Short-time survival and engraftment of bone marrow stromal cells in an ectopic model of bone regeneration

Tissue Engineering - Part A

Volumn 16, Issue 2, 2010, Pages 489-499

  Giannoni, Paolo ^a   Scaglione, Silvia ^a,b   Daga, Antonio ^c   Ilengo, Cristina ^a   Cilli, Michele ^c   Quarto, Rodolfo ^a,b  

^a ADVANCED BIOTECHNOLOGY CENTER   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; SCAFFOLDS;

ANIMAL MODEL; APOPTOTIC; BIOLUMINESCENCE IMAGING; BONE MARROW STROMAL CELLS; BONE REGENERATION; CELL NUMBER; CYTOKINES; DIFFERENTIATION PROCESS; ENGRAFTMENT; IN-VIVO; INITIAL FREQUENCY; LIGHT PRODUCTION; LUCIFERASE GENES; NUDE MICE; OSTEOGENIC POTENTIAL; OSTEOPROGENITORS; TUMOR NECROSIS FACTOR ALPHA;

CELLS;

ANIMALIA; MUS MUSCULUS;

BIOMATERIAL; COLLAGEN; HYDROXYAPATITE; TISSUE SCAFFOLD; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; APOPTOSIS; ARTICLE; BIOLOGICAL MODEL; BONE MARROW CELL; BONE REGENERATION; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; IMPLANT; LIGHT; LUMINESCENCE; MESENCHYMAL STEM CELL; MOUSE; NUDE MOUSE; PHYSIOLOGY; SHEEP; STROMA CELL; THREE DIMENSIONAL IMAGING; TIME;

ANIMALS; APOPTOSIS; BIOCOMPATIBLE MATERIALS; BONE MARROW CELLS; BONE REGENERATION; CELL SURVIVAL; CELLS, CULTURED; COLLAGEN; DURAPATITE; IMAGING, THREE-DIMENSIONAL; IMPLANTS, EXPERIMENTAL; LIGHT; LUMINESCENT MEASUREMENTS; MESENCHYMAL STEM CELLS; MICE; MICE, NUDE; MODELS, BIOLOGICAL; SHEEP; STROMAL CELLS; TIME FACTORS; TISSUE SCAFFOLDS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77049097708     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0041     Document Type: Conference Paper

References (58)

1. Sacchetti, B., Funari, A., Michienzi, S., Di Cesare, S., Pier-santi, S., Saggio, I., Tagliafico, E., Ferrari, S., Robey, P.G., Riminucci, M., and Bianco, P. Self-renewing osteoprogeni-tors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131, 324, 2007.
2. Tampieri, A., Sandri, M., Landi, E., Pressato, D., Francioli, S., Quarto, R., and Martin, I. Design of graded biomimetic os-teochondral composite scaffolds. Biomaterials 29, 3539, 2008.
3. Haynesworth, S.E., Goshima, J., Goldberg, V.M., and Ca-plan, A.I. Characterization of cells with osteogenic potential from human marrow. Bone 13, 81, 1992.
4. Bruder, S.P., Kraus, K.H., Goldberg, V.M., and Kadiyala, S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 80, 985, 1998.
5. Giannoni, P., Mastrogiacomo, M., Alini, M., Pearce, S.G., Corsi, A., Santolini, F., Muraglia, A., Bianco, P., and Cancedda, R. Regeneration of large bone defects in sheep using bone marrow stromal cells. J Tissue Eng Regen Med 2, 253, 2008.
6. Goshima, J., Goldberg, V.M., and Caplan, A.I. Osteogenic potential of culture-expanded rat marrow cells as assayed in vivo with porous calcium phosphate ceramic. Biomaterials 12, 253, 1991.
7. Goshima, J., Goldberg, V.M., and Caplan, A.I. The osteo-genic potential of culture-expanded rat marrow mesenchy-mal cells assayed in vivo in calcium phosphate ceramic blocks. Clin Orthop Relat Res 262, 298, 1991.
8. Ito, K., Yamada, Y., Naiki, T., and Ueda, M. Simultaneous implant placement and bone regeneration around dental implants using tissue-engineered bone with fibrin glue, mesenchymal stem cells and platelet-rich plasma. Clin Oral Implants Res 17, 579, 2006.
9. Kon, E., Muraglia, A., Corsi, A., Bianco, P., Marcacci, M., Martin, I., Boyde, A., Ruspantini, I., Chistolini, P., Rocca, M., Giardino, R., Cancedda, R., and Quarto, R. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res 49, 328, 2000.
10. Krebsbach, P.H., Kuznetsov, S.A., Satomura, K., Emmons, R.V., Rowe, D.W., and Robey, P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63, 1059, 1997.
11. Krebsbach, P.H., Mankani, M.H., Satomura, K., Kuznetsov, S.A., and Robey, P.G. Repair of craniotomy defects using bone marrow stromal cells. Transplantation 66, 1272, 1998.
12. Ohgushi, H., Goldberg, V.M., and Caplan, A.I. Repair of bone defects with marrow cells and porous ceramic: experiments in rats. Acta Orthop Scand 60, 334, 1989.
13. Yamada, Y., Boo, J.S., Ozawa, R., Nagasaka, T., Okazaki, Y., Hata, K., and Ueda, M. Bone regeneration following injection of mesenchymal stem cells and fibrin glue with a biodegradable scaffold. J Craniomaxillofac Surg 31, 27, 2003.
14. Horwitz, E.M., Prockop, D.J., Fitzpatrick, L.A., Koo, W.W., Gordon, P.L., Neel, M., Sussman, M., Orchard, P., Marx, J.C., Pyeritz, R.E., and Brenner, M.K. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5, 309, 1999.
15. Marcacci, M., Kon, E., Moukhachev, V., Lavroukov, A., Kutepov, S., Quarto, R., Mastrogiacomo, M., and Cancedda, R. Stem cells associated with macroporous bioceramics for long bone repair: 6-to 7-year outcome of a pilot clinical study. Tissue Eng 13, 947, 2007.
16. Quarto, R., Mastrogiacomo, M., Cancedda, R., Kutepov, S.M., Mukhachev, V., Lavroukov, A., Kon, E., and Marcacci, M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344, 385, 2001.
17. Choong, P.F. The molecular basis of skeletal metastases. Clin Orthop Relat Res 415 Suppl., S19, 2003.
18. Lee, S.Y., Miwa, M., Sakai, Y., Kuroda, R., Matsumoto, T., Iwakura, T., Fujioka, H., Doita, M., and Kurosaka, M. In vitro multipotentiality and characterization of human unfractured traumatic hemarthrosis-derived progenitor cells: a potential cell source for tissue repair. J Cell Physiol 210, 561, 2007.
19. Potier, E., Ferreira, E., Meunier, A., Sedel, L., Logeart-Avramoglou, D., and Petite, H. Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death. Tissue Eng 13, 1325, 2007.
20. Martensson, K., Chrysis, D., and Savendahl, L. Interleukin-1beta and TNF-alpha act in synergy to inhibit longitudinal growth in fetal rat metatarsal bones. J Bone Miner Res 19, 1805, 2004.
21. Yang, J., Shah, R., Robling, A.G., Templeton, E., Yang, H., Tracey, K.J., and Bidwell, J.P. HMGB1 is a bone-active cy-tokine. J Cell Physiol 214, 730, 2008.
22. Gupta, S. A decision between life and death during TNF-alpha-induced signaling. J Clin Immunol 22, 185, 2002.
23. Daga, A., Muraglia, A., Quarto, R., Cancedda, R., and Corte, G. Enhanced engraftment of EPO-transduced human bone marrow stromal cells transplanted in a 3D matrix in non-conditioned NOD=SCID mice. Gene Ther 9, 915, 2002.
24. Mastrogiacomo, M., Scaglione, S., Martinetti, R., Dolcini, L., Beltrame, F., Cancedda, R., and Quarto, R. Role of scaffold internal structure on in vivo bone formation in macroporous calcium phosphate bioceramics. Biomaterials 27, 3230, 2006.
25. Franz-Odendaal, T.A., Hall, B.K., and Witten, P.E. Buried alive: how osteoblasts become osteocytes. Dev Dyn 235, 176, 2006.
26. Kiel, M.J., and Morrison, S.J. Maintaining hematopoietic stem cells in the vascular niche. Immunity 25, 862, 2006.
27. Palumbo, C., Palazzini, S., Zaffe, D., and Marotti, G. Os-teocyte differentiation in the tibia of newborn rabbit: an ul-trastructural study of the formation of cytoplasmic processes. Acta Anat (Basel) 137, 350, 1990.
28. Braccini, A., Wendt, D., Farhadi, J., Schaeren, S., Heberer, M., and Martin, I. The osteogenicity of implanted engineered bone constructs is related to the density of clonogenic bone marrow stromal cells. J Tissue Eng Regen Med 1, 60, 2007.
29. Cancedda, R., Giannoni, P., and Mastrogiacomo, M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials 28, 4240, 2007.
30. Muraglia, A., Corsi, A., Riminucci, M., Mastrogiacomo, M., Cancedda, R., Bianco, P., and Quarto, R. Formation of a chondro-osseous rudiment in micromass cultures of human bone-marrow stromal cells. J Cell Sci 116, 2949, 2003.
31. Ignowski, J.M., and Schaffer, D.V. Kinetic analysis and modeling of firefly luciferase as a quantitative reporter gene in live mammalian cells. Biotechnol Bioeng 86, 827, 2004.
32. Muraglia, A., Martin, I., Cancedda, R., and Quarto, R. A nude mouse model for human bone formation in unloaded conditions. Bone 22, 131S, 1998.
33. Ryan, P.L., Youngblood, R.C., Harvill, J., and Willard, S.T. Photonic monitoring in real time of vascular endothelial growth factor receptor 2 gene expression under relaxin-induced conditions in a novel murine wound model. Ann NY Acad Sci 1041, 398, 2005.
34. Zhang, W., Purchio, A.F., Chen, K., Wu, J., Lu, L., Coffee, R., Contag, P.R., and West, D.B. A transgenic mouse model with a luciferase reporter for studying in vivo transcriptional regulation of the human CYP3A4 gene. Drug Metab Dispos 31, 1054, 2003.
35. Hwang, D.W., Jang, S.J., Kim, Y.H., Kim, H.J., Shim, I.K., Jeong, J.M., Chung, J.K., Lee, M.C., Lee, S.J., Kim, S.U., Kim, S., and Lee, D.S. Real-time in vivo monitoring of viable stem cells implanted on biocompatible scaffolds. Eur J Nucl Med Mol Imaging 35, 1887, 2008.
36. Kruyt, M.C., Stijns, M.M., Fedorovich, N.E., de Bruijn, J.D., van Blitterswijk, C.A., Verbout, A.J., Rozemuller, H., Hagenbeek, A., Dhert, W.J., and Martens, A.C. Genetic marking with the DeltaLNGFR-gene for tracing goat cells in bone tissue engineering. J Orthop Res 22, 697, 2004.
37. Li, F., Wang, X., and Niyibizi, C. Distribution of single-cell expanded marrow derived progenitors in a developing mouse model of osteogenesis imperfecta following systemic transplantation. Stem Cells 25, 3183, 2007.
38. Ouyang, H.W., Goh, J.C., and Lee, E.H. Viability of alloge-neic bone marrow stromal cells following local delivery into patella tendon in rabbit model. Cell Transplant 13, 649, 2004.
39. Ronsyn, M.W., Daans, J., Spaepen, G., Chatterjee, S., Ver-meulen, K., D'Haese, P., van Tendeloo, V.F., van Marck, E., Ysebaert, D., Berneman, Z.N., Jorens, P.G., and Ponsaerts, P. Plasmid-based genetic modification of human bone marrow-derived stromal cells: analysis of cell survival and transgene expression after transplantation in rat spinal cord. BMC Biotechnol 7, 90, 2007.
40. Shichinohe, H., Kuroda, S., Lee, J.B., Nishimura, G., Yano, S., Seki, T., Ikeda, J., Tamura, M., and Iwasaki, Y. In vivo tracking of bone marrow stromal cells transplanted into mice cerebral infarct by fluorescence optical imaging. Brain Res Brain Res Protoc 13, 166, 2004.
41. Yano, S., Kuroda, S., Lee, J.B., Shichinohe, H., Seki, T., Ikeda, J., Nishimura, G., Hida, K., Tamura, M., and Iwasaki, Y. In vivo fluorescence tracking of bone marrow stromal cells transplanted into a pneumatic injury model of rat spinal cord. J Neurotrauma 22, 907, 2005.
42. Liechty, K.W., MacKenzie, T.C., Shaaban, A.F., Radu, A., Moseley, A.M., Deans, R., Marshak, D.R., and Flake, A.W. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6, 1282, 2000.
43. Boyde, A., Corsi, A., Quarto, R., Cancedda, R., and Bianco, P. Osteoconduction in large macroporous hydroxyapatite ceramic implants: evidence for a complementary integration and disintegration mechanism. Bone 24, 579, 1999.
44. Martin, I., Miot, S., Barbero, A., Jakob, M., and Wendt, D. Osteochondral tissue engineering. J Biomech 40, 750, 2007.
45. Irons, H., Lind, J.G., Wakade, C.G., Yu, G., Hadman, M., Carroll, J., Hess, D.C., and Borlongan, C.V. Intracerebral xenotransplantation of GFP mouse bone marrow stromal cells in intact and stroke rat brain: graft survival and im-munologic response. Cell Transplant 13, 283, 2004.
46. Karadag, A., and Fisher, L.W. Bone sialoprotein enhances migration of bone marrow stromal cells through matrices by bridging MMP-2 to alpha(v)beta3-integrin. J Bone Miner Res 21, 1627, 2006.
47. Yasuda, H., Kuroda, S., Shichinohe, H., Kamei, S., Kawa-mura, R., and Iwasaki, Y. Effect of biodegradable fibrin scaffold on survival, migration, and differentiation of transplanted bone marrow stromal cells after cortical injury in rats. J Neurosurg 2009 (Mar 6), [E-pub ahead of print].
48. Anderson, J.M., Rodriguez, A., and Chang, D.T. Foreign body reaction to biomaterials. Semin Immunol 20, 86, 2008.
49. El-Ghannam, A. Bone reconstruction: from bioceramics to tissue engineering. Expert Rev Med Devices 2, 87, 2005.
50. Erbe, E.M., Marx, J.G., Clineff, T.D., and Bellincampi, L.D. Potential of an ultraporous beta-tricalcium phosphate synthetic cancellous bone void filler and bone marrow aspirate composite graft. Eur Spine J 10 Suppl 2, S141, 2001.
51. Martin, M.J., and Buckland-Wright, J.C. A novel mathematical model identifies potential factors regulating bone apposition. Calcif Tissue Int 77, 250, 2005.
52. Wang, T., Xia, D., Li, N., Wang, C., Chen, T., Wan, T., Chen, G., and Cao, X. Bone marrow stromal cell-derived growth inhibitor inhibits growth and migration of breast cancer cells via induction of cell cycle arrest and apoptosis. J Biol Chem 280, 4374, 2005.
53. Zha, Y.H., He, J.F., Mei, Y.W., Yin, T., and Mao, L. Zinc-finger transcription factor snail accelerates survival, migration and expression of matrix metalloproteinase-2 in human bone mesenchymal stem cells. Cell Biol Int 31, 1089, 2007.
54. Chen, X.D., Shi, S., Xu, T., Robey, P.G., and Young, M.F. Age-related osteoporosis in biglycan-deficient mice is related to defects in bone marrow stromal cells. J Bone Miner Res 17, 331, 2002.
55. Martin, I., Muraglia, A., Campanile, G., Cancedda, R., and Quarto, R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 138, 4456, 1997.
56. Mastrogiacomo, M., Derubeis, A.R., and Cancedda, R. Bone and cartilage formation by skeletal muscle derived cells. J Cell Physiol 204, 594, 2005.
57. Kim, Y.S., Park, H.J., Hong, M.H., Kang, P.M., Morgan, J.P., Jeong, M.H., Cho, J.G., Park, J.C., and Ahn, Y. TNF-alpha enhances engraftment of mesenchymal stem cells into in-farcted myocardium. Front Biosci 14, 2845, 2009.
58. Cao, J.J., Kurimoto, P., Boudignon, B., Rosen, C., Lima, F., and Halloran, B.P. Aging impairs IGF-I receptor activation and induces skeletal resistance to IGF-I. J Bone Miner Res 22, 1271, 2007.