Bone grafts cultured with bone marrow stromal cells for the repair of critical bone defects: An experimental study in mice

Journal of Biomedical Materials Research - Part A

Volumn 90, Issue 4, 2009, Pages 1218-1229

  Dumas, Aline ^a   Moreau, Marie Françoise ^a   Ghérardi, Romain K ^a   Baslé, Michel F ^a   Chappard, Daniel ^a  

^a INSERM   (France)

Author keywords

Bone defect; Bone marrow stromal cells; GFP; Osteoblast; Tissue engineering; Xenograft

Indexed keywords

BONE DEFECT; BONE FORMATION; BONE GRAFT; BONE INGROWTH; BONE MARROW CELLS; BONE MARROW STROMAL CELLS; BONE REGENERATION; C57BL/6 MICE; CALVARIAL DEFECTS; CONNECTIVE TISSUES; CRITICAL SIZE; EXPERIMENTAL STUDIES; FOUR-GROUP; GFP; HISTOMORPHOMETRIC ANALYSIS; IN-CONTROL; OSTEOBLASTIC DIFFERENTIATION; OSTEOCYTES; OSTEOGENIC; OSTEOGENICITY; OSTEOPROGENITOR CELLS; TRABECULAR BONES; XENOGRAFT;

BIOLOGICAL MATERIALS; CELL CULTURE; CELL MEMBRANES; DEBRIS; DEFECTS; GRAFTING (CHEMICAL); GRAFTS; OSTEOBLASTS; TISSUE ENGINEERING;

BONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DEFECT; BONE GRAFT; BONE MARROW CELL; BONE REGENERATION; BONE REMODELING; CELL DIFFERENTIATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OSTEOBLAST; STROMA CELL;

ANIMALS; BONE MARROW CELLS; BONE REGENERATION; BONE TRANSPLANTATION; CATTLE; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; IMPLANTS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOGENESIS; STROMAL CELLS; TISSUE ENGINEERING; TRANSPLANTATION, HETEROLOGOUS;

EID: 68249141261     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.32176     Document Type: Article

References (46)

1. Damien CJ, Parsons JR. Bone graft and bone graft substitutes: a review of current technology and applications. J Appl Biomater 1991;2:187-208.
2. Langer R, Vacanti JP. Tissue engineering. Science 1993;260:920-926.
3. Alsberg E, Hill EE, Mooney DJ. Craniofacial tissue engineering. Crit Rev Oral Biol Med 2001;12:64-75.
4. Yildirim M, Spiekermann H, Handt S, Edelhoff D. Maxillary sinus augmentation with the xenograft Bio-Oss and autogenous intraoral bone for qualitative improvement of the implant site: A histologic and histomorphometric clinical study in humans. Int J Oral Maxillofac Implants 2001;16:23-33.
5. Young C, Sandstedt P, Skoglund A. A comparative study of anorganic xenogenic bone and autogenous bone implants for bone regeneration in rabbits. Int J Oral Maxillofac Implants 1999;14:72-76.
6. Finkemeier CG. Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am 2002;84A:454-464.
7. Fujibayashi S, Neo M, Kim HM, Kokubo T, Nakamura T. Osteoinduction of porous bioactive titanium metal. Biomaterials 2004;25:443-450.
8. Hartman EH, Vehof JW, Spauwen PH, Jansen JA. Ectopic bone formation in rats: The importance of the carrier. Biomaterials 2005;26:1829-1835.
9. Greenwald AS, Boden SD, Goldberg VM, Khan Y, Laurencin CT, Rosier RN. Bone-graft substitutes: Facts, fictions, and applications. J Bone Joint Surg Am 2001;83A:98-103.
10. Krebsbach PH, Kuznetsov SA, Satomura K, Emmons RV, Rowe DW, Robey PG. Bone formation in vivo: Comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 1997;63:1059-1069.
11. Kruyt MC, Dhert WJ, Oner C, van Blitterswijk CA, Verbout AJ, de Bruijn JD. Optimization of bone-tissue engineering in goats. J Biomed Mater Res 2004;69B:113-120.
12. Meinel L, Fajardo R, Hofmann S, Langer R, Chen J, Snyder B, Vunjak-Novakovic G, Kaplan D. Silk implants for the healing of critical size bone defects. Bone 2005;37:688-698.
13. Mendes SC, Sleijster M, Van Den Muysenberg A, De Bruijn JD, Van Blitterswijk CA. A cultured living bone equivalent enhances bone formation when compared to a cell seeding approach. J Mater Sci Mater Med 2002;13:575-581.
14. Krebsbach PH, Mankani MH, Satomura K, Kuznetsov SA, Robey PG. Repair of craniotomy defects using bone marrow stromal cells. Transplantation 1998;66:1272-1278.
15. Goshima J, Goldberg VM, Caplan AI. The origin of bone formed in composite grafts of porous calcium phosphate ceramic loaded with marrow cells. Clin Orthop Relat Res 1991;269:274-283.
16. Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 2004;22:560-567.
17. Ohgushi H, Caplan AI. Stem cell technology and bioceramics: From cell to gene engineering. J Biomed Mater Res 1999;48:913-927.
18. Inoue H, Ohsawa I, Murakami T, Kimura A, Hakamata Y, Sato Y, Kaneko T, Takahashi M, Okada T, Ozawa K, Francis J, Leone P, Kobayashi E. Development of new inbred transgenic strains of rats with LacZ or GFP. Biochem Biophys Res Commun 2005;329:288-295.
19. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitinous green cells. FEBS Lett 1997;407:313-319.
20. Ogawa R, Mizuno H, Watanabe A, Migita M, Shimada T, Hyakusoku H. Osteogenic and chondrogenic differentiation by adipose-derived stem cells harvested from GFP transgenic mice. Biochem Biophys Res Commun 2004;313:871-877.
21. Moreau MF, Gallois Y, Baslé MF, Chappard D. Gamma irradiation of human bone allografts alters medullary lipids and releases toxic compounds for osteoblast-like cells. Biomaterials 2000;21:369-376.
22. Dumas A, Gaudin-Audrain C, Mabilleau G, Massin P, Hubert L, Baslé MF, Chappard D. The influence of processes for the purification of human bone allografts on the matrix surface and cytocompatibility. Biomaterials 2006;27:4204-4211.
23. Peter SJ, Liang CR, Kim DJ, Widmer MS, Mikos AG. Osteoblastic phenotype of rat marrow stromal cells cultured in the presence of dexamethasone, beta-glycerolphosphate, and L-ascorbic acid. J Cell Biochem 1998;71:55-62.
24. Parfitt AM, Drezner MK, Glorieux FG, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 1987;2:595-610.
25. Petite H, Viateau V, Bensaid W, Meunier A, de Pollak C, Bourguignon M, Oudina K, Sedel L, Guillemin G. Tissue-engineered bone regeneration. Nat Biotechnol 2000;18:959-963.
26. Warnke PH, Springer IN, Wiltfang J, Acil Y, Eufinger H, Wehmoller M, Russo PA, Bolte H, Sherry E, Behrens E, Terheyden H. Growth and transplantation of a custom vascularised bone graft in a man. Lancet 2004;364:766-770.
27. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 2001;344:385-386.
28. Chappard D, Guggenbuhl P, Legrand E, Baslé MF, Audran M. Texture analysis of X-ray radiographs is correlated with bone histomorphometry. J Bone Miner Metab 2005;23:24-29.
29. Tsuruga E, Takita H, Itoh H, Wakisaka Y, Kuboki Y. Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. J Biochem 1997;121:317-324.
30. Chang BS, Lee CK, Hong KS, Youn HJ, Ryu HS, Chung SS, Park KW. Osteoconduction at porous hydroxyapatite with various pore configurations. Biomaterials 2000;21:1291-1298.
31. Chappard D, Fressonnet C, Genty C, Baslé MF, Rebel A. Fat in bone xenografts: Importance of the purification procedures on cleanliness, wettability and biocompatibility. Biomaterials 1993;14:507-512.
32. Levai JP, Boisgard S. Acetabular reconstruction in total hip revision using a bone graft substitute. Early clinical and radiographic results. Clin Orthop Relat Res 1996;108-114.
33. Einhorn TA. The cell and molecular biology of fracture healing. Clin Orthop Relat Res 1998;S7-S21.
34. Ringe J, Kaps C, Burmester GR, Sittinger M. Stem cells for regenerative medicine: Advances in the engineering of tissues and organs. Naturwissenschaften 2002;89:338-351.
35. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
36. Puelacher WC, Kim SW, Vacanti JP, Schloo B, Mooney D, Vacanti CA. Tissue-engineered growth of cartilage: the effect of varying the concentration of chondrocytes seeded onto synthetic polymer matrices. Int J Oral Maxillofac Surg 1994;23:49-53.
37. Bareille R, Lafage-Proust MH, Faucheux C, Laroche N, Wenz R, Dard M, Amédée J. Various evaluation techniques of newly formed bone in porous hydroxyapatite loaded with human bone marrow cells implanted in an extra-osseous site. Biomaterials 2000;21:1345-1352.
38. Kneser U, Stangenberg L, Ohnolz J, Buettner O, Stern-Straeter J, Mobest D, Horch RE, Stark GB, Schaefer DJ. Evaluation of processed bovine cancellous bone matrix seeded with syngenic osteoblasts in a critical size calvarial defect rat model. J Cell Mol Med 2006;10:695-707.
39. Xia Z, Ye H, Locklin RM, Ferguson DJ, Cui Z, Triffitt JT. Effi-cient characterisation of human cell-bioceramic interactions in vitro and in vivo by using enhanced GFP-labelled mesenchymal stem cells. Biomaterials 2005;26:5790-5800.
40. Yoshikawa T, Ohgushi H, Nakajima H, Yamada E, Ichijima K, Tamai S, Ohta T. In vivo osteogenic durability of cultured bone in porous ceramics: A novel method for autogenous bone graft substitution. Transplantation 2000;69:128-134.
41. Castano-Izquierdo H, Alvarez-Barreto J, van den Dolder J, Jansen JA, Mikos AG, Sikavitsas VI. Pre-culture period of mesenchymal stem cells in osteogenic media influences their in vivo bone forming potential. J Biomed Mater Res A 2007;82:129-138.
42. Tada M, Shinohara Y, Kato I, Hiraga K, Aizawa T, Demura M, Mori Y, Shinoda H, Mizuguchi M, Kawano K. Preparation and observation of fresh-frozen sections of the green fluorescent protein transgenic mouse head. Acta Histochem Cytochem 2006;39:31-34.
43. Shao XX, Hutmacher DW, Ho ST, Goh JC, Lee EH. Evaluation of a hybrid scaffold/cell construct in repair of high-load-bearing osteochondral defects in rabbits. Biomaterials 2006;27:1071-1080.
44. Dreyfus PA, Chrétien F, Chazaud B, Kirova Y, Caramelle P, Garcia L, Butler-Browne G, Ghérardi RK. Adult bone marrow-derived stem cells in muscle connective tissue and satellite cell niches. Am J Pathol 2004;164:773-779.
45. Irons H, Lind JG, Wakade CG, Yu G, Hadman M, Carroll J, Hess DC, Borlongan CV. Intracerebral xenotransplantation of GFP mouse bone marrow stromal cells in intact and stroke rat brain: Graft survival and immunologic response. Cell Transplant 2004;13:283-294.
46. Imasawa T, Utsunomiya Y, Kawamura T, Zhong Y, Nagasawa R, Okabe M, Maruyama N, Hosoya T, Ohno T. The potential of bone marrow-derived cells to differentiate to glomerular mesangial cells. J Am Soc Nephrol 2001;12:1401-1409.