In vivo and in vitro applications of collagen-GAG scaffolds

Chemical Engineering Journal

Volumn 137, Issue 1, 2008, Pages 102-121

  Harley, Brendan A C ^a   Gibson, Lorna J ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Cellular solids; Collagen; Scaffolds; Tissue engineering

Indexed keywords

COLLAGEN; COMPRESSIVE STRENGTH; ORTHOPEDICS; PORE STRUCTURE; TENSILE STRENGTH;

COLLAGEN-GAG SCAFFOLDS; COLLAGEN-GLYCOSAMINOGLYCAN (CG); VITRO APPLICATIONS;

TISSUE ENGINEERING;

COLLAGEN; COMPRESSIVE STRENGTH; ORTHOPEDICS; PORE STRUCTURE; TENSILE STRENGTH; TISSUE ENGINEERING;

EID: 38949168463     PISSN: 13858947     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cej.2007.09.009     Document Type: Article

References (130)

1. Yannas I.V. Tissue and Organ Regeneration in Adults (2001), Springer, New York
2. O'Brien F.J., Harley B.A., Yannas I.V., and Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 26 4 (2005) 433-441
3. Zeltinger J., Sherwood J.K., Graham D.A., Mueller R., and Griffith L.G. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng. 7 5 (2001) 557-572
4. Nehrer S., Breinan H.A., Ramappa A., Young G., Shortkroff S., Louie L.K., Sledge C.B., Yannas I.V., and Spector M. Matrix collagen type and pore size influence behavior of seeded canine chondrocytes. Biomaterials 18 11 (1997) 769-776
5. Wake M.C., Patrick Jr. C.W., and Mikos A.G. Pore morphology effects on the fibrovascular tissue growth in porous polymer substrates. Cell Transplant. 3 4 (1994) 339-343
6. Yannas I.V., Lee E., Orgill D.P., Skrabut E.M., and Murphy G.F. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc. Natl. Acad. Sci. U.S.A. 86 3 (1989) 933-937
7. Peyton S.R., and Putnam A.J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell Physiol. 204 1 (2005) 198-209
8. Grinnell F., Ho C.H., Lin Y.C., and Skuta G. Differences in the regulation of fibroblast contraction of floating versus stressed collagen matrices. J. Biol. Chem. 274 2 (1999) 918-923
9. Grinnell F., Ho C.H., Tamariz E., Lee D.J., and Skuta G. Dendritic fibroblasts in three-dimensional collagen matrices. Mol. Biol. Cell 14 2 (2003) 384-395
10. Engler A., Bacakova L., Newman C., Hategan A., Griffin M., and Discher D. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86 (2004) 617-628
11. Yeung T., Georges P.C., Flanagan L.A., Marg B., Ortiz M., Funaki M., Zahir N., Ming W., Weaver V., and Janmey P.A. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60 (2005) 24-34
12. Jiang H., and Grinnell F. Cell-matrix entanglements and mechanical anchorage of fibroblasts in three-dimensional collagen matrices. Mol. Biol. Cell 16 11 (2005) 5070-5076
13. Pelham J., Robert J., and Wang Y.-L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 9 (1997) 13661-13665
14. Freyman T.M., Yannas I.V., Yokoo R., and Gibson L.J. Fibroblast contraction of a collagen-GAG matrix. Biomaterials 22 21 (2001) 2883-2891
15. Schulz-Torres D., Freyman T.M., Yannas I.V., and Spector M. Tendon cell contraction of collagen-GAG matrices in vitro: effect of crosslinking. Biomaterials 21 (2000) 1607-1619
16. Zaman M.H., Trapani L.M., Sieminski A.L., Mackellar D., Gong H., Kamm R.D., Wells A., Lauffenburger D.A., and Matsudaira P. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. U.S.A. 103 29 (2006) 10889-10894
17. Hutmacher D.W., Goh J.C., and Teoh S.H. An introduction to biodegradable materials for tissue engineering applications. Ann. Acad. Med. Singapore 30 2 (2001) 183-191
18. Alvarez-Barreto J.F., Shreve M.C., Deangelis P.L., and Sikavitsas V.I. Preparation of a functionally flexible, three-dimensional, biomimetic poly(l-lactic acid) scaffold with improved cell adhesion. Tissue Eng. 13 6 (2007) 1205-1217
19. Webb A.R., Yang J., and Ameer G.A. Biodegradable polyester elastomers in tissue engineering. Expert Opin. Biol. Ther. 4 6 (2004) 801-812
20. Wang S., Cui W., and Bei J. Bulk and surface modifications of polylactide. Anal. Bioanal. Chem. 381 3 (2005) 547-556
21. Tessmar J.K., and Gopferich A.M. Customized PEG-derived copolymers for tissue-engineering applications. Macromol. Biosci. 7 1 (2007) 23-39
22. Sachlos E., and Czernuszka J.T. Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur. Cell Mater. 5 (2003) 29-39 discussion 39-40
23. Carter D.R., and Spengler D.M. Mechanical Properties and Composition of Cortical Bone. Clin. Orthop. Relat. Res. 135 (1978) 192-217
24. LeGeros R.Z. Properties of Osteoconductive Biomaterials: Calcium Phosphates. Clin. Orthop. Relat. Res. 395 (2002) 81-98
25. Doll B., Sfeir C., Winn S., Huard J., and Hollinger J. Critical aspects of tissue-engineered therapy for bone regeneration. Crit. Rev. Eukaryot. Gene Expr. 11 (2001) 173-198
26. Klein C.P., Driessen A.A., de Groot K., and van den Hooff A. Biodegradation behavior of various calcium phosphate materials in bone tissue. J. Biomed. Mater. Res. 17 5 (1983) 769-784
27. Ong J.L., and Chan D.C.N. Hydroxyapatite and their use as coatings in dental implants: a review. Crit. Rev. Biomed. Eng. 28 5/6 (2000) 667A-707A
28. Overgaard S. Calcium phosphate coatings for fixation of bone implants-evaluated mechanically and histologically by stereological methods. Acta Orthop. Scand. 71 6 (Suppl. 297) (2000) 1-74
29. Boden S.D., and Schimandle J.H. Biologic enhancement of spinal fusion. Spine 20 24 (1995) S113-S123
30. Bonfield W., Grynpas M.D., Tully A.E., Bowman J., and Abram J. Hydroxyapatite reinforced polyethylene-a mechanically compatible implant material for bone replacement. Biomaterials 2 3 (1981) 185-186
31. Geyer G. Materials for middle ear reconstruction. HNO 47 2 (1999) 77-91
32. Benebassath H., Klein B.Y., Lermer E., Azoury R., Rahamim E., Shlomai Z., and Sarig S. An in-vitro biocompatibility study of a new hydroxyapatite ceramic HA-SAL1-comparison to bioactive bone substitute ceramics. Cells Mater. 4 (1994) 37-50
33. Hasegawa K., Yamamura S., and Dohmae Y. Enhancing screw stability in osteosynthesis with hydroxyapatite granules. Arch. Orthop. Trauma Surg. 117 (1998) 175-176
34. Bohner M. Calcium orthophosphates in medicine: from ceramics to calcium phosphate cements. Injury 31 Suppl. 4 (2000) 37-47
35. Moreira-Gonzalez A., Jackson I.T., Miyawaki T., DiNick V., and Yavuzer R. Augmentation of the craniomaxillofacial region using porous hydroxyapatite granules. Plast. Reconstr. Surg. 111 (2003) 1808-1817
36. Boccaccini A.R., and Blaker J.J. Bioactive composite materials for tissue engineering scaffolds. Expert Rev. Med. Devices 2 3 (2005) 303-317
37. Maquet V., Boccaccini A.R., Pravata L., Notingher I., and Jerome R. Preparation, characterization, and in vitro degradation of bioresorbable and bioactive composites based on Bioglass-filled polylactide foams. J. Biomed. Mater. Res. 66A 2 (2003) 335-346
38. Brovarone C.V., Verne E., and Appendino P. Macroporous bioactive glass-ceramic scaffolds for tissue engineering. J. Mater. Sci. Mater. Med. 17 11 (2006) 1069-1078
39. Vitale-Brovarone C., Verne E., Robiglio L., Appendino P., Bassi F., Martinasso G., Muzio G., and Canuto R. Development of glass-ceramic scaffolds for bone tissue engineering: characterisation, proliferation of human osteoblasts and nodule formation. Acta Biomater. 3 2 (2007) 199-208
40. Kim H.W., Song J.H., and Kim H.E. Bioactive glass nanofiber-collagen nanocomposite as a novel bone regeneration matrix. J. Biomed. Mater. Res. A 79 3 (2006) 698-705
41. A.K. Lynn, S.M. Best, R.E. Cameron, B.A. Harley, I.V. Yannas, L.J. Gibson, W. Bonfield, Design of a multiphase osteochondral scaffold II: control of chemical composition, J. Biomed. Mater. Res. A, 2007, in review.
42. A.K. Lynn, B.A. Harley, I.V. Yannas, N. Rushton, M. Spector, L.J. Gibson, W. Bonfield, Design of an osteochondral scaffold I: basic design principles, J. Biomed. Mater. Res. B, 2007, in review.
43. Kim H.M. Bioactive ceramics: challenges and perspectives. J. Ceram. Soc. Jpn. 109 4 (2001) S49-S57
44. Lynn A.K., Yannas I.V., and Bonfield W. Antigenicity and immunogenicity of collagen. J. Biomed. Mater. Res. B Appl. Biomater. 71 2 (2005) 343-354
45. Yannas I.V., Burke J.F., Huang C., and Gordon P.L. Suppression of in vivo degradability and of immunogenicity of collagen by reaction with glycosaminoglycans. Polym. Prep. Am. Chem. Soc. 16 2 (1975) 209-214
46. Freyman T.M., Yannas I.V., and Gibson L.J. Cellular materials as porous scaffolds for tissue engineering. Prog. Mater. Sci. 46 (2001) 273-282
47. Sethi K.K., Yannas I.V., Mudera V., Eastwood M., McFarland C., and Brown R.A. Evidence for sequential utilization of fibronectin, vitronectin, and collagen during fibroblast-mediated collagen contraction. Wound Repair Regen. 10 6 (2002) 397-408
48. Yannas I.V. Biologically-active analogs of the extracellular-matrix-artificial skin and nerves. Angew. Chem. Int. Ed. English 29 1 (1990) 20-35
49. Harley B.A., Spilker M.H., Wu J.W., Asano K., Hsu H.P., Spector M., and Yannas I.V. Optimal degradation rate for collagen chambers used for regeneration of peripheral nerves over long gaps. Cells Tissues Organs 176 1-3 (2004) 153-165
50. Tsai C.C., Lin S.D., Lai C.S., and Lin T.M. The use of composite acellular allodermis-ultrathin autograft on joint area in major burn patients-one year follow-up, Kaohsiung. J. Med. Sci. 15 11 (1999) 651-658
51. Badylak S.F. The extracellular matrix as a biologic scaffold material. Biomaterials 28 25 (2007) 3587-3593
52. Sasano Y., Kamakura S., Nakamura M., Suzuki O., Mizoguchi I., Akita H., and Kagayama M. Subperiosteal implantation of octacalcium phosphate (OCP) stimulates both chondrogenesis and osteogenesis in the Tibia, but only osteogenesis in the parietal bone of a rat. Anat. Rec. 242 1 (1995) 40-46
53. Hemmerle J., Leize M., and Voegel J.C. Long-term behavior of a hydroxyapatite collagen-glycosaminoglycan biomaterial used for oral-surgery-a case-report. J. Mater. Sci. Mater. Med. 6 6 (1995) 360-366
54. Muschler G.F., Negami S., Hyodo A., Gaisser D., Easley K., and Kambic H. Evaluation of collagen ceramic composite graft materials in a spinal fusion model. Clin. Orthop. Relat. Res. 328 (1996) 250-260
55. Mehlisch D.R., Leider A.S., and Roberts W.E. Histologic evaluation of the bone-graft interface after mandibular augmentation with hydroxylapatite purified fibrillar collagen composite implants. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 70 6 (1990) 685-692
56. Ten Huisen K.S., Martin R.I., Klimkiewicz M., Brown P.W., and Formation. Properties of a synthetic bone composite: hydroxyapatite-collagen. J. Biomed. Mater. Res. 29 7 (1995) 803-810
57. Kikuchi M., Itoh S., Ichinose S., Shinomiya K., and Tanaka J. Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 22 13 (2001) 1705-1711
58. Rhee S.H., Suetsugu Y., and Tanaka J. Biomimetic configurational arrays of hydroxyapatite nanocrystals on bio-organics. Biomaterials 22 21 (2001) 2843-2847
59. Lynn A.K., Cameron R.E., Best S.M., Brooks R.A., Rushton N., and Bonfield W. Phase mapping: a novel design approach for the production of calcium phosphate-collagen biocomposites. Key Eng. Mater. 254-256 (2004) 593-596
60. Lynn A.K., Nakamura T., Patel N., Porter A.E., Renouf A.C., Laity P.R., Best S.M., Cameron R.E., Shimizu Y., and Bonfield W. Composition-controlled nanocomposites of apatite and collagen incorporating silicon as an osseopromotive agent. J. Biomed. Mater. Res. Part A 74 3 (2005) 447-453
61. Martin A.I., Salinas A.J., and Vallet-Regi M. Bioactive and degradable organic-inorganic hybrids. J. Eur. Ceram. Soc. 25 16 (2005) 3533-3538
62. Kataoka K., Nagao Y., Nukui T., Akiyama I., Tsuru K., Hayakawa S., Osaka A., and Huh N.H. An organic-inorganic hybrid scaffold for the culture of HepG2 cells in a bioreactor. Biomaterials 26 15 (2005) 2509-2516
63. O'Brien F.J., Harley B.A., Yannas I.V., and Gibson L. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials 25 6 (2004) 1077-1086
64. B.A. Harley, M.C. Flemings, Coarsening-mediated solidification is responsible for defining the pore microstructure of collagen-glycosaminoglycan scaffolds: experimental and thermal modeling results, Acta Mater., in revision.
65. Chamberlain L.J., and Yannas I.V. Preparation of collagen-glycosaminoglycan copolymers for tissue regeneration. In: Morgan J.R., and Yarmush M.L. (Eds). Methods of Molecular Medicine (1998), Humana Press, Tolowa, NJ
66. Chamberlain L.J., Yannas I.V., Hsu H.-P., Strichartz G., and Spector M. Collagen-GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp. Neurol. 154 (1998) 315-329
67. Chamberlain L.J., Yannas I.V., Arrizabalaga A., Hsu H.P., Norregaard T.V., and Spector M. Early peripheral nerve healing in collagen and silicone tube implants: myofibroblasts and the cellular response. Biomaterials 19 15 (1998) 1393-1403
68. Harley B.A., Hastings A.Z., Yannas I.V., and Sannino A. Fabricating tubular scaffolds with a radial pore size gradient by a spinning technique. Biomaterials 27 6 (2006) 866-874
69. B.A. Harley, A.K. Lynn, Z. Wissner-Gross, W. Bonfield, I.V. Yannas, L.J. Gibson, Design of a multiphase osteochondral scaffold III: fabrication of a mineralized collagen-GAG scaffold, J. Biomed. Mater. Res. A, 2007, in review.
70. Lynn A.K., and Bonfield W. A novel method for the simultaneous, titrant-free control of pH and calcium phosphate mass yield. Acc. Chem. Rev. 38 3 (2005) 202-207
71. Harley B.A., Lynn A.K., Wissner-Gross Z., Bonfield W., Yannas I.V., and Gibson L.J. Design and fabrication of a multiphase osteochondral scaffold. Proc. First Int. Conf. on Mech. of Biomaterials & Tissues; 2005 (2005)
72. B.A. Harley, A.K. Lynn, Z. Wissner-Gross, W. Bonfield, I.V. Yannas, L.J. Gibson, Design of a multiphase osteochondral scaffold IV: fabrication of layered scaffolds with soft interfaces, J. Biomed. Mater. Res. A, 2007, in review.
73. Yannas I.V., and Tobolsky A.V. Cross linking of gelatine by dehydration. Nature 215 100 (1967) 509-510
74. Harley B.A., Leung J.H., Silva E.C.C.M., and Gibson L.J. Mechanical characterization of collagen-GAG scaffolds. Acta Biomater. 3 4 (2007) 463-474
75. Harley B.A., Freyman T.M., Wong M.Q., and Gibson L.J. A new technique for calculating individual dermal fibroblast contractile forces generated within collagen-GAG scaffolds. Biophys. J. 93 8 (2007) 2911-2922
76. Gibson L.J., and Ashby M.F. Cellular Solids: Structure and Properties. second ed. (1997), Cambridge University Press, Cambridge, UK
77. Williams R.E. Space-filling polyhedron: its relation to aggregates of soap bubbles, plant cells and metal crystallites. Science 161 (1968) 276-277
78. Thompson W. On the division of space with minimum partition energy. Phil. Mag. 24 (1887) 503
79. Kraynik A.M., Reinelt D.A., and van Swol F. Structure of random monodisperse foam. Phys. Rev. 67 (2003) 031403
80. Levick J.R. Flow through interstitium and other fibrous matrices. Q. J. Exp. Physiol. 72 4 (1987) 409-437
81. O'Brien F.J., Harley B.A., Waller M.A., Yannas I.V., Gibson L.J., and Prendergast P.J. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol. Health Care 15 1 (2007) 3-17
82. B.A. Harley, H.-D. Kim, M.H. Zaman, I.V. Yannas, D.A. Lauffenburger, L.J. Gibson, Micro-architecture of three-dimensional scaffolds infleunces cell migration behavior via junction interactions, Biophys. J., 2007, in review.
83. Farrell E., O'Brien F.J., Byrne E., Doyle P., Fischer J., Yannas I.V., Harley B.A., O'Connell B., Prendergast P.J., and Campbell V.A. A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along the osteogenic and chrondrogenic routes. Tissue Eng. 12 3 (2006) 459-468
84. Compton C.C., Butler C.E., Yannas I.V., Warland G., and Orgill D.P. Organized skin structure is regenerated in vivo from collagen-GAG matrices seeded with autologous keratinocytes. J. Invest. Dermatol. 110 6 (1998) 908-916
85. Harley B.A., and Yannas I.V. Induced peripheral nerve regeneration using scaffolds. Minerva Biotechnol. 18 2 (2006) 97-120
86. Chang A.S., Yannas I.V., Perutz S., Loree H., Sethi R.R., Krarup C., Norregaard T., Zervas N.T., and Silver J. Electrophysiological study of recovery of peripheral nerves regenerated by a collagen-glycosaminoglycan copolymer matrix. In: Dunn R.L. (Ed). Progress in Biomedical Polymers (1990), Plenum Press, New York 107-119
87. Chamberlain L.J., Yannas I.V., Hsu H.P., Strichartz G.R., and Spector M. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen-GAG matrix in a ten-millimeter gap. J. Neurosci. Res. 60 5 (2000) 666-677
88. Samuel R.E., Lee C.R., Ghivizzani S.C., Evans C.H., Yannas I.V., Olsen B.R., and Spector M. Delivery of plasmid DNA to articular chondrocytes via novel collagen-glycosaminoglycan matrices. Hum. Gene Ther. 13 7 (2002) 791-802
89. Capito R.M., and Spector M. Scaffold-based articular cartilage repair. IEEE Eng. Med. Biol. Mag. 22 5 (2003) 42-50
90. Lee C.R., Grodzinsky A.J., Hsu H.-P., and Spector M. Effects of a cultured autologous chondrocyte-seeded type II collagen scaffold on the healing of a chondral defect in a canine model. J. Orthop. Res. 21 (2003) 272-281
91. Kinner B., Capito R.M., and Spector M. Regeneration of articular cartilage. Adv. Biochem. Eng. Biotechnol. 94 (2005) 91-123
92. Vickers S.M., Squitieri L.S., and Spector M. The effects of cross-linking type II collagen-GAG scaffolds on chondrogenesis in vitro: dynamic pore reduction promotes cartilage formation. Tissue Eng. 12 5. (2006)
93. Capito R.M., and Spector M. Collagen scaffolds for nonviral IGF-1 gene delivery in articular cartilage tissue engineering. Gene Ther. 14 9 (2007) 721-732
94. Steinert A.F., Palmer G.D., Capito R., Hofstaetter J.G., Pilapil C., Ghivizzani S.C., Spector M., and Evans C.H. Genetically enhanced engineering of meniscus tissue using ex vivo delivery of transforming growth factor-beta1 complementary deoxyribonucleic acid. Tissue Eng. 13 9 (2007) 2227-2237
95. Saad L., and Spector M. Effects of collagen type on the behavior of adult canine annulus fibrosus cells in collagen-glycosaminoglycan scaffolds. J. Biomed. Mater. Res. A 71 2 (2004) 233-241
96. Lynn A.K., Harley B.A., Wissner-Gross Z., Yannas I.V., Gibson L.J., and Bonfield W. Design and fabrication of a mineralized, triple-co-precipitate collagen-glycosaminoglycan scaffold. Proc. First Intl. Conf. on Mech. of Biomaterials & Tissues; 2005 (2005)
97. Jaworski J., and Klapperich C.M. Fibroblast remodeling activity at two- and three-dimensional collagen-glycosaminoglycan interfaces. Biomaterials 27 23 (2006) 4212-4220
98. Lee J., Leonard M., Oliver T., Ishihara A., and Jacobson K. Traction forces generated by locomoting keratocytes. J. Cell. Biol. 127 (1994) 1957-1964
99. Roy P., Petroll W.M., Chuong C.J., Cavanagh H.D., and Jester J.V. Effect of cell migration on the maintenance of tension on a collagen matrix. Ann. Biomed. Eng. 27 (1999) 721-730
100. Harris. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208 (1980) 177-179
101. Oliver T., Dembo M., and Jacobson K. Traction forces in locomoting cells. Cell Motil. Cytoskeleton 31 (1995) 225-240
102. Dembo M., and Wang Y.-L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76 (1999) 2307-2316
103. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., and Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. U.S.A. 100 4 (2003) 1484-1489
104. Lemmon C.A., Sniadecki N.J., Ruiz S.A., Tan J.L., Romer L.H., and Chen C.S. Shear force at the cell-matrix interface: enhanced analysis for microfabricated post array detectors. Mech. Chem. Biosyst. 2 1 (2005) 1-16
105. Roy P., Petroll W.M., Cavanagh H.D., Chuong C.J., and Jster J.V. An in vitro force measurement assay to study the early mechanical interaction between corneal fibroblasts and collagen matrix. Exp. Cell Res. 232 (1997) 106-117
106. Munevar S., Wang Y., and Dembo M. Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80 4 (2001) 1744-1757
107. Munevar S., Wang Y.-L., and Dembo M. Distinct roles of frontal and rear cell-substrate adhesions in fibrolast migration. Mol. Biol. Cell 12 (2001) 3947-3954
108. Lo C.-M., Wang H.-B., Dembo M., and Wang Y.-L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79 (2000) 144-152
109. Chen C.S., and Ingber D.E. Tensegrity and mechanoregulation: from skeleton to cytoskeleton. Osteoarthritis Cartilage 7 (1999) 81-94
110. Wang N., Butler J.P., and Ingber D. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260 (1993) 1124-1127
111. Wang H.-B., Dembo M., and Wang Y.-L. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am. J. Physiol. Cell Physiol. 279 (2000) C1345-C1350
112. Beningo K.A., Dembo M., Kaverina I., Small J.V., and Wang Y.-L. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153 4 (2001) 881-887
113. Wang H.-B., Dembo M., Hanks S.K., and Wang Y.-L. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. U.S.A. 98 20 (2001) 11295-11300
114. Beningo K.A., and Wang Y.-L. Flexible substrata for the detection of cellular traction forces. Trends Cell Biol. 12 2 (2002) 79-84
115. Engler A.J., Sen S., Sweeney H.L., and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 126 4 (2006) 677-689
116. Marquez J.P., Genin G.M., Zahalak G.I., and Elson E.L. The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. Biophys. J. 88 2 (2005) 778-789
117. Guilak F., Erickson G.R., and Ting-Beall H.P. The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys. J. 82 2 (2002) 720-727
118. Zahalak G.I., Wagenseil J.E., Wakatsuki T., and Elson E.L. A cell-based constitutive relation for bio-artificial tissues. Biophys. J. 79 5 (2000) 2369-2381
119. Freyman T.M., Yannas I.V., Pek Y.-S., Yokoo R., and Gibson L.J. Micromechanics of fibroblast contraction of a collagen-GAG matrix. Exp. Cell. Res. 269 (2001) 140-153
120. Freyman T.M., Yannas I.V., Yokoo R., and Gibson L.J. Fibroblast contractile force is independent of the stiffness which resists the contraction. Exp. Cell Res. 272 2 (2002) 153-162
121. Triantafillou T.C., Zhang J., Shercliff T.L., Gibson L.J., and Ashby M.F. Failure surfaces for cellular materials under multiaxial loads. 2. Comparison of models with experiment. Int. J. Mech. Sci. 31 9 (1989) 665-678
122. Lauffenburger D.A., and Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 84 3 (1996) 359-369
123. Friedl P., Zanker K.S., and Brocker E.B. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 43 5 (1998) 369-378
124. Condeelis J., and Segall J.E. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 3 12 (2003) 921-930
125. Lapidot T., Dar A., and Kollet O. How do stem cells find their way home?. Blood 106 6 (2005) 1901-1910
126. Wilson A., and Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 6 2 (2006) 93-106
127. Zaman M.H., Kamm R.D., Matsudaira P., and Lauffenburger D.A. Computational model for cell migration in three-dimensional matrices. Biophys. J. 89 2 (2005) 1389-1397
128. Vogel V., and Sheetz M. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell. Biol. 7 4 (2006) 265-275
129. Loree H.M., Yannas I.V., Mikic B., Chang A.S., Perutz S.M., Norregaard T.V., and Krarup C. A freeze-drying process for fabrication of polymeric bridges for peripheral nerve regeneration. Proc. 15th Annual Northeast Bioeng. Conf.; 1989 (1989) 53-54
130. Pek Y.S., Spector M., Yannas I.V., and Gibson L.J. Degradation of a collagen-chondroitin-6-sulfate matrix by collagenase and by chondroitinase. Biomaterials 25 3 (2004) 473-482