The use of fibrin based matrices and fibrin microbeads (FMB) for cell based tissue regeneration

Expert Opinion on Biological Therapy

Volumn 8, Issue 12, 2008, Pages 1831-1846

  Gorodetsky, Raphael ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

3D cell culture; Fibrin microbeads (FMB); Fibrin(ogen); Mesenchymal stem cells; Microcarriers; Tissue engineering

Indexed keywords

FIBRIN; FIBRINOGEN; THROMBIN;

CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL GROWTH; CELL INTERACTION; CELL ISOLATION; CELL SEPARATION; CELL SUSPENSION; ENDOTHELIUM CELL; FIBRIN MICROBEADS; HUMAN; MEMBRANE MICROPARTICLE; MESENCHYMAL STEM CELL; NONHUMAN; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL TRANSPLANTATION; THERMOSTABILITY; TISSUE ENGINEERING; TISSUE REGENERATION; VASCULARIZATION;

ANIMALS; CELL ADHESION; FIBRIN; HOT TEMPERATURE; HUMANS; MESENCHYMAL STEM CELLS; MICROSPHERES; REGENERATION; TISSUE ENGINEERING;

EID: 57649170622     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712590802494576     Document Type: Review

References (118)

1. Zdrahala R, Zdrahala I. In vivo tissue engineering: Part I. Concept genesis and guidelines for its realization. J Biomater Appl 1999;14:192-209
2. Bonassar L, Vacanti C. Tissue engineering: the first decade and beyond. J Cell Biochem Suppl 1998
3. Young J, Teumer J, Kemp P, Parenteau N, Approaches to Transplanting Engineered Cells and Tissues, in Lanza R, Langer R, Chick W, (editors), Principles of Tissue Engineering. R.G. Landes Company, 1997;297-307
4. Michaeli D, McPherson M. Immunologic study of artificial skin used in the treatment of thermal injuries. J Burn Care Rehabil 1990;11:21-26
5. Truong AT, Kowal-Vern A, Latenser BA, et al. Comparison of dermal substitutes in wound healing utilizing a nude mouse model. J Burns Wounds 2005;4:e4 Published online 14 March 2005 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1501115 [last accessed 30 September 2008]
6. Pham C, Greenwood J, Cleland H, et al. Bioengineered skin substitutes for the management of burns: a systematic review. Burns 2007;33:946-57
7. Ehrenreich M, Ruszczak Z. Update on tissue-engineered biological dressings. Tissue Eng 2006;12:2407-24
8. Gentzkow GD, Iwasaki SD, Hershon KS, et al. Use of dermagraft, a cultured human dermis, to treat diabetic foot ulcers. Diabetes Care 1996;19:350-4
9. Griffith L. Emerging design principles in biomaterials and scaffolds for tissue engineering. Ann NY Acad Sci 2002;961:83-95
10. Lokmic Z, Stillaert F, Morrison WA, et al. An arteriovenous loop in a protected space generates a permanent, highly vascular, tissue-engineered construct. Faseb J 2007;21:511-22
11. Kassis I, Zangi L, Rivkin R, et al. Isolation of mesenchymal stem cells from G-CSF-mobilized human peripheral blood using fibrin microbeads. Bone Marrow Transplant 2006;37:967-76
12. Rivkin R, Ben-Ari A, Kassis I, et al. High-yield isolation, expansion, and differentiation of murine bone marrow-derived mesenchymal stem cells using fibrin microbeads (FMB). Cloning Stem Cells 2007;9:157-75
13. Zangi L, Rivkin R, Kassis I, et al. High-yield isolation, expansion, and differentiation of rat bone marrow-derived mesenchymal stem cells with fibrin microbeads. Tissue Eng 2006;12:2343-54
14. Doolittle RF, Yang Z, Mochalkin I. Crystal structure studies on fibrinogen and fibrin. Ann NY Acad Sci 2001;936:31-43
15. Doolittle RF, Spraggon G, Everse SJ. Crystal structures of fragments D and double-D from fibrinogen and fibrin. Thromb Haemost 1999;82:271-6
16. 2 Blood 2001;98:2448-55
17. Owren PA, Stormorken H. The mechanism of blood coagulation. Ergeb Physiol 1973;68:1-53
18. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-9
19. Marx G, Korner G, Mou X, Gorodetsky R. Packaging zinc, fibrinogen, and factor XIII in platelet α-granules. J Cell Physiol 1993;156:437-42
20. McNicol GP. B. The fibrinolytic mechanism. The mechanism of fibrinolysis. Proc R Soc Lond B Biol Sci 1969;173:285-91
21. Francis CW, Marder VJ. Concepts of clot lysis. Annu Rev Med 1986;37:187-204
22. Gorodetsky R, Vexler A, An J, et al. Haptotactic and growth stimulatory effects of fibrin(ogen) and thrombin on cultured fibroblasts. J Lab Clin Med 1998;131:269-80
23. 1 via the carboxyl-terminal RGD site of the Aα-chain. J Biochem 2000;128:705-10
24. Browder T, Folkman J, Pirie-Shepherd S. The hemostatic system as a regulator of angiogenesis. J Biol Chem 2000;275:1521-4
25. Dejana E, Zanetti A, Conforti G. Biochemical and functional characteristics of fibrinogen interaction with endothelial cells. Haemost 1988;18:262-70
26. Ge M, Tang G, Ryan TJ, Malik AB. Fibrinogen degradation product fragment D induces endothelial cell detachment by activation of cell-mediated fibrinolysis. J Clin Invest 1992;90:2508-16
27. Smith RA, Rooney MM, Lord ST, et al. Evidence for new endothelial cell binding sites on fibrinogen. Thromb Haemost 2000;84:819-25
28. Zhang G, Hu Q, Braunlin EA, et al. Enhancing efficacy of stem cell transplantation to the heart with a PEGylated fibrin biomatrix. Tissue Eng Part A 2008;14:1025-36
29. Hall H. Modified fibrin hydrogel matrices: both, 3D-scaffolds and local and controlled release systems to stimulate angiogenesis. Curr Pharm Des 2007;13:3597-607
30. Laurens N, Koolwijk P, De Maat MP. Fibrin structure and wound healing. J Thromb Haemost 2006;4:932-9
31. Horch RE, Munster AM, Achauer BM. Cultured Human Keratinocytes and Tissue Engineered Skin Substitutes. Stuttgart: Thieme, 2001
32. Acevedo CA, Weinstein-Oppenheimer C, Brown DI, et al. A mathematical model for the design of fibrin microcapsules with skin cells. Bioprocess Biosyst Eng 2008: Published online 15 August 2008, 10.1007/ s00449-008-0253-1
33. Hunyadi J, Farkas B, Bertenyi C, et al. Keratinocyte grafiing: covering of skin defects by separated autologous keratinocytes in a fibrin net. J Invest Dermatol 1987;89:119-20
34. Currie LJ, Martin R, Sharpe JR, James SE. A comparison of keratinocyte cell sprays with and without fibrin glue. Burns 2003;29:677-85
35. Weiss E, Yamaguchi Y, Falabella A, et al. Un-cross-linked fibrin substrates inhibit keratinocyte spreading and replication: correction with fibronectin and factor XIII cross-linking. J Cell Physiol 1998;174:58-65
36. Kubo M, Van De Water L, Plantefaber LC, et al. Fibrinogen and fibrin are anti-adhesive for keratinocytes: a mechanism for fibrin eschar slough during wound repair. J Invest Dermatol 2001;117:1369-81
37. Donaldson DJ, Mahan JT, et al. Further studies on the interaction of migrating keratinocytes with fibrinogen. Cell Commun Adhes 1994;2:299-308
38. Gorodetsky R, Clark RA, An J, et al. Fibrin microbeads (FMB) as biodegradable carriers for culturing cells and for accelerating wound healing. J Invest Dermatol 1999;112:866-72
39. Simon DI, Rao NK, Xu H, et al. Mac-1 (CD11b/CD18) and the urokinase receptor (CD87) form a functional unit on monocytic cells. Blood 1996;88:3185-94
40. Wojtecka-Lukasik E, Maslinski S. Fibronectin and fibrinogen degradation products stimulate PMN-leukocyte and mast cell degranulation. J Physiol Pharmacol 1992;43:173-81
41. Guo X, Wang C, Zhang Y, et al. Repair of large articular cartilage defects with implants of autologous mesenchymal stem cells seeded into β-tricalcium phosphate in a sheep model. Tissue Eng 2004;10:1818-29
42. Clark RA, An JQ, Greiling D, et al. Fibroblast migration on fibronectin requires three distinct functional domains. J Invest Dermatol 2003;121:695-705
43. Turley EA, Noble PW, Bourguignon LY. Signaling properties of hyaluronan receptors. J Biol Chem 2002;277:4589-92
44. Meinel L, Karageorgiou V, Hofmann S, et al. Engineering bone-like tissue in vitro using human bone marrow stem cells and silk scaffolds. J Biomed Mater Res A 2004;71:25-34
45. Bajorath J. Molecular organization, structural features, and ligand binding characteristics of CD44, a highly variable cell surface glycoprotein with multiple functions. Proteins Struct Funct Genet 2000;39:103-11
46. Sherman L, Wainwright D, Ponta H, Herrlich P. A splice variant of CD44 expressed in the apical ectodermal ridge presents fibroblast growth factors to limb mesenchyme and is required for limb outgrowth. Genes Dev 1998;12:1058-71
47. Eshkar Sebban L, Ronen D, Levartovsky D, et al. The involvement of CD44 and its novel ligand galectin-8 in apoptotic regulation of autoimmune inflammation. J Immunol 2007;179:1225-35
48. Henke CA, Roongta U, Mickelson DJ, et al. CD44-related chondroitin sulfate proteoglycan, a cell surface receptor implicated with tumor cell invasion, mediates endothelial cell migration on fibrinogen and invasion into a fibrin matrix. J Clin Invest 1996;97:2541-52
49. Nehls V, Hayen W. Are hyaluronan receptors involved in three-dimensional cell migration? Histol Histopathol 2000;15:629-36
50. Gorodetsky R, Vexler A, Shamir M, et al. New cell attachment peptide sequences from conserved epitopes in the carboxy termini of fibrinogen. Exp Cell Res 2003;287:116-29
51. Marx G, Hotovely-Salomon A, Levdansky L, et al. Haptide-coated collagen sponge as a bioactive matrix for tissue regeneration. J Biomed Matrix Res B Appl Biomater 2008;84:571-83
52. Radosevich M, Goubran HI, Burnouf T. Fibrin sealant: scientific rationale, production methods, properties, and current clinical use. Vox Sang 1997;72:133-43
53. Alving BM, Weinstein MJ, Finlayson JS, et al. Fibrin sealant: summary of a conference on characteristics and clinical uses. Transfus 1995;35:783-90
54. Marx G, Mou X, Hotovely-Salomon A, et al. Heat denaturation of fibrinogen to develop a biomedical matrix. J Biomed Mater Res B Appl Biomater 2008;84:49-57
55. Cox S, Cole M, Tawil B. Behavior of human dermal fibroblasts in three-dimensional fibrin clots: dependence on fibrinogen and thrombin concentration. Tissue Eng 2004;10:942-54
56. Catelas I, Sese N, Wu BM, et al. Human mesenchymal stem cell proliferation and osteogenic differentiation in fibrin gels in vitro. Tissue Eng 2006;12:2385-96
57. Ho W, Tawil B, Dunn JC, Wu BM. The behavior of human mesenchymal stem cells in 3D fibrin clots: dependence on fibrinogen concentration and clot structure. Tissue Eng 2006;12:1587-95
58. Marx G, Mou X, Hotovely-Salomon A, et al. Heat denaturation of fibrinogen to develop a biomedical matrix. J Biomed Mater Res B Appl Biomater 2008;84:49-57
59. Perka C, Arnold U, Spitzer R-S, Lindenhayn K. The use of fibrin beads for tissue engineering and subsequential transplantation. Tissue Eng 2001;7:359-61
60. Almqvist KF, Wang L, Wang J, et al. Culture of chondrocytes in alginate surrounded by fibrin gel: characteristics of the cells over a period of eight weeks. Ann Rheum Dis 2001;60:781-90
61. Almany L, Seliktar D. Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures. Biomaterials 2005;26:2467-77
62. Schmidt O, Mizrahi J, Elisseeff J, Seliktar D. Immobilized fibrinogen in PEG hydrogels does not improve chondrocyte-mediated matrix deposition in response to mechanical stimulation. Biotechnol Bioeng 2006;95:1061-9
63. Peled E, Boss J, Bejar J, et al. A novel poly(ethylene glycol)-fibrinogen hydrogel for tibial segmental defect repair in a rat model. J Biomed Mater Res A 2007;80:874-84
64. Gorodetsky R, Vexler A, Levdansky L, Marx G. Fibrin microbeads (FMB) as biodegradable carriers for culturing cells and for accelerating wound healing. Methods Mol Biol 2004;238:11-24
65. Shimony N, Avrahami I, Gorodetsky R, et al. A 3D rotary renal and mesenchymal stem cell culture model unveils cell death mechanisms induced by matrix deficiency and low shear stress. Nephrol Dial Transplant 2008;23(6):2071-80
66. Shimony N, Gorodetsky R, Marx G, et al. Fibrin microbeads (FMB) as a 3D platform for kidney gene and cell therapy. Kidney Int 2006;69:625-33
67. Chalupowicz DG, Chowdhury ZA, Bach TL, et al. Fibrin II induces endothelial cell capillary tube formation. J Cell Biol 1995;130:207-15
68. Trochon V, Mabilat C, Bertrand P, et al. Evidence of involvement of CD44 in endothelial cell proliferation, migration and angiogenesis in vitro. Int J Cancer 1996;66:664-8
69. Nehls V, Drenckhahn D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc Res 1995;50:311-22
70. Martineau L, Doillon C. Angiogenic response of endothelial cells seeded dispersed versus on beads in fibrin gels. Angiogenesis 2007;10:269-77
71. Christman KL, Vardanian AJ, Fang Q, et al. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol 2004;44:654-60
72. Van Hinsbergh VW, Collen A, Koolwijk P. Role of fibrin matrix in angiogenesis. Ann NY Acad Sci 2001;936:426-37
73. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987;20:263-72
74. Friedenstein A, Gorskaja J, Kulagina N. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976;4:267-74
75. Baddoo M, Hill K, Wilkinson R, et al. Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. J Cell Biochem 2003;89:1235-49
76. Tropel P, Noel D, Platet N, et al. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res 2004;295:395-406
77. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 1998;80:985-96
78. Shang Q, Wang Z, Liu W, et al. Tissue-engineered bone repair of sheep cranial defects with autologous bone marrow stromal cells. J Craniofac Surg 2001;12:586-93; discussion 594-585
79. Ringe J, Kaps C, Burmester G-R, Sittinger M. Stem cells for regenerative medicine: advances in the engineering of tissues and organs. Naturwissenschaften 2002;89:338-51
80. Worster AA, Nixon AJ, Brower-Toland BD, Williams J. Effect of transforming growth factor β1 on chondrogenic differentiation of cultured equine mesenchymal stem cells. Am J Vet Res 2000;61:1003-10
81. Niku M, Ilmonen L, Pessa-Morikawa T, Iivanainen A. Limited contribution of circulating cells to the development and maintenance of nonhematopoietic bovine tissues. Stem Cells 2004;22:12-20
82. Bartholomew A, Patil S, Mackay A, et al. Baboon mesenchymal stem cells can be genetically modified to secrete human erythropoietin in vivo. Hum Gene Ther 2001;12:1527-41
83. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7
84. Noth U, Osyczka AM, Tuli R, et al. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res 2002;20:1060-9
85. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-95
86. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-42
87. Wada MR, Inagawa-Ogashiwa M, Shimizu S, et al. Generation of different fates from multipotent muscle stem cells. Development 2002;129:2987-95
88. Kuznetsov SA, Mankani MH, Gronthos S, et al. Circulating skeletal stem cells. J Cell Biol 2001;153:1133-40
89. Miao Z, Jin J, Chen L, et al. Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 2006;30:681-7
90. Rosada C, Justesen J, Melsvik D, et al. The human umbilical cord blood: a potential source for osteoblast progenitor cells. Calcif Tissue Int 2003;72:135-42
91. Kim YJ, Yu JM, Joo HJ, et al. Role of CD9 in proliferation and proangiogenic action of human adipose-derived mesenchymal stem cells. Pflugers Arch 2007;455(2):283-96
92. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization of cells with osteogenic potential from human marrow. Bone 1992;13:81-8
93. Galmiche MC, Koteliansky VE, Briere J, et al. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 1993;82:66-76
94. Paulette A. Conget JJM: phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 1999;181:67-73
95. Sordi V, Malosio ML, Marchesi F, et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005;106:419-27
96. Peister A, Mellad JA, Larson BL, et al. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 2004;103:1662-8
97. Javazon EH, Beggs KJ, Flake AW, Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 2004;32:414-25
98. Gurevich O, Vexler A, Marx G, et al. Fibrin microbeads for isolating and growing bone marrow-derived progenitor cells capable of forming bone tissue. Tissue Eng 2002;8:661-72
99. Chen CT, Lin J, Li Q, et al. Antiangiogenic gene therapy for cancer via systemic administration of adenoviral vectors expressing secretable endostatin. Hum Gene Ther 2000;11:1983-96
100. Ruegg C, Mutter N. Anti-angiogenic therapies in cancer: achievements and open questions. Bull Cancer 2007;94:753-62
101. Cheema U, Brown RA, Alp B, MacRobert AJ. Spatially defined oxygen gradients and vascular endothelial growth factor expression in an engineered 3D cell model. Cell Mol Life Sci 2008;65:177-86
102. Kedem A, Perets A, Gamlieli-Bonshtein I, et al. Vascular endothelial growth factor-releasing scaffolds enhance vascularization and engraftment of hepatocytes transplanted on liver lobes. Tissue Eng 2005;11:715-22
103. Fedorovich NE, Alblas J, De Wijn JR, et al. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng 2007;13:1905-25
104. Vacanti JP, Langer R, Upton J, Marler JJ. Transplantation of cells in matrices for tissue regeneration. Adv Drug Deliv Rev 1998;33:165-82
105. Wang X, Qiao Q, Burd A, Qi K. Reconstruction of distal foot wounds with reverse first dorsal metatarsal artery flap. Burns 2005;31:1025-8
106. Hudson DA. Other ways to use tissue expanded flaps. Br J Plast Surg 2004;57:336-41
107. Morritt AN, Bortolotto SK, Dilley RJ, et al. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 2007;115:353-60
108. Yang CF, Chou KY, Weng ZC, et al. Cardiac myocyte progenitors from adult hearts for myocardial regenerative therapy. J Chin Med Assoc 2008;71:79-85
109. Sha'ban M, Kim S, Idrus R, Khang G. Fibrin and poly(lactic-co-glycolic acid) hybrid scaffold promotes early chondrogenesis of articular chondrocytes: an in vitro study. J Orthop Surg 2008;3:17; Published online 25 April 2008, doi: 10.1186/1749-799X-3-17
110. Braga LM, Rosa K, Rodrigues B, et al. Systemic delivery of adult stem cells improves cardiac function in spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 2008;35:113-9
111. Roseti L, Serra M, Tigani D, et al. Cell manipulation in autologous chondrocyte implantation: from research to cleanroom. Chir Organi Mov 2008;91:147-51
112. Saadeh PB, Brent B, Mehrara BJ, et al. Human cartilage engineering: chondrocyte extraction, proliferation, and characterization for construct development. Ann Plast Surg 1999;42:509-13
113. Paige KT, Cima LG, Yaremchuk MJ, et al. Injectable cartilage. Plast Reconstr Surg 1995;96:1390-8; discussion 1399-1400
114. Vacanti CA, Upton J. Tissue-engineered morphogenesis of cartilage and bone by means of cell transplantation using synthetic biodegradable polymer matrices. Clin Plast Surg 1994;21:445-62
115. Wong M, Siegrist M, Wang X, Hunziker E. Development of mechanically stable alginate/chondrocyte constructs: effects of guluronic acid content and matrix synthesis. J Orthop Res 2001;19:493-9
116. Shortkroff S, Barone L, Hsu HP, et al. Healing of chondral and osteochondral defects in a canine model: the role of cultured chondrocytes in regeneration of articular cartilage. Biomaterials 1996;17:147-54
117. Manfredini M, Zerbinati F, Gildone A, Faccini R. Autologous chondrocyte implantation: a comparison between an open periosteal-covered and an arthroscopic matrix-guided technique. Acta Orthop Belg 2007;73:207-18
118. Tan CF, Ng KK, Ng SH, Cheung YC. Magnetic resonance imaging of hyaline cartilage regeneration in neocartilage graft implantation. Transplant Proc 2003;35:3105-7