Modulation of annulus fibrosus cell alignment and function on oriented nanofibrous polyurethane scaffolds under tension

Spine Journal

Volumn 14, Issue 3, 2014, Pages 424-434

  Turner, Kathleen G ^a,b   Ahmed, Nazish ^b   Santerre, J Paul ^a,c   Kandel, Rita A ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Annulus fibrosus; Intervertebral disc; Polyurethane; Scaffolds; Tension

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; POLYURETHAN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; BIOMECHANICS; BOVINE; CELL CULTURE; CYTOLOGY; EXTRACELLULAR MATRIX; IN VITRO STUDY; INTERVERTEBRAL DISK; METABOLISM; PHYSIOLOGY; PROCEDURES; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ANIMALS; BIOMECHANICAL PHENOMENA; CATTLE; CELLS, CULTURED; COLLAGEN; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; IN VITRO TECHNIQUES; INTERVERTEBRAL DISC; POLYURETHANES; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84894421120     PISSN: 15299430     EISSN: 18781632     Source Type: Journal    
DOI: 10.1016/j.spinee.2013.08.047     Document Type: Article

References (64)

1. P.J. Roughley Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix Spine 29 2004 2691 2699
2. H.L. Guerin, and D.M. Elliott Quantifying the contributions of structure to annulus fibrosus mechanical function using a nonlinear, anisotropic, hyperelastic model J Orthop Res 25 2007 508 516
3. S.B. Bruehlmann, P.A. Hulme, and N.A. Duncan In situ intercellular mechanics of the bovine outer annulus fibrosus subjected to biaxial strains J Biomech 37 2004 223 231
4. S.B. Bruehlmann, J.B. Rattner, and J.R. Matyas et al. Regional variations in the cellular matrix of the annulus fibrosus of the intervertebral disc J Anat 201 2002 159 171
5. J.H. Wang, F. Jia, and T.W. Gilbert et al. Cell orientation determines the alignment of cell-produced collagenous matrix J Biomech 36 2003 97 102
6. A.J. Hayes, M. Benjamin, and J.R. Ralphs Role of actin stress fibres in the development of the intervertebral disc: cytoskeletal control of extracellular matrix assembly Dev Dyn 215 1999 179 189
7. S. Rhee, H. Jiang, and C.H. Ho et al. Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions Proc Natl Acad Sci U S A 104 2007 5425 5430
8. M.L. Bayer, C.Y. Yeung, and K.E. Kadler et al. The initiation of embryonic-like collagen fibrillogenesis by adult human tendon fibroblasts when cultured under tension Biomaterials 31 2010 4889 4897
9. J.C. Lotz, T. Hadi, and C. Bratton et al. Anulus fibrosus tension inhibits degenerative structural changes in lamellar collagen Eur Spine J 17 2008 1149 1159
10. J.R. Ralphs, A.D. Waggett, and M. Benjamin Actin stress fibres and cell-cell adhesion molecules in tendons: organisation in vivo and response to mechanical loading of tendon cells in vitro Matrix Biol 21 2002 67 74
11. H. Wilda, and J.E. Gough In vitro studies of annulus fibrosus disc cell attachment, differentiation and matrix production on PDLLA/45S5 Bioglass composite films Biomaterials 27 2006 5220 5229
12. H. Mizuno, A.K. Roy, and C.A. Vacanti et al. Tissue-engineered composites of anulus fibrosus and nucleus pulposus for intervertebral disc replacement Spine 29 2004 1290 1297 discussion 1297-8
13. M. Alini, W. Li, and P. Markovic et al. The potential and limitations of a cell-seeded collagen/hyaluronan scaffold to engineer an intervertebral disc-like matrix Spine 28 2003 446 454 discussion 453
14. X. Shao, and C.J. Hunter Developing an alginate/chitosan hybrid fiber scaffold for annulus fibrosus cells J Biomed Mater Res A 82 2007 701 710
15. G. Chang, H.J. Kim, and D. Kaplan et al. Porous silk scaffolds can be used for tissue engineering annulus fibrosus Eur Spine J 16 2007 1848 1857
16. N.L. Nerurkar, S. Sen, and A.H. Huang et al. Engineered disc-like angle-ply structures for intervertebral disc replacement Spine 35 2010 867 873
17. J.P. Santerre, K. Woodhouse, and G. Laroche et al. Understanding the biodegradation of polyurethanes: from classical implants to tissue engineering materials Biomaterials 26 2005 7457 7470
18. J.J. Stankus, J. Guan, and W.R. Wagner Fabrication of biodegradable elastomeric scaffolds with sub-micron morphologies J Biomed Mater Res A 70 2004 603 614
19. N.L. Nerurkar, D.M. Elliott, and R.L. Mauck Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering J Orthop Res 25 2007 1018 1028
20. L. Yang, R.A. Kandel, and G. Chang et al. Polar surface chemistry of nanofibrous polyurethane scaffold affects annulus fibrosus cell attachment and early matrix accumulation J Biomed Mater Res A 91 2009 1089 1099
21. I. Stokes, and D.M. Greenapple Measurement of surface deformation of soft tissue J Biomech 18 1985 1 7
22. S.D. Waldman, M.D. Grynpas, and R.M. Pilliar et al. Characterization of cartilaginous tissue formed on calcium polyphosphate substrates in vitro J Biomed Mater Res 62 2002 323 330
23. N. Ahmed, L. Gan, and A. Nagy et al. Cartilage tissue formation using redifferentiated passaged chondrocytes in vitro Tissue Eng Part A 15 2009 665 673
24. M. Attia, J.P. Santerre, and R.A. Kandel The response of annulus fibrosus cell to fibronectin-coated nanofibrous polyurethane-anionic dihydroxyoligomer scaffolds Biomaterials 32 2010 450 460
25. M. Benallaoua, P. Richette, and M. Francois et al. Modulation of proteoglycan production by cyclic tensile stretch in intervertebral disc cells through a post-translational mechanism Biorheology 43 2006 303 310
26. J. Deschner, B. Rath-Deschner, and S. Agarwal Regulation of matrix metalloproteinase expression by dynamic tensile strain in rat fibrochondrocytes Osteoarthritis Cartilage 14 2006 264 272
27. G. Sowa, and S. Agarwal Cyclic tensile stress exerts a protective effect on intervertebral disc cells Am J Phys Med Rehabil 87 2008 537 544
28. K.D. Fong, R.P. Nacamuli, and E.G. Loboa et al. Equibiaxial tensile strain affects calvarial osteoblast biology J Craniofac Surg 14 2003 348 355
29. K. Honda, S. Ohno, and K. Tanimoto et al. The effects of high magnitude cyclic tensile load on cartilage matrix metabolism in cultured chondrocytes Eur J Cell Biol 79 2000 601 609
30. E.J. Vanderploeg, S.M. Imler, and K.R. Brodkin et al. Oscillatory tension differentially modulates matrix metabolism and cytoskeletal organization in chondrocytes and fibrochondrocytes J Biomech 37 2004 1941 1952
31. M. Yoshigi, E.B. Clark, and H.J. Yost Quantification of stretch-induced cytoskeletal remodeling in vascular endothelial cells by image processing Cytometry A 55 2003 109 118
32. M. Marenzana, N. Wilson-Jones, and V. Mudera et al. The origins and regulation of tissue tension: identification of collagen tension-fixation process in vitro Exp Cell Res 312 2006 423 433
33. W.E. Johnson, A. Wootton, and A. El Haj et al. Topographical guidance of intervertebral disc cell growth in vitro: towards the development of tissue repair strategies for the anulus fibrosus Eur Spine J 15 3 Suppl 2006 S389 S396
34. C.H. Lee, H.J. Shin, and I.H. Cho et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast Biomaterials 26 2005 1261 1270
35. G.R. Houtchens, M.D. Foster, and T.A. Desai et al. Combined effects of microtopography and cyclic strain on vascular smooth muscle cell orientation J Biomech 41 2008 762 769
36. C.A. Lambert, E.P. Soudant, and B.V. Nusgens et al. Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces Lab Invest 66 1992 444 451
37. C.G. Bellows, A.H. Melcher, and J.E. Aubin Contraction and organization of collagen gels by cells cultured from periodontal ligament, gingiva and bone suggest functional differences between cell types J Cell Sci 50 1981 299 314
38. E.H. Danen, and A. Sonnenberg Integrins in regulation of tissue development and function J Pathol 201 2003 632 641
39. C.H. Damsky, and D. Ilic Integrin signaling: it's where the action is Curr Opin Cell Biol 14 2002 594 602
40. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat Rev Mol Cell Biol 10 2009 21 33
41. S. Wiesner, K.R. Legate, and R. Fassler Integrin-actin interactions Cell Mol Life Sci 62 2005 1081 1099
42. A.L. Berrier, and K.M. Yamada Cell-matrix adhesion J Cell Physiol 213 2007 565 573
43. T. Tetsunaga, T. Furumatsu, and N. Abe et al. Mechanical stretch stimulates integrin alphaVbeta3-mediated collagen expression in human anterior cruciate ligament cells J Biomech 42 2009 2097 2103
44. D.R. Henshaw, E. Attia, and M. Bhargava et al. Canine ACL fibroblast integrin expression and cell alignment in response to cyclic tensile strain in three-dimensional collagen gels J Orthop Res 24 2006 481 490
45. D. Karamichos, R.A. Brown, and V. Mudera Collagen stiffness regulates cellular contraction and matrix remodeling gene expression J Biomed Mater Res A 83 2007 887 894
46. G. De Santis, A.B. Lennon, and F. Boschetti et al. How can cells sense the elasticity of a substrate? An analysis using a cell tensegrity model Eur Cell Mater 22 2011 202 213
47. J.M. Jenner, F. van Eijk, and D.B. Saris et al. Effect of transforming growth factor-beta and growth differentiation factor-5 on proliferation and matrix production by human bone marrow stromal cells cultured on braided poly lactic-co-glycolic acid scaffolds for ligament tissue engineering Tissue Eng 13 2007 1573 1582
48. K. Masuda, and H.S. An Growth factors and the intervertebral disc Spine J 4 2004 330S 340S
49. P.J. Wipff, and B. Hinz Integrins and the activation of latent transforming growth factor beta1-an intimate relationship Eur J Cell Biol 87 2008 601 615
50. U.B. Kottler, A.G. Junemann, and T. Aigner et al. Comparative effects of TGF-beta 1 and TGF-beta 2 on extracellular matrix production, proliferation, migration, and collagen contraction of human Tenon's capsule fibroblasts in pseudoexfoliation and primary open-angle glaucoma Exp Eye Res 80 2005 121 134
51. A. Moustakas, and C.H. Heldin Dynamic control of TGF-beta signaling and its links to the cytoskeleton FEBS Lett 582 2008 2051 2065
52. J. Lee, M. Ko, and C.K. Joo Rho plays a key role in TGF-beta1-induced cytoskeletal rearrangement in human retinal pigment epithelium J Cell Physiol 216 2008 520 526
53. D. Kessler, S. Dethlefsen, and I. Haase et al. Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype J Biol Chem 276 2001 36575 36585
54. R. Bonart X-ray investigations concerning the physical structure of cross-linking in segments urethane elastomers J Macromol Sci Phys 2 1968 115 138
55. G.A. Skarja, and K.A. Woodhouse Structure-property relationships of degradable polyurethane elastomers containing an amino-acid based chain extender J Appl Polym Sci 75 2000 1522 1534
56. M. Yeganegi, R.A. Kandel, and J.P. Santerre Characterization of a biodegradable electrospun polyurethane nanofiber scaffold: mechanical properties and cytotoxicity Acta Biomater 6 2010 3847 3855
57. L.T. Korley, B.D. Pate, and E.L. Thomas et al. Effect of the degree of soft and hard segment ordering on the morphology and mechanical behavior of semicrystalline segmented polyurethanes Polymer 47 2006 3073 3082
58. J.S. Soares, K.R. Rajagopal, and J.E. Moore Jr. Deformation-induced hydrolysis of a degradable polymeric cylindrical annulus Biomech Model Mechanobiol 9 2009 177 186
59. D.L. Skaggs, M. Weidenbaum, and J.C. Iatridis et al. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus Spine 19 1994 1310 1319
60. F. Grinnell Fibroblast biology in three-dimensional collagen matrices Trends Cell Biol 13 2003 264 269
61. Y.W. Tang, R.S. Labow, and J.P. Santerre Enzyme-induced biodegradation of polycarbonate polyurethanes: dependence on hard-segment concentration J Biomed Mater Res 56 2001 516 528
62. R.S. Labow, E. Meek, and J.P. Santerre Hydrolytic degradation of poly(carbonate)-urethanes by monocyte-derived macrophages Biomaterials 22 2001 3025 3033
63. S. Roberts, B. Caterson, and J. Menage et al. Matrix metalloproteinases and aggrecanase: their role in disorders of the human intervertebral disc Spine 25 2000 3005 3013
64. G. Wypych Expectation of plasticizers. Handbook of plasticizers 2004 ChemTec Publishing Toronto, Ontario, Canada