Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection

Journal of Cellular Biochemistry

Volumn 89, Issue 6, 2003, Pages 1235-1249

  Baddoo, Melody ^a   Hill, Katy ^a   Wilkinson, Robin ^a   Gaupp, Dina ^a   Hughes, Catherine ^a   Kopen, Gene C ^b   Phinney, Donald G ^a,c  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b Neuronyx Inc   (United States)

^c Center for Gene Therapy   (United States)

Author keywords

FGF2; Marrow stromal cells; Mesenchymal stem cells

Indexed keywords

BETA1 INTEGRIN; CD11B ANTIGEN; CD135 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CD48 ANTIGEN; CD81 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; HERMES ANTIGEN; LEUKEMIA INHIBITORY FACTOR; MITOGENIC AGENT; MURINE STEM CELL FACTOR; NUCLEOSTEMIN; OCTAMER TRANSCRIPTION FACTOR 4; SCA 1 ANTIGEN; SOMATOMEDIN; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GROWTH RATE; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; IMMUNOCYTOCHEMISTRY; MALE; MESENCHYMAL STEM CELL; MESENCHYME CELL; MOUSE; NEGATIVE SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; OSTEOCYTE; PHENOTYPE; PRIORITY JOURNAL; TIBIA FRACTURE;

ANIMALS; ANTIGENS, CD; BONE MARROW CELLS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL SEPARATION; DNA PRIMERS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION; GROWTH SUBSTANCES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELLS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASTICS; POLYMERASE CHAIN REACTION;

MURINAE;

EID: 0043071544     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.10594     Document Type: Article

References (55)

1. Ashton BA, Eaglesom CC, Bab I, Owen ME. 1984. Distribution of fibroblastic colony-forming cells in rabbit bone marrow and assay of their osteogenic potential by an in vivo diffusion chamber method. Calcif Tissue Int 36:83-94.
2. Bearpark AD, Gordon MY. 1989. Adhesive properties distinguish sub-populations of hematopoietic stem cells with different spleen colony-forming and marrow repopulating capacities. Bone Marrow Transplant 4:625-628.
3. Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M. 2001. Therapeutic benefit of intracerebra transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 189:49-57.
4. Colter DC, Class R, DiGirolamo CM, Prockop DJ. 2000. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 97:3213-3218.
5. Debiais F, Hott M, Graulet AM, Marie PJ. 1998. The effects of fibroblast growth factor-2 on human neonatal calvaria osteoblastic cells are differentiation stage specific. J Bone Miner Res 13:645-654.
6. Deryugina EI, Muller-Sieburg CE. 1993. Stromal cells in long-term cultures: Keys to the elucidation of hematopoietic development. Crit Rev Immunol 13:115-150.
7. DiGirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. 1999. 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. Brit J Hematol 107:275-281.
8. Enomoto-Iwamoto M, Nakamura T, Aikawa T, Higuchi Y, Yuasa T, Yamaguchi A, Nohno T, Noji S, Matsuya T, Kurisu K, Koyama E, Pacifici M, Iwamoto M. 2000. Hedgehog proteins stimulate chondrogenic cell differentiation and cartilage formation. J Bone Miner Res 15:1659-1668.
9. Friedenstein AJ, Chailakhjan RK, Lalykina KS. 1970. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3:393-403.
10. Friedenstein AJ, Gorskaja UF, Kulagina NN. 1976. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Expt Hematol 4:267-274.
11. Hanada K, Dennis JE, Caplan AI. 1997. Stimulatory effects of basic fibroblast growth factor and bone morphogenetic protein-2 on osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells. J Bone Miner Res 12:1606-1614.
12. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L. 2002. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 99:2199-2204.
13. Hurwitz DR, Kirchgesser M, Merrill W, Galanopoulos T, McGrath CS, Emami S, Hansen M, Cherington V, Appel JM, Bizinkauskas CB, Brackmann HH, Levine PH, Greenberger JS. 1997. Systemic delivery of human growth hormone or human Factor IX in dogs by reintroduced genetically modified autologous bone marrow stromal cells. Hum Gene Ther 8:137-156.
14. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
15. Jiang Y, Balkrishna N, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
16. Jin HK, Carter JE, Huntley GW, Schuchman EH. 2002. Intracerebral transplantation of mesenchymal stem cells into acid sphingomyelinase-deficient mice delays the onset of neurological abnormalities and extends their life span. J Clin Invest 109:1183-1191.
17. Kerk DK, Henry EA, Eaves AC, Eaves CJ. 1985. Two classes of primitive pluripotent hematopoietic progenitors: Separation by adherence. J Cell Physiol 125:127-134.
18. Kopen GC, Prockop DJ, Phinney DG. 1999. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci USA 96:10711-10716.
19. Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, Fine A. 2001. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Integr Annu Indexes 128:5181-5188.
20. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, Robey PG. 1997. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 12:1335-1347.
21. Kuznetsov SA, Friedenstein AJ, Robey PG. 1997a. Factors required for bone marrow stromal fibroblast colony formation in vitro. Brit J Hematol 97:561-570.
22. Lee MS, Lowe GN, Strong DD, Wergedal JE, Glackin CA. 1999. TWIST, a basic helix-loop-helix transcription factor, can regulate the human osteogenic lineage. J Cell Biochem 75:566-577.
23. Lennon DP, Haynesworth SE, Young RG, Dennis JE, Caplan AI. 1995. A chemically defined medium supports in vitro proliferation and maintains the osteochondral potential of rat marrow-derived mesenchymal stem cells. Exp Cell Res 219:211-222.
24. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF. 1998. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4:415-428.
25. Martin I, Muraglia A, Campanile G, Cancedda R, Quarto R. 1997. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 138:4456-4462.
26. Mauraglia A, Cancedda R, Quarto R. 2000. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 113:1161-1166.
27. McBride C, Gaupp D, Phinney DG. 2003. Quantifying levels of murine and human mesenchymal stem cells in vivo by real-time PCR. Cytotherapy 5:7-18.
28. Modderman WE, Vrijheid-Lammers T, Lowik CW, Nijweide PJ. 1994. Removal of hematopoietic cells and macrophages from mouse bone marrow cultures: Isolation of fibroblast-like stromal cells. Expt Hematol 22:194-201.
29. Nakajima F, Ogasawara A, Goto K, Moriya H, Ninomiya Y, Einhorn TA, Yamazaki M. 2001. Spatial and temporal gene expression in chondrogenesis during fracture healing and the effects of basic fibroblast growth factor. J Orthaped Res 19:935-944.
30. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell 95:379-391.
31. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. 2003. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. (in press).
32. Pereira RF, O'Hara MD, Laptev AV, Halford KW, Pollard MD, Class R, Simon D, Livezey K, Prockop DJ. 1998. Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci USA 95:1142-1147.
33. Phinney DG, Kopen G, Righter W, Webster S, Tremain N, Prockop DJ. 1999. Donor variation in the growth properties and osteogenic potential of human marrow stromal cells. J Cell Biochem 75:424-436.
34. Phinney DG, Kopen G, Isaacson RL, Prockop DJ. 1999a. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: Variation in yield, growth, and differentiation. J Cell Biochem 72:570-585.
35. Pitaru S, Kotev-Emeth S, Noff D, Kaffuler S, Savion N. 1993. Effect of basic fibroblast growth factor on the growth and differentiation of adult stromal bone marrow cells: Enhanced development of mineralized bone-like tissue in culture. J Bone Miner Res 8:919-929.
36. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
37. Pittenger MF, Mbalaviele G, Black M, Mosca JD, Marshak DR. 2001. Mesenchymal stem cells. In: Koller MR, Palsson BO, Master JRW, editors. Human cell culture. Great Britain: Kluwer Academic Publishers. pp 189-207.
38. Pri-Chen S, Pitaru S, Lokiec F, Savion N. 1998. Basic fibroblast growth factor enhances the growth and expression of the osteogenic phenotype of dexamethasone-treated human bone marrow-derived bone-like cells in culture. Bone 23:111-117.
39. Shake JG, Gruber PJ, Baumgartner WA, Senechal G, Meyers J, Redmond JM, Pittenger MF, Martin BJ. 2002. Mesenchymal stem cell implantation in a swine myocardial infarct model: Engraftment and functional effects. Ann Thoracic Surg 73:1919-1925.
40. Simmons PJ, Torok-Storb B. 1991. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78:55-62.
41. Simmons PJ, Masinovsky B, Longenecker BM, Berenson R, Torok-Storb B, Gallatin WM. 1992. Vascular cell adhesion molecule-1 expressed by bone marrow stromal cells mediates the binding of hematopoietic progenitor cells. Blood 80:388.
42. Tanaka H, Ogasa H, Barnes J, Liang CT. 1999. Actions of bFGF on mitogenic activity and lineage expression in rat osteoprogenitor cells: Effect of age. Mol Cell Endo 150:1-10.
43. Thomson BM, Bennett J, Dean V, Triffitt J, Meikle MC, Loveridge N. 1993. Preliminary characterization of porcine bone marrow stromal cells: Skeletogenic potential, colony-forming activity, and response to dexamethasone, transforming growth factor β, and basic fibroblast growth factor. J Bone Miner Res 8:1173-1183.
44. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. 2002. Human mesenchymal stem cells differentiate to a cardiomyocytes phenotype in the adult murine heart. Circulation 105:93-98.
45. Tremain N, Korkko J, Ibberson D, Kopen GC, DiGirolamo C, Phinney DG. 2001. MicroSAGE analysis of 2353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 19:408-418.
46. Tsai RYL, McKay RDG. 2002. A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16:2991-3003.
47. Tsuji K, Noda M. 2001. Transient suppression of core-binding factor alpha 1 expression by basic fibroblast growth factor in rat osteoblast-like osteosarcoma ROS17/2.8 cells. J Bone Miner Res 19:213-219.
48. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, Takagishi K, Kato Y. 2001. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Comm 288:413-419.
49. van den Bos C, Mosca JD, Winkles J, Kerrigan L, Burgess WH, Marshak DR. 1997. Human mesenchymal stem cells respond to fibroblast growth factors. Hum Cell 10:45-50.
50. Van Vlasselaer P, Falla N, Snoeck H, Mathieu E. 1994. Characterization and purification of osteogenic cells from murine bone marrow by two-color cell sorting using anti-Sca-1 monoclonal antibody and wheat germ agglutinin. Blood 84:753-763.
51. Walsh S, Jefferies C, Stewart K, Jordan GR, Screen J, Beresford JN. 2000. Expression of the developmental marker STRO-1 and alkaline phosphatase in cultures of human marrow stromal cells: Regulation by fibroblast growth factor (FGF)-2 and relationship to the expression of FGF receptors 1-4. Bone 27:185-195.
52. Wang Q-R, Wolf NS. 1990. Dissecting the hematopoietic microenvironment. VIII. Clonal isolation and identification of cell types in murine CFU-F colonies by limiting dilution. Expt Hematol 18:355-359.
53. Witte PL, Robinson M, Henley A, Low MG, Stiers DL, Perkins S, Fleischman RA, Kincade PW. 1987. Relationships between B-lineage lymphocytes and stromal cells in long-term bone marrow cultures. Eur J Immunol 17:1473-1484.
54. Xu CX, Hendry JH, Testa NG, Allen TD. 1983. Stromal colonies from mouse marrow: Characterization of cell types, optimization of plating efficiency and its effects on radiosensitivity. J Cell Sci 61:453-466.
55. Zhang X, Sobue T, Hurley M. 2002. FGF-2 increases colony formation, PTH receptor, and IGF-1 mRNA in mouse marrow stromal cells. Biochem Biophys Res Comm 290:526-531.