Inferior ectopic bone formation of mesenchymal stromal cells from adipose tissue compared to bone marrow: Rescue by chondrogenic pre-induction

Stem Cell Research

Volumn 11, Issue 3, 2013, Pages 1393-1406

  Brocher, J ^a   Janicki, P ^a   Voltz, P ^a   Seebach, E ^a   Neumann, E ^b,c   Mueller Ladner, U ^b,c   Richter, W ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c KERCKHOFF HEART CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ALKALINE PHOSPHATASE; ANGIOPOIETIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; INTERLEUKIN 6; VASCULOTROPIN;

ADIPOSE TISSUE; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE CONDUCTION; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; FEMALE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STROMA CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; POLYADENYLATION; PRIORITY JOURNAL;

ADIPOSE TISSUE; ADULT; AGED; ANIMALS; BIOLOGICAL MARKERS; BONE AND BONES; BONE MARROW CELLS; BONE MORPHOGENETIC PROTEIN 6; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, SCID; MIDDLE AGED; OSTEOGENESIS; REGENERATION; TISSUE ENGINEERING; TRANSFORMING GROWTH FACTOR BETA;

EID: 84886946494     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.07.008     Document Type: Article

References (56)

1. Agata H., Asahina I., Watanabe N., Ishii Y., Kubo N., Ohshima S., et al. Characteristic change and loss of in vivo osteogenic abilities of human bone marrow stromal cells during passage. Tissue Eng. Part A 2010, 16(2):663-673.
2. Bianchi G., Banfi A., Mastrogiacomo M., Notaro R., Luzzatto L., Cancedda R., et al. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp. Cell Res. 2003, 287(1):98-105.
3. Bianco P., Cao X., Frenette P.S., Mao J.J., Robey P.G., Simmons P.J., et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med. 2013, 19(1):35-42.
4. Caplan A.I. The mesengenic process. Clin. Plast. Surg. 1994, 21(3):429-435.
5. Caplan A.I., Goldberg V.M. Principles of tissue engineered regeneration of skeletal tissues. Clin. Orthop. Relat. Res. 1999, (Suppl. 367):12-16.
6. da Silva Meirelles L., Chagastelles P.C., Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006, 119(Pt 11):2204-2213.
7. De Bari C., Dell'Accio F., Tylzanowski P., Luyten F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001, 44(8):1928-1942.
8. de Guzman R.C., Saul J.M., Ellenburg M.D., Merrill M.R., Coan H.B., Smith T.L., et al. Bone regeneration with BMP-2 delivered from keratose scaffolds. Biomaterials 2013, 34(6):1644-1656.
9. De Ugarte D.A., Morizono K., Elbarbary A., Alfonso Z., Zuk P.A., Zhu M., et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003, 174(3):101-109.
10. Dexheimer V., Frank S., Richter W. Proliferation as a requirement for in vitro chondrogenesis of human mesenchymal stem cells. Stem Cells Dev. 2012, 21(12):2160-2169.
11. Dickhut A., Gottwald E., Steck E., Heisel C., Richter W. Chondrogenesis of mesenchymal stem cells in gel-like biomaterials in vitro and in vivo. Front. Biosci. 2008, 13:4517-4528.
12. Dickhut A., Pelttari K., Janicki P., Wagner W., Eckstein V., Egermann M., et al. Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage. J. Cell. Physiol. 2009, 219(1):219-226.
13. Dmitrieva R.I., Minullina I.R., Bilibina A.A., Tarasova O.V., Anisimov S.V., Zaritskey A.Y. Bone marrow- and subcutaneous adipose tissue-derived mesenchymal stem cells: differences and similarities. Cell Cycle 2012, 11(2).
14. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8(4):315-317.
15. Frommer K.W., Schaffler A., Buchler C., Steinmeyer J., Rickert M., Rehart S., et al. Adiponectin isoforms: a potential therapeutic target in rheumatoid arthritis?. Ann. Rheum. Dis. 2012, 71(10):1724-1732.
16. Hattori H., Sato M., Masuoka K., Ishihara M., Kikuchi T., Matsui T., et al. Osteogenic potential of human adipose tissue-derived stromal cells as an alternative stem cell source. Cells Tissues Organs 2004, 178(1):2-12.
17. Hattori H., Masuoka K., Sato M., Ishihara M., Asazuma T., Takase B., et al. Bone formation using human adipose tissue-derived stromal cells and a biodegradable scaffold. J. Biomed. Mater. Res. B Appl. Biomater. 2006, 76(1):230-239.
18. Hayashi O., Katsube Y., Hirose M., Ohgushi H., Ito H. Comparison of osteogenic ability of rat mesenchymal stem cells from bone marrow, periosteum, and adipose tissue. Calcif. Tissue Int. 2008, 82(3):238-247.
19. Hennig T., Lorenz H., Thiel A., Goetzke K., Dickhut A., Geiger F., et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J. Cell. Physiol. 2007, 211(3):682-691.
20. Ike M., Urist M.R. Recycled dentin root matrix for a carrier of recombinant human bone morphogenetic protein. J. Oral Implantol. 1998, 24(3):124-132.
21. Im G.I., Shin Y.W., Lee K.B. Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells?. Osteoarthritis Cartilage 2005, 13(10):845-853.
22. Janicki P., Kasten P., Kleinschmidt K., Luginbuehl R., Richter W. Chondrogenic pre-induction of human mesenchymal stem cells on beta-TCP: enhanced bone quality by endochondral heterotopic bone formation. Acta Biomater. 2010, 6(8):3292-3301.
23. Janicki P., Boeuf S., Steck E., Egermann M., Kasten P., Richter W. Prediction of in vivo bone forming potency of bone marrow-derived human mesenchymal stem cells. Eur. Cell. Mater. 2011, 21:488-507.
24. Kasten P., Vogel J., Luginbuhl R., Niemeyer P., Tonak M., Lorenz H., et al. Ectopic bone formation associated with mesenchymal stem cells in a resorbable calcium deficient hydroxyapatite carrier. Biomaterials 2005, 26(29):5879-5889.
25. Kasten P., Beyen I., Niemeyer P., Luginbuhl R., Bohner M., Richter W. Porosity and pore size of beta-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: an in vitro and in vivo study. Acta Biomater. 2008, 4(6):1904-1915.
26. Krebsbach P.H., Kuznetsov S.A., Satomura K., Emmons R.V., Rowe D.W., Robey P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 1997, 63(8):1059-1069.
27. Lin Y., Li H., Huang J., Zeng S. Following the fate of murine epidermal stem cells in a syngeneic dermal equivalent in vivo. Burns 2005, 31(8):1007-1012.
28. Liu T.M., Martina M., Hutmacher D.W., Hui J.H., Lee E.H., Lim B. Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells 2007, 25(3):750-760.
29. Mankani M.H., Kuznetsov S.A., Fowler B., Kingman A., Robey P.G. In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape. Biotechnol. Bioeng. 2001, 72(1):96-107.
30. Mankani M.H., Kuznetsov S.A., Wolfe R.M., Marshall G.W., Robey P.G. In vivo bone formation by human bone marrow stromal cells: reconstruction of the mouse calvarium and mandible. Stem Cells 2006, 24(9):2140-2149.
31. Martin I., Muraglia A., Campanile G., Cancedda R., Quarto R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 1997, 138(10):4456-4462.
32. Meier F.M., Frommer K.W., Peters M.A., Brentano F., Lefevre S., Schroder D., et al. Visfatin/pre-B-cell colony-enhancing factor (PBEF), a proinflammatory and cell motility-changing factor in rheumatoid arthritis. J. Biol. Chem. 2012, 287(34):28378-28385.
33. Mendes S.C., Sleijster M., Van Den Muysenberg A., De Bruijn J.D., Van Blitterswijk C.A. A cultured living bone equivalent enhances bone formation when compared to a cell seeding approach. J. Mater. Sci. Mater. Med. 2002, 13(6):575-581.
34. Mendes S.C., Tibbe J.M., Veenhof M., Both S., Oner F.C., van Blitterswijk C.A., et al. Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells. J. Mater. Sci. Mater. Med. 2004, 15(10):1123-1128.
35. Mitchell J.B., McIntosh K., Zvonic S., Garrett S., Floyd Z.E., Kloster A., et al. Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 2006, 24(2):376-385.
36. Mizumoto Y., Moseley T., Drews M., Cooper V.N., Reddi A.H. Acceleration of regenerate ossification during distraction osteogenesis with recombinant human bone morphogenetic protein-7. J. Bone Joint Surg. Am. 2003, 85-A(Suppl. 3):124-130.
37. Moghadam H.G., Urist M.R., Sandor G.K., Clokie C.M. Successful mandibular reconstruction using a BMP bioimplant. J. Craniofac. Surg. 2001, 12(2):119-127. (discussion 128).
38. Niemeyer P., Fechner K., Milz S., Richter W., Suedkamp N.P., Mehlhorn A.T., et al. Comparison of mesenchymal stem cells from bone marrow and adipose tissue for bone regeneration in a critical size defect of the sheep tibia and the influence of platelet-rich plasma. Biomaterials 2010, 31(13):3572-3579.
39. Noel D., Caton D., Roche S., Bony C., Lehmann S., Casteilla L., et al. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp. Cell Res. 2008, 314(7):1575-1584.
40. Owen M. Marrow stromal stem cells. J. Cell Sci. Suppl. 1988, 10:63-76.
41. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
42. Sacchetti B., Funari A., Michienzi S., Di Cesare S., Piersanti S., Saggio I., et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007, 131(2):324-336.
43. 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. [Research Support, Non-U.S. Gov't]. Stem Cells 2007, 25(7):1823-1829.
44. Schubert T., Xhema D., Veriter S., Schubert M., Behets C., Delloye C., et al. The enhanced performance of bone allografts using osteogenic-differentiated adipose-derived mesenchymal stem cells. Biomaterials 2011, 32(34):8880-8891.
45. Shafiee A., Seyedjafari E., Soleimani M., Ahmadbeigi N., Dinarvand P., Ghaemi N. A comparison between osteogenic differentiation of human unrestricted somatic stem cells and mesenchymal stem cells from bone marrow and adipose tissue. Biotechnol. Lett. 2011, 33(6):1257-1264.
46. Steck E., Burkhardt M., Ehrlich H., Richter W. Discrimination between cells of murine and human origin in xenotransplants by species specific genomic in situ hybridization. Xenotransplantation 2010, 17(2):153-159.
47. Suga H., Matsumoto D., Eto H., Inoue K., Aoi N., Kato H., et al. Functional implications of CD34 expression in human adipose-derived stem/progenitor cells. Stem Cells Dev. 2009, 18(8):1201-1210.
48. Teixeira J.O., Urist M.R. Bone morphogenetic protein induced repair of compartmentalized segmental diaphyseal defects. Arch. Orthop. Trauma Surg. 1998, 117(1-2):27-34.
49. van der Bogt K.E., Schrepfer S., Yu J., Sheikh A.Y., Hoyt G., Govaert J.A., et al. Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 2009, 87(5):642-652.
50. Wagner W., Wein F., Seckinger A., Frankhauser M., Wirkner U., Krause U., et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 2005, 33:1402-1416.
51. Wagner W., Horn P., Castoldi M., Diehlmann A., Bork S., Saffrich R., et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008, 3(5):e2213.
52. Weiss S., Hennig T., Bock R., Steck E., Richter W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J. Cell. Physiol. 2010, 223(1):84-93.
53. Winter A., Breit S., Parsch D., Benz K., Steck E., Hauner H., et al. Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum. 2003, 48(2):418-429.
54. Wurzler K.K., DeWeese T.L., Sebald W., Reddi A.H. Radiation-induced impairment of bone healing can be overcome by recombinant human bone morphogenetic protein-2. J. Craniofac. Surg. 1998, 9(2):131-137.
55. Zannettino A.C., Paton S., Arthur A., Khor F., Itescu S., Gimble J.M., et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J. Cell. Physiol. 2008, 214(2):413-421.
56. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., et al. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 2002, 13(12):4279-4295.