Engineering cellular fibers for musculoskeletal soft tissues using directed self-assembly

Tissue Engineering - Part A

Volumn 19, Issue 9-10, 2013, Pages 1223-1232

  Schiele, Nathan R ^a   Koppes, Ryan A ^a   Chrisey, Douglas B ^b   Corr, David T ^a  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b Tulane University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGY; BIOMECHANICS; CELL ADHESION; DYNAMIC LOADS; DYNAMICS; FIBERS; LOADING; SELF ASSEMBLY; STIFFNESS; TENDONS; TENSILE STRAIN;

ACCELERATED MATURATION; DEVELOPMENTAL BIOLOGY; DIRECTED SELF-ASSEMBLY; EMBRYONIC DEVELOPMENT; EXTRACELLULAR MATRICES; HUMAN DERMAL FIBROBLASTS; MECHANICAL CHARACTERISTICS; SOFT TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

CADHERIN; FIBRONECTIN; OSTEOBLAST CADHERIN; TISSUE SCAFFOLD;

ARTICLE; CELL CULTURE; CHEMISTRY; CYTOLOGY; FIBROBLAST; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; SKELETAL MUSCLE; TISSUE ENGINEERING;

CADHERINS; CELLS, CULTURED; FIBROBLASTS; FIBRONECTINS; HUMANS; IMMUNOHISTOCHEMISTRY; MUSCLE, SKELETAL; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84875619413     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0321     Document Type: Article

References (48)

1. Provenzano, P.P., & Vanderby, R., Jr. Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25, 71, 2006.
2. Butler, D.L., Juncosa, N., & Dressler, M.R. Functional efficacy of tendon repair processes. Annu Rev Biomed Eng 6, 303, 2004.
3. Cohen, S., Leschansky, L., Zussman, E., Burman, M., Srouji, S., Abramov, N., & Itskovitz-Eldor, J. Repair of fullthickness tendon injury using connective tissue progenitors efficiently derived from human embryonic stem cells and fetal tissues. Tissue Eng Part A 16, 3119, 2010.
4. Calve, S., Lytle, I.F., Grosh, K., Brown, D.L., & Arruda, E.M. Implantation increases tensile strength and collagen content of self-assembled tendon constructs. J Appl Physiol 108, 875, 2010.
5. Calve, S., Dennis, R.G., Kosnik, P.E., 2nd, Baar, K., Grosh, K., and Arruda, E.M. Engineering of functional tendon. Tissue Eng 10, 755, 2004.
6. Larkin, L.M., Calve, S., Kostrominova, T.Y., & Arruda, E.M. Structure and functional evaluation of tendon-skeletal muscle constructs engineered in vitro. Tissue Eng 12, 3149, 2006.
7. Hairfield-Stein, M., England, C., Paek, H.J., Gilbraith, K.B., Dennis, R., Boland, E., & Kosnik, P. Development of selfassembled, tissue-engineered ligament from bone marrow stromal cells. Tissue Eng 13, 703, 2007.
8. de Wreede, R., & Ralphs, J.R. Deposition of collagenous matrices by tendon fibroblasts in vitro: a comparison of fibroblast behavior in pellet cultures and a novel threedimensional long-term scaffoldless culture system. Tissue Eng Part A 15, 2707, 2009.
9. Patz, T.M., Doraiswamy, A., Narayan, R.J., Modi, R., and Chrisey, D.B. Two-dimensional differential adherence and alignment of C2C12 myoblasts. Mater Sci Eng 123, 242, 2005.
10. Vukicevic, S., Kleinman, H.K., Luyten, F.P., Roberts, A.B., Roche, N.S., & Reddi, A.H. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res 202, 1, 1992.
11. Kleinman, H.K., Mcgarvey, M.L., Liotta, L.A., Robey, P.G., Tryggvason, K., & Martin, G.R. Isolation and characterization of type-Iv procollagen, laminin, and heparan-sulfate proteoglycan from the Ehs sarcoma. Biochemistry 21, 6188, 1982.
12. Liu, C.F., Aschbacher-Smith, L., Barthelery, N.J., Dyment, N., Butler, D., & Wylie, C. What we should know before using tissue engineering techniques to repair injured tendons: a developmental biology perspective. Tissue Eng Part B Rev 17, 165, 2011.
13. Thomopoulos, S., Genin, G.M., & Galatz, L.M. The development and morphogenesis of the tendon-to-bone insertion-what development can teach us about healing. J Musculoskelet Neuronal Interact 10, 35, 2010.
14. Brown, J.P., Lind, R.M., Burzesi, A.F., & Kuo, C.K. Elastogenic protein expression of a highly elastic murine spinal ligament: the ligamentum flavum. PLoS One 7, e38475, 2012.
15. Oryan, A., & Shoushtari, A.H. Histology and ultrastructure of the developing superficial digital flexor tendon in rabbits. Anat Histol Embryol 37, 134, 2008.
16. Ansorge, H.L., Adams, S., Birk, D.E., & Soslowsky, L.J. Mechanical, compositional, and structural properties of the post-natal mouse Achilles tendon. Ann Biomed Eng 39, 1904, 2011.
17. Chaplin, D.M., & Greenlee, T.K., Jr. The development of human digital tendons. J Anat 120, 253, 1975.
18. McNeilly, C.M., Banes, A.J., Benjamin, M., & Ralphs, J.R. Tendon cells in vivo form a three dimensional network of cell processes linked by gap junctions. J Anat 189 (Pt 3), 593, 1996.
19. 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 27, 6218, 2007.
20. Kiener, H.P., & Brenner, M.B. Building the synovium: cadherin-11 mediates fibroblast-like synoviocyte cell-to-cell adhesion. Arthritis Res Ther 7, 49, 2005.
21. Suzue, T., & Shinoda, Y. Highly reproducible spatiotemporal patterns of mammalian embryonic movements at the developmental stage of the earliest spontaneous motility. Eur J Neurosci 11, 2697, 1999.
22. Wu, K.C., Streicher, J., Lee, M.L., Hall, B.K., & Muller, G.B. Role of motility in embryonic development I: embryo movements and amnion contractions in the chick and the influence of illumination. J Exp Zool 291, 186, 2001.
23. Kuo, C.K., Petersen, B.C., & Tuan, R.S. Spatiotemporal protein distribution of TGF-betas, their receptors, and extracellular matrix molecules during embryonic tendon development. Dev Dyn 237, 1477, 2008.
24. Connell, D., Datir, A., Alyas, F., & Curtis, M. Treatment of lateral epicondylitis using skin-derived tenocyte-like cells. Br J Sports Med 43, 293, 2009.
25. Deng, D., Liu, W., Xu, F., Yang, Y., Zhou, G., Zhang, W.J., Cui, L., & Cao, Y. Engineering human neo-tendon tissue in vitro with human dermal fibroblasts under static mechanical strain. Biomaterials 30, 6724, 2009.
26. Clarke, A.W., Alyas, F., Morris, T., Robertson, C.J., Bell, J., and Connell, D.A. Skin-derived tenocyte-like cells for the treatment of patellar tendinopathy. Am J Sports Med 39, 614, 2011.
27. Ng, C.P., & Swartz, M.A. Mechanisms of interstitial flowinduced remodeling of fibroblast-collagen cultures. Ann Biomed Eng 34, 446, 2006.
28. Glawe, J.D., Hill, J.B., Mills, D.K., & McShane, M.J. Influence of channel width on alignment of smooth muscle cells by high-aspect-ratio microfabricated elastomeric cell culture scaffolds. J Biomed Mater Res A 75, 106, 2005.
29. Ng, C.P., Hinz, B., & Swartz, M.A. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118, 4731, 2005.
30. Palmer, B.M., & Bizios, R. Quantitative characterization of vascular endothelial cell morphology and orientation using Fourier transform analysis. J Biomech Eng 119, 159, 1997.
31. Wang, J.H. Mechanobiology of tendon. J Biomech 39, 1563, 2006.
32. Eldred, C.C., Simeonov, D.R., Koppes, R.A., Yang, C., Corr, D.T., & Swank, D.M. The mechanical properties of Drosophila jump muscle expressing wild-type and embryonic Myosin isoforms. Biophys J 98, 1218, 2010.
33. Nguyen, T.D., Liang, R., Woo, S.L.Y., Burton, S.D., Wu, C.F., Almarza, A., Sacks, M.S., & Abramowitch, S. Effects of cell seeding and cyclic stretch on the fiber remodeling in an extracellular matrix-derived bioscaffold. Tissue Eng Part A 15, 957, 2009.
34. Ma, J., Goble, K., Smietana, M., Kostrominova, T., Larkin, L., and Arruda, E.M. Morphological and functional characteristics of three-dimensional engineered bone-ligament-bone constructs following implantation. J Biomech Eng 131, 101017, 2009.
35. Yin, Z., Chen, X., Chen, J.L., Shen, W.L., Nguyen, T.M.H., Gao, L., & Ouyang, H.W. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 31, 2163, 2010.
36. Nirmalanandhan, V.S., Shearn, J.T., Juncosa-Melvin, N., Rao, M., Gooch, C., Jain, A., Bradica, G., & Butler, D.L. Improving linear stiffness of the cell-seeded collagen sponge constructs by varying the components of the mechanical stimulus. Tissue Eng Part A 14, 1883, 2008.
37. Shearn, J.T., Juncosa-Melvin, N., Boivin, G.P., Galloway, M.T., Goodwin, W., Gooch, C., Dunn, M.G., & Butler, D.L. Mechanical stimulation of tendon tissue engineered constructs: effects on construct stiffness, repair biomechanics, and their correlation. J Biomech Eng 129, 848, 2007.
38. Garvin, J., Qi, J., Maloney, M., & Banes, A.J. Novel system for engineering bioartificial tendons and application of mechanical load. Tissue Eng 9, 967, 2003.
39. Issa, R.I., Engebretson, B., Rustom, L., McFetridge, P.S., and Sikavitsas, V.I. The effect of cell seeding density on the cellular and mechanical properties of a mechanostimulated tissue-engineered tendon. Tissue Eng Part A 17, 1479, 2011.
40. Kannus, P. Structure of the tendon connective tissue. Scand J Med Sci Sports 10, 312, 2000.
41. Kuo, C.K., & Tuan, R.S. Mechanoactive tenogenic differentiation of human mesenchymal stem cells. Tissue Eng Part A 14, 1615, 2008.
42. Juncosa-Melvin, N., Shearn, J.T., Boivin, G.P., Gooch, C., Galloway, M.T., West, J.R., Nirmalanandhan, V.S., Bradica, G., & Butler, D.L. Effects of mechanical stimulation on the biomechanics and histology of stem cell-collagen sponge constructs for rabbit patellar tendon repair. Tissue Eng 12, 2291, 2006.
43. Lee, J.Y., Zhou, Z., Taub, P.J., Ramcharan, M., Li, Y., Akinbiyi, T., Maharam, E.R., Leong, D.J., Laudier, D.M., Ruike, T., Torina, P.J., Zaidi, M., Majeska, R.J., Schaffler, M.B., Flatow, E.L., & Sun, H.B. BMP-12 treatment of adult mesenchymal stem cells in vitro augments tendon-like tissue formation and defect repair in vivo. PLoS One 6, e17531, 2011.
44. Zhang, J., Li, B., & Wang, J.H.C. The role of engineered tendon matrix in the stemness of tendon stem cells in vitro and the promotion of tendon-like tissue formation in vivo. Biomaterials 32, 6972, 2011.
45. Bi, Y., Ehirchiou, D., Kilts, T.M., Inkson, C.A., Embree, M.C., Sonoyama, W., Li, L., Leet, A.I., Seo, B.-M., Zhang, L., Shi, S., and Young, M.F. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13, 1219, 2007.
46. Kapacce, Z., Richardson, S.H., Lu, Y.H., Starborg, T., Holmes, D.F., Baar, K., & Kadler, K.E. Tension is required for fibripositor formation. Matrix Biol 27, 371, 2008.
47. Edom-Vovard, F., Schuler, B., Bonnin, M.A., Teillet, M.A., and Duprez, D. Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev Biol 247, 351, 2002.
48. Edom-Vovard, F., Bonnin, M., & Duprez, D. Fgf8 transcripts are located in tendons during embryonic chick limb development. Mech Dev 108, 203, 2001.