Fibrous hyaluronic acid hydrogels that direct MSC chondrogenesis through mechanical and adhesive cues

Biomaterials

Volumn 34, Issue 22, 2013, Pages 5571-5580

  Kim, Iris L ^a   Khetan, Sudhir ^a   Baker, Brendon M ^a   Chen, Christopher S ^a   Burdick, Jason A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biomaterials; Biomechanics; Chondrogenesis; Electrospinning; Hyaluronic acid; Mesenchymal stem cells

Indexed keywords

CHONDROGENESIS; CHONDROGENIC MARKERS; CROSS-LINK DENSITIES; CYTOSKELETAL ORGANIZATION; EXTRACELLULAR MATRICES; HUMAN MESENCHYMAL STEM CELLS; HYALURONIC ACID HYDROGELS; MESENCHYMAL STEM CELL;

BIOMATERIALS; BIOMECHANICS; CARTILAGE; CELL CULTURE; CROSSLINKING; ELECTROSPINNING; FIBERS; GENE EXPRESSION; HYALURONIC ACID; HYDROGELS; NANOFIBERS; ORGANIC ACIDS; REPAIR; STEM CELLS; TISSUE;

SCAFFOLDS (BIOLOGY);

BIOMATERIAL; HYALURONIC ACID;

ADHESION; ARTICLE; BIOMECHANICS; CELL DENSITY; CELL INTERACTION; CELL PROLIFERATION; CELL SPREADING; CHONDROGENESIS; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYME CELL; PRIORITY JOURNAL; STEM CELL;

ADHESIVENESS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHONDROGENESIS; FOCAL ADHESIONS; GENE EXPRESSION REGULATION; HUMANS; HYALURONIC ACID; HYDROGELS; MECHANICAL PHENOMENA; MESENCHYMAL STROMAL CELLS; METHACRYLATES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; MICROSPHERES; OLIGOPEPTIDES; TISSUE SCAFFOLDS; VINCULIN;

EID: 84877601845     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.04.004     Document Type: Article

References (54)

1. Marklein R.A., Burdick J.A. Controlling stem cell fate with material design. Adv Mater 2010, 22:175-189.
2. Wade R.J., Burdick J.A. Engineering ECM signals into biomaterials. Mater Today 2012, 15:454-459.
3. Engler A., Sen S., Sweeney H., Discher D. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
4. Guvendiren M., Burdick J.A. Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat Commun 2012, 3:792.
5. Huebsch N., Arany P.R., Mao A.S., Shvartsman D., Ali O.A., Bencherif S.A., et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010, 9:518-526.
6. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712.
7. Kato M., Mrksich M. Using model substrates to study the dependence of focal adhesion formation on the affinity of integrin-ligand complexes. Biochemistry 2004, 43:2699-2707.
8. Wang X., Yan C., Ye K., He Y., Li Z., Ding J. Effect of RGD nanospacing on differentiation of stem cells. Biomaterials 2013, 34:2865-2874.
9. Comisar W.A., Kazmers N.H., Mooney D.J., Linderman J. Engineering RGD nanopatterned hydrogels to control preosteoblast behavior: a combined computational and experimental approach. Biomaterials 2007, 28:4409-4417.
10. Connelly J.T., García A.J., Levenston M.E. Inhibition of invitro chondrogenesis inRGD-modified three-dimensional alginate gels. Biomaterials 2007, 28:1071-1083.
11. Rowlands A.S., George P.A., Cooper-White J.J. Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation. Am J Physiol Cell Physiol 2008, 295:C1037-C1044.
12. Chung C., Burdick J. Engineering cartilage tissue. Adv Drug Deliv Rev 2008, 60:243-262.
13. Ahmed T.A.E., Hincke M.T. Strategies for articular cartilage lesion repair and functional restoration. Tissue Eng Part B Rev 2010, 16:305-329.
14. Gao L., McBeath R., Chen C.S. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 2010, 28:564-572.
15. Woods A., Beier F. RhoA/ROCK signaling regulates chondrogenesis in a context-dependent manner. JBiol Chem 2006, 281:13134-13140.
16. Salinas C., Anseth K. The influence of the RGD peptide motif and its contextual presentation in PEG gels on human mesenchymal stem cell viability. JTissue Eng Regen Med 2008, 2:296-304.
17. Huang A.H., Farrell M.J., Mauck R.L. Mechanics and mechanobiology of mesenchymal stem cell-based engineered cartilage. JBiomech 2010, 43:128-136.
18. Baker B.M., Handorf A.M., Ionescu L.C., Li W.-J., Mauck R.L. New directions in nanofibrous scaffolds for soft tissue engineering and regeneration. Expert Rev Med Devices 2009, 6:515-532.
19. Baker B.M., Gee A.O., Metter R.B., Nathan A.S., Marklein R.A., Burdick J.A., et al. The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials 2008, 29:2348-2358.
20. Nerurkar N.L., Sen S., Baker B.M., Elliott D.M., Mauck R.L. Dynamic culture enhances stem cell infiltration and modulates extracellular matrix production on aligned electrospun nanofibrous scaffolds. Acta Biomater 2011, 7:485-491.
21. Alves da Silva M.L., Martins A., Costa-Pinto A.R., Costa P., Faria S., Gomes M., et al. Cartilage tissue engineering using electrospun PCL nanofiber meshes and MSCs. Biomacromolecules 2010, 11:3228-3236.
22. Li W.-J., Tuli R., Okafor C., Derfoul A., Danielson K.G., Hall D.J., et al. Athree-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 2005, 26:599-609.
23. Wise J.K., Yarin A.L., Megaridis C.M., Cho M. Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superifical zone of articular cartilage. Tissue Eng Part A 2009, 15:913-921.
24. Spaddacio C., Rainer A., Trombetta M., Vadala G., Chello M., Covino E., et al. Poly-l-lactic acid/hydroxyapatite electrospun nanocomposites induce chondrogenic differentiation of human MSC. Ann Biomed Eng 2009, 37:1376-1389.
25. Xin X., Hussain M., Mao J. Continuing differentiation of human mesenchymal stem cells and induced chondrogenic and osteogenic lineages in electrospun PLGA nanofiber scaffold. Biomaterials 2007, 28:316-325.
26. Noriega S., Hasanova G., Schneider M., Larsen G., Subramanian A. Effect of fiber diameter on the spreading, proliferation and differentiation of chondrocytes on electrospun chitosan matrices. Cells Tissues Organs 2012, 195:207-221.
27. Shafiee A., Soleimani M., Chamheidari G., Seyedjafari E., Dodel M., Atashi A., et al. Electrospun nano-fiber based regeneration of cartilage enhanced by mesenchymal stem cells. JBiomed Mater Res A 2011, 99:467-478.
28. Chen M., Patra P.K., Lovett M.L., Kaplan D.L., Bhowmick S. Role of electrospun fibre diameter and corresponding specific surface area (SSA) on cell attachment. JTissue Eng Regen Med 2009, 3:269-279.
29. Nam J., Johnson J., Lannutti J.J., Agarwal S. Modulation of embryonic mesenchymal progenitor cell differentiation via control over pure mechanical modulus in electrospun nanofibers. Acta Biomater 2011, 7:1516-1524.
30. Burdick J.A., Prestwich G.D. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 2011, 23:H41-H56.
31. Kim I.L., Mauck R.L., Burdick J.A. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 2011, 32:8771-8782.
32. DeLise A., Fischer L., Tuan R.S. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 2000, 8:309-334.
33. Chung C., Burdick J.A. Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng Part A 2009, 15:243-254.
34. Burdick J.A., Chung C., Jia X.Q., Randolph M.A., Langer R. Controlled degradation and mechanical behavior of photopolymerized hyaluronic acid networks. Biomacromolecules 2005, 6:386-391.
35. Sundararaghavan H.G., Burdick J.A. Gradients with depth in electrospun fibrous scaffolds for directed cell behavior. Biomacromolecules 2011, 12:2344-2350.
36. Sundararaghavan H.G., Metter R.B., Burdick J.A. Electrospun fibrous scaffoldswith multiscale and photopatterned porosity. Macromol Biosci 2010, 10:265-270.
37. Marklein R.A., Burdick J.A. Spatially controlled hydrogel mechanics to modulate stem cell interactions. Soft Matter 2009, 6:136-143.
38. Tan E., Lim C. Physical properties of a single polymeric nanofiber. Appl Phys Lett 2004, 84:1603-1605.
39. Bian L., Zhai D.Y., Tous E., Rai R., Mauck R.L., Burdick J.A. Enhanced MSC chondrogenesis following delivery of TGF-beta 3 from alginate microspheres within hyaluronic acid hydrogels invitro and invivo. Biomaterials 2011, 32:6425-6434.
40. Legant W.R., Miller J.S., Blakely B.L., Cohen D.M., Genin G.M., Chen C.S. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat Methods 2010, 7:969-971.
41. Schuh E., Hofmann S., Stok K., Notbohm H., Müller R., Rotter N. Chondrocyte redifferentiation in 3D: the effect of adhesion site density and substrate elasticity. JBiomed Mater Res A 2012, 100:38-47.
42. Brenner E.K., Schiffman J.D., Thompson E.A., Toth L.J., Schauer C.L. Electrospinning of hyaluronic acid nanofibers from aqueous ammonium solutions. Carbohyd Polym 2012, 87:926-929.
43. Lee K., Jeong L., Kang Y., Lee S. Electrospinning of polysaccharides for regenerative medicine. Adv Drug Deliv Rev 2009, 61:1020-1032.
44. Um I.C., Fang D., Hsiao B.S., Okamoto A., Chu B. Electro-spinning and electro-blowing of hyaluronic acid. Biomacromolecules 2004, 5:1428-1436.
45. Carlisle C.R., Coulais C., Guthold M. The mechanical stress-strain properties ofsingle electrospun collagen type I nanofibers. Acta Biomater 2010, 6:2997-3003.
46. Gu S., Wu Q., Ren J., Vancso G. Mechanical properties of a single electrospun fiber and its structures. Macromol Rapid Comm 2005, 26:716-720.
47. Yang L., Fitie C.F.C., van der Werf K.O., Bennink M.L., Dijkstra P.J., Feijen J. Mechanical properties of single electrospun collagen type I fibers. Biomaterials 2008, 29:955-962.
48. Croisier F., Duwez A.-S., JérÔme C., Léonard A., van der Werf K.O., Dijkstra P.J., et al. Mechanical testing of electrospun PCL fibers. Acta Biomater 2012, 8:218-224.
49. Biggs M., Richards R., McFarlane S., Wilkinson C., Oreffo R., Dalby M. Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330nm deep microgrooves. JR Soc Interface 2008, 5:1231-1242.
50. Biggs M., Richards R., Gadegaard N., McMurray R., Affrossman S., Wilkinson C., et al. Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. JBiomed Mater Res A 2009, 91:195-208.
51. Yim E., Pang S., Leong K. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 2007, 313:1820-1829.
52. Huang S., Chen C.S., Ingber D.E. Control of cyclin D1, p27Kip1, and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol Biol Cell 1998.
53. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004, 6:483-495.
54. Legant W.R., Choi C., Miller J.S., Shao L., Gao L., Betzig E., et al. Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions. Proc Natl Acad Sci 2013, 110:881-886.