Gradient biomaterials for soft-to-hard interface tissue engineering

Acta Biomaterialia

Volumn 7, Issue 4, 2011, Pages 1441-1451

  Seidi, Azadeh ^a   Ramalingam, Murugan ^a,b   Elloumi Hannachi, Imen ^c   Ostrovidov, Serge ^a   Khademhosseini, Ali ^a,d,e  

^a TOHOKU UNIVERSITY   (Japan)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Gradient biomaterials; Hard tissues; Interface tissue engineering; Scaffolds; Soft tissues

Indexed keywords

CARTILAGE; CELL ENGINEERING; CELL SIGNALING; FABRICATION; HISTOLOGY; INTERFACES (MATERIALS); NANOTECHNOLOGY; SCAFFOLDS (BIOLOGY); TISSUE REGENERATION;

BIOLOGICAL TISSUES; DAMAGED ZONES; GRADIENT BIOMATERIALS; HARD TISSUES; HUMAN BODIES; INTERFACE TISSUE ENGINEERINGS; MICRO TECHNOLOGY; SOFT TISSUE; TENDON TO BONES; TISSUE TYPES;

BONE;

AGAROSE; ARGINYLGLYCYLASPARTIC ACID; BIOMATERIAL; COLLAGEN; GELATIN; HYDROXYAPATITE; MACROGOL; NANOFIBER; POLY(2 HYDROXYETHYLMETHACRYLATE); POLYACRYLAMIDE GEL; POLYGLACTIN; POLYMETHACRYLIC ACID DERIVATIVE; TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

BIODEGRADABILITY; BONE; CARTILAGE; CELL DIFFERENTIATION; CELL MIGRATION; CELL TYPE; CHEMICAL COMPOSITION; CHEMICAL STRUCTURE; COMPOSITE MATERIAL; DIFFUSION; HUMAN; HYDROGEL; INKJET PRINTING; LIGAMENT; MECHANICS; MICROFLUIDICS; MICROTECHNOLOGY; MOLECULAR DYNAMICS; NANOFABRICATION; NANOTECHNOLOGY; NONHUMAN; PARTICLE SIZE; PHENOTYPE; PHOTODEGRADATION; PHOTOPOLYMERIZATION; POLYMERIZATION; POROSITY; PRINTING; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TENDON; TISSUE ENGINEERING; TISSUE TYPES;

EID: 79952189467     PISSN: 17427061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actbio.2011.01.011     Document Type: Review

References (94)

1. R. Murugan, and S. Ramakrishna Development of nanocomposites for bone grafting Compos Sci Technol 65 2005 2385 2406 (Pubitemid 41574394)
2. R. Langer, and J.P. Vacanti Tissue engineering Science 260 1993 920 926 (Pubitemid 23209960)
3. R. Murugan, and S. Ramakrishna Nano-featured scaffolds for tissue engineering: a review of spinning methodologies Tissue eng 12 2006 435 447 (Pubitemid 43673449)
4. L.S. Lohmander, A. Ostenberg, M. Englund, and H. Roos High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury Arthritis Rheum 50 2004 3145 3152 (Pubitemid 39371990)
5. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689 (Pubitemid 44233625)
6. H.H. Lu, and J. Jiang Interface tissue engineering and the formulation of multiple-tissue systems Adv Biochem Eng Biotechnol 102 2006 91 111 (Pubitemid 44608154)
7. A.G. Mikos Engineering complex tissues Tissue Eng 12 2006 3307 3339 (Pubitemid 46037158)
8. K.L. Moffat, I.N. Wang, S.A. Rodeo, and H.H. Lu Orthopedic interface tissue engineering for the biological fixation of soft tissue grafts Clin Sports Med 28 2009 157 176
9. S. Ramakrishna, M. Ramalingam, S. Kumar, and W. Soboyejo Biomaterials: a nano approach 2010 CRC Press Boca Raton, FL
10. R.R. Cooper, and S. Misol Tendon and ligament insertion A light and electron microscopic study. J Bone Joint Surg Am 52 1970 1 20
11. I.E. Wang, S. Mitroo, F.H. Chen, H.H. Lu, and S.B. Doty Age-dependent changes in matrix composition and organization at the ligament-to-bone insertion J Orthop Res 24 2006 1745 1755 (Pubitemid 44203306)
12. J.P. Spalazzi, J. Gallina, S.D. Fung-Kee-Fung, E.E. Konofagou, and H.H. Lu Elastographic imaging of strain distribution in the anterior cruciate ligament and at the ligament-bone insertions J Orthop Res 24 2006 2001 2010 (Pubitemid 44559961)
13. Moffat K, Chahine N, Hung C, Ateshian G, Lu HH. Characterization of the mechanical properties of the ACL-bone insertion. In: Proceedings of the ASME summer bioengineering conference; 2005. p. 54.
14. Spalazzi JP, Doty SB, Costa KD, Lu HH. Characterization of the mechanical properties, structure, and composition of the anterior cruciate ligament-bone insertion site. Transactions of the Orthopaedic Research Society; 2004.
15. I.E. Wang, J. Shan, R. Choi, S. Oh, C.K. Kepler, and F.H. Chen Role of osteoblast-fibroblast interactions in the formation of the ligament-to-bone interface J Orthop Res 25 2007 1609 1620 (Pubitemid 350293809)
16. M. Kobayashi, N. Watanabe, Y. Oshima, Y. Kajikawa, M. Kawata, and T. Kubo The fate of host and graft cells in early healing of bone tunnel after tendon graft Am J Sports Med 33 2005 1892 1897 (Pubitemid 41720590)
17. J.K. Lim, J. Hui, L. Li, A. Thambyah, J. Goh, and E.H. Lee Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction Arthroscopy 20 2004 899 910 (Pubitemid 39452262)
18. R. Murugan, P. Molnar, K.P. Rao, and J.J. Hickman Biomaterial surface patterning of self assembled monolayers for controlling neuronal cell behavior Int J Biomed Eng Technol 2 2009 104 134
19. J. He, Y. Du, J.L. Villa-Uribe, C. Hwang, D. Li, and A. Khademhosseini Rapid generation of biologically relevant hydrogels containing long-range chemical gradients Adv Funct Mater 20 2010 131 137
20. M. Spector, M.J. Michno, W.H. Smarook, and G.T. Kwiatkowski A high-modulus polymer for porous orthopedic implants: biomechanical compatibility of porous implants J Biomed Mater Res 12 1978 665 677 (Pubitemid 9022032)
21. C.D. Harner, G.H. Baek, T.M. Vogrin, G.J. Carlin, S. Kashiwaguchi, and S.L. Woo Quantitative analysis of human cruciate ligament insertions Arthroscopy 15 1999 741 749 (Pubitemid 29473357)
22. M. Ding, M. Dalstra, F. Linde, and I. Hvid Mechanical properties of the normal human tibial cartilage-bone complex in relation to age Clin Biomech (Bristol, Avon) 13 1998 351 358 (Pubitemid 28331628)
23. J.A. Cooper, H.H. Lu, F.K. Ko, J.W. Freeman, and C.T. Laurencin Fiber-based tissue-engineered scaffold for ligament replacement: design considerations and in vitro evaluation Biomaterials 26 2005 1523 1532 (Pubitemid 39441385)
24. E. Schlos, and J. Czernuszka Making tissue engineering scaffolds work. Review on the application of solid freeform fabrication technology to the production of tissue engineering scaffolds Eur Cells Mat 5 2003 29 40 (Pubitemid 38957399)
25. A. Khademhosseini, and R. Langer Microengineered hydrogels for tissue engineering Biomaterials 28 2007 5087 5092 (Pubitemid 47488484)
26. M.P. Lutolf Integration column: artificial ECM: expanding the cell biology toolbox in 3D Integr Biol (Camb) 1 2009 235 241
27. B.V. Slaughter, S.S. Khurshid, O.Z. Fisher, A. Khademhosseini, and N. Peppas Hydrogels in regenerative medicine Adv Mater 21 2009 3307 3329
28. P. Johnson, T. Reynolds, J. Stanbury, and C. Bowman High throughput kinetic analysis of photopolymer conversion using composition and exposure time gradients Polymer 46 2005 3300 3306 (Pubitemid 40466065)
29. A. Tirella, M. Marano, F. Vozzi, and A. Ahluwalia A microfluidic gradient maker for toxicity testing of bupivacaine and lidocaine Toxicol In Vitro 22 2008 1957 1964
30. S. DeLong, J. Moon, and J. West Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration Biomaterials 26 2004 3227 3234
31. T.A. Kapur, and M.S. Shoichet Immobilized concentration gradients of nerve growth factor guide neurite outgrowth J Biomed Mater Res A 68 2004 235 243 (Pubitemid 38524717)
32. S. Ilkhanizadeh, A.I. Teixeira, and O. Hermanson Inkjet printing of macromolecules on hydrogels to steer neural stem cell differentiation Biomaterials 28 2007 3936 3943 (Pubitemid 47048366)
33. J. Wong, A. Velasco, P. Rajagopalan, and Q. Pham Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels Langmuir 19 2003 1908 1913
34. P. Dubruel, R. Unger, S.V. Vlierberghe, V. Cnudde, P.J. Jacobs, and E. Schacht Porous gelatin hydrogels: 2. In vitro cell interaction study Biomacromolecules 8 2007 338 344 (Pubitemid 46323245)
35. F. Yang, R. Murugan, S. Wang, and S. Ramakrishna Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering Biomaterials 26 2005 2603 2610 (Pubitemid 39600712)
36. R. Murugan, and S. Ramakrishna Design strategies of tissue engineering scaffolds with controlled fiber orientation Tissue eng 13 2007 1845 1866 (Pubitemid 47293986)
37. N. Bhardwaj, and S.C. Kundu Electrospinning: a fascinating fiber fabrication technique Biotechnol Adv 28 2010 325 347
38. Z. Huang, Y. Zhang, M. Kotaki, and S. Ramakrishna A review on polymer nanofibers by electrospinning and their applications in nanocomposites Compos Sci Technol 63 2003 2223 2253 (Pubitemid 37124181)
39. D. Reneker, and I. Chun Nanometer diameter fibers of polymer, produced by electrospinning Nanotechnology 7 1996 216 223 (Pubitemid 126558355)
40. D. Guarnieri, A. Borzacchiello, A.D. Capua, M. Ruvo, and P.A. Netti Engineering of covalently immobilized gradients of RGD peptides on hydrogel scaffolds: effect on cell behaviour Macromol Symp 266 2008 36 40
41. X. Li, J. Xie, J. Lipner, X. Yuan, S. Thomopoulos, and Y. Xia Nanofiber scaffolds with gradations in mineral content for mimicking the tendon-to-bone insertion site Nano Lett 9 2009 2763 2768
42. C. Liu, Z. Han, and J.T. Czernuszka Gradient collagen/nanohydroxyapatite composite scaffold: development and characterization Acta Biomater 5 2009 661 669
43. A. Tripathi, N. Kathuria, and A. Kumar Elastic and macroporous agarose-gelatin cryogels with isotropic and anisotropic porosity for tissue engineering J Biomed Mater Res A 90 2009 680 694
44. C.T. Lo, D.J. Throckmorton, A.K. Singh, and A.E. Herr Photopolymerized diffusion-defined polyacrylamide gradient gels for on-chip protein sizing Lab Chip 8 2008 1273 1279
45. A.C. Lawson, and J.T. Czernuszka Collagen-calcium phosphate composites Proc Inst Mech Eng H 212 1998 413 425 (Pubitemid 128775832)
46. C.M. Lo, H.B. Wang, M. Dembo, and Y.L. Wang Cell movement is guided by the rigidity of the substrate Biophys J 79 2000 144 152 (Pubitemid 30436733)
47. N.L. Jeon, S.K.W. Dertinger, D.T. Chiu, I.S. Choi, A.D. Stroock, and G.M. Whitesides Generation of solution and surface gradients using microfluidic system Langmuir 16 2000 8311 8316
48. S.K.W. Dertinger, D.T. Chiu, N.L. Jeon, and G.M. Whitesides Generation of gradients having complex shapes using microfluidic networks Anal Chem 73 2001 1240 1246 (Pubitemid 32861911)
49. J.A. Burdick, A. Khademhosseini, and R. Langer Fabrication of gradient hydrogels using a microfluidics/photopolymerization process Langmuir 20 2004 5153 5156
50. Y. Du, M.J. Hancock, J. He, J.L. Villa-Uribe, B. Wang, and D.M. Cropek Convection-driven generation of long-range material gradients Biomaterials 31 2010 2686 2694
51. T. Boland, T. Xu, B. Damon, and X. Cui Application of inkjet printing to tissue engineering Biotechnol J 1 2006 910 917
52. J.A. Phillippi, E. Miller, L. Weiss, J. Huard, A. Waggoner, and P. Campbell Microenvironments engineered by inkjet bioprinting spatially direct adult stem cells toward muscle- and bone-like subpopulations Stem cells 26 2008 127 134
53. T. Xu, J. Jin, C. Gregory, J.J. Hickman, and T. Boland Inkjet printing of viable mammalian cells Biomaterials 26 2005 93 99 (Pubitemid 38759475)
54. M.C. Dodla, and R.V. Bellamkonda Anisotropic scaffolds facilitate enhanced neurite extension in vitro J Biomed Mater Res A 78 2006 213 221 (Pubitemid 44061058)
55. B.J. Peret, and W.L. Murphy Controllable soluble protein concentration gradients in hydrogel networks Adv Funct Mater 18 2008 3410 3417
56. M. Yamamoto, K. Yanase, and Y. Tabata Generation of type I collagen gradient in polyacrylamide hydrogels by a simple diffusion-controlled hydrolysis of amide groups Materials 3 2010 2393 2404
57. S.A. DeLong, A.S. Gobin, and J.L. West Covalent immobilization of RGDS on hydrogel surfaces to direct cell alignment and migration J Control Release 109 2005 139 148 (Pubitemid 41737260)
58. K. Chatterjee The effect of 3D hydrogel scaffold modulus on osteoblast differentiation and mineralization revealed by combinatorial screening Biomaterials 31 2010 5051 5062
59. R.A. Marklein, and J.A. Burdick Spatially controlled hydrogel mechanics to modulate stem cell interactions Soft Matter 6 2010 136 143
60. A.M. Kloxin, J.A. Benton, and K.S. Anseth In situ elasticity modulation with dynamic substrates to direct cell phenotype Biomaterials 31 2010 1 8
61. H. Yoshimoto, Y.M. Shin, H. Terai, and J.P. Vacanti A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering Biomaterials 24 2003 2077 2082 (Pubitemid 36298779)
62. E. Garreta, D. Gasset, C. Semino, and S. Borros Fabrication of a three-dimensional nanostructured biomaterial for tissue engineering of bone Biomol Eng 24 2007 75 80 (Pubitemid 46223550)
63. B.M. Baker, and R.L. Mauck The effect of nanofiber alignment on the maturation of engineered meniscus constructs Biomaterials 28 2007 1967 1977 (Pubitemid 46176172)
64. 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 (Pubitemid 47233078)
65. W.J. Li, K.G. Danielson, P.G. Alexander, and R.S. Tuan Biological response of chondrocytes cultured in three-dimensional nanofibrous poly(epsilon-caprolactone) scaffolds J Biomed Mater Res A 67 2003 1105 1114 (Pubitemid 37522722)
66. C.H. Lee, H.J. Shin, I.H. Cho, Y.M. Kang, I.A. Kim, and K.D. Park Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast Biomaterials 26 2005 1261 1270 (Pubitemid 39314500)
67. C.A. Bashur, L.A. Dahlgren, and A.S. Goldstein Effect of fiber diameter and orientation on fibroblast morphology and proliferation on electrospun poly(d,l-lactic-co-glycolic acid) meshes Biomaterials 27 2006 5681 5688 (Pubitemid 44279062)
68. W.J. Li, C.T. Laurencin, E.J. Caterson, R.S. Tuan, and F.K. Ko Electrospun nanofibrous structure: a novel scaffold for tissue engineering J Biomed Mater Res 60 2002 613 621 (Pubitemid 34492600)
69. Z. Ma, M. Kotaki, R. Inai, and S. Ramakrishna Potential of nanofiber matrix as tissue-engineering scaffolds Tissue Eng 11 2005 101 109 (Pubitemid 40515178)
70. E.M. Christenson Nanobiomaterial applications in orthopedics J Orthop Res 25 2007 11 22 (Pubitemid 46070727)
71. Q.P. Pham, U. Sharma, and A.G. Mikos Electrospinning of polymeric nanofibers for tissue engineering applications: a review Tissue eng 12 2006 1197 1211 (Pubitemid 44024491)
72. W.J. Li, R.L. Mauck, J.A. Cooper, X. Yuan, and R.S. Tuan Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering J Biomech 40 2007 1686 1693 (Pubitemid 46702147)
73. Q.P. Pham, U. Sharma, and A.G. Mikos Electrospun poly(epsilon- caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration Biomacromolecules 7 2006 2796 2805 (Pubitemid 44615263)
74. S. Liao, R. Murugan, C.K. Chan, and S. Ramakrishna Processing nanoengineered scaffolds through electrospinning and mineralization suitable for biomimetic bone tissue engineering J Mech Behav Biomed Mater 1 2008 252 260
75. C.K. Chan, T.S. Kumar, S. Liao, R. Murugan, M. Ngiam, and S. Ramakrishnan Biomimetic nanocomposites for bone graft applications Nanomedicine (Lond) 1 2006 177 188
76. J. Shi, L. Wang, F. Zhang, H. Li, L. Lei, and L. Liu Incorporating protein gradient into electrospun nanofibers as scaffolds for tissue engineering ACS Appl Mater Interfaces 2 2010 1025 1030
77. J. Xie, X. Li, J. Lipner, C.N. Manning, A.G. Schwartz, and S. Thomopoulos "Aligned-to-random" nanofiber scaffolds for mimicking the structure of the tendon-to-bone insertion site Nanoscale 2 2010 923 926
78. D. Kalyon, and M. Malik An integrated approach for numerical analysis of coupled flow and heat transfer in co-rotating twin screw extruders Int Polym Proc 22 2007 293 302
79. C. Erisken, D.M. Kalyon, and H. Wang Functionally graded electrospun polycaprolactone and beta-tricalcium phosphate nanocomposites for tissue engineering applications Biomaterials 29 2008 4065 4073
80. L. Kang, B.G. Chung, R. Langer, and A. Khademhosseini Microfluidics for drug discovery and development: from target selection to product lifecycle management Drug Discov Today 13 2008 1 13
81. B.G. Chung, L. Kang, and A. Khademhosseini Micro- and nanoscale technologies for tissue engineering and drug discovery applications Expert Opin Drug Discov 2 2007 1 16
82. R.L. Juliano, and S. Haskill Signal transduction from the extracellular matrix J Cell Biol 120 1993 577 585 (Pubitemid 23035126)
83. L. Parente, M.S. Koh, D.A. Willoughby, and A. Kitchen Studies on cell motility in inflammation. I. The chemotactic activity of experimental, immunological and non-immunological, inflammatory exudates Agents Actions 9 1979 190 195 (Pubitemid 9203884)
84. L. Parente, M.S. Koh, D.A. Willoughby, and A. Kitchen Studies on cell motility in inflammation. II. The in vivo effect of anti-inflammatory and anti-rheumatic drugs on chemotaxis in vitro Agents Actions 9 1979 196 200 (Pubitemid 9203885)
85. P. Martin Wound healing-aiming for perfect skin regeneration Science 276 1997 75 81 (Pubitemid 27161246)
86. T. Luhmann, P. Hanseler, B. Grant, and H. Hall The induction of cell alignment by covalently immobilized gradients of the 6th Ig-like domain of cell adhesion molecule L1 in 3D-fibrin matrices Biomaterials 30 2009 4503 4512
87. D.M. Knapp, E.F. Helou, and R.T. Tranquillo A fibrin or collagen gel assay for tissue cell chemotaxis: assessment of fibroblast chemotaxis to GRGDSP Exp Cell Res 247 1999 543 553 (Pubitemid 29394792)
88. S. Kidoaki, and T. Matsuda Microelastic gradient gelatinous gels to induce cellular mechanotaxis J Biotechnol 133 2008 225 230 (Pubitemid 350266897)
89. J.P. Spalazzi, S.B. Doty, K.L. Moffat, W.N. Levine, and H.H. Lu Development of controlled matrix heterogeneity on a triphasic scaffold for orthopedic interface tissue engineering Tissue eng 12 2006 3497 3508 (Pubitemid 46037172)
90. J.P. Spalazzi, E. Dagher, S.B. Doty, X.E. Guo, S.A. Rodeo, and H.H. Lu In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration J Biomed Mater Res A 86 2008 1 12 (Pubitemid 351799482)
91. J.E. Phillips, K.L. Burns, J.M. Le Doux, R.E. Guldberg, and A.J. Garcia Engineering graded tissue interfaces Proc Natl Acad Sci USA 105 2008 12170 12175
92. X. Wang, E. Wenk, X. Zhang, L. Meinel, G. Vunjak-Novakovic, and D.L. Kaplan Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering J Control Release 134 2009 81 90
93. J. Konikoff, W. Billings, L. Nelson, and J. Hunter Development of a single stage active tendon prosthesis. I. Distal end attachment J Bone Jt Surg Am 56 1974 848
94. A. Von Recum Handbook of biomaterials evaluation: scientific, technical and clinical testing of implant materials 1986 Macmillan New York