Propagation and senescence of human marrow stromal cells in culture: A simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate

British Journal of Haematology

Volumn 107, Issue 2, 1999, Pages 275-281

  Digirolamo, Carla M ^a   Stokes, David ^a   Colter, David ^a   Phinney, Donald G ^a   Class, Reiner ^a   Prockop, Darwin J ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Adipogenesis; Colony forming assays; Marrow stromal cells; Osteogenesis; Propagation and senescence

Indexed keywords

ADIPOCYTE; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; COLONY FORMING UNIT F; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SENESCENCE; STROMA CELL;

EID: 0032748173     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.1999.01715.x     Document Type: Article

References (35)

1. Anklesaria, P., Klassen, V, Sakakeeny, M.A., FitzGerald, T.J., Harrison, D., Rybak. M.E. & Greenbcrger, J.S. (1987) Biological characterization of cloned permanent stromal cell lines from anemic Sl/Sld mice and +/+ littermates. Experimental Hematology. 15,636-644.
2. Azizi, S.A., Stokes, D.G., Augelli. B.J., DiGirolamo. C.M. & Prockop. D.J. (1998) Engraftmerrt and migration of human bone marrow stromal cells implanted in the brains of albino rats: similarities to astrocyte grafts. Proceedings of the National Academy of Sciences of the United States of America. 95, 3908-3913.
3. Bcresford, J.N.. Bcnnett, J.H., Devlin, C., Leboy, P.S. & Owen, M.E. (1992) Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. Journal of Cell Science, 102, 341-351.
4. Brader, S.P., Jaiswal, N. & Haynesworth, S.E. (1997) Growth kinetics, self-renewal and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation following cryopreservation. Journal of Cellular Biochemistry. 64, 278-294.
5. Caplan, A.I. (1991) Mesenchymal stem cells. Journal of Orthopedic Research, 9, 641-650.
6. Castro-Malaspina, H., Gay, R.E., Resnick, G., Kapoor, N., Meyers, P., Chiarieri, D., McKenz, S., Broxmeyer, H.E. & Moore, M.A.S. (1980) Characterization of human bone marrow fibroblast colonyforming cells (CFU-F) and their progeny. Blood, 56, 289-301.
7. Cheng, S.L., Yang, J.W.. Rifas, L., Zhang. S.-F. & Avioli, L.V. (1994) Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology, 134,277-286.
8. Clark, B.R. & Keating, A. (1995) Biology of bone marrow stroma. Annals of the New York Academy of Sciences, 770, 70-78.
9. Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G. & Mavilio, F. (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science, 279, 1456, 1528-1530.
10. Friedenstein, A.J., Chailakhyan, R.K. & Gerasimov, U.V. (1987) Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell and Tissue Kinetics, 20, 263-272.
11. Friedenstein, A.J.. Gorskaja, U. & Kalugina, N.N. (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Experimental Hematoloay, 4, 267-274.
12. Goldberg, V.M. & Caplan, A.I. (1994) Biological resurfacing: an alternative to total Joint arthroplasty. Orthopedics, 17, 819-821.
13. Gronthos, S., Graves, S.E., Ohta. S. & Simmons. P.J. (1994) The STRO-11 fraction of adult human bone marrow contains the osteogenic precursors. Blood, 84, 4164-4173.
14. Gronthos, S. & Simmons, P.J. (1995) The growth factor requirements of STRO-l:r-üive human bone marrow stromal precursors under serum-deprived conditions in vitro. Blood, 85, 929-940.
15. Gronthos, S. & Simmons, P.J. (1996) The biology and application of human bone marrow stromal cell precursors. Journal of llematotherapy, 5, 15-23.
16. Houghton, A., Oyajobi, B.O., Foster, G.A., Rüssel, R.G.G. & Stringer, B.M.J. (1998) Immortalization of human marrow stromal cells by retroviral transduction with a temperature sensitive oncogene: identification of bipotential precursor cells capable of directed differentiation to either an osteoblast or adipocyte phenotype. Bone. 22, 7-16.
17. Howlett, C.R., Cave, J., Williamson, M., Farmer, J., All, S.Y., Bab, I. & Owen, M.E. (1986) Mineralization in in vitro cultures of rabbit marrow stromal cells. Clinical Orthopedics and Related Research, 213,251-263.
18. Hurwitz. D.R., Kirchgesser, M., Merrill. W., Galanopoulos, T., McGrath, C.A.. Emami, S., Hansen, M., Cherington, V, Appel, J.M., Bizinkauskas, C.B., Brackmann, H.H., Levine, P.H. & Greenberger, S. (1997) Systemic delivery of human growth hormone or human factor IX in dogs by reintroduced genetically modified autologous bone marrow stromal cells. Human Gene Tlierapy, 8, 137-156.
19. Joyner. C.J., Bennett, A. & Triffitt, J.T. (1997) Identification and enrichment of human osteoprogenitor cells by using differentiation stage-specific monoclonal antibodies. Bone, 21, 1-6.
20. Kelly, K.A. & Gimble, J.M. (1998) 1,25-Dihydroxy vitamin D3 inhibits adipocyte differentiation and gene expression in murine bone marrow stromal cell clones and primary cultures. Endocrinology. 139,2622-2628.
21. Kuznetsov, S.A., Krebsbach, P.H., Satomura, K., Kerr, J., Riminucci, M., Benayahu, D. & Robey, P.G. (1997) Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. Journal of Bone and Mineral Research, 12, 1335-1347.
22. Long, M.W.. Robinson, J.A., Ashcraft, E.A. & Mann, K.G. (1995) Regulation of human bone marrow-derived osteoprogenitor cells by osteogenic growth factors. Journal of Clinical Investigation, 95, 881-887.
23. Mets, T. & Verdonk, G. ( 19 81 ) In vitro aging of human bone marrowderived stromal cells. Meclianisms of Ageing and Development, 16, 81-89.
24. Owen, M.E. & Friedenstein, A.J. (1988) Stromal stem cells: marrowderived osteogenic precursors. Cell and Molecular Biology of Vertebrate Hard Tissues: Ciba Foundation Symposium, Chichester, U.K., pp. 42-60.
25. Pereira, R.F., O'Hara, M.D., Laptev, A.V., Haiford, K.W., Pollard. M.D., Class, R., Simon, D., Livezey, K. & Prockop, D.J. (1998) Marrow stromal cells as a source of progenitor cells for non-hematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proceedings of the National Academy of Sciences of the United States of America. 95, 1142-1147.
26. Phinney, D.G., Kopen, G., Isaaeson, R.L. & Prockop, D.J. (1999) Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth and differentiation. Journal of Cellular Biochemistry. 72, 570-585.
27. Piersma, A.H., Brockbank, K.G.M., Ploemacher, R.E.. van Vilet, E.. Brakel-van Peer, K.M.). & Visser. PJ. (1985) Characterization of fibroblastic stromal cells from murine bone marrow. Experimental Hematology. 13, 237-243.
28. Prockop, D.J. (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science, 276, 71-74.
29. Rickard, D.J., Kassem, M., Hefferan, T.E., Sarkar, G., Speisberg. T.C. & Riggs, B.L. (1996) Isolation and characterization of osteoblast precursor cells from human bone marrow. Journal of Bone and Mineral Research, 11, 312-324.
30. Rickard, D.J., Sullivan, T.A., Shenker, B.J., Leboy, P.S. & Kazhdan, I. (1994) Induction of rapid osteoblast differentiation in rat marrow stromal cell cultures by dexamethasone and BMP-2. Developmental Biology. 161,218-228.
31. Satomura, K., Derubeis, A.R., Fedarko, N.S., Ibaraki-O'Connor, K., Kuznetsov, S.A., Rowe, D.W., Young, M.F. & Robey. P.G. (1998) Receptor tyrosine kinase expression in human bone marrow stromal cells. Journal of Cellular Physiology. 177, 426-438.
32. Simmons, P.J. & Torok-Storb, B. (1991) Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood. 78, 55-62.
33. Stanford, C.M., Jacobson, P.A., Eanes, E.D., Lembke, L.A. & Midura, R.J. (1995) Rapidly forming apoptotic mineral in an osteoblastic cell line (UMR 106-01 BSP). Journal of Biological Chemistry. 270, 9420-9428.
34. Wakitani, S., Saito, T. & Caplan, A.I. (1995) Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5azacytidine. Muscle and Nerve, 18, 1417-1426.
35. Waller, E.K., Olweus, J., Lund-Johansen, F., Huang, S., Nguyen, M., Guo, G.R. & Terstappen, L. (1995) The 'common stem cell' hypothesis evaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. Blood. 85, 2422-2435.