Materials as morphogenetic guides in tissue engineering

Current Opinion in Biotechnology

Volumn 14, Issue 5, 2003, Pages 551-558

  Hubbell, Jeffrey A ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; COLLAGEN TYPE 1; COLLAGEN TYPE 3; FIBRIN; GROWTH FACTOR; HYALURONIC ACID;

CELL ADHESION; CELL REGENERATION; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; TISSUE ENGINEERING; TISSUE REPAIR;

EID: 0142122292     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.copbio.2003.09.004     Document Type: Review

References (92)

1. Knapp D.M., Tower T.T., Tranquillo R.T., Barocas V.H. Estimation of cell traction and migration in an isometric cell traction assay. AIChE J. 45:1999;2628-2640.
2. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:2003;267-277 Working in collagen gels, the ability of cells to switch their paradigm for migration is demonstrated. Under some conditions, cells migrate employing proteolytic mechanisms in an elongated morphology, under other conditions they migrate in a non-proteolytic fashion in an amoeba-like morphology. The results have clear implications for materials design, specifically regarding nanofibrillar materials and protease-sensitive gels.
3. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 13:2003;264-269.
4. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J. Pathol. 200:2003;500-503.
5. Shreiber D.I., Barocas V.H., Tranquillo R.T. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophys. J. 84:2003;4102-4114.
6. Hinz B., Gabbiani G., Chaponnier C. The NH2-terminal peptide of α-smooth muscle actin inhibits force generation by the myofibroblast in vitro and in vivo. J. Cell Biol. 157:2002;657-663.
7. Girton T.S., Oegema T.R., Grassl E.D., Isenberg B.C., Tranquillo R.T. Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation. J. Biomech. Eng. 122:2000;216-223.
8. Uludag H., D'Augusta D., Golden J., Li J., Timony G., Riedel R., Wozney J.M. Implantation of recombinant human bone morphogenetic proteins with biomaterial carriers: a correlation between protein pharmacokinetics and osteoinduction in the rat ectopic model. J. Biomed. Mater. Res. 50:2000;227-238.
9. Okamoto T., Yamamoto Y., Gotoh M., Liu D., Kihara M., Kameyama K., Hayashi E., Nakamura K., Yamauchi A., Huang C.L.et al. Cartilage regeneration using slow release of bone morphogenetic protein-2 from a gelatin sponge to treat experimental canine tracheomalacia: a preliminary report. ASAIO J. 49:2003;63-69.
10. Ceballos D., Navarro X., Dubey N., Wendelschafer-Crabb G., Kennedy W.R., Tranquillo R.T. Magnetically aligned collagen gel filling a collagen nerve guide improves peripheral nerve regeneration. Exp. Neurol. 158:1999;290-300 The ability to induce alignment in fibrillar collagen matrices under magnetic fields is demonstrated. This alignment remains after the field is removed. Neurites are induced to migrate preferentially in the direction of fibril alignment, demonstrating local guidance by the material matrix.
11. Dubey N., Letourneau P.C., Tranquillo R.T. Neuronal contact guidance in magnetically aligned fibrin gels: effect of variation in gel mechano-structural properties. Biomaterials. 22:2001;1065-1075.
12. Friedlaender G.E., Perry C.R., Cole J.D., Cook S.D., Cierny G., Muschler G.F., Zych G.A., Calhoun J.H., LaForte A.J., Yin S. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J. Bone Joint Surg. Am. 83A:2001;S151-S158.
13. Toman P.D., Chisholm G., McMullin H., Gieren L.M., Olsen D.R., Kovach R.J., Leigh S.D., Fong B.E., Chang R., Daniels G.A.et al. Production of recombinant human type I procollagen trimers using a four-gene expression system in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275:2000;23303-23309.
14. Milella E., Brescia E., Massaro C., Ramires P.A., Miglietta M.R., Fiori V., Aversa P. Physico-chemical properties and degradability of non-woven hyaluronan benzylic esters as tissue engineering scaffolds. Biomaterials. 23:2002;1053-1063.
15. Tomihata K., Ikada Y. Crosslinking of hyaluronic acid with water-soluble carbodiimide. J. Biomed. Mater. Res. 37:1997;243-251.
16. Bulpitt P., Aeschlimann D. New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J. Biomed. Mater. Res. 47:1999;152-169.
17. Johns D.B., Rodgers K.E., Donahue W.D., Kiorpes T.C., diZerega G.S. Reduction of adhesion formation by postoperative administration of ionically cross-linked hyaluronic acid. Fertil. Steril. 68:1997;37-42.
18. Solchaga L.A., Goldberg V.M., Caplan A.I. Cartilage regeneration using principles of tissue engineering. Clin. Orthop. 391(Suppl):2001;S161-S170.
19. Freyman T.M., Yannas I.V., Gibson L.J. Cellular materials as porous scaffolds for tissue engineering. Prog. Mater. Sci. 46:2001;273-282.
20. Butler C.E., Yannas I.V., Compton C.C., Correia C.A., Orgill D.P. Comparison of cultured and uncultured keratinocytes seeded into a collagen-GAG matrix for skin replacements. Br. J. Plast. Surg. 52:1999;127-132.
21. Chamberlain L.J., Yannas I.V., Hsu H.P., Strichartz G.R., 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. 60:2000;666-677.
22. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4:2003;140-156.
23. Ryan E.A., Mockros L.F., Stern A.M., Lorand L. Influence of a natural and a synthetic inhibitor of factor XIIIa on fibrin clot rheology. Biophys. J. 77:1999;2827-2836.
24. Rocco M., Bernocco S., Turci M., Profumo A., Cuniberti C., Ferri F. Early events in the polymerization of fibrin. Ann. NY Acad Sci. 936:2001;167-184.
25. Herbert C.B., Nagaswami C., Bittner G.D., Hubbell J.A., Weisel J.W. Effects of fibrin micromorphology on neurite growth from dorsal root ganglia cultured in three-dimensional fibrin gels. J. Biomed. Mater. Res. 40:1998;551-559.
26. Herbert C.B., Bittner G.D., Hubbell J.A. Effects of fibrinolysis on neurite growth from dorsal root ganglia cultured in two- and three-dimensional fibrin gels. J. Comp. Neurol. 365:1996;380-391.
27. Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell. 91:1997;439-442.
28. Vu T.H., Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14:2000;2123-2133.
29. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17:2001;463-516.
30. Currie L.J., Sharpe J.R., Martin R. The use of fibrin glue in skin grafts and tissue-engineered skin replacements: a review. Plast. Reconstr. Surg. 108:2001;1713-1726.
31. Horch R.E., Bannasch H., Stark G.B. Transplantation of cultured autologous keratinocytes in fibrin sealant biomatrix to resurface chronic wounds. Transplant Proc. 33:2001;642-644 Fibrin is demonstrated as an effective cell transplantation matrix in the repair of dermal burns with cells isolated from healthy skin. The clinical implications of this paper are substantial.
32. Tassiopoulos A.K., Greisler H.P. Angiogenic mechanisms of endothelialization of cardiovascular implants: a review of recent investigative strategies. J. Biomater. Sci. Polym. Ed. 11:2000;1275-1284.
33. Xue L., Greisler H.P. Angiogenic effect of fibroblast growth factor-1 and vascular endothelial growth factor and their synergism in a novel in vitro quantitative fibrin-based 3-dimensional angiogenesis system. Surgery. 132:2002;259-267.
34. Mackenzie D.J., Sipe R., Buck D., Burgess W., Hollinger J. Recombinant human acidic fibroblast growth factor and fibrin carrier regenerates bone. Plast. Reconstr. Surg. 107:2001;989-996.
35. Schense J.C., Hubbell J.A. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug. Chem. 10:1999;75-81.
36. Langer R. Biomaterials in drug delivery and tissue engineering: one laboratory's experience. Acc. Chem. Res. 33:2000;94-101.
37. Vacanti J.P., Langer R. Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet. 354:1999;SI32-SI34.
38. Marler J.J., Upton J., Langer R., Vacanti J.P. Transplantation of cells in matrices for tissue regeneration. Adv. Drug Deliv. Rev. 33:1998;165-182.
39. Fridrikh S.V., Yu J.H., Brenner M.P., Rutledge G.C. Controlling the fiber diameter during electrospinning. Phys. Rev. Lett. 90:2003;144502.
40. Yoshimoto H., Shin Y.M., Terai H., Vacanti J.P. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials. 24:2003;2077-2082.
41. Huang L., Nagapudi K., Apkarian R.P., Chaikof E.L. Engineered collagen-PEO nanofibers and fabrics. J. Biomater. Sci. Polym. Ed. 12:2001;979-993.
42. Matthews J.A., Wnek G.E., Simpson D.G., Bowlin G.L. Electrospinning of collagen nanofibers. Biomacromolecules. 3:2002;232-238.
43. Wnek G.E., Carr M.E., Simpson D.G., Bowlin G.L. Electrospinning of nanofiber fibrinogen structures. Nano. Lett. 3:2003;213-216.
44. Goosen M.F.A., King G.A., McKnight C.A., Marcotte N. Animal-cell culture engineering using alginate polycation microcapsules of controlled membrane molecular-weight cutoffs. J. Membr. Sci. 41:1989;323-343.
45. Lim F., Sun A.M. Microencapsulated islets in diabetic rats. Science. 213:1981;1146-1146.
46. Soon-Shiong P. Treatment of type I diabetes using encapsulated islets. Adv. Drug Deliv. Rev. 35:1999;259-270.
47. Wong M., Siegrist M., Wang X.H., Hunziker E. Development of mechanically stable alginate/chondrocyte constructs: effects of guluronic acid content and matrix synthesis. J. Orthop. Res. 19:2001;493-499.
48. Atala A., Kim W., Paige K.T., Vacanti C.A., Retik A.B. Endoscopic treatment of vesicoureteral reflux with a chondrocyte-alginate suspension. J. Urol. 152:1994;641-643.
49. Cellesi F., Tirelli N., Hubbell J.A. Materials for cell encapsulation via a new tandem approach combining reverse thermal gelation and covalent crosslinking. Macromol. Chem. Phys. 203:2002;1466-1472.
50. Sawhney A.S., Pathak C.P., Hubbell J.A. Modification of islet of Langerhans surfaces with immunoprotective poly(ethylene glycol) coatings via interfacial photopolymerization. Biotechnol. Bioeng. 44:1994;383-386.
51. Sawhney A.S., Pathak C.P., Hubbell J.A. Bioerodible hydrogels based on photopolymerized poly(ethylene glycol)-co-poly(α-hydroxy acid) diacrylate macromers. Macromolecules. 26:1993;581-587.
52. Sperinde J.J., Griffith L.G. Control and prediction of gelation kinetics in enzymatically cross-linked poly(ethylene glycol) hydrogels. Macromolecules. 33:2000;5476-5480.
53. Sanborn T.J., Messersmith P.B., Barron A.E. In situ crosslinking of a biomimetic peptide-PEG hydrogel via thermally triggered activation of factor XIII. Biomaterials. 23:2002;2703-2710 An extremely gentle process for in situ gelation of materials is described, utilizing synthetic polymers that are substrates for transglutaminases and a recombinant transglutaminase to induce cross-linking.
54. Elbert D.L., Hubbell J.A. Conjugate addition reactions combined with free-radical cross-linking for the design of materials for tissue engineering. Biomacromolecules. 2:2001;430-441.
55. Elbert D.L., Pratt A.B., Lutolf M.P., Halstenberg S., Hubbell J.A. Protein delivery from materials formed by self-selective conjugate addition reactions. J. Control Release. 76:2001;11-25.
56. Lutolf M.P., Raeber G.P., Zisch A.H., Tirelli N., Hubbell J.A. Cell-responsive synthetic hydrogels. Adv. Mater. 15:2003;888-892 A novel class of biointeractive gels is introduced. Gel precursors are mixed in the presence of cells, using a cross-linking chemistry that preserves cell viability. The resulting materials mimic key characteristics of the ECM: adhesion to cells, proteolytic sensitivity, and ability to entrap growth factors.
57. Cruise G.M., Hegre O.D., Lamberti F.V., Hager S.R., Hill R., Scharp D.S., Hubbell J.A. In vitro and in vivo performance of porcine islets encapsulated in interfacially photopolymerized poly(ethylene glycol) diacrylate membranes. Cell Transplant. 8:1999;293-306.
58. Bryant S.J., Anseth K.S. Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. J. Biomed. Mater. Res. 64A:2003;70-79.
59. Park Y.D., Tirelli N., Hubbell J.A. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials. 24:2003;893-900.
60. Leach J.B., Bivens K.A., Patrick C.W., Schmidt C.E. Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol. Bioeng. 82:2003;578-589.
61. Nagapudi K., Brinkman W.T., Leisen J.E., Huang L., McMillan R.A., Apkarian R.P., Conticello V.P., Chaikof E.L. Photomediated solid-state cross-linking of an elastin-mimetic recombinant protein polymer. Macromolecules. 35:2002;1730-1737.
62. Ruoslahti E., Pierschbacher M.D. New perspectives in cell-adhesion - RGD and integrins. Science. 238:1987;491-497.
63. Sakiyama-Elbert S.E., Hubbell J.A. Functional biomaterials: design of novel biomaterials. Annu. Rev. Mater. Res. 31:2001;183-201.
64. Massia S.P., Hubbell J.A. An RGD spacing of 440nm is sufficient for integrin α-V-β-3-mediated fibroblast spreading and 140nm for focal contact and stress fiber formation. J. Cell Biol. 114:1991;1089-1100.
65. Hubbell J.A. Bioactive biomaterials. Curr. Opin. Biotechnol. 10:1999;123-129.
66. Hubbell J.A. Biomaterials in tissue engineering. Biotechnology. 13:1995;565-576.
67. Neff J.A., Tresco P.A., Caldwell K.D. Surface modification for controlled studies of cell-ligand interactions. Biomaterials. 20:1999;2377-2393.
68. VandeVondele S., Voros J., Hubbell J.A. RGD-Grafted poly-l-lysine-graft- (polyethylene glycol) copolymers block non-specific protein adsorption while promoting cell adhesion. Biotechnol. Bioeng. 82:2003;784-790.
69. Drumheller P.D., Hubbell J.A. Densely cross-linked polymer networks of poly(ethylene glycol) in trimethylolpropane triacrylate for cell-adhesion- resistant surfaces. J. Biomed. Mater. Res. 29:1995;207-215.
70. Banerjee P., Irvine D.J., Mayes A.M., Griffith L.G. Polymer latexes for cell-resistant and cell-interactive surfaces. J. Biomed. Mater. Res. 50:2000;331-339.
71. Desai N.P., Hubbell J.A. Solution technique to incorporate polyethylene oxide and other water-soluble polymers into surfaces of polymeric biomaterials. Biomaterials. 12:1991;144-153.
72. Bearinger J.P., Castner D.G., Healy K.E. Biomolecular modification of p(AAm-co-EG/AA) IPNs supports osteoblast adhesion and phenotypic expression. J. Biomater. Sci. Polym. Ed. 9:1998;629-652.
73. Maheshwari G., Brown G., Lauffenburger D.A., Wells A., Griffith L.G. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113:2000;1677-1686 Clustering of adhesion ligands is shown to induce qualitatively and quantitatively different cell adhesion than the same adhesion ligand density distributed randomly on a surface. Implications for materials design are substantial.
74. Irvine D.J., Ruzette A.V.G., Mayes A.M., Griffith L.G. Nanoscale clustering of RGD peptides at surfaces using comb polymers. 2. Surface segregation of comb polymers in polylactide. Biomacromolecules. 2:2001;545-556.
75. Irvine D.J., Mayes A.M., Griffith L.G. Nanoscale clustering of RGD peptides at surfaces using comb polymers. 1. Synthesis and characterization of comb thin films. Biomacromolecules. 2:2001;85-94.
76. Hern D.L., Hubbell J.A. Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J. Biomed. Mater. Res. 39:1998;266-276.
77. Kong H.J., Smith M.K., Mooney D.J. Designing alginate hydrogels to maintain viability of immobilized cells. Biomaterials. 24:2003;4023-4029.
78. Schense J., Hubbell J. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug. Chem. 10:1999;75-81.
79. Schense J.C., Hubbell J.A. Three-dimensional migration of neurites is mediated by adhesion site density and affinity. J. Biol. Chem. 275:2000;6813-6818.
80. Schense J.C., Bloch J., Aebischer P., Hubbell J.A. Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat. Biotechnol. 18:2000;415-419 The character of an ECM molecule, laminin, is conferred upon a natural healing matrix, fibrin. Improved peripheral nerve regeneration is observed in vivo.
81. Panitch A., Yamaoka T., Fournier M.J., Mason T.L., Tirrell D.A. Design and biosynthesis of elastin-like artificial extracellular matrix proteins containing periodically spaced fibronectin CS5 domains. Macromolecules. 32:1999;1701-1703.
82. Sakiyama-Elbert S.E., Panitch A., Hubbell J.A. Development of growth factor fusion proteins for cell-triggered drug delivery. FASEB J. 15:2001;1300-1302.
83. DeLong S.A., Mann B.K., West J.L. Scaffolds modified with tethered growth factors to influence smooth muscle cell behavior. FASEB J. 16:2002;A36-A36.
84. Sakiyama-Elbert S.E., Hubbell J.A. Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J. Control Release. 69:2000;149-158 Materials are formed that function in vivo essentially as affinity adsorption matrices, binding growth factors through bound heparin and releasing that growth factor as cells invade the matrix, locally degrading it.
85. Sakiyama-Elbert S.E., Hubbell J.A. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J. Control Release. 65:2000;389-402.
86. Zisch A.H., Schenk U., Schense J.C., Sakiyama-Elbert S.E., Hubbell J.A. Covalently conjugated VEGF-fibrin matrices for endothelialization. J. Control Release. 72:2001;101-113.
87. Gobin A.S., West J.L. Cell migration through defined, synthetic extracellular matrix analogues. FASEB J. 16:2002;751-753 Photopolymerization of a functional PEG-peptide copolymer is used to form matrices into which cells can invade under the chemotactic influence of a growth factor.
88. Halstenberg S., Panitch A., Rizzi S., Hall H., Hubbell J.A. Biologically engineered protein-graft-poly(ethylene glycol) hydrogels: a cell adhesive and plasmin-degradable biosynthetic material for tissue repair. Biomacromolecules. 3:2002;710-723.
89. Lutolf M.R., Weber F.E., Schmoekel H.G., Schense J.C., Kohler T., Muller R., Hubbell J.A. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat. Biotechnol. 21:2003;513-518 The biointeractive gels mentioned elsewhere are capable of inducing bone healing in animal models as effectively as natural, biologically derived materials.
90. Lutolf M.P., Lauer-Fields J.L., Schmoekel H.G., Metters A.T., Weber F.E., Fields G.B., Hubbell J.A. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc. Natl. Acad Sci. USA. 100:2003;5413-5418.
91. Kisiday J., Jin M., Kurz B., Hung H., Semino C., Zhang S., Grodzinsky A.J. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair. Proc. Natl. Acad Sci. USA. 99:2002;9996-10001 Using self-assembling peptides, it is possible to assemble a number of different material morphologies, ranging from amorphous to nanofibrillar. The assembly process can be sufficiently gentle as to induce the transformation in situ, in the presence of cells. Here, application in chontrocyte transplantation and cartilage repair is highlighted.
92. Zhang S.G., Marini D.M., Hwang W., Santoso S. Design of nanostructured biological materials through self-assembly of peptides and proteins. Curr. Opin. Chem. Biol. 6:2002;865-871 The ability to form a number of gel nanomorphologies through self-assembly of peptide precursors is demonstrated. The gentleness of the transformation conditions is conducive to in situ conversion from liquids to gels.