Age-dependent neuroectodermal differentiation capacity of human mesenchymal stromal cells: limitations for autologous cell replacement strategies

References

• Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002;20:530–41.
   PubMed Web of Science ®Google Scholar
• Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001;98:2615–25.
   PubMed Web of Science ®Google Scholar
• Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, . Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 2000;164:247–56.
   PubMed Web of Science ®Google Scholar
• Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000;61:364–70.
   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;69:908–17.
   PubMed Web of Science ®Google Scholar
• Black IB, Woodbury D. Adult rat and human bone marrow stromal stem cells differentiate into neurons. Blood Cells Mol Dis 2001;27:632–6.
   PubMed Web of Science ®Google Scholar
• Deng W, Obrocka M, Fischer I, Prockop DJ. In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem Biophys Res Commun 2001;282:148–52.
   PubMed Web of Science ®Google Scholar
• Tondreau T, Lagneaux L, Dejeneffe M, Massy M, Mortier C, Delforge A, . Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Diff Res Biol Div 2004;72:319–26.
   Google Scholar
• D’Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Science 2004;117:2971–81.
   PubMed Web of Science ®Google Scholar
• Mezey E, Key S, Vogelsang G, Szalayova I, Lange GD, Crain B. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci USA 2003;100:1364–9.
   PubMed Web of Science ®Google Scholar
• Dezawa M, Kanno H, Hoshino M, Cho H, Matsumoto N, Itokazu Y, . Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest 2004;113:1701–10.
   PubMed Web of Science ®Google Scholar
• Tatard VM, D’Ippolito G, Diabira S, Valeyev A, Hackman J, McCarthy M, . Neurotrophin-directed differentiation of human adult marrow stromal cells to dopaminergic-like neurons. Bone 2007;40:360–73.
   PubMed Web of Science ®Google Scholar
• Lee J, Elkahloun AG, Messina SA, Ferrari N, Xi D, Smith CL, . Cellular and genetic characterization of human adult bone marrow-derived neural stem-like cells: a potential antiglioma cellular vector. Cancer Res 2003;63:8877–89.
   PubMed Web of Science ®Google Scholar
• Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, . Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 2004;117:4411–22.
   PubMed Web of Science ®Google Scholar
• Fu L, Zhu L, Huang Y, Lee TD, Forman SJ, Shih CC. Derivation of neural stem cells from mesenchymal stem cells: evidence for a bipotential stem cell population. Stem Cells Develop 2008;17:1109–21.
   PubMed Web of Science ®Google Scholar
• Hermann A, Liebau S, Gastl R, Fickert S, Habisch HJ, Fiedler J, . Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J Neurosci Res 2006;83:1502–14.
   PubMed Web of Science ®Google Scholar
• Zeng Z, Yuan X, Liu G, Zeng X, Zeng X, Ng H, . Manipulation of proliferation and differentiation of human bone marrow-derived neural stem cells in vitro and in vivo. J Neurosci Res 2007;85:310–20.
   PubMed Web of Science ®Google Scholar
• Bunnell BA, Ylostalo J, Kang SK. Common transcriptional gene profile in neurospheres-derived from pATSCs, pBMSCs, and pNSCs. Biochem Biophys Res Commun 2006;343:762–71.
   PubMed Web of Science ®Google Scholar
• Kang SK, Putnam LA, Ylostalo J, Popescu IR, Dufour J, Belousov A, . Neurogenesis of Rhesus adipose stromal cells. J Cell Sci 2004;117:4289–99.
   PubMed Web of Science ®Google Scholar
• Yang Q, Mu J, Li Q, Li A, Zeng Z, Yang J, . A simple and efficient method for deriving neurospheres from bone marrow stromal cells. Biochem Biophys Res Commun 2008;372:520–4.
   PubMed Web of Science ®Google Scholar
• Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003;33:919–26.
   PubMed Web of Science ®Google Scholar
• Stenderup K, Rosada C, Justesen J, Al-Soubky T, Dagnaes-Hansen F, Kassem M. Aged human bone marrow stromal cells maintaining bone forming capacity in vivo evaluated using an improved method of visualization. Biogerontology 2004;5:107–18.
   PubMed Web of Science ®Google Scholar
• Song L, Tuan RS. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J 2004;18:980–2.
   PubMed Web of Science ®Google Scholar
• Hermann A, Gerlach M, Schwarz J, Storch A. Neuro-restoration in Parkinson's disease by cell replacement and endogenous regeneration. Expert Opin Biol Ther 2004;4:131–43.
   PubMed Web of Science ®Google Scholar
• Lee SH, Lumelsky N, Studer L, Auerbach JM, McKay RD. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 2000;18:675–9.
   PubMed Web of Science ®Google Scholar
• Fiedler J, Roderer G, Gunther KP, Brenner RE. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J Cell Biochem 2002;87:305–12.
   PubMed Web of Science ®Google Scholar
• Fickert S, Fiedler J, Brenner RE. Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarth Cart 2003;11:790–800.
   PubMed Web of Science ®Google Scholar
• Fickert S, Fiedler J, Brenner RE. Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res Ther 2004;6:R422–32.
   PubMed Web of Science ®Google Scholar
• Bernstein P, Dong M, Graupher S, Corbeil D, Gelinsky M, Gunther KP, . Sox9 expression of alginate-encapsulated chondrocytes is stimulated by low cell density. J Biomed Mat Res 2008. DOI: 10.1002/jbm.a.32308
   Web of Science ®Google Scholar
• Hermann A, Maisel M, Liebau S, Gerlach M, Kleger A, Schwarz J, . Mesodermal cell types induce neurogenesis from adult human hippocampal progenitor cells. J Neurochem 2006;98:629–40.
   PubMed Web of Science ®Google Scholar
• Hermann A, Maisel M, Wegner F, Liebau S, Kim DW, Gerlach M, . Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells (Dayton, Ohio) 2006;24:949–64.
   PubMed Web of Science ®Google Scholar
• Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, . Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 2000;28:31–40.
   PubMed Web of Science ®Google Scholar
• Baerlocher GM, Lansdorp PM. Telomere length measurements in leukocyte subsets by automated multicolor flow-FISH. Cytometry A 2003;55:1–6.
   PubMed Web of Science ®Google Scholar
• Urquidi V, Tarin D, Goodison S. Role of telomerase in cell senescence and oncogenesis. Annu Rev Med 2000;51:65–79.
   PubMed Web of Science ®Google Scholar
• Seshi B, Kumar S, King D. Multilineage gene expression in human bone marrow stromal cells as evidenced by single-cell microarray analysis. Blood Cells Mol Dis 2003;31:268–85.
   PubMed Web of Science ®Google Scholar
• Tremain N, Korkko J, Ibberson D, Kopen GC, DiGirolamo C, Phinney DG. 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
• Bossolasco P, Cova L, Calzarossa C, Rimoldi SG, Borsotti C, Deliliers GL, . Neuro-glial differentiation of human bone marrow stem cells in vitro. Exp Neurol 2005;193:312–25.
   PubMed Web of Science ®Google Scholar
• Corti S, Locatelli F, Strazzer S, Guglieri M, Comi GP. Neuronal generation from somatic stem cells: current knowledge and perspectives on the treatment of acquired and degenerative central nervous system disorders. Curr Gene Ther 2003;3:247–72.
   PubMedGoogle Scholar
• Lu P, Tuszynski MH. Can bone marrow-derived stem cells differentiate into functional neurons?. Exp Neurol 2005;193:273–8.
   PubMed Web of Science ®Google Scholar
• Siddappa R, Licht R, van Blitterswijk C, de Boer J. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 2007;25:1029–41.
   PubMed Web of Science ®Google Scholar
• Reyes M, Verfaillie CM. Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann NY Acad Sci 2001;938:231–3; discussion 3–5.
   PubMed Web of Science ®Google Scholar
• Wenisch S, Trinkaus K, Hild A, Hose D, Herde K, Heiss C, . Human reaming debris: a source of multipotent stem cells. Bone 2005;36:74–83.
   PubMed Web of Science ®Google Scholar
• Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 2008;129:163–73.
   PubMed Web of Science ®Google Scholar
• Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, . A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006;20:857–69.
   PubMed Web of Science ®Google Scholar
• Sauerzweig S, Munsch T, Lessmann V, Reymann KG, Braun H. A population of serum deprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp Cell Res 2009;315:50–66.
   PubMed Web of Science ®Google Scholar
• Colter DC, Sekiya I, Prockop DJ. Identification of a sub-population 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
• Pesce M, Scholer HR. Oct-4: control of totipotency and germ-line determination. Molecular Repro Devel 2000;55:452–7.
   PubMed Web of Science ®Google Scholar
• Pochampally RR, Smith JR, Ylostalo J, Prockop DJ. Serum deprivation of human marrow stromal cells (hMSCs) selects for a subpopulation of early progenitor cells with enhanced expression of OCT-4 and other embryonic genes. Blood 2004;103:1647–52.
   PubMed Web of Science ®Google Scholar
• Joannides A, Gaughwin P, Scott M, Watt S, Compston A, Chandran S. Postnatal astrocytes promote neural induction from adult human bone marrow-derived stem cells. J Hematother Stem Cell Res 2003;12:681–8.
   PubMedGoogle Scholar
• Scharstuhl A, Schewe B, Benz K, Gaissmaier C, Buhring HJ, Stoop R. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells (Dayton, Ohio) 2007;25:3244–51.
   PubMed Web of Science ®Google Scholar