Engineering a microvascular capillary bed in a tissue-like collagen construct

Tissue Engineering - Part A

Volumn 20, Issue 19-20, 2014, Pages 2656-2665

  Alekseeva, Tijna ^a   Unger, Ronald E ^a   Brochhausen, Christoph ^a   Brown, Robert A ^b   Kirkpatrick, James C ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; BLOOD VESSELS; CELL CULTURE; CELL PROLIFERATION; COLLAGEN; FIBROBLASTS; OSTEOBLASTS; SCAFFOLDS (BIOLOGY); SELF ASSEMBLY; TISSUE;

COLLAGEN CONSTRUCTS; EXOGENOUS GROWTH; FIBROBLAST CULTURES; GEL CONTRACTION; HUMAN OSTEOBLAST; MICROVASCULAR ENDOTHELIAL CELLS; PLASTIC COMPRESSION; VESSEL-LIKE STRUCTURES;

ENDOTHELIAL CELLS;

CD31 ANTIGEN; COLLAGEN GEL; COLLAGEN TYPE 4; LAMININ; VASCULOTROPIN; BIOMIMETIC MATERIAL; COLLAGEN;

ARTICLE; CAPILLARY; CELL INVASION; COCULTURE; COLLAGEN FIBER; CONTROLLED STUDY; DERMAL MICROVASCULAR ENDOTHELIAL CELL; ENDOTHELIUM CELL; FIBROBLAST CULTURE; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROCIRCULATION; MICROVASCULAR CAPILLARY BED; MONOCULTURE; OSTEOBLAST; SCANNING ELECTRON MICROSCOPY; SURFACE PROPERTY; TISSUE ENGINEERING; CELL CULTURE; CHEMISTRY; CYTOLOGY; DERMIS; FIBROBLAST; MALE; METABOLISM;

BIOMIMETIC MATERIALS; CELLS, CULTURED; COLLAGEN; DERMIS; ENDOTHELIAL CELLS; FIBROBLASTS; HUMANS; MALE; OSTEOBLASTS; TISSUE ENGINEERING;

EID: 84911880191     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0570     Document Type: Article

References (57)

1. Grillo, H.C., and Gross, J. Thermal reconstitution of collagen from solution and the response to its heterologous implantation. J Surg Res 2, 69, 1962
2. Bell, E., Ivarsson, B., and Merrill, C. Production of a tissuelike structure by contraction of collagen lattices by humanfibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci U S A 76, 1274, 1979
3. Abou Neel, E.A., Bozec, L., Knowles, J.C., Syed, O., Mudera, V., Day, R., and Hyun, J.K. Collagen-emerging collagen based therapies hit the patient. Adv Drug Deliv Rev 65, 429, 2013
4. Elsdale, T., and Bard, J. Collagen substrata for studies on cell behavior. J Cell Biol 54, 626, 1972
5. Helary, C., Bataille, I., Abed, A., Illoul, C., Anglo, A., Louedec, L., Letourneur, D., Meddahi-Pelle, A., and Giraud-Guille, M.M. Concentrated collagen hydrogels as dermal substitutes. Biomaterials 31, 481, 2010
6. Dallon, J.C., and Ehrlich, H.P. A review of fibroblastpopulated collagen lattices. Wound Repair Regen 16, 472, 2008
7. Damink, L., Dijkstra, P.J., Vanluyn, M.J.A., Vanwachem, P.B., Nieuwenhuis, P., and Feijen, J. Cross-linking of dermal sheep collagen using hexamethylene diisocyanate. J Mater Sci Mater Med 6, 429, 1995
8. Weadock, K.S., Miller, E.J., Bellincampi, L.D., Zawadsky, J.P., and Dunn, M.G. Physical cross-linking of collagenfibers-comparison of ultraviolet-irradiation and dehydrothermal treatment. J Biomed Mater Res 29, 1373, 1995
9. Kagan, H.M., and Li, W.D. Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 88, 660, 2003
10. Vernon, R.B., Gooden, M.D., Lara, S.L., and Wight, T.N. Native fibrillar collagen membranes of micron-scale and submicron thicknesses for cell support and perfusion. Biomaterials 26, 1109, 2005
11. Parenteau-Bareil, R., Gauvin, R., Cliche, S., Gariepy, C., Germain, L., and Berthod, F. Comparative study of bovine, porcine and avian collagens for the production of a tissue engineered dermis. Acta Biomater 7, 3757, 2011
12. Charulatha, V., and Rajaram, A. Influence of different crosslinking treatments on the physical properties of collagen membranes. Biomaterials 24, 759, 2003
13. Brown, R.A. In the beginning there were soft collagen-cell gels: towards better 3D connective tissue models?. Exp Cell Res 319, 2460, 2013
14. Brown, R.A., Wiseman, M., Chuo, C.B., Cheema, U., and Nazhat, S.N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano-and microstructures by plastic compression. Adv Funct Mater 15, 1762, 2005
15. Ghezzi, C.E., Muja, N., Marelli, B., and Nazhat, S.N. Real time responses of fibroblasts to plastically compressed fibrillar collagen hydrogels. Biomaterials 32, 4761, 2011
16. Hadjipanayi, E., Mudera, V., and Brown, R.A. Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness. J Tissue Eng Regen Med 3, 77, 2009
17. Kureshi, A., Cheema, U., Alekseeva, T., Cambrey, A., and Brown, R. Alignment hierarchies: engineering architecture from the nanometre to the micrometre scale. J R Soc Interface 7, S707, 2010
18. Abou Neel, E.A., Cheema, U., Knowles, J.C., Brown, R.A., and Nazhat, S.N. Use of multiple unconfined compression for control of collagen gel scaffold density and mechanical properties. Soft Matter 2, 986, 2006
19. Buxton, P.G.,Bitar,M.,Gellynck,K., Parkar,M.,Brown,R.A., Young, A.M., Knowles, J.C., and Nazhat, S.N. Dense collagen matrix accelerates osteogenic differentiation and rescues the apoptotic response to MMP inhibition. Bone 43, 377, 2008
20. Ananta, M., Brown, R.A., and Mudera, V. A rapid fabricated living dermal equivalent for skin tissue engineering: an in vivo evaluation in an acute wound model. Tissue Eng Part A 18, 353, 2012
21. East, E., de Oliveira, D.B., Golding, J.P., and Phillips, J.B. Alignment of astrocytes increases neuronal growth in threedimensional collagen gels and is maintained following plastic compression to form a spinal cord repair conduit. Tissue Eng Part A 16, 3173, 2010
22. Micol, L.A., da Silva, L.F.A., Geutjes, P.J., Oosterwijk, E., Hubbell, J.A., Feitz, W.F.J., and Frey, P. In-vivo performance of high-density collagen gel tubes for urethral regeneration in a rabbit model. Biomaterials 33, 7447, 2012
23. Levis, H.J., Brown, R.A., and Daniels, J.T. Plastic compressed collagen as a biomimetic substrate for human limbal epithelial cell culture. Biomaterials 31, 7726, 2010
24. Kirkpatrick, C.J., Fuchs, S., and Unger, R.E. Co-culture systems for vascularization-learning from nature. Adv Drug Deliv Rev 63, 291, 2011
25. Unger, R.E., Sartoris, A., Peters, K., Motta, A., Migliaresi, C., Kunkel, M., Bulnheim, U., Rychly, J., and Kirkpatrick, C.J. Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillarylike structures on three-dimensional porous biomaterials. Biomaterials 28, 3965, 2007
26. Santos, M.I., Unger, R.E., Sousa, R.A., Reis, R.L., and Kirkpatrick, C.J. Crosstalk between osteoblasts and endothelial cells co-cultured on a polycaprolactone-starch scaffold and the in vitro development of vascularization. Biomaterials 30, 4407, 2009
27. Buschmann, J., Welti M., Hemmi S., Neuenschwander P., Baltes C., Giovanoli P., Rudin M., and Calcagni M. Threedimensional co-cultures of osteoblasts and endothelial cells in degrapol foam: histological and high-field magnetic resonance imaging analyses of pre-engineered capillary networks in bone grafts. Tissue Eng Part A 17, 291, 2011
28. Peters, K., Schmidt, H., Unger, R.E., Kamp, G., Prols, F., Berger, B.J., and Kirkpatrick, C.J. Paradoxical effects of hypoxia-mimicking divalent cobalt ions in human endothelial cells in vitro. Mol Cell Biochem 270, 157, 2005
29. Alekseeva, T., Jawad, H., Purser, M., and Brown, R.A. New improved technique of plastic compression of collagen using upward fluid flow. In: 8th International Conference on Cell& Stem Cell Engineering (ICCE), 2011, p. 5
30. Bitar, M., Brown, R.A., Salih, V., Kidane, A.G., Knowles, J.C., and Nazhat, S.N. Effect of cell density on osteoblastic differentiation and matrix degradation of biomimetic dense collagen scaffolds. Biomacromolecules 9, 129, 2008
31. Kirkpatrick, C.J., Krump-Konvalinkova, V., Unger, R.E., Bittinger, F., Otto, M., and Peters, K. Tissue response and biomaterial integration: the efficacy of in vitro methods. Biomol Eng 19, 211, 2002
32. Kirkpatrick, C.J., Unger, R.E., Krump-Konvalinkova, V., Peters, K., Schmidt, H., and Kamp, G. Experimental approaches to study vascularization in tissue engineering and biomaterial applications. J Mater Sci Mater Med 14, 677, 2003
33. Hadjipanayi, E., Brown, R.A., Mudera, V., Deng, D., Liu, W., and Cheema, U. Controlling physiological angiogenesis by hypoxia-induced signaling. J Control Release 146, 309, 2010
34. Swerlick, R.A., Lee, K.H., Wick, T.M., and Lawley, T.J. Human dermal microvascular endothelial but not human umbilical vein endothelial-cells express cd36 in vivo and in vitro. J Immunol 148, 78, 1992
35. Burrows, M.C., Zamarion, V.M., Filippin-Monteiro, F.B., Schuck, D.C., Toma, H.E., Campa, A., Garcia, C.R.S., and Catalani, L.H. Hybrid scaffolds built from PET and collagen as a model for vascular graft architecture. Macromol Biosci 12, 1660, 2012
36. Oh, J.H., Lee, J.S., Park, K.M., Moon, H.T., and Park, K.D. Tyrosinase-mediated surface grafting of cell adhesion peptide onto micro-fibrous polyurethane for improved endothelialization. Macromol Res 20, 1150, 2012
37. Bayramoglu, G., Kayaman-Apohan, N., Kahraman, M.V., Karadenizli, S., Kuruca, S.E., and Gungor, A. Preparation of bow tie-type methacrylated poly(caprolactone-co-lactic acid) scaffolds: effect of collagen modification on cell growth. Polym Adv Technol 23, 1403, 2012
38. Sgarioto, M., Vigneron, P., Patterson, J., Malherbe, F., Nagel, M.D., and Egles, C. Collagen type I together with fibronectin provide a better support for endothelialization. C R Biol 335, 520, 2012
39. Albelda, S.M., Muller, W.A., Buck, C.A., and Newman, P.J. Molecular and cellular properties of pecam-1 (endocam/ cd31)-a novel vascular cell cell-adhesion molecule. J Cell Biol 114, 1059, 1991
40. Park, S., DiMaio, T.A., Scheef, E.A., Sorenson, C.M., and Sheibani, N. PECAM-1 regulates proangiogenic properties of endothelial cells through modulation of cell-cell and cell-matrix interactions. Am J Physiol Cell Physiol 299, C1468, 2010
41. Davis, G.E., and Senger, D.R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97, 1093, 2005
42. Levis, H.J., Menzel-Severing, J., Drake, R.A.L., and Daniels, J.T. Plastic compressed collagen constructs for ocular cell culture and transplantation: a new and improved technique of confined fluid loss. Curr Eye Res 38, 41, 2013
43. Davis, G.E., Black, S.M., and Bayless, K.J. Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev Biol Anim 36, 513, 2000
44. Cross, V.L., Zheng, Y., Choi, N.W., Verbridge, S.S., Sutermaster, B.A., Bonassar, L.J., Fischbach, C., and Stroock, A.D. Dense type I collagen matrices that support cellular remodeling and microfabrication for studies of tumor angiogenesis and vasculogenesis in vitro. Biomaterials 31, 8596, 2010
45. Mudera, V.,Morgan,M.,Cheema, U.,Nazhat, S., and Brown, R. Ultra-rapid engineered collagen constructs tested in an in vivo nursery site. J Tissue Eng Regen Med 1, 192, 2007
46. Kemeny, S.F., Cicalese, S., Figueroa, D.S., and Clyne, A.M. Glycated collagen and altered glucose increase endothelial cell adhesion strength. J Cell Physiol 228, 1727, 2013
47. Kirkpatrick, C.J., Fuchs, S., Hermanns, M.I., Peters, K., and Unger, R.E. Cell culture models of higher complexity in tissue engineering and regenerative medicine. Biomaterials 28, 5193, 2007
48. Unger, R.E., Ghanaati, S., Orth, C., Sartoris, A., Barbeck, M., Halstenberg, S., Motta, A., Migliaresi, C., and Kirkpatrick, C.J. The rapid anastomosis between prevascularized networks on silk fibroin scaffolds generated in vitro with cocultures of human microvascular endothelial and osteoblast cells and the host vasculature. Biomaterials 31, 6959, 2010
49. Bitar, M., Salih, V., Brown, R.A., and Nazhat, S.N. Effect of multiple unconfined compression on cellular dense collagen scaffolds for bone tissue engineering. J Mater Sci Mater Med 18, 237, 2007
50. Stahl, A.,Wenger, A.,Weber,H., Stark, G.B.,Augustin, H.G., and Finkenzeller, G. Bi-directional cell contact-dependent regulation of gene expression between endothelial cells and osteoblasts in a three-dimensional spheroidal coculturemodel. Biochem Biophys Res Commun 322, 684, 2004
51. Stahl, A., Wu, X., Wenger, A., Klagsburn, M., and Kurschat, P. Endothelial progenitor cell sprouting in spheroid cultures is resistant to inhibition by osteoblasts: a model for bone replacement grafts. FEBS Lett 579, 5338, 2005
52. Hadjipanayi, E., Cheema, U., Mudera, V., Deng, D., Liu, W., and Brown, R.A. First implantable device for hypoxiamediated angiogenic induction. J Control Release 153, 217, 2011
53. Ajalloueian, F., Zeiai, S., Rojas, R., Fossum, M., and Hilborn, J. One-stage tissue engineering of bladder wall patches for an easy-to-use approach at the surgical table. Tissue Eng Part C Methods 19, 688, 2013
54. Ananta, M., Aulin, C.E., Hilborn, J., Aibibu, D., Houis, S., Brown, R.A., and Mudera, V. A poly(lactic acid-cocaprolactone)-collagen hybrid for tissue engineering applications. Tissue Eng Part A 15, 1667, 2009
55. Ghezzi, C.E., Marelli, B., Muja, N., Hirota, N., Martin, J.G., Barralet, J.E., Alessandrino, A., Freddi, G., and Nazhat, S.N. Mesenchymal stem cell-seeded multilayered dense collagen-silk fibroin hybrid for tissue engineering applications. Biotechnol J 6, 1198, 2011
56. Wong, J.P.F., MacRobert, A.J., Cheema, U., and Brown, R.A. Mechanical anisotropy in compressed collagen produced by localised photodynamic cross-linking. J Mech Behav Biomed Mater 18, 132, 2013
57. Anandagoda, N., Ezra, D.G., Cheema, U., Bailly, M., and Brown, R.A. Hyaluronan hydration generates threedimensional meso-scale structure in engineered collagen tissues. J R Soc Interface 9, 2680, 2012