Human mesenchymal stromal cells from adult and neonatal sources: comparative analysis of their morphology, immunophenotype, differentiation patterns and neural protein expression

References

• Prockop DJ. Marrow stromal cells as stem cells for non-hematopoietic tissues. Science 1997; 276: 71–4
   PubMed Web of Science ®Google Scholar
• Pittenger MF, MacKay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143–7
   PubMed Web of Science ®Google Scholar
• Sanchez-Ramos J, Song S, Cardozo-Pelaez F, et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 2000; 164: 247–56
   PubMed Web of Science ®Google Scholar
• Jiang Y, Jahagirdar BN, Reinhardt LR, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418: 41–9
   PubMed Web of Science ®Google Scholar
• Oswald J, Boxberger S, Jorgensen B, et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 2004; 22: 377–84
   PubMed Web of Science ®Google Scholar
• Koc ON, Gerson SL, Cooper BW, et al. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol 2000; 18: 307–16
   PubMed Web of Science ®Google Scholar
• Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 2002; 99: 8932–7
   PubMed Web of Science ®Google Scholar
• Giordano A, Galderisi U, Marino IR. From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J Cell Physiol 2007; 211: 27–35
   PubMed Web of Science ®Google Scholar
• Short B, Brouard N, Occhiodoro-Scott T, et al. Mesenchymal stem cells. Arch Med Res 2003; 34: 565–71
   PubMed Web of Science ®Google Scholar
• Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315–17
   PubMed Web of Science ®Google Scholar
• Haynesworth SE, Baber MA, Caplan AI. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 1992; 13: 69–80
   PubMed Web of Science ®Google Scholar
• Gronthos S, Zannettino AC, Hay SJ, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003; 116: 1827–35
   PubMed Web of Science ®Google Scholar
• Minguell JJ, Fierro FA, Epunan MJ, et al. Nonstimulated human uncommitted mesenchymal stem cells express cell markers of mesenchymal and neural lineages. Stem Cells Dev 2005; 14: 408–14
   PubMed Web of Science ®Google Scholar
• Tondreau T, Lagneaux L, Dejeneffe M, et al. Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 2004; 72: 319–26
   PubMed Web of Science ®Google Scholar
• Woodbury D, Schwarz EJ, Prockop DJ, et al. Adult rat and human bone marrow stromal cells differentiated into neurons. J Neurosci Res 2000; 61: 364–70
   PubMed Web of Science ®Google Scholar
• Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998; 279: 1528–30
   PubMed Web of Science ®Google Scholar
• Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci USA 1999; 96: 10711–16
   PubMed Web of Science ®Google Scholar
• Mezey E, Chandross KJ, Harta G, et al. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000; 290: 1779–82
   PubMed Web of Science ®Google Scholar
• Tse HF, Kwong YL, Chan JK, et al. Angiogenesis in ischaemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation. Lancet 2003; 361: 45–6
   PubMedGoogle Scholar
• Hess D, Li L, Martin M, et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 2003; 21: 763–70
   PubMed Web of Science ®Google Scholar
• Wislet-Gendebien S, Hans G, Leprince P, et al. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 2005; 3: 392–402
   Google Scholar
• Campagnoli C, Roberts I, Kumar S, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001; 98: 2396–402
   PubMed Web of Science ®Google Scholar
• Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7: 211–28
   PubMedGoogle Scholar
• Jiang Y, Jahagirdar BN, Reinhardt LR, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418: 41–9
   PubMed Web of Science ®Google Scholar
• Miura M, Gronthos S, Zhao M, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100: 5807–12
   PubMed Web of Science ®Google Scholar
• Aust L, Delvin SJ, Halvorsen YDC, et al. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 2004; 6: 7–14
   PubMed Web of Science ®Google Scholar
• in ‘tAnker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004; 22: 1338–45
   PubMedGoogle Scholar
• Delo DM, De Coppi P, Bartsh G, Jr, et al. Amniotic fluid and placental stem cells. Methods Enzymol 2006; 419: 426–38
   PubMed Web of Science ®Google Scholar
• Parolini O, Alviano F, Bagnara GP, et al. Isolation and characterization of cells from human term placenta: outcome of the first international workshop on placenta derived stem cells. Stem Cells 2008; 26: 300–11
   PubMed Web of Science ®Google Scholar
• Wexler SA, Donaldson C, Denning-Kendall P, et al. Adult bone marrow is a rich source of human mesenchymal ‘stem’ cells but umbilical cord and mobilized adult blood are not. Br J Haematol 2003; 121: 368–74
   PubMed Web of Science ®Google Scholar
• Tondreau T, Meuleman N, Delforge A, et al. Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 2005; 23: 1105–12
   PubMed Web of Science ®Google Scholar
• Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Hematol 2000; 109: 235–42
   PubMed Web of Science ®Google Scholar
• Goodwin HS, Bicknese AR, Chien SN, et al. Multilineage differentiation activity by cells isolated from umbilical cord blood: expression of bone, fat, and neural markers. Biol Blood Marrow Transplant 2001; 7: 581–8
   PubMed Web of Science ®Google Scholar
• Mareschi K, Biasin E, Piacibello W, et al. Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Hematologica 2001; 86: 1099–100
   PubMed Web of Science ®Google Scholar
• Yu M, Xiao Z, Shen L, et al. Mid-trimester fetal blood-derived adherent cells share characteristics similar to mesenchymal stem cells but full-term umbilical cord blood does not. Br J Hematol 2004; 124: 666–75
   PubMed Web of Science ®Google Scholar
• Lee OK, Kuo TK, Chen WM, et al. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004; 103: 1669–75
   PubMed Web of Science ®Google Scholar
• Flores-Figueroa E, Arana-Trejo RM, Gutierrez-Espíndola G, et al. Mesenchymal stem cells in myelodysplastic syndromes: phenotypic and cytogenetic characterization. Leuk Res 2005; 29: 215–24
   PubMed Web of Science ®Google Scholar
• Flores-Figueroa E, Montesinos JJ, Flores-Guzmán P, et al. Functional analysis of myelodisplastic syndrome-derived mesenchymal stem cell. Leuk Res 2008; 32: 1407–16
   PubMed Web of Science ®Google Scholar
• Battula VL, Bareiss PM, Treml S, et al. Human placenta and bone marrow derived MSC cultured in serum-free, b-FGF-containing medium express cell surface frizzled-9 and SSEA-4 and give rise to multilineage differentiation. Differentiation 2007; 75: 279–91
   PubMed Web of Science ®Google Scholar
• Jeffrey DR, Watt I. Imaging hyaline cartilage. Br J Radiol 2003; 76: 777–87
   PubMedGoogle Scholar
• Benjamin M, Ralphs JR. Biology of fibrocartilage cells. Int Rev Cytol 2004; 233: 1–45
   PubMed Web of Science ®Google Scholar
• Tremain N, Korkko J, Ibberson D, et al. MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 2001; 19: 408–18
   PubMed Web of Science ®Google Scholar
• Woodbury D, Reynolds K, Black IB. Adult bone marrow stromal stem cells express germline ectodermal, endodermal and mesodermal genes prior to neurogenesis. J Neurosci Res 2002; 96: 908–17
   Google Scholar
• Deng J, Petersen BE, Steindler DA, et al. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 2006; 24: 1054–4
   PubMed Web of Science ®Google Scholar
• Yang J, Zhou W, Zheng W, et al. Effects of myocardial transplantation of marrow mesenchymal stem cells transfected with vascular endothelial growth factor for the improvement of heart function and angiogenesis after myocardial infarction. Cardiology 2007; 107: 17–29
   PubMed Web of Science ®Google Scholar
• Prockop DJ, Sekiya I, Colter DC. Isolation and characterization of rapidly self-renewing stem cells from cultures of human marrow stromal cells. Cytotherapy 2001; 3: 393–6
   PubMed Web of Science ®Google Scholar
• Tropel P, Noel D, Platet N. Isolation and characterization of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res 2004; 295: 395–406
   PubMed Web of Science ®Google Scholar
• Eslaminejad MB, Nikmahzar A, Taghiyar L, et al. Murine mesenchymal stem cells isolated by low density primary culture system. Dev Growth Differ 2006; 48: 361–70
   PubMed Web of Science ®Google Scholar
• Fehrer C, Laschober G, Lepperdinger G. Aging of murine mesenchymal stem cells. Ann NY Acad Sci 2006; 1067: 235–42
   PubMed Web of Science ®Google Scholar
• Bieback K, Kern S, Kluter H, et al. Critical parameters for isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 2004; 22: 625–34
   PubMed Web of Science ®Google Scholar
• Kogler G, Radke TF, Lefort A, et al. Cytokine production and hematopoiesis supporting activity of cord blood-derived unrestricted somatic stem cells. Exp Hematol 2005; 33: 573–83
   PubMed Web of Science ®Google Scholar
• Gang E, Jeong J, Han S, et al. In vitro endothelial potential of human UC blood-derived mesenchymal stem cells. Cytotherapy 2006; 8: 215–27
   PubMed Web of Science ®Google Scholar
• Soncini M, Vertua E, Gibelli L, et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007; 1: 296–305
   PubMed Web of Science ®Google Scholar
• Miao Z, Jin J, Chen L, et al. Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 2006; 30: 681–7
   PubMed Web of Science ®Google Scholar
• Majumdar MK, Thiede MA, Mosca JD, et al. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 1998; 176: 57–66
   PubMed Web of Science ®Google Scholar
• Colter DC, Class R, DiGiralomo CM, et al. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 2000; 97: 3213–18
   PubMed Web of Science ®Google Scholar
• Kern S, Eichler H, Stoeve J, et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006; 24: 1294–301
   PubMed Web of Science ®Google Scholar
• Wagner W, Wein F, Seckinger A, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33: 1402–16
   PubMed Web of Science ®Google Scholar
• Yen BL, Huang HI, Chien CC, et al. Isolation of multipotent cells from human term placenta. Stem Cells 2005; 23: 3–9
   PubMed Web of Science ®Google Scholar
• Mets T, Verdonk G. In vitro aging of human bone marrow derived stromal cells. Mech Ageing Dev 1981; 16: 81–9
   PubMed Web of Science ®Google Scholar
• Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 2001; 98: 7841–5
   PubMed Web of Science ®Google Scholar
• Markov V, Kusumi K, Tadesse MG, et al. Identification of cord blood-derived mesenchymal stem/stromal cell populations with distinct growth kinetics, differentiation potentials, and gene expression profiles. Stem Cell Devel 2007; 16: 53–73
   PubMed Web of Science ®Google Scholar
• Bailo M, Soncini M, Vertua E, et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 2004; 78: 1439–48
   PubMed Web of Science ®Google Scholar
• Chang YJ, Shih DT, Tseng CP, et al. Disparate mesenchymal-lineage tendencies in mesenchymal stem cells from human bone marrow and umbilical cord blood. Stem Cells 2006; 24: 679–85
   PubMed Web of Science ®Google Scholar
• Reinisch A, Bartmann C, Rohde E, et al. Humanized system to propagate cord blood-derived multipotent mesenchymal stromal cells for clinical application. Regen Med 2007; 2: 371–82
   PubMed Web of Science ®Google Scholar
• Chang CJ, Yen ML, Chen YC, et al. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-γ. Stem Cells 2006; 24: 2466–77
   PubMed Web of Science ®Google Scholar
• Portmann-Lanz CB, Shoeberlein A, Huber A, et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 2006; 194: 664–73
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li C, Jiang X, et al. Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34+ cells. Exp Hematol 2004; 32: 657–64
   PubMed Web of Science ®Google Scholar
• Bernardo ME, Emons JA, Karperien M, et al. Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources. Connect Tissue Res 2007; 48: 132–40
   PubMed Web of Science ®Google Scholar
• Blondheim NR, Levy YS, Ben-Zur T, et al. Human mesenchymal stem cells express neural genes suggesting a neural predisposition. Stem Cell Devel 2006; 15: 141–64
   PubMed Web of Science ®Google Scholar
• Buzanska L, Machaj EK, Zablocka B, et al. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 2002; 115: 2131–8
   PubMed Web of Science ®Google Scholar