Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells

Biomaterials

Volumn 30, Issue 7, 2009, Pages 1329-1338

  Fuchs, Sabine ^a   Jiang, Xin ^a   Schmidt, Harald ^b   Dohle, Eva ^a   Ghanaati, Shahram ^a   Orth, Carina ^a   Hofmann, Alexander ^a   Motta, Antonella ^c   Migliaresi, Claudio ^c   Kirkpatrick, Charles J ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b MetaPhysiol ^*  (Germany)

^c UNIVERSITY OF TRENTO   (Italy)

Author keywords

Angiogenesis; Bone tissue engineering; Co culture; Endothelial progenitor cells; Image analysis

Indexed keywords

ANGIOGENESIS; BONE CONSTRUCTS; BONE REGENERATIONS; BONE TISSUE ENGINEERING; CELL TYPES; CO-CULTURE; CULTURE CONDITIONS; CULTURE TIMES; DYNAMIC PROCESSES; ENDOTHELIAL MARKERS; ENDOTHELIAL PROGENITOR CELLS; IMMUNOHISTOCHEMISTRY; IN CELLS; MATRIX COMPONENTS; NUMBER OF NODES; OSTEOGENIC DIFFERENTIATIONS; OSTEOGENIC MARKERS; OSTEOGENIC POTENTIALS; PERIPHERAL BLOODS; PRIMARY HUMAN OSTEOBLASTS; SILK FIBROINS; TEMPORAL CHANGES; TISSUE CONSTRUCTS; TUBE FORMATIONS; TUBE LENGTHS; VASCULAR NETWORKS; VASCULAR STRUCTURES; VASCULARIZATION;

BLOOD VESSEL PROSTHESES; BONE; CELL CULTURE; COBALT; COSMIC RAYS; FLOW CYTOMETRY; IMAGE ANALYSIS; OSTEOBLASTS; SELF ASSEMBLY; SILK; TISSUE ENGINEERING; TUBES (COMPONENTS);

ENDOTHELIAL CELLS;

COLLAGEN TYPE 1; SILK FIBROIN;

ARTICLE; BONE REGENERATION; CELL CULTURE; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; DYNAMICS; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TISSUE ENGINEERING; TISSUE GROWTH; VASCULARIZATION;

BIOLOGICAL MARKERS; BONE REGENERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; FIBROINS; GUIDED TISSUE REGENERATION; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOGENESIS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 58149280225     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2008.11.028     Document Type: Article

References (44)

1. Guillotin B., Bareille R., Bourget C., Bordenave L., and Amedee J. Interaction between human umbilical vein endothelial cells and human osteoprogenitors triggers pleiotropic effect that may support osteoblastic function. Bone (2008)
2. Meury T., Verrier S., and Alini M. Human endothelial cells inhibit BMSC differentiation into mature osteoblasts in vitro by interfering with osterix expression. J Cell Biochem 98 4 (2006) 992-1006
3. Finkenzeller G., Arabatzis G., Geyer M., Wenger A., Bannasch H., and Stark G.B. Gene expression profiling reveals platelet-derived growth factor receptor alpha as a target of cell contact-dependent gene regulation in an endothelial cell-osteoblast co-culture model. Tissue Eng (2006)
4. Geiger F., Bertram H., Berger I., Lorenz H., Wall O., Eckhardt C., et al. Vascular endothelial growth factor gene-activated matrix (VEGF165-GAM) enhances osteogenesis and angiogenesis in large segmental bone defects. J Bone Miner Res 20 11 (2005) 2028-2035
5. Villars F., Guillotin B., Amedee T., Dutoya S., Bordenave L., Bareille R., et al. Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol 282 4 (2002) C775-C785
6. Scherberich A., Galli R., Jaquiery C., Farhadi J., and Martin I. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 25 7 (2007) 1823-1829
7. Levenberg S., Rouwkema J., Macdonald M., Garfein E.S., Kohane D.S., Darland D.C., et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23 7 (2005) 879-884
8. Sanz L., Santos-Valle P., Alonso-Camino V., Salas C., Serrano A., Vicario J.L., et al. Long-term in vivo imaging of human angiogenesis: critical role of bone marrow-derived mesenchymal stem cells for the generation of durable blood vessels. Microvasc Res 75 3 (2008) 308-314
9. Melero-Martin J.M., Khan Z.A., Picard A., Wu X., Paruchuri S., and Bischoff J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109 11 (2007) 4761-4768
10. Au P., Tam J., Fukumura D., and Jain R.K. Bone marrow derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood (2008)
11. Bondar B., Fuchs S., Motta A., Migliaresi C., and Kirkpatrick C.J. Functionality of endothelial cells on silk fibroin nets: comparative study of micro- and nanometric fibre size. Biomaterials 29 5 (2008) 561-572
12. Uebersax L., Merkle H.P., and Meinel L. Insulin-like growth factor I releasing silk fibroin scaffolds induce chondrogenic differentiation of human mesenchymal stem cells. J Controlled Release 127 1 (2008) 12-21
13. Kim H.J., Kim U.-J., Kim H.S., Li C., Wada M., Leisk G.G., et al. Bone tissue engineering with premineralized silk scaffolds. Bone 42 6 (2008) 1226-1234
14. Hofmann A., Konrad L., Gotzen L., Printz H., Ramaswamy A., and Hofmann C. Bioengineered human bone tissue using autogenous osteoblasts cultured on different biomatrices. J Biomed Mater Res A 67 1 (2003) 191-199
15. Hagenmüller H., Hofmann S., Kohler T., Merkle H., Kaplan D., Vunjak-Novakovic G., et al. Non-invasive time-lapsed monitoring and quantification of engineered bone-like tissue. Ann Biomed Eng 35 10 (2007) 1657-1667
16. Hofmann S., Hagenmüller H., Koch A.M., Müller R., Vunjak-Novakovic G., Kaplan D.L., et al. Control of in vitro tissue-engineered bone-like structures using human mesenchymal stem cells and porous silk scaffolds. Biomaterials 28 6 (2007) 1152-1162
17. Unger R.E., Peters K., Wolf M., Motta A., Migliaresi C., and Kirkpatrick C.J. Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of human endothelial cells. Biomaterials 25 21 (2004) 5137-5146
18. Fuchs S., Motta A., Migliaresi C., and Kirkpatrick C.J. Outgrowth endothelial cells isolated and expanded from human peripheral blood progenitor cells as a potential source of autologous cells for endothelialization of silk fibroin biomaterials. Biomaterials 27 31 (2006) 5399-5408
19. Unger R.E., Sartoris A., Peters K., Motta A., Migliaresi C., Kunkel M., et al. Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials. Biomaterials 28 27 (2007) 3965-3976
20. Fuchs S., Hofmann A., and Kirkpatrick C.J. Microvessel-like structures from outgrowth endothelial cells from human peripheral blood in 2-dimensional and 3-dimensional co-cultures with osteoblastic lineage cells. Tissue Eng 13 10 (2007) 2577-2588
21. Fuchs S., Hermanns M., and Kirkpatrick C. Retention of a differentiated endothelial phenotype by outgrowth endothelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res (2006) 1-14
22. Unger R.E., Wolf M., Peters K., Motta A., Migliaresi C., and James Kirkpatrick C. Growth of human cells on a non-woven silk fibroin net: a potential for use in tissue engineering. Biomaterials 25 6 (2004) 1069-1075
23. Rasband W.S. ImageJ (1997-2007). Cited 2008; Available from:
24. Ridler T.W., and Calvard S. Picture thresholding using an iterative selection method. IEEE Trans Syst Man Cybern 8 8 (1978) 630-632
25. Landini G. Morphological operators for ImageJ. Cited 2008; Available from: .
26. Russ J.C. The image processing handbook. 5th ed. (2007), CRC Press, Boca Raton, FL
27. Movat H.Z. Demonstration of all connective tissue elements in a single section; pentachrome stains. AMA Arch Pathol 60 3 (1955) 289-295
28. Sweat F., Puchtler H., and Rosenthal S.I. Sirius red F3ba as a stain for connective tissue. Arch Pathol 78 (1964) 69-72
29. Peters K., Troyer D., Kummer S., Kirkpatrick C.J., and Rauterberg J. Apoptosis causes lumen formation during angiogenesis in vitro. Microvasc Res 64 2 (2002) 334-338
30. Ruth M., and Hirschberg M.S.J.P. Electron microscopy of cultured angiogenic endothelial cells. Microsc Res Tech 67 5 (2005) 248-259
31. Fierlbeck W., Liu A., Coyle R., and Ballermann B.J. Endothelial cell apoptosis during glomerular capillary lumen formation in vivo. J Am Soc Nephrol 14 5 (2003) 1349-1354
32. Lian J.B., and Stein G.S. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med 3 3 (1992) 269-305
33. Aubin J.E. Advances in the osteoblast lineage. Biochem Cell Biol 76 6 (1998) 899-910
34. Liu F., Malaval L., Gupta A.K., and Aubin J.E. Simultaneous detection of multiple bone-related mRNAs and protein expression during osteoblast differentiation: polymerase chain reaction and immunocytochemical studies at the single cell level. Dev Biol 166 1 (1994) 220-234
35. Meinel L., Karageorgiou V., Hofmann S., Fajardo R., Snyder B., Li C., et al. Engineering bone-like tissue in vitro using human bone marrow stem cells and silk scaffolds. J Biomed Mater Res A 71 1 (2004) 25-34
36. Kim H.J., Kim U.J., Vunjak-Novakovic G., Min B.H., and Kaplan D.L. Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells. Biomaterials 26 21 (2005) 4442-4452
37. Owen T.A., Aronow M., Shalhoub V., Barone L.M., Wilming L., Tassinari M.S., et al. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143 3 (1990) 420-430
38. Sato M., Yasui N., Nakase T., Kawahata H., Sugimoto M., Hirota S., et al. Expression of bone matrix proteins mRNA during distraction osteogenesis. J Bone Miner Res 13 8 (1998) 1221-1231
39. Nakase T., Takaoka K., Hirakawa K., Hirota S., Takemura T., Onoue H., et al. Alterations in the expression of osteonectin, osteopontin and osteocalcin mRNAs during the development of skeletal tissues in vivo. Bone Miner 26 2 (1994) 109-122
40. Usami K, Mizuno H, Okada K, Narita Y, Aoki M, Kondo T, et al. Composite implantation of mesenchymal stem cells with endothelial progenitor cells enhances tissue-engineered bone formation. J Biomed Mater Res A, in press, Epub 20 June 2008.
41. Dye J.F., Lawrence L., Linge C., Leach L., Firth J.A., and Clark P. Distinct patterns of microvascular endothelial cell morphology are determined by extracellular matrix composition. Endothelium 11 3 (2004) 151-167
42. Whelan M.C., and Senger D.R. Collagen I initiates endothelial cell morphogenesis by inducing actin polymerization through suppression of cyclic AMP and protein kinase A. J Biol Chem. 278 1 (2003) 327-334
43. *GER sequence and possibly p38 MAPK activation and focal adhesion disassembly. J Biol Chem 278 33 (2003) 30516-30524
44. Fuchs S., Ghanaati S., Orth C., Barbeck M., Kolbe M., Hofmann A., et al. Contribution of outgrowth endothelial cells from human peripheral blood on in vivo vascularization of bone tissue engineered constructs based on starch polycaprolactone scaffolds. Biomaterials 30 4 (2009) 526-534