Endothelial progenitor cells (EPCs) and mesenchymal stem cells (MSCs) in bone healing

Current Stem Cell Research and Therapy

Volumn 7, Issue 4, 2012, Pages 293-301

  Keramaris, Nikolaos C ^a   Kaptanis, Sarandos ^c   Moss, Helen Lucy ^d   Loppini, Mattia ^e   Pneumaticos, Spyridon ^a   Maffulli, Nicola ^b  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c MAYDAY UNIVERSITY HOSPITAL   (United Kingdom)

^d AIREDALE GENERAL HOSPITAL   (United Kingdom)

^e UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

Angiogenesis; Bone and bones; Endothelial cells; EPCs; Fracture healing; Mesenchymal stem cells

Indexed keywords

CALCIUM PHOSPHATE; CD133 ANTIGEN; CD34 ANTIGEN; COLLAGEN FIBER; POLYLACTIC ACID;

ANGIOGENESIS; BONE DEVELOPMENT; BONE GRAFT; BONE MARROW CELL; BONE REGENERATION; BONE TURNOVER; CANCELLOUS BONE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; COCHRANE LIBRARY; EMBASE; ENDOTHELIAL PROGENITOR CELL; FRACTURE HEALING; HUMAN; MEDLINE; MESENCHYMAL STEM CELL; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; REVIEW; STROMA CELL; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANIMALS; BONE REGENERATION; ENDOTHELIAL CELLS; ENDOTHELIUM; FRACTURE HEALING; GUIDED TISSUE REGENERATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84862595902     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488812800793081     Document Type: Review

References (63)

1. Einhorn TA. Enhancement of fracture healing. J Bone Joint Surg Am 1995; 77(6): 940-56.
2. Weitzel PP, Esterhai JL, Jr. Delayed union, nonunion and synovial pseudarthrosis. In: Brighton CT, Friedlaender GE, Lane JM, editors. Bone formation and repair. 1st ed. ed. Rosemont, IL: American Academy of Orthopaedic Surgeons; 1994.
3. Lee DY, Cho TJ, Kim JA, et al. Mobilization of endothelial progenitor cells in fracture healing and distraction osteogenesis. Bone 2008; 42(5): 932-41.
4. Kaigler D, Krebsbach PH, Wang Z, West ER, Horger K, Mooney DJ. Transplanted endothelial cells enhance orthotopic bone regeneration. J Dent Res 2006; 85(7): 633-7.
5. Porter RL, Calvi LM. Communications between bone cells and hematopoietic stem cells. Arch Biochem Biophys 2008; 473(2): 193-200.
6. Fuchs JR, Nasseri BA, Vacanti JP. Tissue engineering: a 21st century solution to surgical reconstruction. Ann Thorac Surg 2001; 72(2): 577-91.
7. Cassell OC, Hofer SO, Morrison WA, Knight KR. Vascularisation of tissue-engineered grafts: the regulation of angiogenesis in reconstructive surgery and in disease states. Br J Plast Surg 2002; 55(8): 603-10.
8. McKee JA, Banik SS, Boyer MJ, et al. Human arteries engineered in vitro. EMBO Rep 2003; 4(6): 633-8.
9. Murphy WL, Simmons CA, Kaigler D, Mooney DJ. Bone regeneration via a mineral substrate and induced angiogenesis. J Dent Res 2004; 83(3): 204-10.
10. Tabata Y, Yamada K, Miyamoto S, et al. Bone regeneration by basic fibroblast growth factor complexed with biodegradable hydrogels. Biomaterials 1998; 19(7-9): 807-15.
11. Tanihara M, Suzuki Y, Yamamoto E, Noguchi A, Mizushima Y. Sustained release of basic fibroblast growth factor and angiogenesis in a novel covalently crosslinked gel of heparin and alginate. J Biomed Mater Res 2001; 56(2): 216-21.
12. Carano RA, Filvaroff EH. Angiogenesis and bone repair. Drug Discov Today 2003; 8(21): 980-9.
13. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005; 23(1): 47-55.
14. Huang YC, Kaigler D, Rice KG, Krebsbach PH, Mooney DJ. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res 2005; 20(5): 848-57.
15. Stosich MS, Bastian B, Marion NW, Clark PA, Reilly G, Mao JJ. Vascularized adipose tissue grafts from human mesenchymal stem cells with bioactive cues and microchannel conduits. Tissue Eng 2007; 13(12): 2881-90.
16. Nomi M, Atala A, Coppi PD, Soker S. Principals of neovascularization for tissue engineering. Mol Aspects Med 2002; 23(6): 463-83.
17. Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol 2001; 19(11): 1029-34.
18. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275(5302): 964-7.
19. Hristov M, Erl W, Weber PC. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 2003; 23(7): 1185-9.
20. Dignat-George F, Sampol J. Circulating endothelial cells in vascular disorders: new insights into an old concept. Eur J Haematol 2000; 65(4): 215-20.
21. Masuda H, Asahara T. Post-natal endothelial progenitor cells for neovascularization in tissue regeneration. Cardiovasc Res 2003 1; 58(2): 390-8.
22. Papathanasopoulos A, Giannoudis PV. Biological considerations of mesenchymal stem cells and endothelial progenitor cells. Injury 2008; 39 (Suppl 2): S21-32.
23. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976; 4(5): 267-74.
24. Castro-Malaspina H, Gay RE, Resnick G, et al. Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 1980; 56(2): 289-301.
25. Jones E, McGonagle D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford) 2008; 47(2): 126-31.
26. Schechner JS, Nath AK, Zheng L, et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 2000; 97(16): 9191-6.
27. Johnson PC, Mikos AG, Fisher JP, Jansen JA. Strategic directions in tissue engineering. Tissue Eng 2007; 13(12): 2827-37.
28. Tondreau T, Meuleman N, Delforge A, et al. Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 2005; 23(8): 1105-12.
29. Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 1999; 103(9): 1231-6.
30. Coleman BD, Khan KM, Maffulli N, Cook JL, Wark JD. Studies of surgical outcome after patellar tendinopathy: clinical significance of methodological deficiencies and guidelines for future studies. Victorian Institute of Sport Tendon Study Group. Scand J Med Sci Sports 2000; 10(1): 2-11.
31. Cohen J. A Coefficient of Agreement for Nominal Scales. Educational and Psychological Measurement 1960; 20(1): 37-46.
32. StataCorp. Stata Statistical Software. Release 11 ed. College Station, TX: StataCorp LP; 2009.
33. Papadimitropoulos A, Scherberich A, Guven S, et al. A 3D in vitro bone organ model using human progenitor cells. Eur Cell Mater 2011; 21: 445-58; discussion 58.
34. Scherberich A, Galli R, Jaquiery C, Farhadi J, Martin I. Threedimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 2007; 25(7): 1823-9.
35. Muller AM, Mehrkens A, Schafer DJ, et al. Towards an intraoperative engineering of osteogenic and vasculogenic grafts from the stromal vascular fraction of human adipose tissue. Eur Cell Mater 2010; 19: 127-35.
36. Usami K, Mizuno H, Okada K, et al. Composite implantation of mesenchymal stem cells with endothelial progenitor cells enhances tissue-engineered bone formation. J Biomed Mater Res A 2009; 90(3): 730-41.
37. Koob S, Torio-Padron N, Stark GB, Hannig C, Stankovic Z, Finkenzeller G. Bone formation and neovascularization mediated by mesenchymal stem cells and endothelial cells in critical-sized calvarial defects. Tissue Eng Part A 2011; 17(3-4): 311-21.
38. Kim JY, Jin GZ, Park IS, et al. Evaluation of solid free-form fabrication-based scaffolds seeded with osteoblasts and human umbilical vein endothelial cells for use in vivo osteogenesis. Tissue Eng Part A 2010; 16(7): 2229-36.
39. Geuze RE, Wegman F, Oner FC, Dhert WJ, Alblas J. Influence of endothelial progenitor cells and platelet gel on tissue-engineered bone ectopically in goats. Tissue Eng Part A 2009; 15(11): 3669-77.
40. Moioli EK, Clark PA, Chen M, et al. Synergistic actions of hematopoietic and mesenchymal stem/progenitor cells in vascularizing bioengineered tissues. PLoS One 2008; 3(12): e3922.
41. Yu H, Vandevord PJ, Gong W, et al. Promotion of osteogenesis in tissue-engineered bone by pre-seeding endothelial progenitor cellsderived endothelial cells. J Orthop Res 2008; 26(8): 1147-52.
42. Yu H, VandeVord PJ, Mao L, et al. Improved tissue-engineered bone regeneration by endothelial cell mediated vascularization. Biomaterials 2009; 30(4): 508-17.
43. Zhou J, Lin H, Fang T, et al. The repair of large segmental bone defects in the rabbit with vascularized tissue engineered bone. Biomaterials 2010; 31(6): 1171-9.
44. Kaigler D, Krebsbach PH, West ER, Horger K, Huang YC, Mooney DJ. Endothelial cell modulation of bone marrow stromal cell osteogenic potential. Faseb J 2005; 19(6): 665-7.
45. Sun H, Qu Z, Guo Y, Zang G, Yang B. In vitro and in vivo effects of rat kidney vascular endothelial cells on osteogenesis of rat bone marrow mesenchymal stem cells growing on polylactide-glycoli acid (PLGA) scaffolds. Biomed Eng Online 2007; 6: 41.
46. Fedorovich NE, Haverslag RT, Dhert WJ, Alblas J. The role of endothelial progenitor cells in prevascularized bone tissue engineering: development of heterogeneous constructs. Tissue Eng Part A 2010; 16(7): 2355-67.
47. Xing Z, Xue Y, Danmark S, et al. Effect of endothelial cells on bone regeneration using poly(L-lactide-co-1,5-dioxepan-2-one) scaffolds. J Biomed Mater Res A 2011; 96(2): 349-57.
48. Kim SS, Park MS, Cho SW, et al. Enhanced bone formation by marrow-derived endothelial and osteogenic cell transplantation. J Biomed Mater Res A 2010; 92(1): 246-53.
49. Seebach C, Henrich D, Kahling C, et al. Endothelial progenitor cells and mesenchymal stem cells seeded onto beta-TCP granules enhance early vascularization and bone healing in a critical-sized bone defect in rats. Tissue Eng Part A 2010; 16(6): 1961-70.
50. Nakagawa K, Abukawa H, Shin MY, Terai H, Troulis MJ, Vacanti JP. Osteoclastogenesis on tissue-engineered bone. Tissue Eng 2004; 10(1-2): 93-100.
51. Tortelli F, Pujic N, Liu Y, Laroche N, Vico L, Cancedda R. Osteoblast and osteoclast differentiation in an in vitro threedimensional model of bone. Tissue Eng Part A 2009; 15(9): 2373-83.
52. Bernhardt A, Thieme S, Domaschke H, Springer A, Rosen-Wolff A, Gelinsky M. Crosstalk of osteoblast and osteoclast precursors on mineralized collagen--towards an in vitro model for bone remodeling. J Biomed Mater Res A 2010; 95(3): 848-56.
53. Domaschke H, Gelinsky M, Burmeister B, et al. In vitro ossification and remodeling of mineralized collagen I scaffolds. Tissue Eng 2006; 12(4): 949-58.
54. Mbalaviele G, Jaiswal N, Meng A, Cheng L, Van Den Bos C, Thiede M. Human mesenchymal stem cells promote human osteoclast differentiation from CD34+ bone marrow hematopoietic progenitors. Endocrinology 1999; 140(8): 3736-43.
55. Matsumoto T, Kawamoto A, Kuroda R, et al. Therapeutic potential of vasculogenesis and osteogenesis promoted by peripheral blood CD34-positive cells for functional bone healing. Am J Pathol 2006; 169(4): 1440-57.
56. Rozen N, Bick T, Bajayo A, et al. Transplanted blood-derived endothelial progenitor cells (EPC) enhance bridging of sheep tibia critical size defects. Bone 2009; 45(5): 918-24.
57. Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 2004; 8(3): 301-16.
58. Yoder MC, Mead LE, Prater D, et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007; 109(5): 1801-9.
59. Rehman J, Li J, Orschell CM, March KL. Peripheral blood endothelial progenitor cells are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003; 107(8): 1164-9.
60. Rouwkema J, Westerweel PE, de Boer J, Verhaar MC, van Blitterswijk CA. The use of endothelial progenitor cells for prevascularized bone tissue engineering. Tissue Eng Part A 2009; 15(8): 2015-27.
61. Melero-Martin JM, De Obaldia ME, Kang SY, et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 2008; 103(2): 194-202.
62. Matsumoto T, Kuroda R, Mifune Y, et al. Circulating endothelial/skeletal progenitor cells for bone regeneration and healing. Bone 2008; 43(3): 434-9.
63. Khosla S, Eghbali-Fatourechi GZ. Circulating cells with osteogenic potential. Ann N Y Acad Sci 2006; 1068: 489-97.