Beneficial effect of autologous transplantation of endothelial progenitor cells on steroid-induced femoral head osteonecrosis in rabbits

Cell Transplantation

Volumn 20, Issue 2, 2011, Pages 233-243

  Sun, Yuan ^a   Feng, Yong ^a   Zhang, Changqing ^a   Cheng, Xiangguo ^a   Chen, Shengbao ^a   Ai, Zisheng ^a   Zeng, Bingfang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Bone regeneration; Endothelial progenitor cells (EPCs); Osteonecrosis; Steroid; Vascularization

Indexed keywords

METHYLPREDNISOLONE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOTRANSPLANTATION; BONE REGENERATION; COMPARATIVE STUDY; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; EXPERIMENTAL RABBIT; FEMUR HEAD NECROSIS; HISTOPATHOLOGY; MALE; MICROANGIOGRAPHY; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME; VASCULARIZATION;

ANGIOGRAPHY; ANIMALS; COLONY-FORMING UNITS ASSAY; ENDOTHELIAL CELLS; FEMUR; FEMUR HEAD NECROSIS; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; MALE; NECROSIS; NEOVASCULARIZATION, PATHOLOGIC; ORGAN SIZE; OSTEOGENESIS; RABBITS; STEM CELL TRANSPLANTATION; STEM CELLS; STEROIDS; TRANSPLANTATION, AUTOLOGOUS; X-RAY MICROTOMOGRAPHY;

ORYCTOLAGUS CUNICULUS;

EID: 79955371603     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X522234     Document Type: Article

References (54)

1. Aldridge, 3rd, J. M.; Urbaniak, J. R. Avascular necrosis of the femoral head: Role of vascularized bone grafts. Orthop. Clin. North Am. 38:13-22; 2007.
2. Asada, T.; Kushida, T.; Umeda, M.; Matsuya, H.; Wada, T.; Sasai, K.; Ikehara, S.; Iida, H. Prevention of corticoste-roid-induced osteonecrosis in rabbits by intra-bone marrow injection of autologous bone marrow cells. Rheumatology 47:591-596; 2008.
3. Assouline-Dayan, Y.; Chang, C.; Greenspan, A.; Shoen-feld, Y.; Gershwin, M. E. Pathogenesis and natural history of osteonecrosis. Semin. Arthritis Rheum. 32:94-124; 2002.
4. Barcelos, L. S.; Duplaa, C.; Kränkel, N.; Graiani, G.; Invernici, G.; Katare, R.; Siragusa, M. Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ. Res. 104:1095-1102; 2009.
5. Biswal, S.; Hazra, S.; Yun, H. H.; Hur, C. Y.; Shon, W. Y. Transtrochanteric rotational osteotomy for nontraumatic osteonecrosis of the femoral head in young adults. Clin. Orthop. Relat. Res. 467:1529-1537; 2009.
6. Bolland, B. J.; Kanczler, J. M.; Dunlop, D. G.; Oreffo, R. O. Development of in vivo muCT evaluation of neovascularisation in tissue engineered bone constructs. Bone 43:195-202; 2008.
7. Caplan, A. I.; Goldberg, V. M. Principles of tissue engineered regeneration of skeletal tissues. Clin. Orthop. Relat. Res. 367(Suppl.):S12-16; 1999.
8. Ding, D. C.; Shyu, W. C.; Lin, S. Z.; Li, H. The role of endothelial progenitor cells in ischemic cerebral and heart diseases. Cell Transplant. 16:273-284; 2007.
9. Fuchs, S.; Ghanaati, S.; Orth, C.; Barbeck, M. 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; 2009.
10. Gangji, V.; Hauzeur, J. P.; Matos, C.; De Maertelaer, V.; Toungouz, M.; Lambermont, M. Treatment of osteonecrosis of the femoral head with implantation of autologous bone-marrow cells. A pilot study. J. Bone Joint Surg. Am. 86:1153-1160; 2004.
11. Geiger, F.; Bertram, H.; Berger, I.; Lorenz, H.; Wall, O.; Eckhardt, C.; Simank, H. G.; Richter, W. Vascular endothelial growth factor gene-activated matrix (VEGF165-GAM) enhances osteogenesis and angiogenesis in large segmental bone defects. J. Bone Miner. Res. 20:2028-2035; 2005.
12. Griese, D. P.; Ehsan, A.; Melo, L. G.; Kong, D.; Zhang, L.; Mann, M. J.; Pratt, R. E. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: Implications for cell-based vascular therapy. Circulation 108:2710-2715; 2003.
13. Heinzer, S.; Krucker, T.; Stampanoni, M.; Abela, R.; Meyer, E. P.; Schneider, P. Hierarchical microimaging for multiscale analysis of large vascular networks. Neuroimage 32:626-636; 2006.
14. Helmlinger, G.; Endo, M.; Ferrara, N.; Hlatky, L.; Jain, R. K. Formation of endothelial cell networks. Nature 405: 139-141; 2000.
15. Hernigou, P.; Beaujean, F. Treatment of osteonecrosis with autologous bone marrow grafting. Clin. Orthop. Relat. Res. 405:14-23; 2002.
16. Huang, L.; Hou, D.; Thompson, M. A.; Baysden, S. E.; Shelley, W. C.; Ingram, D. A.; March, K. L.; Yoder, M. C. Acute myocardial infarction in swine rapidly and selectively releases highly proliferative endothelial colony forming cells (ECFCs) into circulation. Cell Transplant. 16:887-897; 2007.
17. Jones, K. B.; Seshadri, T.; Krantz, R.; Keating, A.; Ferguson, P. C. Cell-based therapies for osteonecrosis of the femoral head. Biol. Blood Marrow Transplant. 14:1081-1087; 2008.
18. Kabata, T.; Kubo, T.; Matsumoto, T.; Hirata, T.; Fujioka, M.; Takahashi, K. A. Onset of steroid-induced osteone-crosis in rabbits and its relationship to hyperlipaemia and increased free fatty acids. Rheumatology 44:1233-1237; 2005.
19. Kaigler, D.; Krebsbach, E. R.; West, K.; Horger, Y. C.; Huang, D. J. Endothelial cell modulation of bone marrow stromal cell osteogenic potential. FASEB J. 19:665-692; 2005.
20. Kalka, C.; Masuda, H.; Takahashi, T.; Kalka-Moll, W. M.; Silver, M.; Kearney, M.; Li, T.; Isner, J. M.; Asahara, T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA 97:3422-3427; 2000.
21. Kawamoto, A.; Asahara, T.; Losordo, D. W. Transplantation of endothelial progenitor cells for therapeutic neovascularization. Cardiovasc. Radiat. Med. 3:221-225; 2002.
22. Kawamoto, A.; Gwon, H. C.; Iwaguro, H.; Yamaguchi, J. I.; Uchida, S.; Masuda, H.; Silver, M. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103:634-637; 2001.
23. Kim, K. L.; Han, D. K.; Park, K. Enhanced dermal wound neovascularization by targeted delivery of endothelial progenitor cells using an RGD-g-PLLA scaffold. Biomaterials 30:3742-3748; 2009.
24. Kindlmann, G. L.; Weinstein, D. M.; Jones, G. M. Practical vessel imaging by computed tomography in live transgenic mouse models for human tumors. Mol. Imaging 4: 417-424; 2005.
25. Korompilias, A. V.; Lykissas, M. G.; Beris, A. E.; Urbaniak, J. R.; Soucacos, P. N. Vascularised fibular graft in the management of femoral head osteonecrosis: Twenty years later. J. Bone Joint Surg. Br. 91:287-293; 2009.
26. Lee, D. Y.; Cho, T. J.; Kim, J. A.; Lee, H. R.; Yoo, W. J.; Chung, C. Y. Mobilization of endothelial progenitor cells in fracture healing and distraction osteogenesis. Bone 42: 932-941; 2008.
27. Malyar, N. M.; Gossl, M.; Beighley, P. E.; Ritman, E. L. Relationship between arterial diameter and perfused tissue volume in myocardial microcirculation: A micro-CT based analysis. Am. J. Physiol. Heart Circ. Physiol. 286:H2386-2392; 2004.
28. Matsumoto, T.; Kuroda, R.; Mifune, Y.; Kawamoto, A.; Shoji, T.; Miwa, M.; Asahara, T.; Kurosaka, M. Circulating endothelial/skeletal progenitor cells for bone regeneration and healing. Bone 43:434-439; 2008.
29. Miyanishi, K.; Yamamoto, T.; Irisa, T.; Motomura, G.; Jingushi, S.; Sueishi, K.; Iwamoto, Y. Effects of different corticosteroids on the development of osteonecrosis in rabbits. Rheumatology 44:332-336; 2005.
30. Mont, M. A.; Jones, L. C.; Hungerford, D. S. Nontraumatic osteonecrosis of the femoral head: Ten years later. J. Bone Joint Surg. Am. 88:1117-1132; 2006.
31. Mont, M. A.; Marulanda, G. A.; Seyler, T. M.; Plate, J. F.; Delanois, R. E. Core decompression and nonvascularized bone grafting for the treatment of early stage osteonecrosis of the femoral head. Instr. Course Lect. 56:213-220; 2007.
32. Moore, D. C.; Leblanc, C. W.; Muller, R. Physiologic weight-bearing increases new vessel formation during distraction osteogenesis: A micro-tomographic imaging study. J. Orthop. Res. 21:489-496; 2003.
33. Murohara, T.; Ikeda, H.; Duan, J.; Shintani, S.; Sasaki, K.; Eguchi, H.; Onitsuka, I.; Matsui, K.; Imaizumi, T. Transplanted cord blood derived endothelial precursor cells augment postnatal neovascularization. J. Clin. Invest. 105: 1527-1536; 2000.
34. Neugebauer, V.; Han, J. S.; Adwanikar, H.; Fu, Y. Techniques for assessing knee joint pain in arthritis. Mol. Pain 5:3-8; 2007.
35. Nevskaya, T.; Ananieva, L.; Bykovskaia, S.; Eremin, I.; Karandashov, E. Autologous progenitor cell implantation as a novel therapeutic intervention for ischaemic digits in systemic sclerosis. Rheumatology 48:61-64; 2009.
36. Nevskaya, T.; Bykovskaia, S.; Lyssuk, E. Circulating endothelial progenitor cells in systemic sclerosis: Relation to impaired angiogenesis and cardiovascular manifestations. Clin. Exp. Rheumatol. 26:421-219; 2008.
37. Ochiai, N.; Ohtori, S.; Sasho, T.; Saisu, T. Extracorporeal shock wave therapy improves motor dysfunction and pain originating from knee osteoarthritis in rats. Osteoarthritis Cartilage 15:1093-1096; 2007.
38. Ohzono, K.; Takaoka, K.; Saito, S.; Saito, M.; Matsui, M.; Ono, K. Intraosseous arterial architecture in nontraumatic avascular necrosis of the femoral head. Microangiographic and histologic study. Clin. Orthop. 277:79-88; 1992.
39. Petrigliano, F. A.; Lieberman, J. R. Osteonecrosis of the hip. Clin. Orthop. Relat. Res. 465:53-62; 2007.
40. Qin, L.; Zhang, G.; Sheng, H.; Yeung, K.; Yeung, H.; Chan, C. Multiple imaging modalities in evaluation of experimental osteonecrosis induced by a combination of lippolysaccharide and methylprednisolone. Bone 39:863-871; 2006.
41. Santos, M. I.; Tuzlakoglu, K.; Fuchs, S.; Gomes, M. E.; Peters, K.; Unger, R. E. Endothelial cell colonization and angiogenic potential of combined nano-and micro-fibrous scaffolds for bone tissue engineering. Biomaterials 29: 4306-4313; 2008.
42. Scherberich, A.; Galli, R.; Jaquiery, C.; Farhadi, J.; Martin, I. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 25:1823-1829; 2007.
43. Seguin, C.; Kassis, J.; Busque, L.; Bestawros, A.; Theod-oropoulos, J.; Alonso, M. L.; Harvey, E. J. Non-traumatic necrosis of bone (osteonecrosis) is associated with endothelial cell activation but not thrombophilia. Rheumatology 47:1151-1155; 2008.
44. Street, J.; Bao, M.; deGuzman, L.; Bunting, S.; Ferrara, N. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc. Natl. Acad. Sci. USA 99:9656-9661; 2002.
45. Tammela, T.; Zarkada, G.; Wallgard, E.; Murtomäki, A.; Suchting, S. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454: 656-660; 2008.
46. Tan, H.; Yang, B.; Duan, X.; Wang, F.; Zhang, Y.; Jin, X.; Dai, G.; Yang, L. The promotion of the vascularization of decalcified bone matrix in vivo by rabbit bone marrow mononuclear cell-derived endothelial cells. Biomaterials 30:3560-3566; 2009.
47. Tang, T. T.; Lu, B.; Yue, B.; Xie, X. H.; Xie, Y. Z.; Dai, K. R. Treatment of osteonecrosis of the femoral head with hBMP-2-gene-modified tissue-engineered bone in goats. J. Bone Joint Surg. Br. 89:127-129; 2007.
48. Toyota, E.; Fujimoto, K.; Ogasawara, Y.; Kajita, T.; Shigeto, F.; Matsumoto, T.; Goto, M.; Kajiya, F. Dynamic changes in three-dimensional architecture and vascular volume of transmural coronary microvasculature between diastolicand systolic-arrested rat hearts. Circulation 105:621-626; 2002.
49. Wang, C. J.; Wang, F. S.; Ko, J. Y.; Huang, H. Y.; Chen, C. J.; Sun, Y. C.; Yang, Y. J. Extracorporeal shockwave therapy shows regeneration in hip necrosis. Rheumatology 47:542-546; 2008.
50. Wang, G. J.; Dughman, S. S.; Reger, S. I.; Stamp, W. G. The effect of core decompression on femoral head blood flow in steroid-induced avascular necrosis of the femoral head. J. Bone Joint Surg. Am. 67:121-124; 1985.
51. Yasunaga, Y.; Terayama, H.; Yamasaki, T.; Ishikawa, M.; Ochi, M. Treatment of osteonecrosis of the femoral head with implantation of autologous bone-marrow mononuclear cells. Clin. Calcium 17:910-915; 2007.
52. Yoo, M. C.; Kim, K. I.; Hahn, C. S.; Parvizi, J. Long-term followup of vascularized fibular grafting for femoral head necrosis. Clin. Orthop. Relat. Res. 466:1133-1140; 2008.
53. Yu, H.; VandeVord, P. J.; Mao, L.; Matthew, H. W.; Wooley, P. H.; Yang, S. Y. Improved tissue-engineered bone regeneration by endothelial cell mediated vascularization. Biomaterials 30:508-517; 2009.
54. Zhang, F.; Tang, Z.; Hou, X.; Lennartsson, J.; Li, Y.; Koch, A. W.; Scotney, P. VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc. Natl. Acad. Sci. USA 106:6152-6157; 2009.