Role of angiogenesis in bone repair

Archives of Biochemistry and Biophysics

Volumn 561, Issue , 2014, Pages 109-117

  Saran, Uttara ^a   Gemini Piperni, Sara ^c   Chatterjee, Suvro ^a,b  

^a ANNA UNIVERSITY   (India)

^b ANNA UNIVERSITY   (India)

^c UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Angiogenesis; Endothelial cells; Endothelial progenitor cells; Osteoblasts; Osteogenesis; VEGF

Indexed keywords

ANGIOGENIC FACTOR;

ANGIOGENESIS; ANGIOGENIC GENE THERAPY; ARTICLE; BONE BLOOD FLOW; BONE DEVELOPMENT; BONE INJURY; BONE REGENERATION; BONE REMODELING; BONE TISSUE; ENDOTHELIAL PROGENITOR CELL; FRACTURE HEALING; HUMAN; MATERIAL COATING; MICROENVIRONMENT; NONHUMAN; ORGAN CIRCULATION; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TISSUE SCAFFOLD; VASCULAR ENDOTHELIUM; WOUND; ANIMAL; CELL COMMUNICATION; CYTOLOGY; DEVICES; ENDOTHELIUM CELL; OSTEOBLAST; PHYSIOLOGY; PROCEDURES;

ANIMALS; BONE DEVELOPMENT; BONE REMODELING; CELL COMMUNICATION; ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOBLASTS; OSTEOGENESIS; TISSUE ENGINEERING;

EID: 84907943251     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2014.07.006     Document Type: Review

References (233)

1. N. Dirckx, M. Van Hul, and C. Maes Birth Defects Res C Embryo Today. 99 3 2013 Sep 170 191
2. X. He, R. Dziak, and X. Yuan PLoS ONE 8 4 2013 e60473 10.1371/journal.pone.0060473
3. M.L. Brandi, and P. Collin-Osdoby Journal of Bone and Mineral Research 21 2006 2
4. S.M. Chim, J. Tickner, and S.T. Chow Cytokine Growth Factor Rev. 24 3 2013 297 310
5. Kanczler JM and Oreffo R.O.C. Osteogenesis and angiogenesis: the potential for engineering bone. European cells and materials (2008), 15:100-114.
6. H.P. Gerber, and N. Ferrara Trends Cardiovasc. Med. 10 2000 223
7. Jian Zhou and Jian Dong. Vascularization in the Bone Repair, Osteogenesis, (2012) Prof. Yunfeng Lin (Ed.), ISBN: 978-953-51-0030-0, InTech, DOI: 10.5772/36325.
8. C. Maes Calcif. Tissue Int. 92 2013 307 323
9. A. Horner, N.J. Bishop, and S. Bord J. Anat. 194 4 1999 519 524
10. E. Schipani, C. Maes, G. Carmeliet, and G.L. Semenza J. Bone Miner Res. 24 2009 1347 1353
11. Clemens TL. Vasoactive Agents and Bone metabolism. In: Principles of Bone Biology. (1996) BilezekianJP, Raisz LG, Rodan GA (eds). Academic Press, San Diego. pp. 597-605.
12. J. Trueta. The role of the vessels in Osteogenesis. J Bone Joint Surg. - British Volume 1963, 45, 402.
13. Santos MI and Reis RL. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macro mol Biosci (2010), 11;10(1):12-27.
14. M. Laroche Joint Bone Spine 69 2002 262
15. A. Wilson Nat. Rev. Immunol. 6 2006 93
16. K. Hayashi Nippon Seikeigeka Gakkai Zasshi 66 1992 548 559
17. K. Imai, M. Kobayashi, and J. Wang Blood 93 1999 149 156
18. K. Imai, M. Kobayashi, and J. Wang Br. J. Haematol. 106 1999 905 911
19. A. Peled, O. Kollet, and T. Ponomaryov Blood 95 2000 3289 3296
20. G. Karsenty Nat. Med. 6 2000 970
21. O. Barou, S. Mekraldi, and L. Vico Bone 30 2002 604 612
22. E.M. Hauge, D. Qvesel, and E.F. Eriksen J. Bone Miner. Res. 16 2001 1575 1582
23. H. Yasuda, N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, E. Tsuda, T. Morinaga, K. Higashio, N. Udagawa, N. Takahashi, and T. Suda Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL Proc. Natl. Acad. Sci. USA 95 7 1998 3597 3602
24. T.J. Martin, and E. Seeman Best Pract. Res. Clin. Endocrinol. Metab. 22 5 2008 701 722 10.1016/j.beem.2008.07.006
25. N.A. Sims, and J.H. Gooi Semin. Cell. Dev. Biol. 19 2008 444 451
26. K. Henriksen, A.V. Neutzsky-Wulff, L.F. Bonewald, and M.A. Karsdal Bone 44 2009 1026 1033
27. L. Kindle, L. Rothe, and M. Kriss J. Bone Miner. Res. 21 2006 193 206
28. A. De Becker, P. Van Hummelen, and M. Bakkus Haematologica 92 2007 440 449
29. Eshkar-Oren I1, Viukov SV, Salameh S, Krief S, Oh CD, Akiyama H, Gerber HP, Ferrara N, Zelzer E. The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation of Vegf. Development. 2009 Apr; 136(8), pp. 1263-72, 2009 Mar 4, doi: 10.1242/dev.034199. Epub.
30. C. Maes, T. Kobayashi, and M.K. Selig Dev. Cell 19 2010 329 344
31. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature. 2014 Mar 20;507(7492), pp. 323-8, 2014 Mar 12, doi: 10.1038/nature13145. Epub.
32. Ramasamy SK, Kusumbe AP, Wang L, Adams RH. Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature. 2014 Mar 20;507(7492), pp. 376-80, 2014 Mar 12, doi: 10.1038/nature13146. Epub.
33. Qiang Zhao1, Xing Shen1, Wei Zhang et al. Mice with increased angiogenesis and osteogenesis due to conditional activation of HIF pathway in osteoblasts are protected from ovariectomy induced bone loss. Bone (2012), Volume 50, Issue 3, Pages 763-770.
34. M. Egermann, E. Schneider, C.H. Evans et al. The potential of gene therapy for fracture healing in osteoporosis, Osteoporos. Int. (Suppl. 2) (2005), S120-S128.
35. B. Burkhardt, G. Kettner, and W. Bohm Bone 8 1987 157 164
36. W.G. Ding, Z.X. Wei, and J.B. Liu Connect. Tissue Res. 52 2011 25 29
37. A.W.A. Baltzer, J.D. Whalen, P. Wooley, and C. Latterman Gene Ther. 8 2001 1770 1776
38. Frederic. Deschaseaux, and Luc Sensebeand Dominique. Heymann Trends Mol. Med. 15 9 2009 417 429
39. A. Schindeler, M.M. Mcdonald, P. Bokko, and D.G. Little Semin. Cell. Dev. Biol. 19 2008 459 466
40. B. Beamer, C. Hettrich, and J. Lane HSS J. 6 2010 85 94
41. K.D. Hankenson, M. Dishowitz, and C. Gray Injury 42 6 2011 556 561 10.1016/j.injury.2011.03.035
42. J. Malda, and T.J. Klein Tissue Eng. 13 2007 2153
43. Faller DV Endothelial cell responses to hypoxic stress. Clin. Exp. Pharmacol. Physiol. (1999), 26: 74.
44. C. Lu, R. Marcucio, and T. Miclau The Iowa Orthopaedic Journal 26 2006 17 26
45. Street J, Bao M, deGuzman L et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. PNAS. (2002), 99(15): 9656-9661.
46. Eckardt H, Ding M, Lind M, et al. Recombinant human vascular endothelial growth factor enhances bone healing in an experimental nonunion model. J Bone Joint Surg (2005), 87-B: 1434-8.
47. U. Mayr-Wohlfart, J. Waltenberger, and H. Hausser Bone 30 2002 472 477
48. J. Street, D. Winter, and J.H. Wang Clin. Orthop. 378 2000 224 237
49. Street, J.T. Wang JH, Wu QD et al. The angiogenic response to skeletal injury is preserved in the elderly. J. Orthop. Res. (2001), 19: 1057-1066.
50. O. Grundnes, and O. Reikeras Acta Orthop. Scand. 64 1993 340 342
51. Mizuno K, Mineo K, Tachibana T et al. The osteogenetic potential of fracture haematoma. Subperiosteal and intramuscular transplantation of the haematoma. J. Bone Joint Surg. Br. (1990), 72; 822-829.
52. Karin A. Hing. Bone repair in the twenty-first century: biology, chemistry or engineering? Phil. Trans. R. Soc. Lond. A (2004), 362.
53. M.R. Hausman, M.B. Schaffler, and R.J. Majeska Bone 29 2001 560 564
54. T.D. Fang, A. Salim, and W. Xia J.Bone Miner. Res. 20 2005 1114 1124
55. J.H. Holstein, M. Klein, and P. Garcia Brit. J. Pharmacol. 154 2008 1055 1062
56. C. Seebach, D. Henrich, and K. Wilhelm Cell. Transplant. 21 8 2012 1667 1677
57. R.S. Carvalho, T.A. Einhorn, and W. Lehmann Bone 34 2004 849 861
58. K. Sojo, Y. Sawaki, and H. Hattori J. Craniomaxillofac. Surg. 33 4 2005 238 245
59. G.Z. Eghbali-Fatourechi, J. Lamsam, and D. Fraser N. Engl. J. Med. 352 19 2005 1959 1966
60. G.A. Clines Curr. Opin. Organ. Transplant. 15 1 2010 73 78 10.1097/MOT.0b013e328333d52c
61. K. Usami, H. Mizuno, and K. Okada J. Biomed. Mater. Res. A 90 3 2009 730 741 10.1002/jbm.a.32142
62. G.D. Roodman Exp. Hematol. 27 8 1999 1229 1241
63. A.M. Parfitt Bone 26 4 2000 319 323
64. N.C. Rivron, J. Liu, and J. Rouwkema Eur. Cell.Mat. 15 2008 27 40
65. B. Guillotin, C. Bourget, and M. Remy-Zolgadri Cell. Physiol. Biochem. 14 4-6 2004 325 332
66. F. Villars, B. Guillotin, and T. Amédée Am. J. Physiol. Cell. Physiol. 282 4 2002 C775 C785
67. M.M. Deckers, R.L. van Bezooijen, and G. van der Horst Endocrinology 143 4 2002 1545 1553
68. L.C. Yeh, and J.C. Lee Mol. Cell. Endocrinol. 153 1-2 1999 113 124
69. D.L. Goad, J. Rubin, and H. Wang Endocrinology 137 6 1996 2262 2268
70. H. Peng, A. Usas, and A. Olshanski J. Bone Miner. Res. 20 11 2005 2017 2027
71. N. Ferrara, H.P. Gerber, and J. LeCouter Nat. Med. 9 6 2003 669 676
72. Street J, Power C, Wang JH et al. Multiple angiogenic cytokines protect against osteoblast apoptosis. J Am Coll Surg (2000), 191: S91-S92.
73. E. Zelzer, W. McLean, and Y.S. Ng Development 129 2002 1893 1904
74. M.M. Deckers, M. Karperien, and C. van der Bent Endocrinology 141 2000 1667 1674
75. M. Nakagawa, T. Kaneda, and T. Arakawa FEBS Lett 473 2000 161 164
76. K. Henriksen, M. Karsdal, and J.M. Delaisse J. Biol. Chem. 278 2003 48745 48753
77. J.C. Utting, A.M. Flanagan, and A. Brandao-Burch Cell. Biochem. Funct. 28 2010 374 380
78. D.P. Trebec-Reynolds, I. Voronov, and J.N. Heersche J. Cell. Biochem. 110 2010 343 351
79. Clarkin CE, Gerstenfeld LC.VEGF and bone cell signalling: an essential vessel for communication? Cell BiochemFunct. (2013), 31(1), pp. 1-11, doi: 10.1002/cbf.2911.
80. Y. Wang, C. Wan, and L. Deng J. Clin. Invest. 117 6 2007 1616 1626
81. D.E. Komatsu, M. Bosch-Marce, and G.L. Semenza J. Bone. Miner. Res. 22 3 2007 366 374
82. J. Min, Y. Kim, and E. Kim J. Biol. Chem. 278 2003 39548 39557
83. Kim HH, Shin HS, Kwak HJ et al. RANKL regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. FASEB Journal (2003), 17: 2163-5.
84. Y. Kim, Y. Kim, and Y. Lee J. Biol. Chem. 277 2002 6799 6805
85. J. Fiedler, F. Leucht, and J. Waltenberger Biochem. Biophys. Res. Commun. 334 2005 561 568
86. N.E. Hengartner, J. Fiedler, A. Ignatius, and R.E. Brenner Mol. Med. 19 2013 36 42
87. G. Li, Y. Cui, and L. Mcilmurray J. Orthop. Res. 23 2005 680 685
88. J. Harper, L.C. Gerstenfeld, and M. Klagsbrun J. Cell. Biochem. 81 2001 82 92
89. C. Colnot, Z. Thompson, and T. Miclau Development 130 2003 4123 4133
90. P. Carmeliet, V. Ferreira, and G. Breier Nature 380 1996 435 439
91. N. Ferrara, K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K.S. O'Shea, L. Powell-Braxton, K.J. Hillan, and M.W. Moore Nature 380 6573 1996 Apr 4 439 442
92. C. Maes, E. Araldi, and K. Haigh J. Bone Miner. Res. 27 2012 596 609
93. E. Zelzer, R. Mamluk, and N. Ferrara Development 131 2004 2161 2171
94. H.P. Gerber, T.H. Vu, and A.M. Ryan Nat. Med. 5 6 1999 623 628
95. J.J. Haigh, H.P. Gerber, and N. Ferrara Development 127 7 2000 1445 1453
96. C. Maes, P. Carmeliet, and K. Moermans Mech. Dev. 111 2002 61 73
97. C. Maes, I. Stockmans, and K. Moermans J. Clin. Invest. 113 2004 188 199
98. Y. Liu, A.D. Berendsen, and S. Jia J. Clin. Invest. 122 2012 3101 3113
99. T. Tarkka, A. Sipola, and T. Jamsa J. Gene Med. 5 2003 560 566
100. R. Li, D.J. Stewart, and H.P. von Schroeder J. Orthop. Res. 27 1 2009 8 14
101. K.A. Jacobsen, Z.S. Al Aql, and C. Wan J. Bone Miner. Res. 23 2008 596 609
102. N.C. Keramaris, G.M. Calori, and V.S. Nikolaou Injury 39 Suppl 2 2008 S45 S57
103. P. Collin-Osdoby, L. Rothe, and S. Bekker J. Bone Miner. Res. 17 2002 1859 1871
104. M. Goldfarb Cytokine and Growth Factor Reviews 7 1996 311 325
105. E. Arman, R. Haffner-Krausz, and M. Gorivodsky Proceedings of the National Academy of Sciences of the United States of America 96 1999 11895 11899
106. G. Seghezzi, S. Patel, and C.J. Ren J. Cell Biol. 141 1998 1659 1673
107. S. Klein, F.G. Giancotti, and M. Presta Mol. Biol. Cell 4 1993 973 982
108. S. Klein, A. Bikfalvi, and T.M. Birkenmeier J.Biol. Chem. 271 1996 22583 22590
109. M.G. Sabbieti, L. Marchetti, and M.G. Gabrielli Cell Tissue Res. 319 2005 267 278
110. T. Sobue, T. Gravely, and A. Hand J. Bone Miner. Res. 17 2002 502 512
111. N. Nakagawa, H. Yasuda, and K. Yano Biochem. Biophys. Res. Commun. 265 1999 158 163
112. H. Kawaguchi, D. Chikazu, and K. Nakamura J. Bone Miner. Res. 15 2000 466 473
113. M.M. Hurley, S.K. Lee, and L.G. Raisz Bone 22 1998 309 316
114. J.O. Hollinger, C.E. Hart, and S.N. Hirsch J. Bone Joint Surg. Am 90 1 2008 48 54
115. A. Colciago, F. Celotti, and L. Casati Int. J. Biomed. Sci. 5 2009 380 389
116. J. Fiedler, N. Etzel, and R.E. Brenner J. Cell Biochem 93 2004 990 998
117. J. Fiedler, G. Roderer, K.P. Gunther, and R.E. Brenner J Cell Biochem 87 2002 305 312
118. M.A. Sanchez-Fernandez, A. Gallois, and T. Riedl PLoS One 3 2008 e3537
119. M. Mehrotra, S.M. Krane, K. Walters, and C. Pilbeam J. Cell Biochem. 93 2004 741 752
120. Y. Tang, X. Wu, and W. Lei Nat. Med. 15 2009 757 765
121. A. Erlebacher Mol. Biol. Cell 9 1998 1903 1918
122. E.S. Shao, L. Lin, and Y.C. Yao Blood 114 2009 2197 2206
123. C. He, and X. Chen Biochem. Biophys. Res. Commun. 329 2005 324 330
124. C. Gamell, N. Osses, and R. Bartrons J. Cell Sci. 121 2008 3960 3970
125. D.H. Lee, B.J. Park, and M.S. Lee Tissue Eng. 12 2006 1577 1586
126. B.E. Bax, J.M. Wozney, and D.E. Ashhurst Calcif. Tissue Int. 65 1999 83 89
127. S.D. Cook, G.C. Baffes, and M.W. Wolfe Clin. Orthop. 301 1994 302 312
128. M. Raida, A.C. Heymann, and C. Gunther Int. J. Mol. Med. 18 2006 735 739
129. H. Peng, V. Wright, and A. Usas J Clin Invest 110 2002 751 759
130. S. Kumar, C. Wan, and G. Ramaswamy Mol Ther 18 2010 1026 1034
131. G. Valdimarsdottir, M.J. Goumans, and A. Rosendahl Circulation 106 2002 2263 2270
132. A. Luttun, G. Carmeliet, and P. Carmeliet Trends Cardiovasc Med. 12 2 2002 88 96
133. M. Hristov, W. Erl, and P.C. Weber Trends Cardiovasc Med. 13 5 2003 201 206
134. S. Yazar, C.H. Lin, and Y.T. Lin Plast Reconstr Surg 117 7 2006 2468 2475
135. N. Rozen, T. Bick, A. Bajayo, B. Shamian, M. Schrift-Tzadok, Y. Gabet, A. Yayon, I. Bab, M. Soudry, and D. Lewinson Bone. 45 5 2009 Nov 918 924
136. O.M. Tepper, J.M. Capla, and R.D. Galiano Blood 105 3 2005 1068 1077
137. A.N. Veleva, D.E. Heath, and S.L. Cooper Biomaterials 29 2008 3656
138. Chang.-Hwan. Yoon, Jin. Hur, and Kyung.-Woo. Park Circulation 112 2005 1618 1627
139. Lin, Y. Weisdorf, D.J.;Solovey, A et al. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest (2000), 105 (1): 71-77.
140. S. Rafii, and D. Lyden Nat Med 9 6 2003 702 712
141. D.Y. Lee, T.-J. Cho, and J.A. Kim Bone 42 5 2008 932 941
142. C.L. Cetrulo Jr., K.R. Knox, D.J. Brown, R.L. Ashinoff, M. Dobryansky, D.J. Ceradini et al. Stem cells and distraction osteogenesis: endothelial progenitor cells home to the ischaemic generate in activation and consolidation Plast. Reconstr. Surg., 116 (2005), pp. 1053-1064 discussion 1065-7.
143. D.M. Smadja, I. Bièche, J.S. Silvestre, S. Germain, A. Cornet, and I. Laurendeau Arterioscler. Thromb. Vasc. Biol. 28 12 2008 2137 2143
144. K. Atesok, R. Li, and D.J. Stewart J Orthop Res 28 2010 1007 1014
145. T. Matsumoto, A. Kawamoto, and R. Kuroda Am J Pathol 169 2006 1440 1457
146. M. Kado, J.K. Lee, K. Hidaka, K. Miwa, T. Murohara, and K. Kasai Biochem. Biophys. Res. Commun. 377 2 2008 413 418
147. C. Mathieu, K. Sii-Felice, P. Fouchet, O. Etienne, C. Haton, and A. Mabondzo Cell. Neurosci. 38 2008 569 577
148. T. Imura, K. Tane, N. Toyoda, and S. Fushiki Eur. J. Neurosci. 27 2008 1596 1606
149. T. Bick, N. Rozen, E. Dreyfuss, M. Soudry, and D. Lewinson J. Bone Miner. Res. 22 2007 S143
150. V.K. Popov, A.V. Evseev, and A.L. Ivanov J Mater Sci-Mater Med 15 2004 123 128
151. E.N. Antonov, V.N. Bagratashvili, and M.J. Whitaker Advanced Materials 17 2005 327 330
152. Oreffo RO, Triffitt JT Future potentials for using osteogenic stem cells and biomaterials in orthopedics. Bone (1999), 25(2suppl): 5S-9S.
153. T.W. Bauer, and G.F. Muschler Clin Orthop Relat Res 371 2000 10 27
154. B.F. Aurori, R.J. Weierman, and H.A. Lowell Clin Orthop 199 1985 153 158
155. Q. Lu, K. Ganesan, and D.T. Simionescu Biomaterials 25 2004 5227 5237
156. P. Lubiatowski, J. Kruczynski, and A. Gradys Transplant Proc 38 2006 320 322
157. H. Domaschke, M. Gelinsky, and B. Burmeister Tissue Eng 12 2006 949 958
158. T. Nakasa, O. Ishida, and T. Sunagawa Journal of Biomedical Materials Research Part A 75A 2 2005 350 355
159. K. Kawamura, H. Yajima, and H. Ohgushi Plastic and Reconstructive Surgery 117 5 2006 1471 1479
160. Formiga, F.R., Pelacho, B., Garbayo, E et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia-reperfusion model. J Control Release (2010) 147, 30.
161. Vogelin E, Jones NF, Huang JI et al. Healing of a critical-sized defect in the rat femur with use of a vascularized periosteal flap, a biodegradable matrix, and bone morphogenetic protein. J Bone Joint Surg Am(2005), 87: 1323-1331.
162. D. Logeart-Avramoglou, F. Anagnostou, and R. Bizios J Cell Mol Med 9 2005 72 84
163. W.J. Chen, S. Jingushi, and I. Aoyama J Bone Miner Metab 22 2004 303 309
164. J.L. Andreshak Anat. Rec 248 1997 198 204
165. M.L. Radomsky J. Orthop. Res. 17 1999 607 614
166. F. Nakajima J. Orthop. Res 19 2001 935 944
167. F.R. Rose, Q. Hou, and R.O. Oreffo J Pharm Pharmacol 56 2004 415 427
168. Tomanek, R.J., Lotun, K., Clark, E.B et al. VEGF and bFGF stimulate myocardial vascularization in embryonic chick. Am J Physiol (1998), 274, H1620.
169. Darnell. Kaigler, Zhuo. Wang, and Kim. Horger Journal of Bone and Mineral Research 21 2006 5
170. J.K. Leach, D. Kaigler, and Z. Wang Biomaterials 27 2006 3249 3255
171. A. Leu, S.M. Stieger, and P. Dayton Tissue Eng Part A. 15 2008 877 885
172. A. Leu, and J.K. Leach Pharmaceut Res 25 2008 1122 1129
173. E. Jabbarzadeh, M. Deng, and Q. Lv J Biomed Mater Res B Appl Biomater 100 8 2012 2187 2196
174. T.M. Chu, S.J. Warden, and C.H. Turner Biomaterials 28 2007 459 467
175. Solorio, L., Zwolinski, C., Lund, A.W et al. Gelatin microspheres crosslinked with genipin for local delivery of growth factors. J Tissue Eng Regen Med (2010), 4, 514.
176. Moya, M.L., Garfinkel, M.R., Liu, X et al. Fibroblast growth factor-1 (FGF-1) loaded microbeads enhance local capillary neovascularization. J Surg Res (2010), 160(2): 208-212.
177. S. Uriel Am J Surg 192 5 2006 604 609
178. T.J. Nash, C.R. Howlett, and C. Martin Bone 15 2 1994 203 208
179. Kempen, D.H., Creemers, L.B., Alblas, J et al. Growth factor interactions in bone regeneration. Tissue Eng Part B Rev (2010), 16, 551.
180. J.A. Jansen, J.W. Vehof, and P.Q. Ruhe J Control Release 101 2005 127 136
181. M.E. Oest, K.M. Dupont, and H.J. Kong J Orthop Res 25 2007 941 950
182. N. Duneas, J. Crooks, and U. Ripamonti Growth Factors 15 1998 259
183. Simmons, C.A., Alsberg, E., Hsiong, S et al. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone (2004), 35, 562.
184. T.P. Richardson, M.C. Peters, A.B. Ennett, and D.J. Mooney Nat Biotech 19 2001 1029
185. Patel, Z.S., Young, S., Tabata, Y et al. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone (2008), 43, 931.
186. N.J. Shah, M.L. Macdonald, and Y.M. Beben Biomaterials 32 2011 6183
187. Young, S., Patel Zarana, S., Kretlow James, D et al. Dose effect of dual delivery of vascular endothelial growth factor and bone morphogenetic protein-2 on bone regeneration in a rat critical-size defect model. Tissue Eng Part A (2009), 15, 2347.
188. F.B. Basmanav, G.T. Kose, and V. Hasirci Biomaterials 29 31 2008 4195 4204 10.1016/j.biomaterials.2008.07.017
189. P. Yilgor, N. Hasirci, and V. Hasirci J Biomed Mater Res A. 93 2 2010 528 536 10.1002/jbm.a.32520
190. A.H. Zisch, M.P. Lutolf, and J.A. Hubbell Cardiovasc Pathol 12 6 2003 295 310
191. N. Davies, S. Dobner, and D. Bezuidenhout Biomaterials 29 26 2008 3531 3538 10.1016/j.biomaterials.2008.05.007
192. Clare R. Ozawa, Andrea. Banfi, and Nicole L. Glazer J Clin Invest. 113 4 2004 516 527
193. L. Moldovan, and N.I. Moldovan Arch Pathol Lab Med 126 3 2002 310 316
194. R.E. Unger, A. Sartoris, and K. Peters Biomaterials 28 27 2007 3965 3976 Epub 2007 Jun 19
195. J. Rouwkema, J. de Boer, and C.A. Van Blitterswijk Tissue Eng. 12 9 2006 2685 2693
196. L.H. Nguyen, N. Annabi, and M. Nikkhah Tissue Eng Part B Rev 18 5 2012 363 382
197. Jeffrey S. Schechner, Anjali K. Nath, and Lian. Zheng PNAS 97 16 2000 9191 9196
198. Naoto. Koike, Dai. Fukumura, and Oliver. Gralla Nature 428 2004 138 139 10.1038/428138a
199. Shulamit. Levenberg, Jeroen. Rouwkema, and Mara. Macdonald Nature Biotechnology 23 2005 879 884 10.1038/nbt1109
200. Walter D.Holder, Helen E. Gruber, Wendy D. Roland et al. Increased Vascularization and Heterogeneity of Vascular Structures Occurring in Polyglycolide Matrices Containing Aortic Endothelial Cells Implanted in the Rat. Tissue Engineering (1997) Volume 3, Number 2, 1997 Mary Ann Liebert Inc.
201. D. Kaigler, P.H. Krebsbach, and Z. Wang J Dent Res. 85 7 2006 633 637
202. H. Matsubara, D.E. Hogan, and E.F. Morgan Bone. 51 1 2012 168 180 10.1016/j.bone.2012.02.017
203. D.S. Wang, M. Miura, and H. Demura Endocrinology 138 7 1997 2953 2962
204. H. Yu, P.J. VandeVord, and L. Mao Biomaterials 30 4 2009 508 517 10.1016/j.biomaterials.2008.09.047
205. J. Zhou, H. Lin, and T. Fang Biomaterials 31 6 2010 1171 1179 10.1016/j.biomaterials.2009.10.043
206. C. Seebach, D. Henrich, and C. Kähling Tissue Eng Part A 16 6 2010 1961 1970 10.1089/ten.TEA.2009.0715.N
207. D. Henrich, C. Seebach, and C. Kaehling Tissue Eng Part C Methods 15 4 2009 551 560 10.1089/ten.TEC.2008.0385
208. S. Murasawa, and T. Asahara Curr Gene Ther 7 1 2007 1 6
209. Anna Zampetaki, John Paul Kirton, Qingbo Xu. Vascular repair by endothelial progenitor cells. Cardiovas Res (2008) 78, 413-421.
210. T. Asahara, T. Murohara, and A. Sullivan Sci 275 1997 964 967
211. W.J. Li, R. Tuli, X. Huang, P. Laquerriere, and R.S. Tuan Biomaterials 26 2005 5158 5166
212. R.E. Geuze, F. Wegman, and F.C. Oner Tissue Eng Part A 15 11 2009 3669 3677 10.1089/ten.TEA.2009.0289
213. N.E. Fedorovich, R.T. Haverslag, and W.J. Dhert Tissue Eng Part A 16 7 2010 2355 2367 10.1089/ten.TEA.2009.0603
214. 1, Bick T, Morgan EF, Lewinson D, Machtei EE. Peripheral Blood-Derived Endothelial Progenitor Cells Enhance VerticalBone Formation. Clin Implant Dent Relat Res. 2013 Apr 30. doi: 10.1111/cid.12078. [Epub ahead of print].
215. 1, Bick T, Lewinson D, Machtei EE.Mesenchymal Stem Cells and Endothelial Progenitor Cells Stimulate BoneRegeneration and Mineral Density. J Periodontol. 2013 Oct 23. [Epub ahead of print].
216. 1, Bick T, Lewinson D, Machtei EE. Co-Transplantation of Endothelial Progenitor Cells and Mesenchymal StemCells Promote Neovascularization and Bone Regeneration. Clin Implant Dent Relat Res. 2013 Jul 12. doi: 10.1111/cid.12104. [Epub ahead of print].
217. X. He, R. Dziak, and K. Mao Tissue Eng Part A 19 3-4 2013 508 518 10.1089/ten.TEA.2012.0244
218. J. Kim, I.S. Kim, and T.H. Cho Biomaterials 28 2007 1830 1837
219. X.B. Yang, M.J. Whitaker, and W. Sebald Tissue Eng 10 2004 1037 1045
220. B. Peterson, J. Zhang, and R. Iglesias Tissue Eng 11 2005 120 129
221. M. Nomi, A. Atala, and P.D. Coppi Mol Aspects Med 23 2002 463 483
222. P.P. Young, A.A. Hofling, and M.S. Sands Proc Natl Acad Sci 99 2002 11951 11956
223. Xiaobin. Song, Shaohua. Liu, and Qu. Xun Acta Biochim Biophys Sin 43 2011 796 804
224. H. Wang, Y. Yu, and R.W. Guo Mol Cell Biochem 335 2010 19 27
225. A. Ciarrocchi, V. Jankovic, and Y. Shaked PLoS One 2 2007 e1338
226. Y. Chen J Orthop Sci 6 2001 199 207
227. Groppe J, Greenwald J, Wiater E, et al. Structural basis of BMP signalling inhibition by Noggin, a novel twelve-membered cystine knot protein. J Bone Joint Surg [Am] (2003), 85- A(Suppl. 3):52-8.
228. J. Yang, U. Nagavarapu, and K. Relloma Nat Biotechnol 19 2001 219 224
229. H. Ito, M. Koefoed, and P. Tiyapatanaputi Nat. Med. 11 2005 291 297
230. A.W. Baltzer, C. Lattermann, and J.D. Whalen Gene Ther 7 2000 734 739
231. J.R. Lieberman, A. Daluiski, and S. Stevenson J Bone Joint Surg [Am] 81 1999 905 917
232. H.C. Shen, H. Peng, and A. Usas J Gene Med 6 2004 984 991
233. J.R. Lieberman, L.Q. Le, and L. Wu J. Orthop. Res 16 1998 330 339