold; Differentiation; Stem cell; Stiffness

Indexed keywords

AMINOPROPYL; CARBODIIMIDES; CELL BEHAVIOURS; CHONDROGENIC; CHONDROGENIC DIFFERENTIATION; CHONDROITIN SULPHATE; CROSSLINKING TREATMENT; EXTRACELLULAR MATRICES; GLYCOSAMINOGLYCANS; HYALURONIC ACIDS; IN-VIVO; INTRINSIC PROPERTY; MESENCHYMAL STEM CELL; MICROENVIRONMENTS; OSTEOGENIC; PHYSICAL EFFECTS; STEM CELL BIOLOGY; STEM CELL DIFFERENTIATION; STIFFNESS VALUES; THERAPEUTIC USE; UP-REGULATION;

CELL CULTURE; COLLAGEN; DIFFERENTIATION (CALCULUS); ELASTICITY; FLOWCHARTING; ORGANIC ACIDS; STEM CELLS; STIFFNESS; TISSUE;

SCAFFOLDS (BIOLOGY);

CHONDROITIN SULFATE; COLLAGEN; GENOMIC DNA; GLYCOSAMINOGLYCAN; RNA; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; COMPRESSION; CONTROLLED STUDY; CROSS LINKING; EXTRACELLULAR MATRIX; GENE EXPRESSION; MACHINE; MECHANICAL STRESS; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; STRESS STRAIN RELATIONSHIP;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CHONDROGENESIS; CHONDROITIN SULFATES; COLLAGEN; COMPRESSIVE STRENGTH; GLYCOSAMINOGLYCANS; HYALURONIC ACID; MALE; MECHANICAL PROCESSES; MESENCHYMAL STEM CELLS; MYOSIN TYPE II; OSTEOGENESIS; RATS; RATS, WISTAR; TISSUE SCAFFOLDS;

EID: 84861704819     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2011.11.009     Document Type: Article

References (49)

1. Acosta F.L., Lotz J., Ames C.P. The potential role of mesenchymal stem cell therapy for intervertebral disc degeneration: a critical overview. Neurosurg. Focus 2005, 19(3):E4.
2. Banu N., Tsuchiya T. Markedly different effects of hyaluronic acid and chondroitin sulfate-A on the differentiation of human articular chondrocytes in micromass and 3-D honeycomb rotation cultures. J. Biomed. Mater. Res. Part A 2007, 80(2):257-267.
3. Chamberlain L.J., Yannas I.V., Hsu H.P., Strichartz G., Spector M. Collagen-GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp. Neurol. 1998, 154(2):315-329.
4. Chen J., Li H., SundarRaj N., Wang J.H. Alpha-smooth muscle actin expression enhances cell traction force. Cell Motil. Cytoskelet. 2007, 64(4):248-257.
5. Dado D., Levenberg S. Cell-scaffold mechanical interplay within engineered tissue. Semin. Cell Dev. Biol. 2009, 20(6):656-664.
6. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310(5751):1139-1143.
7. Duffy G.P., McFadden T.M., Byrne E.M., Gill S.L., Farrell E., O'Brien F.J. Towards in vitro vascularisation of collagen-GAG scaffolds. Eur. Cells Mater. 2011, 21:15-30.
8. Dugina V., Fontao L., Chaponnier C., Vasiliev J., Gabbiani G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J. Cell Sci. 2001, 114(Pt. 18):3285-3296.
9. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689.
10. Farrell E., O'Brien F.J., Doyle P., Fischer J., Yannas I., Harley B.A., et al. A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along osteogenic and chondrogenic routes. Tissue Eng. 2006, 12(3):459-468.
11. Franceschi R.T., Xiao G. Regulation of the osteoblast-specific transcription factor, runx2: responsiveness to multiple signal transduction pathways. J. Cell. Biochem. 2003, 88(3):446-454.
12. Friedl P., Zanker K.S., Brocker E.B. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 1998, 43(5):369-378.
13. Harley B.A., Leung J.H., Silva E.C., Gibson L.J. Mechanical characterization of collagen-glycosaminoglycan scaffolds. Acta Biomater. 2007, 3(4):463-474.
14. Haugh M.G., Murphy C.M., McKiernan R.C., Altenbuchner C., O'Brien F.J. Crosslinking and mechanical properties significantly influence cell attachment, proliferation, and migration within collagen glycosaminoglycan scaffolds. Tissue Eng. Part A 2011, 17(9-10):1201-1208.
15. Haugh M.G., Murphy C.M., O'Brien F.J. Novel freeze-drying methods to produce a range of collagen-glycosaminoglycan scaffolds with tailored mean pore sizes. Tissue Eng. Part C Methods 2010, Epub adead of print.
16. Huang H., Kamm R.D., Lee R.T. Cell mechanics and mechanotransduction: pathways, probes, and physiology. Am. J. Physiol. Cell Physiol. 2004, 287(1):C1-C11.
17. Jungreuthmayer C., Donahue S.W., Jaasma M.J., Al-Munajjed A.A., Zanghellini J., Kelly D.J., et al. A comparative study of shear stresses in collagen-glycosaminoglycan and calcium phosphate scaffolds in bone tissue-engineering bioreactors. Tissue Eng. Part A 2009, 15(5):1141-1149.
18. Jungreuthmayer C., Jaasma M.J., Al-Munajjed A.A., Zanghellini J., Kelly D.J., O'Brien F.J. 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(4):420-427.
19. Karsenty G., Ducy P., Starbuck M., Priemel M., Shen J., Geoffroy V., et al. Cbfa1 as a regulator of osteoblast differentiation and function. Bone 1999, 25(1):107-108.
20. Keogh M.B., O'Brien F.J., Daly J.S. Substrate stiffness and contractile behaviour modulate the functional maturation of osteoblasts on a collagen-GAG scaffold. Acta Biomater. 2010, 6(11):4305-4313.
21. Ko K.S., McCulloch C.A. Intercellular mechanotransduction: cellular circuits that coordinate tissue responses to mechanical loading. Biochem. Biophys. Res. Commun. 2001, 285(5):1077-1083.
22. Krieg M., Arboleda-Estudillo Y., Puech P.H., Kafer J., Graner F., Muller D.J., et al. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 2008, 10(4):429-436.
23. Lee C.R., Grodzinsky A.J., Spector M. The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials 2001, 22(23):3145-3154.
24. Lee C.R., Grodzinsky A.J., Spector M. Modulation of the contractile and biosynthetic activity of chondrocytes seeded in collagen-glycosaminoglycan matrices. Tissue Eng. 2003, 9(1):27-36.
25. Lyons F.G., Al-Munajjed A.A., Kieran S.M., Toner M.E., Murphy C.M., Duffy G.P., et al. The healing of bony defects by cell-free collagen-based scaffolds compared to stem cell-seeded tissue engineered constructs. Biomaterials 2010, 31(35):9232-9243.
26. Martino M.M., Mochizuki M., Rothenfluh D.A., Rempel S.A., Hubbell J.A., Barker T.H. Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. Biomaterials 2009, 30(6):1089-1097.
27. Murphy C.M., Haugh M.G., O'Brien F.J. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010, 31(3):461-466.
28. Murphy C.M., O'Brien F.J. Understanding the effect of mean pore size on cell activity in collagen-glycosaminoglycan scaffolds. Cell Adh. Migr. 2010, 4(3).
29. Nehrer S., Domayer S., Dorotka R., Schatz K., Bindreiter U., Kotz R. Three-year clinical outcome after chondrocyte transplantation using a hyaluronan matrix for cartilage repair. Eur. J. Radiol. 2006, 57(1):3-8.
30. Ng L.J., Wheatley S., Muscat G.E., Conway-Campbell J., Bowles J., Wright E., et al. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 1997, 183(1):108-121.
31. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials 2004, 25(6):1077-1086.
32. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26(4):433-441.
33. Park J.S., Chu J.S., Tsou A.D., Diop R., Tang Z., Wang A., et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-[beta]. Biomaterials 2011, 32(16):3921-3930.
34. Pieper J.S., van Wachem P.B., van Luyn M.J.A., Brouwer L.A., Hafmans T., Veerkamp J.H., et al. Attachment of glycosaminoglycans to collagenous matrices modulates the tissue response in rats. Biomaterials 2000, 21(16):1689-1699.
35. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284(5411):143-147.
36. Rehfeldt F., Engler A.J., Eckhardt A., Ahmed F., Discher D.E. Cell responses to the mechanochemical microenvironment-implications for regenerative medicine and drug delivery. Adv. Drug Delivery. Rev. 2007, 59(13):1329-1339.
37. Reilly G.C., Engler A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 2010, 43(1):55-62.
38. Taylor K.R., Gallo R.L. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. Faseb J. 2006, 20(1):9-22.
39. Tierney C.M., Jaasma M.J., O'Brien F.J. Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations. J. Biomed. Mater. Res. Part A 2009, 91(1):92-101.
40. Tse J.R., Engler A.J. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 2011, 6(1):e15978.
41. van Susante J.L.C., Pieper J., Buma P., van Kuppevelt T.H., van Beuningen H., van Der Kraan P.M., et al. Linkage of chondroitin-sulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials 2001, 22(17):2359-2369.
42. Weadock K., Olson R.M., Silver F.H. Evaluation of collagen crosslinking techniques. Biomater. Med. Devices Artif. Organs 1983, 11(4):293-318.
43. Wollenweber M., Domaschke H., Hanke T., Boxberger S., Schmack G., Gliesche K., et al. Mimicked bioartificial matrix containing chondroitin sulphate on a textile scaffold of poly(3-hydroxybutyrate) alters the differentiation of adult human mesenchymal stem cells. Tissue Eng. 2006, 12(2):345-359.
44. Wu C.H., Ko C.S., Huang J.W., Huang H.J., Chu I.M. Effects of exogenous glycosaminoglycans on human chondrocytes cultivated on type II collagen scaffolds. J. Mater. Sci. Mater. Med. 2010, 21(2):725-729.
45. Yannas I.V. Tissue and Organ Regeneration in Adults 2001, Springer, New York.
46. Yannas I.V., Burke J.F., Huang C., Gordon P.L. Correlation of in vivo collagen degradation rate with in vitro measurement. J. Biomed. Mater. Res. 1975, 9:623-628.
47. Yannas I.V., Burke J.F., Huang C., Gordon P.L. Suppression of in vivo degradability and of immunogenicity of collagen by reaction with glycosaminoglycans. Polym. Prepr. (Am. Chem. Soc., Div. Polym. Chem.) 1975, 16(2):209-214.
48. Zajac A.L., Discher D.E. Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr. Opin. Cell Biol. 2008, 20(6):609-615.
49. Zeltinger J., Sherwood J.K., Graham D.A., Mueller R., Griffith L.G. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng. 2001, 7(5):557-572.