The guidance of stem cell differentiation by substrate alignment and mechanical stimulation

Biomaterials

Volumn 34, Issue 8, 2013, Pages 1942-1953

  Subramony, Siddarth D ^a   Dargis, Booth R ^a   Castillo, Mario ^a   Azeloglu, Evren U ^a   Tracey, Michael S ^a   Su, Amanda ^a   Lu, Helen H ^a  

^a Columbia University ^*  (United States)

Author keywords

Biomimetic material; Bioreactor; Integrin; Ligament; Mesenchymal stem cell; Nanotopography

Indexed keywords

CELL SOURCES; CELL-MATERIAL INTERACTION; CHEMICAL STIMULATION; CHEMICAL STIMULI; COMBINED EFFECT; CONCENTRATION GRADIENTS; CONNECTIVE TISSUES; DIFFERENTIATION PROCESS; FUNDAMENTAL DESIGN; INTEGRINS; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; NANOFIBER MATRIX; NANOTOPOGRAPHIES; PHYSIOLOGICAL LOADINGS; REGENERATIVE MEDICINE; RELATIVE CONTRIBUTION; STEM CELL DIFFERENTIATION; SUBSTRATE ALIGNMENT; SYSTEMATIC INVESTIGATIONS; TISSUE ENGINEERING APPLICATIONS;

ALIGNMENT; BIOMIMETIC MATERIALS; BIOMIMETICS; BIOREACTORS; COLLAGEN; FLOWCHARTING; LIGAMENTS; LOADING; MUSCULOSKELETAL SYSTEM; PHYSIOLOGICAL MODELS; STEM CELLS; TISSUE ENGINEERING;

CELL CULTURE;

NANOFIBER;

ARTICLE; BIOMIMETICS; BIOSYNTHESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; TISSUE REGENERATION;

BIOREACTORS; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; MALE; MESENCHYMAL STROMAL CELLS; NANOFIBERS; PROTEIN SUBUNITS; STRESS, MECHANICAL; TISSUE SCAFFOLDS; YOUNG ADULT;

HARNESS;

EID: 84871487509     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.11.012     Document Type: Article

References (63)

1. 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.
2. Altman G.H., Horan R.L., Martin I., Farhadi J., Stark P.R., Volloch V., et al. Cell differentiation by mechanical stress. FASEB J 2002, 16(2):270-272.
3. Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997, 276(5309):71-74.
4. Darby I.A., Hewitson T.D. Fibroblast differentiation in wound healing and fibrosis. International review of cytology a survey of cell biology 2007, vol. 257:143-179. Academic Press.
5. Da Silva Meirelles L., Caplan A.I., Nardi N.B. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008, 26(9):2287-2299.
6. Alhadlaq A., Mao J.J. Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev 2004, 13(4):436-448.
7. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260(5110):920-926.
8. DiGirolamo C.M., Stokes D., Colter D., Phinney D.G., Class R., Prockop D.J. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 1999, 107(2):275-281.
9. Yoshimoto H., Shin Y.M., Terai H., Vacanti J.P. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 2003, 24(12):2077-2082.
10. Garreta E., Gasset D., Semino C., Borros S. Fabrication of a three-dimensional nanostructured biomaterial for tissue engineering of bone. Biomol Eng 2007, 24(1):75-80.
11. Baker B.M., Mauck R.L. The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials 2007, 28(11):1967-1977.
12. Nerurkar N.L., Elliott D.M., Mauck R.L. Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res 2007, 25(8):1018-1028.
13. Li W.J., Danielson K.G., Alexander P.G., Tuan R.S. Biological response of chondrocytes cultured in three-dimensional nanofibrous poly(epsilon-caprolactone) scaffolds. J Biomed Mater Res A 2003, 67(4):1105-1114.
14. Moffat K.L., Kwei A.S., Spalazzi J.P., Doty S.B., Levine W.N., Lu H.H. Novel nanofiber-based scaffold for rotator cuff repair and augmentation. Tissue Eng Part A 2009, 15(1):115-126.
15. Kumbar S.G., James R., Nukavarapu S.P., Laurencin C.T. Electrospun nanofiber scaffolds: engineering soft tissues. Biomed Mater 2008, 3(3):034002.
16. Li W.J., Mauck R.L., Cooper J.A., Yuan X., Tuan R.S. Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J Biomech 2007, 40(8):1686-1693.
17. Barber J.G., Handorf A.M., Allee T.J., Li W.J. Braided nanofibrous scaffold for tendon and ligament tissue engineering. Tissue Eng Part A 2011, Epub.
18. Sahoo S., Ouyang H., Goh J.C., Tay T.E., Toh S.L. Characterization of a novel polymeric scaffold for potential application in tendon/ligament tissue engineering. Tissue Eng 2006, 12(1):91-99.
19. Sahoo S., Ang L.T., Cho-Hong G.J., Toh S.L. Bioactive nanofibers for fibroblastic differentiation of mesenchymal precursor cells for ligament/tendon tissue engineering applications. Differentiation 2010, 79(2):102-110.
20. Erisken C., Zhang X., Moffat K.L., Levine W.N., Lu H. Scaffold fiber diameter regulates human tendon fibroblast growth and differentiation. Tissue Eng Part A 2012, Accepted.
21. Pham Q.P., Sharma U., Mikos A.G. Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 2006, 7(10):2796-2805.
22. Murugan R., Ramakrishna S. Design strategies of tissue engineering scaffolds with controlled fiber orientation. Tissue Eng 2007, 13(8):1845-1866.
23. Ma J., He X., Jabbari E. Osteogenic differentiation of marrow stromal cells on random and aligned electrospun poly(L-lactide) nanofibers. Ann Biomed Eng 2011, 39(1):14-25.
24. Skutek M., Griensven M., Zeichen J., Brauer N., Bosch U. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 2001, 86(1):48-52.
25. Schofer M., Boudriot U., Wack C., Leifeld I., Grabedunkel C., Dersch R., et al. Influence of nanofibers on the growth and osteogenic differentiation of stem cells: a comparison of biological collagen nanofibers and synthetic PLLA fibers. J Mater Sci Mater Med 2009, 20(3):767-774.
26. Jiang X., Cao H.Q., Shi L.Y., Ng S.Y., Stanton L.W., Chew S.Y. Nanofiber topography and sustained biochemical signaling enhance human mesenchymal stem cell neural commitment. Acta Biomater 2012, 8(3):1290-1302.
27. Terraciano V., Hwang N., Moroni L., Park H.B., Zhang Z., Mizrahi J., et al. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 2007, 25(11):2730-2738.
28. Grayson W.L., Frohlich M., Yeager K., Bhumiratana S., Chan M.E., Cannizzaro C., et al. Engineering anatomically shaped human bone grafts. Proc Natl Acad Sci U S A 2010, 107(8):3299-3304.
29. Reneker D.H., Chun I. Nanometre diameter fibres of polymer, produced by electrospinning. Nanotechnology 1996, 7:216-223.
30. Nathan A.S., Baker B.M., Nerurkar N.L., Mauck R.L. Mechano-topographic modulation of stem cell nuclear shape on nanofibrous scaffolds. Acta Biomaterialia 2011, 7(1):57-66.
31. De Z.M., Bojsen-Moller F., Voigt M. Dynamic viscoelastic behavior of lower extremity tendons during simulated running. J Appl Physiol 2000, 89(4):1352-1359.
32. Nirmalandhan V.S., Shearn J.T., Juncosa-Melvin N., Rao M., Gooch C., Jain A., et al. Improving linear stiffness of the cell-seeded collagen sponge constructs by varying the components of the mechanical stimulus. Tissue Eng Part A 2008, 14(11):1883-1891.
33. Hanson A.D., Marvel S.W., Bernacki S.H., Banes A.J., van A.J., Loboa E.G. Osteogenic effects of rest inserted and continuous cyclic tensile strain on hASC lines with disparate osteodifferentiation capabilities. Ann Biomed Eng 2009, 37(5):955-965.
34. Riboh J., Chong A.K.S., Pham H., Longaker M., Jacobs C., Chang J. Optimization of flexor tendon tissue engineering with a cyclic strain bioreactor. J Hand Surg Am 2008, 33(8):1388-1396.
35. Lu H.H., Cooper J.A., Manuel S., Freeman J.W., Attawia M.A., Ko F.K., et al. Anterior cruciate ligament regeneration using braided biodegradable scaffolds: in vitro optimization studies. Biomaterials 2005, 26(23):4805-4816.
36. Costa K.D., Lee E.J., Holmes J.W. Creating alignment and anisotropy in engineered heart tissue: role of boundary conditions in a model three-dimensional culture system. Tissue Eng 2003, 9(4):567-577.
37. Wang N., Tytell J.D., Ingber D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009, 10(1):75-82.
38. Ruoslahti E. Stretching is good for a cell. Science 1997, 276(5317):1345-1346.
39. Friedl G., Schmidt H., Rehak I., Kostner G., Schauenstein K., Windhager R. Undifferentiated human mesenchymal stem cells (hMSCs) are highly sensitive to mechanical strain: transcriptionally controlled early osteo-chondrogenic response in vitro. Osteoarthritis Cartilage 2007, 15(11):1293-1300.
40. Bhargava M.M., Beavis A.J., Edberg J.C., Warren R.F., Attia E.T., Hannafin J.A. Differential expression of integrin subunits in canine knee ligament fibroblasts. J Orthop Res 1999, 17(5):748-754.
41. Huang C., Fu X., Liu J., Qi Y., Li S., Wang H. The involvement of integrin beta1 signaling in the migration and myofibroblastic differentiation of skin fibroblasts on anisotropic collagen-containing nanofibers. Biomaterials 2012, 33(6):1791-1800.
42. Henshaw D.R., Attia E., Bhargava M., Hannafin J.A. Canine ACL fibroblast integrin expression and cell alignment in response to cyclic tensile strain in three-dimensional collagen gels. J Orthop Res 2006, 24(3):481-490.
43. Wang J.H., Grood E.S. The strain magnitude and contact guidance determine orientation response of fibroblasts to cyclic substrate strains. Connect Tissue Res 2000, 41(1):29-36.
44. Baker B.M., Shah R.P., Huang A.H., Mauck R.L. Dynamic tensile loading improves the functional properties of mesenchymal stem cell-laden nanofiber-based fibrocartilage. Tissue Eng Part A 2011, 17(9-10):1445-1455.
45. Lee C.H., Shin H.J., Cho I.H., Kang Y.M., Kim I.A., Park K.D., et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 2005, 26(11):1261-1270.
46. Amiel D., Frank C., Harwood F., Fronek J., Akeson W. Tendons and ligaments: a morphological and biochemical comparison. J Orthop Res 1983, 1(3):257-265.
47. Waggett A.D., Ralphs J.R., Kwan A.P.L., Woodnutt D., Benjamin M. Characterization of collagens and proteoglycans at the insertion of the human achilles tendon. Matrix Biol 1998, 16(8):457-470.
48. Amiel D., Kleiner J.B., Roux R.D., Harwood F.L., Akeson W.H. The phenomenon of "ligamentization": anterior cruciate ligament reconstruction with autogenous patellar tendon. J Orthop Res 1986, 4(2):162-172.
49. Eriksen H.A., Pajala A., Leppilahti J., Risteli J. Increased content of type III collagen at the rupture site of human achilles tendon. J Orthop Res 2002, 20(6):1352-1357.
50. Moreau J.E., Bramono D.S., Horan R.L., Kaplan D.L., Altman G.H. Sequential biochemical and mechanical stimulation in the development of tissue-engineered ligaments. Tissue Eng Part A 2008, 14(7):1161-1172.
51. Murphy P.G., Loitz B.J., Frank C.B., Hart D.A. Influence of exogenous growth factors on the synthesis and secretion of collagen types I and III by explants of normal and healing rabbit ligaments. Biochem Cell Biol 1994, 72(9-10):403-409.
52. Brent A.E., Schweitzer R., Tabin C.J. A somitic compartment of tendon progenitors. Cell 2003 Apr 18, 113(2):235-248.
53. Schweitzer R., Chyung J.H., Murtaugh L.C., Brent A.E., Rosen V., Olson E.N., et al. Analysis of the tendon cell fate using scleraxis, a specific marker for tendons and ligaments. Development 2001, 128(19):3855-3866.
54. Kuo C.K., Tuan R.S. Mechanoactive tenogenic differentiation of human mesenchymal stem cells. Tissue Eng Part A 2008, 14(10):1615-1627.
55. Shukunami C., Takimoto A., Oro M., Hiraki Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol 2006, 298(1):234-247.
56. Docheva D., Hunziker E.B., Fassler R., Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol 2005, 25(2):699-705.
57. Chen J., Horan R.L., Bramono D., Moreau J.E., Wang Y., Geuss L.R., et al. Monitoring mesenchymal stromal cell developmental stage to apply on-time mechanical stimulation for ligament tissue engineering. Tissue Eng 2006, 12(11):3085-3095.
58. Garcia A.J. Get a grip: integrins in cell-biomaterial interactions. Biomaterials 2005, 26(36):7525-7529.
59. Lin T.W., Cardenas L., Soslowsky L.J. Biomechanics of tendon injury and repair. J Biomech 2004, 37(6):865-877.
60. Petrie T.A., Capadona J.R., Reyes C.D., Garcia A.J. Integrin specificity and enhanced cellular activities associated with surfaces presenting a recombinant fibronectin fragment compared to RGD supports. Biomaterials 2006, 27(31):5459-5470.
61. Hannafin J.A., Attia E.A., Henshaw R., Warren R.F., Bhargava M.M. Effect of cyclic strain and plating matrix on cell proliferation and integrin expression by ligament fibroblasts. J Orthop Res 2006, 24(2):149-158.
62. Giancotti F.G. Integrin signaling: specificity and control of cell survival and cell cycle progression. Curr Opin Cell Biol 1997, 9(5):691-700.
63. Schiro J.A., Chan B.M., Roswit W.T., Kassner P.D., Pentland A.P., Hemler M.E., et al. Integrin alpha 2 beta 1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells. Cell 1991 Oct 18, 67(2):403-410.