Micro-scale and meso-scale architectural cues cooperate and compete to direct aligned tissue formation

Biomaterials

Volumn 35, Issue 38, 2014, Pages 10015-10024

  Gilchrist, Christopher L ^a   Ruch, David S ^a   Little, Dianne ^a   Guilak, Farshid ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Duke University   (United States)

Author keywords

Actin; Ligament; Mesenchymal stem cell; Micropatterning; Nanotopography; Tendon

Indexed keywords

ADHESIVES; ALIGNMENT; ARCHITECTURE; ASPECT RATIO; CELL CULTURE; COLLAGEN; DEPOSITION; GENE EXPRESSION; LIGAMENTS; STEM CELLS; TENDONS;

ACTIN; ARCHITECTURAL FEATURES; DIFFERENT LENGTH SCALE; FIBRILLAR COLLAGENS; HUMAN MESENCHYMAL STEM CELLS; MESENCHYMAL STEM CELL; MICRO PATTERNING; NANOTOPOGRAPHIES;

SCAFFOLDS (BIOLOGY);

BIOMATERIAL; FIBRILLAR COLLAGEN; NANOMATERIAL;

ARTICLE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESO SCALE ARCHITECTURAL CUE; MICRO SCALE ARCHITECTURAL CUE; PARAMETERS; TISSUES; BATCH CELL CULTURE; CELL ADHESION; CELL COMMUNICATION; CELL CULTURE; CELL MOTION; CELL POLARITY; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; MESENCHYMAL STROMA CELL; PARTICLE SIZE; PHYSIOLOGY; PROCEDURES; SURFACE PROPERTY; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE SCAFFOLD; TUMOR MICROENVIRONMENT; ULTRASTRUCTURE;

BATCH CELL CULTURE TECHNIQUES; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; CELL POLARITY; CELL PROLIFERATION; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; GUIDED TISSUE REGENERATION; HUMANS; MESENCHYMAL STROMAL CELLS; NANOSTRUCTURES; PARTICLE SIZE; SURFACE PROPERTIES; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84908101846     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.08.047     Document Type: Article

References (56)

1. Richardson S.H., Starborg T., Lu Y., Humphries S.M., Meadows R.S., Kadler K.E. Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions. Mol Cell Biol 2007, 27:6218-6228.
2. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
3. Kshitiz, Park J., Kim P., Helen W., Engler A.J., Levchenko A., et al. Control of stem cell fate and function by engineering physical microenvironments. Integr Biol (Camb) 2012, 4:1008-1018.
4. Baker B.M., Shah R.P., Silverstein A.M., Esterhai J.L., Burdick J.A., Mauck R.L. Sacrificial nanofibrous composites provide instruction without impediment and enable functional tissue formation. Proc Natl Acad Sci U S A 2012, 109:14176-14181.
5. Burdick J.A., Anseth K.S. Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials 2002, 23:4315-4323.
6. DeForest C.A., Anseth K.S. Advances in bioactive hydrogels to probe and direct cell fate. Annu Rev Chem Biomol Eng 2012, 3:421-444.
7. DeLong S.A., Moon J.J., West J.L. Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration. Biomaterials 2005, 26:3227-3234.
8. Duclos G., Garcia S., Yevick H.G., Silberzan P. Perfect nematic order in confined monolayers of spindle-shaped cells. Soft Matter 2014, 10:2346-2353.
9. Petrie T.A., Raynor J.E., Dumbauld D.W., Lee T.T., Jagtap S., Templeman K.L., et al. Multivalent integrin-specific ligands enhance tissue healing and biomaterial integration. Sci Transl Med 2010, 2. 45ra60.
10. Baranski J.D., Chaturvedi R.R., Stevens K.R., Eyckmans J., Carvalho B., Solorzano R.D., et al. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc Natl Acad Sci U S A 2013, 110:7586-7591.
11. Leslie-Barbick J.E., Shen C., Chen C., West J.L. Micron-scale spatially patterned, covalently immobilized vascular endothelial growth factor on hydrogels accelerates endothelial tubulogenesis and increases cellular angiogenic responses. Tissue Eng Part A 2011, 17:221-229.
12. Dickinson R.B., Guido S., Tranquillo R.T. Biased cell migration of fibroblasts exhibiting contact guidance in oriented collagen gels. Ann Biomed Eng 1994, 22:342-356.
13. Dunn G.A., Heath J.P. Anew hypothesis of contact guidance in tissue cells. Exp Cell Res 1976, 101:1-14.
14. Nelson C.M., Jean R.P., Tan J.L., Liu W.F., Sniadecki N.J., Spector A.A., et al. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 2005, 102:11594-11599.
15. Nelson C.M., Vanduijn M.M., Inman J.L., Fletcher D.A., Bissell M.J. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 2006, 314:298-300.
16. Gallant N.D., Charest J.L., King W.P., Garcia A.J. Micro- and nano-patterned substrates to manipulate cell adhesion. JNanosci Nanotechnol 2007, 7:803-807.
17. Kolind K., Leong K.W., Besenbacher F., Foss M. Guidance of stem cell fate on 2D patterned surfaces. Biomaterials 2012, 33:6626-6633.
18. Kulangara K., Yang Y., Yang J., Leong K.W. Nanotopography as modulator of human mesenchymal stem cell function. Biomaterials 2012, 33:4998-5003.
19. Yim E.K., Darling E.M., Kulangara K., Guilak F., Leong K.W. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 2010, 31:1299-1306.
20. Clark P., Connolly P., Curtis A.S., Dow J.A., Wilkinson C.D. Topographical control of cell behaviour. I. Simple step cues. Development 1987, 99:439-448.
21. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276:1425-1428.
22. Dalby M.J., Riehle M.O., Yarwood S.J., Wilkinson C.D., Curtis A.S. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res 2003, 284:274-282.
23. Wojciak-Stothard B., Madeja Z., Korohoda W., Curtis A., Wilkinson C. Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol Int 1995, 19:485-490.
24. Flemming R.G., Murphy C.J., Abrams G.A., Goodman S.L., Nealey P.F. Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials 1999, 20:573-588.
25. 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, 15:115-126.
26. Yin Z., Chen X., Chen J.L., Shen W.L., Hieu Nguyen T.M., Gao L., et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 2010, 31:2163-2175.
27. Chainani A., Hippensteel K.J., Kishan A., Garrigues N.W., Ruch D.S., Guilak F., et al. Multilayered electrospun scaffolds for tendon tissue engineering. Tissue Eng Part A 2013, 19:2594-2604.
28. 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, 19(11-12):1265-1274.
29. Klumpers D.D., Mao A.S., Smit T.H., Mooney D.J. Linear patterning of mesenchymal condensations is modulated by geometric constraints. JR Soc Interface 2014, 11:20140215.
30. Gomez E.W., Chen Q.K., Gjorevski N., Nelson C.M. Tissue geometry patterns epithelial-mesenchymal transition via intercellular mechanotransduction. JCell Biochem 2010, 110:44-51.
31. Raghavan S., Nelson C.M., Baranski J.D., Lim E., Chen C.S. Geometrically controlled endothelial tubulogenesis in micropatterned gels. Tissue Eng Part A 2010, 16:2255-2263.
32. Gjorevski N., Nelson C.M. Mapping of mechanical strains and stresses around quiescent engineered three-dimensional epithelial tissues. Biophys J 2012, 103:152-162.
33. Ruiz S.A., Chen C.S. Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells 2008, 26:2921-2927.
34. Li B., Li F., Puskar K.M., Wang J.H. Spatial patterning of cell proliferation and differentiation depends on mechanical stress magnitude. JBiomech 2009, 42:1622-1627.
35. Li J.Y., Ho Y.C., Chung Y.C., Lin F.C., Liao W.L., Tsai W.B. Preparation of micron/submicron hybrid patterns via a two-stage UV-imprint technique and their dimensional effects on cell adhesion and alignment. Biofabrication 2013, 5:035003.
36. Seunarine K., Curtis A.S., Meredith D.O., Wilkinson C.D., Riehle M.O., Gadegaard N. Ahierarchical response of cells to perpendicular micro- and nanometric textural cues. IEEE Trans Nanobioscience 2009, 8:219-225.
37. Crouch A.S., Miller D., Luebke K.J., Hu W. Correlation of anisotropic cell behaviors with topographic aspect ratio. Biomaterials 2009, 30:1560-1567.
38. Lopez-Bosque M.J., Tejeda-Montes E., Cazorla M., Linacero J., Atienza Y., Smith K.H., et al. Fabrication of hierarchical micro-nanotopographies for cell attachment studies. Nanotechnology 2013, 24:255305.
39. Doyle A.D., Wang F.W., Matsumoto K., Yamada K.M. One-dimensional topography underlies three-dimensional fibrillar cell migration. JCell Biol 2009, 184:481-490.
40. Bowles R.D., Williams R.M., Zipfel W.R., Bonassar L.J. Self-assembly of aligned tissue-engineered annulus fibrosus and intervertebral disc composite via collagen gel contraction. Tissue Eng Part A 2010, 16:1339-1348.
41. Garrigues N.W., Little D., O'Conor C.J., Guilak F. Use of an insulating mask for controlling anisotropy in multilayer electrospun scaffolds for tissue engineering. JMater Chem 2010, 20:8962-8968.
42. Preibisch S., Saalfeld S., Tomancak P. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 2009, 25:1463-1465.
43. Birk D.E., Mayne R. Localization of collagen types I, III and V during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter. Eur J Cell Biol 1997, 72:352-361.
44. Riley G.P., Harrall R.L., Cawston T.E., Hazleman B.L., Mackie E.J. Tenascin-C and human tendon degeneration. Am J Pathol 1996, 149:933-943.
45. Kalson N.S., Starborg T., Lu Y., Mironov A., Humphries S.M., Holmes D.F., et al. Nonmuscle myosin II powered transport of newly formed collagen fibrils at the plasma membrane. Proc Natl Acad Sci U S A 2013, 110:E4743-E4752.
46. Kapacee Z., Richardson S.H., Lu Y., Starborg T., Holmes D.F., Baar K., et al. Tension is required for fibripositor formation. Matrix Biol 2008, 27:371-375.
47. Legant W.R., Pathak A., Yang M.T., Deshpande V.S., McMeeking R.M., Chen C.S. Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc Natl Acad Sci U S A 2009, 106:10097-10102.
48. Stopak D., Harris A.K. Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. Dev Biol 1982, 90:383-398.
49. Angelini T.E., Hannezo E., Trepat X., Marquez M., Fredberg J.J., Weitz D.A. Glass-like dynamics of collective cell migration. Proc Natl Acad Sci U S A 2011, 108:4714-4719.
50. Londono C., Loureiro M.J., Slater B., Lucker P.B., Soleas J., Sathananthan S., et al. Nonautonomous contact guidance signaling during collective cell migration. Proc Natl Acad Sci U S A 2014, 111:1807-1812.
51. Doxzen K., Vedula S.R., Leong M.C., Hirata H., Gov N.S., Kabla A.J., et al. Guidance of collective cell migration by substrate geometry. Integr Biol (Camb) 2013, 5:1026-1035.
52. Chou C.L., Rivera A.L., Sakai T., Caplan A.I., Goldberg V.M., Welter J.F., et al. Micrometer scale guidance of mesenchymal stem cells to form structurally oriented cartilage extracellular matrix. Tissue Eng Part A 2013, 19:1081-1090.
53. Derwin K.A., Soslowsky L.J. Aquantitative investigation of structure-function relationships in a tendon fascicle model. JBiomech Eng 1999, 121:598-604.
54. Thorpe C.T., Udeze C.P., Birch H.L., Clegg P.D., Screen H.R. Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: a possible mechanism for age-related tendinopathy?. Eur Cell Mater 2013, 25:48-60.
55. Kuo C.K., Tuan R.S. Mechanoactive tenogenic differentiation of human mesenchymal stem cells. Tissue Eng Part A 2008, 14:1615-1627.
56. Guilak F., Butler D.L., Goldstein S.A., Baaijens F.P.T. Biomechanics and mechanobiology in functional tissue engineering. J Biomech 2014, 47:1933-1940.