3D scaffolds co-seeded with human endothelial progenitor and mesenchymal stem cells: Evidence of prevascularisation within 7 days

European Cells and Materials

Volumn 26, Issue , 2013, Pages 49-65

  Duttenhoefer, F ^a,b   Lara De Freitas, R ^a,c   Meury, T ^a,d   Loibl, M ^a,e   Benneker, L M ^f   Richards, R G ^a   Alini, M ^a   Verrier, Sophie ^a  

^a AO RESEARCH INSTITUTE   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

3D; Autologous; Bone; Co cultures; Endothelial progenitor cells; Mesenchymal stem cells; Neovascularisation; Platelet lysates

Indexed keywords

CD133 ANTIGEN; CD146 ANTIGEN; CD309 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; GROWTH FACTOR; LECTIN; LYMPHOCYTE ANTIGEN; MOLECULAR SCAFFOLD; POLYURETHAN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ARTICLE; CELL COMPONENT; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; PERICYTE; REVASCULARIZATION; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING; TREATMENT DURATION;

EID: 84883795646     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967.
2. Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111: 4551-4558.
3. Berthod F, Germain L, Tremblay N, Auger FA (2006) Extracellular matrix deposition by fibroblasts is necessary to promote capillary-like tube formation in vitro. J Cell Physiol 207: 491-498.
4. Bondjers C, He L, Takemoto M, Norlin J, Asker N, Hellstrom M, Lindahl P, Betsholtz C (2006) Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytes. FASEB J 20: 1703-1705.
5. Bouletreau PJ, Warren SM, Spector JA, Peled ZM, Gerrets RP, Greenwald JA, Longaker MT (2002) Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 109: 2384-2397.
6. Caplan AI, Correa D (2011) PDGF in bone formation and regeneration: new insights into a novel mechanism involving MSCs. J Orthop Res 29: 1795-1803.
7. Capobianco S, Chennamaneni V, Mittal M, Zhang N, Zhang C (2010) Endothelial progenitor cells as factors in neovascularization and endothelial repair. World J Cardiol 2: 411-420.
8. Carano RA, Filvaroff EH (2003) Angiogenesis and bone repair. Drug Discov Today 8: 980-989.
9. Covas DT, Panepucci RA, Fontes AM, Silva WA Jr, Orellana MD, Freitas MC, Neder L, Santos AR, Peres LC, Jamur MC, Zago MA (2008) Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 36: 642-654.
10. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3: 301-313.
11. Deckers MM, Van Bezooijen RL, Van der Horst G, Hoogendam J, Van Der Bent C, Papapoulos SE, Lowik CW (2002) Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 143: 1545-1553.
12. Deleu J, Trueta J (1965) Vascularisation of bone grafts in the anterior chamber of the eye. J Bone Joint Surg Br 47: 319-329.
13. Feng J, Mantesso A, De BC, Nishiyama A, Sharpe PT (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A 108: 6503-6508.
14. Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288: 551-556.
15. Fuchs S, Ghanaati S, Orth C, Barbeck M, Kolbe M, Hofmann A, Eblenkamp M, Gomes M, Reis RL, Kirkpatrick CJ (2009) 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: 526-534.
16. Fuchs S, Hofmann A, Kirkpatrick CJ (2007) 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: 2577-2588.
17. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schafer B, Hossfeld DK, Fiedler W (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95: 3106-3112.
18. Gorna K, Gogolewski S (2000) Novel biodegradable polyurethanes for medical application. In: Synthetic bioabsorbable polymers for implants, ASTM STP 1396 (Agrawal CM, Parr JE, Lin ST, eds). American Society for Testing and Materials, West Conshohocken, PA, 39-57.
19. Gorna K, Gogolewski S (2003) Preparation, degradation, and calcification of biodegradable polyurethane foams for bone graft substitutes. J Biomed Mater Res A 67: 813-827.
20. Gorna K, Gogolewski S (2006) Biodegradable porous polyurethane scaffolds for tissue repair and regeneration. J Biomed Mater Res A 79: 128-138.
21. Grellier M, Bordenave L, Amedee J (2009) Cell-to-cell communication between osteogenic and endothelial lineages: implications for tissue engineering. Trends Biotechnol 27: 562-571.
22. Hofmann A, Ritz U, Verrier S, Eglin D, Alini M, Fuchs S, Kirkpatrick CJ, Rommens PM (2008) The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds. Biomaterials 29: 4217-4226.
23. Hoying JB, Boswell CA, Williams SK (1996) Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In Vitro Cell Dev Biol Anim 32: 409-419.
24. Hristov M, Erl W, Weber PC (2003) Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23: 1185-1189.
25. Hristov M, Weber C (2004) Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 8: 498-508.
26. Huang YC, Kaigler D, Rice KG, Krebsbach PH, Mooney DJ (2005) Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res 20: 848-857.
27. Johnson EO, Troupis T, Soucacos PN (2011) Tissue-engineered vascularized bone grafts: Basic science and clinical relevance to trauma and reconstructive microsurgery. Microsurgery 31: 176-182.
28. Jones AR, Clark CC, Brighton CT (1995) Microvessel endothelial cells and pericytes increase proliferation and repress osteoblast phenotypic markers in rat calvarial bone cell cultures. J Orthop Res 13: 553-561.
29. Kaigler D, Krebsbach PH, Polverini PJ, Mooney DJ (2003) Role of vascular endothelial growth factor in bone marrow stromal cell modulation of endothelial cells. Tissue Eng 9: 95-103.
30. Killingsworth MC, Wu X (2011) Vascular pericyte density and angiogenesis associated with adenocarcinoma of the prostate. Pathobiology 78: 24-34.
31. Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107: 1589-1598.
32. Laschke MW, Menger MD (2012) Vascularization in tissue engineering: angiogenesis versus inosculation. Eur Surg Res 48: 85-92.
33. Laschke MW, Rucker M, Jensen G, Carvalho C, Mulhaupt R, Gellrich NC, Menger MD (2008) Improvement of vascularization of PLGA scaffolds by inosculation of in situ-preformed functional blood vessels with the host microvasculature. Ann Surg 248: 939-948.
34. Laschke MW, Strohe A, Menger MD, Alini M, Eglin D (2010) In vitro and in vivo evaluation of a novel nanosize hydroxyapatite particles/poly(ester-urethane) composite scaffold for bone tissue engineering. Acta Biomater 6: 2020-2027.
35. Leboy PS, Beresford JN, Devlin C, Owen ME (1991) Dexamethasone induction of osteoblast mRNAs in rat marrow stromal cell cultures. J Cell Physiol 146: 370-378.
36. Lev EI, Estrov Z, Aboulfatova K, Harris D, Granada JF, Alviar C, Kleiman NS, Dong JF (2006) Potential role of activated platelets in homing of human endothelial progenitor cells to subendothelial matrix. Thromb Haemost 96: 498-504.
37. Lian JB, Stein GS (1995) Development of the osteoblast phenotype: molecular mechanisms mediating osteoblast growth and differentiation. Iowa Orthop J 15: 118-140.
38. Lin SS, Landesberg R, Chin HS, Lin J, Eisig SB, Lu HH (2006) Controlled release of PRP-derived growth factors promotes osteogenic differentiation of human mesenchymal stem cells. Conf Proc IEEE Eng Med Biol Soc 1: 4358-4361.
39. Lippross S, Loibl M, Hoppe S, Meury T, Benneker L, Alini M, Verrier S (2011) Platelet released growth factors boost expansion of bone marrow derived CD34(+) and CD133(+) endothelial progenitor cells for autologous grafting. Platelets 22: 422-432.
40. Lucarelli E, Fini M, Beccheroni A, Giavaresi G, Di Bella C, Aldini NN, Guzzardella G, Martini L, Cenacchi A, Di Maggio N, Sangiorgi L, Fornasari PM, Mercuri M, Giardino R, Donati D (2005) Stromal stem cells and platelet-rich plasma improve bone allograft integration. Clin Orthop Relat Res 435: 62-68.
41. Maier CL, Shepherd BR, Yi T, Pober JS (2010) Explant outgrowth, propagation and characterization of human pericytes. Microcirculation 17: 367-380.
42. Mandracchia VJ, Nelson SC, Barp EA (2001) Current concepts of bone healing. Clin Podiatr Med Surg 18: 55-77.
43. Martin I, Muraglia A, Campanile G, Cancedda R, Quarto R (1997) Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 138: 4456-4462.
44. Meury T, Verrier S, Alini M (2006) Human endothelial cells inhibit BMSC differentiation into mature osteoblasts in vitro by interfering with osterix expression. J Cell Biochem 98: 992-1006.
45. Nehls V, Drenckhahn D (1991) Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J Cell Biol 113: 147-154.
46. Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63: 300-311.
47. Ozerdem U, Alitalo K, Salven P, Li A (2005) Contribution of bone marrow-derived pericyte precursor cells to corneal vasculogenesis. Invest Ophthalmol Vis Sci 46: 3502-3506.
48. Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9: 702-712.
49. Rhinelander FW (1965) Some Aspects of the microcirculation of healing bone. Clin Orthop Relat Res 40: 12-16.
50. Roussy Y, Bertrand Duchesne MP, Gagnon G (2007) Activation of human platelet-rich plasmas: effect on growth factors release, cell division and in vivo bone formation. Clin Oral Implants Res 18: 639-648.
51. Salgado AJ, Gomes ME, Coutinho OP, Reis RL (2004) Isolation and osteogenic differentiation of bone-marrow progenitor cells for application in tissue engineering. Methods Mol Biol 238: 123-130.
52. Santos MI, Unger RE, Sousa RA, Reis RL, Kirkpatrick CJ (2009) Crosstalk between osteoblasts and endothelial cells co-cultured on a polycaprolactone-starch scaffold and the in vitro development of vascularization. Biomaterials 30: 4407-4415.
53. Sato N, Sawasaki Y, Senoo A, Fuse Y, Hirano Y, Goto T (1987) Development of capillary networks from rat microvascular fragments in vitro: the role of myofibroblastic cells. Microvasc Res 33: 194-210.
54. Schlingemann RO, Rietveld FJ, Kwaspen F, Van de Kerkhof PC, De Waal RM, Ruiter DJ (1991) Differential expression of markers for endothelial cells, pericytes, and basal lamina in the microvasculature of tumors and granulation tissue. Am J Pathol 138: 1335-1347.
55. Sims DE (2000) Diversity within pericytes. Clin Exp Pharmacol Physiol 27: 842-846.
56. Stein GS, Lian JB, Owen TA (1990) Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 4: 3111-3123.
57. Street J, Bao M, DeGuzman L, Bunting S, Peale FV Jr, Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, Van Bruggen N, Redmond HP, Carano RA, Filvaroff EH (2002) Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 99: 9656-9661.
58. Tsigkou O, Pomerantseva I, Spencer JA, Redondo PA, Hart AR, O'Doherty E, Lin Y, Friedrich CC, Daheron L, Lin CP, Sundback CA, Vacanti JP, Neville C (2010) Engineered vascularized bone grafts. Proc Natl Acad Sci USA 107: 3311-3316.
59. Unger RE, Sartoris A, Peters K, Motta A, Migliaresi C, Kunkel M, Bulnheim U, Rychly J, Kirkpatrick CJ (2007) 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: 3965-3976.
60. Verrier S, Meury TR, Kupcsik L, Heini P, Stoll T, Alini M (2010) Platelet-released supernatant induces osteoblastic differentiation of human mesenchymal stem cells: potential role of BMP-2. Eur Cell Mater 20: 403-414.
61. Villars F, Bordenave L, Bareille R, Amedee J (2000) Effect of human endothelial cells on human bone marrow stromal cell phenotype: role of VEGF? J Cell Biochem 79: 672-685.
62. Villars F, Guillotin B, Amedee T, Dutoya S, Bordenave L, Bareille R, Amedee J (2002) Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol 282: C775.
63. Wang DS, Miura M, Demura H, Sato K (1997) Anabolic effects of 1,25-dihydroxyvitamin D3 on osteoblasts are enhanced by vascular endothelial growth factor produced by osteoblasts and by growth factors produced by endothelial cells. Endocrinology 138: 2953-2962.
64. Zammaretti P, Zisch AH (2005) Adult 'endothelial progenitor cells'. Renewing vasculature. Int J Biochem Cell Biol 37: 493-503.
65. Whitney MJ, Lee A, Ylostalo J, Zeitouni S, Tucker A, Gregory CA (2009) Leukemia inhibitory factor secretion is a predictor and indicator of early progenitor status in adult bone marrow stromal cells. Tissue Eng Part A 15: 33-44.