Engineering fibrin-binding TGF-β1 for sustained signaling and contractile function of MSC based vascular constructs

Biomaterials

Volumn 32, Issue 33, 2011, Pages 8684-8693

  Liang, Mao Shih ^a   Andreadis, Stelios T ^a,b  

^a State University of New York ^*  (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

3D matrix for protein presentation; Biomimetic growth factor delivery; Fibrin hydrogels; Peptide domains; Stem cells; Vascular tissue engineering

Indexed keywords

3D MATRIX FOR PROTEIN PRESENTATION; BIOMIMETIC GROWTH FACTOR DELIVERY; BONE MARROW; CLEAVAGE SITES; DIFFERENT EFFECTS; ENGINEERED TISSUES; FUNCTIONAL PROTEINS; FUSION PROTEINS; GROWTH FACTOR; GROWTH FACTOR DELIVERY; HAIR FOLLICLES; IMMUNOPRECIPITATIONS; IN-VITRO; IN-VIVO; LATENCY ASSOCIATED PEPTIDES; MESENCHYMAL STEM CELL; MICROENVIRONMENTS; OPTIMAL INSERTION; PEPTIDE DOMAINS; PROMOTER ACTIVITIES; SMOOTH MUSCLE CELLS; TISSUE CONSTRUCTS; VASCULAR CONSTRUCT; VASCULAR TISSUE ENGINEERING;

BIOACTIVITY; BIOMIMETICS; CELL CULTURE; CELL PROLIFERATION; HYDROGELS; PEPTIDES; PHOSPHORYLATION; STEM CELLS; THREE DIMENSIONAL; TISSUE;

SCAFFOLDS (BIOLOGY);

BLOOD CLOTTING FACTOR 13; FIBRIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; BIOLOGICAL ACTIVITY; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; GENETIC ENGINEERING; HAIR FOLLICLE; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; PHOSPHORYLATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TISSUE ENGINEERING;

ANIMALS; BASE SEQUENCE; CELL LINE; DNA PRIMERS; FIBRIN; HUMANS; MINK; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TRANSFORMING GROWTH FACTOR BETA1;

EID: 80052965029     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.07.079     Document Type: Article

References (64)

1. Liu J.Y., Peng H.F., Gopinath S., Tian J., Andreadis S.T. Derivation of functional smooth muscle cells from multipotent human hair follicle mesenchymal stem cells. Tissue Eng Part A 2010, 16:2553-2564.
2. Liu J.Y., Peng H.F., Andreadis S.T. Contractile smooth muscle cells derived from hair-follicle stem cells. Cardiovasc Res 2008, 79:24-33.
3. Narita Y., Yamawaki A., Kagami H., Ueda M., Ueda Y. Effects of transforming growth factor-beta 1 and ascorbic acid on differentiation of human bone-marrow-derived mesenchymal stem cells into smooth muscle cell lineage. Cell Tissue Res 2008, 333:449-459.
4. Gong Z., Niklason L.E. Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs). FASEB J 2008, 22:1635-1648.
5. Wang D., Park J.S., Chu J.S., Krakowski A., Luo K., Chen D.J., et al. Proteomic profiling of bone marrow mesenchymal stem cells upon transforming growth factor beta1 stimulation. J Biol Chem 2004, 279:43725-43734.
6. Yao L., Liu J., Andreadis S.T. Composite fibrin scaffolds increase mechanical strength and preserve contractility of tissue engineered blood vessels. Pharm Res 2008, 25:1212-1221.
7. Han J., Liu J.Y., Swartz D.D., Andreadis S.T. Molecular and functional effects of organismal ageing on smooth muscle cells derived from bone marrow mesenchymal stem cells. Cardiovasc Res 2010, 87:147-155.
8. Liu J.Y., Swartz D.D., Peng H.F., Gugino S.F., Russell J.A., Andreadis S.T. Functional tissue-engineered blood vessels from bone marrow progenitor cells. Cardiovasc Res 2007, 75:618-628.
9. Long J.L., Tranquillo R.T. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol. 2003, 22:339-350.
10. Ross J.J., Tranquillo R.T. ECM gene expression correlates with in vitro tissue growth and development in fibrin gel remodeled by neonatal smooth muscle cells. Matrix Biol 2003, 22:477-490.
11. Kawaguchi J., Mee P.J., Smith A.G. Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone 2005, 36:758-769.
12. Kim J.H., Do H.J., Yang H.M., Oh J.H., Choi S.J., Kim D.K., et al. Overexpression of SOX9 in mouse embryonic stem cells directs the immediate chondrogenic commitment. Exp Mol Med 2005, 37:261-268.
13. Chiou M., Xu Y., Longaker M.T. Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adipose-derived mesenchymal cells. Biochem Biophys Res Commun 2006, 343:644-652.
14. Wahl S.M., Chen W. TGF-beta: how tolerant can it be?. Immunol Res 2003, 28:167-179.
15. Strober W., Fuss I., Boirivant M., Kitani A. Insights into the mechanism of oral tolerance derived from the study of models of mucosal inflammation. Ann N Y Acad Sci 2004, 1029:115-131.
16. Powrie F. Immune regulation in the intestine: a balancing act between effector and regulatory T cell responses. Ann N Y Acad Sci 2004, 1029:132-141.
17. Staines N.A., Derry C.J., Marinova-Mutafchieva L., Ali N., Davies D.H., Murphy J.J. Constraints on the efficacy of mucosal tolerance in treatment of human and animal arthritic diseases. Ann N Y Acad Sci 2004, 1029:250-259.
18. Okamoto A., Kawamura T., Kanbe K., Kanamaru Y., Ogawa H., Okumura K., et al. Suppression of serum IgE response and systemic anaphylaxis in a food allergy model by orally administered high-dose TGF-beta. Int Immunol 2005, 17:705-712.
19. Wahl S.M., Swisher J., McCartney-Francis N., Chen W. TGF-beta: the perpetrator of immune suppression by regulatory T cells and suicidal T cells. J Leukoc Biol 2004, 76:15-24.
20. Goncalves L.M., Epstein S.E., Piek J.J. Controlling collateral development: the difficult task of mimicking mother nature. Cardiovasc Res 2001, 49:495-496.
21. Lu L., Stamatas G.N., Mikos A.G. Controlled release of transforming growth factor beta1 from biodegradable polymer microparticles. J Biomed Mater Res 2000, 50:440-451.
22. Lu L., Yaszemski M.J., Mikos A.G. TGF-beta1 release from biodegradable polymer microparticles: its effects on marrow stromal osteoblast function. J Bone Joint Surg Am 2001, 83-A(Suppl. 1):S82-S91.
23. Peter S.J., Lu L., Kim D.J., Stamatas G.N., Miller M.J., Yaszemski M.J., et al. Effects of transforming growth factor beta1 released from biodegradable polymer microparticles on marrow stromal osteoblasts cultured on poly(propylene fumarate) substrates. J Biomed Mater Res 2000, 50:452-462.
24. DeFail A.J., Chu C.R., Izzo N., Marra K.G. Controlled release of bioactive TGF-beta 1 from microspheres embedded within biodegradable hydrogels. Biomaterials 2006, 27:1579-1585.
25. Drinnan C.T., Zhang G., Alexander M.A., Pulido A.S., Suggs L.J. Multimodal release of transforming growth factor-beta1 and the BB isoform of platelet derived growth factor from PEGylated fibrin gels. J Control Release 2010, 147:180-186.
26. Jung Y., Chung Y.I., Kim S.H., Tae G., Kim Y.H., Rhie J.W. In situ chondrogenic differentiation of human adipose tissue-derived stem cells in a TGF-beta1 loaded fibrin-poly(lactide-caprolactone) nanoparticulate complex. Biomaterials 2009, 30:4657-4664.
27. Ueda H., Hong L., Yamamoto M., Shigeno K., Inoue M., Toba T., et al. Use of collagen sponge incorporating transforming growth factor-beta1 to promote bone repair in skull defects in rabbits. Biomaterials 2002, 23:1003-1010.
28. Bannasch H., Fohn M., Unterberg T., Bach A.D., Weyand B., Stark G.B. Skin tissue engineering. Clin Plast Surg 2003, 30:573-579.
29. Geer D.J., Andreadis S.T. A novel role of fibrin in epidermal healing: plasminogen-mediated migration and selective detachment of differentiated keratinocytes. J Invest Dermatol 2003, 121:1210-1216.
30. Geer D.J., Swartz D.D., Andreadis S.T. Fibrin promotes migration in a three-dimensional in vitro model of wound regeneration. Tissue Eng 2002, 8:787-798.
31. Peretti G.M., Xu J.W., Bonassar L.J., Kirchhoff C.H., Yaremchuk M.J., Randolph M.A. Review of injectable cartilage engineering using fibrin gel in mice and swine models. Tissue Eng 2006, 12:1151-1168.
32. 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 2001, 72:101-113.
33. Grassl E.D., Oegema T.R., Tranquillo R.T. A fibrin-based arterial media equivalent. J Biomed Mater Res A 2003, 66:550-561.
34. Isenberg B.C., Williams C., Tranquillo R.T. Small-diameter artificial arteries engineered in vitro. Circ Res 2006, 98:25-35.
35. Swartz D.D., Russell J.A., Andreadis S.T. Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am J Physiol Heart Circ Physiol 2005, 288:H1451-H1460.
36. Flanagan T.C., Sachweh J.S., Frese J., Schnoring H., Gronloh N., Koch S., et al. In vivo remodeling and structural characterization of fibrin-based tissue-engineered heart valves in the adult sheep model. Tissue Eng Part A 2009, 15:2965-2976.
37. Syedain Z.H., Tranquillo R.T. Controlled cyclic stretch bioreactor for tissue-engineered heart valves. Biomaterials 2009, 30:4078-4084.
38. Black L.D., Meyers J.D., Weinbaum J.S., Shvelidze Y.A., Tranquillo R.T. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A 2009, 15:3099-3108.
39. Schense J.C., Hubbell J.A. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug Chem 1999, 10:75-81.
40. Sakiyama-Elbert S.E., Panitch A., Hubbell J.A. Development of growth factor fusion proteins for cell-triggered drug delivery. FASEB J 2001, 15:1300-1302.
41. Geer D.J., Swartz D.D., Andreadis S.T. Biomimetic delivery of keratinocyte growth factor upon cellular demand for accelerated wound healing in vitro and in vivo. Am J Pathol 2005, 167:1575-1586.
42. Zou Z., Sun P.D. Overexpression of human transforming growth factor-beta1 using a recombinant CHO cell expression system. Protein Expr Purif 2004, 37:265-272.
43. Lei P., Andreadis S.T. Stoichiometric limitations in assembly of active recombinant retrovirus. Biotechnol Bioeng 2005, 90:781-792.
44. Zou Z., Sun P.D. An improved recombinant mammalian cell expression system for human transforming growth factor-beta2 and -beta3 preparations. Protein Expr Purif 2006, 50:9-17.
45. Abe M., Harpel J.G., Metz C.N., Nunes I., Loskutoff D.J., Rifkin D.B. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1994, 216:276-284.
46. Yao L., Swartz D.D., Gugino S.F., Russell J.A., Andreadis S.T. Fibrin-based tissue-engineered blood vessels: differential effects of biomaterial and culture parameters on mechanical strength and vascular reactivity. Tissue Eng 2005, 11:991-1003.
47. Sakiyama S.E., Schense J.C., Hubbell J.A. Incorporation of heparin-binding peptides into fibrin gels enhances neurite extension: an example of designer matrices in tissue engineering. FASEB J 1999, 13:2214-2224.
48. Hervio L.S., Coombs G.S., Bergstrom R.C., Trivedi K., Corey D.R., Madison E.L. Negative selectivity and the evolution of protease cascades: the specificity of plasmin for peptide and protein substrates. Chem Biol. 2000, 7:443-453.
49. Ikeda T., Lioubin M.N., Marquardt H. Human transforming growth factor type beta 2: production by a prostatic adenocarcinoma cell line, purification, and initial characterization. Biochemistry 1987, 26:2406-2410.
50. Bannasch H., Unterberg T., Fohn M., Weyand B., Horch R.E., Stark G.B. Cultured keratinocytes in fibrin with decellularised dermis close porcine full-thickness wounds in a single step. Burns 2008, 34:1015-1021.
51. Raut S.D., Lei P., Padmashali R.M., Andreadis S.T. Fibrin-mediated lentivirus gene transfer: implications for lentivirus microarrays. J Control Release 2010, 144:213-220.
52. Lei P., Padmashali R.M., Andreadis S.T. Cell-controlled and spatially arrayed gene delivery from fibrin hydrogels. Biomaterials 2009, 30:3790-3799.
53. Hinck A.P., Archer S.J., Qian S.W., Roberts A.B., Sporn M.B., Weatherbee J.A., et al. Transforming growth factor beta 1: three-dimensional structure in solution and comparison with the X-ray structure of transforming growth factor beta 2. Biochemistry 1996, 35:8517-8534.
54. Hyytiainen M., Penttinen C., Keski-Oja J. Latent TGF-beta binding proteins: extracellular matrix association and roles in TGF-beta activation. Crit Rev Clin Lab Sci 2004, 41:233-264.
55. Clarke D.C., Brown M.L., Erickson R.A., Shi Y., Liu X. Transforming growth factor beta depletion is the primary determinant of Smad signaling kinetics. Mol Cell Biol 2009, 29:2443-2455.
56. Centrella M., Horowitz M.C., Wozney J.M., McCarthy T.L. Transforming growth factor-beta gene family members and bone. Endocr Rev 1994, 15:27-39.
57. Centrella M., McCarthy T.L., Canalis E. Transforming growth factor-beta and remodeling of bone. J Bone Joint Surg Am 1991, 73:1418-1428.
58. Hwang N.S., Kim M.S., Sampattavanich S., Baek J.H., Zhang Z., Elisseeff J. Effects of three-dimensional culture and growth factors on the chondrogenic differentiation of murine embryonic stem cells. Stem Cells 2006, 24:284-291.
59. Pelttari K., Steck E., Richter W. The use of mesenchymal stem cells for chondrogenesis. Injury 2008, 39(Suppl. 1):S58-S65.
60. Degat M.C., Dahri-Correia L., Lavigne F., Meunier A., Sedel L., Correia J., et al. Benzylaminated dextran-modified hydrogels: a long-term bioactive TGF-beta1 carrier. J Biomed Mater Res A 2009, 91:1178-1188.
61. Han Y., Wei Y., Wang S., Song Y. Enhanced chondrogenesis of adipose-derived stem cells by the controlled release of transforming growth factor-beta1 from hybrid microspheres. Gerontology 2009, 55:592-599.
62. Hu X., Ma L., Wang C., Gao C. Gelatin hydrogel prepared by photo-initiated polymerization and loaded with TGF-beta1 for cartilage tissue engineering. Macromol Biosci 2009, 9:1194-1201.
63. Park J.S., Yang H.J., Woo D.G., Yang H.N., Na K., Park K.H. Chondrogenic differentiation of mesenchymal stem cells embedded in a scaffold by long-term release of TGF-beta 3 complexed with chondroitin sulfate. J Biomed Mater Res A 2010, 92:806-816.
64. Solorio L.D., Fu A.S., Hernandez-Irizarry R., Alsberg E. Chondrogenic differentiation of human mesenchymal stem cell aggregates via controlled release of TGF-beta1 from incorporated polymer microspheres. J Biomed Mater Res A 2010, 92:1139-1144.