Population dynamics of mesenchymal stromal cells during culture expansion

References

• Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, . Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy. 2005;7:393–5.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, . Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.
   PubMed Web of Science ®Google Scholar
• Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970;3:393–403.
   PubMedGoogle Scholar
• Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, . Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol. 1974;2:83–92.
   PubMed Web of Science ®Google Scholar
• Dexheimer V, Mueller S, Braatz F, Richter W. Reduced reactivation from dormancy but maintained lineage choice of human mesenchymal stem cells with donor age. PLoS ONE. 2011;6:e22980.
   Google Scholar
• Phinney DG. Biochemical heterogeneity of mesenchymal stem cell populations: clues to their therapeutic efficacy. Cell Cycle. 2007;6:2884–9.
   PubMed Web of Science ®Google Scholar
• DiGirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. 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. Br J Haematol. 1999;107:275–81.
   PubMed Web of Science ®Google Scholar
• Ho AD, Wagner W, Franke W. Heterogeneity of mesenchymal stromal cell preparations. Cytotherapy. 2008;10:320–30.
   PubMed Web of Science ®Google Scholar
• Wagner W, Ho AD. Mesenchymal stem cell preparations: comparing apples and oranges. Stem Cell Rev. 2007;3: 239–48.
   PubMed Web of Science ®Google Scholar
• Griesche N, Luttmann W, Luttmann A, Stammermann T, Geiger H, Baer PC. A simple modification of the separation method reduces heterogeneity of adipose-derived stem cells. Cells Tissues Organs. 2010;192:106–15.
   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
• Horn P, Bork S, Diehlmann A, Walenda T, Eckstein V, Ho AD, . Isolation of human mesenchymal stromal cells is more efficient by red blood cell lysis. Cytotherapy. 2008;10: 676–85.
   PubMed Web of Science ®Google Scholar
• Buhring HJ, Treml S, Cerabona F, de Zwart P, Kanz L, Sobiesiak M. Phenotypic characterization of distinct human bone marrow-derived MSC subsets. Ann NY Acad Sci. 2009; 1176:124–34.
   PubMed Web of Science ®Google Scholar
• Battula VL, Treml S, Bareiss PM, Gieseke F, Roelofs H, de ZP, . Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica. 2009;94: 173–84.
   PubMed Web of Science ®Google Scholar
• Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci. 2000; 113:1161–6.
   PubMed Web of Science ®Google Scholar
• Delorme B, Ringe J, Pontikoglou C, Gaillard J, Langonne A, Sensebe L, . Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity. Stem Cells. 2009;27:1142–51.
   PubMedGoogle Scholar
• Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells. 2010;28:788–98.
   PubMed Web of Science ®Google Scholar
• Russell KC, Lacey MR, Gilliam JK, Tucker HA, Phinney DG, O'Connor KC. Clonal analysis of the proliferation potential of human bone marrow mesenchymal stem cells as a function of potency. Biotechnol Bioeng. 2011;108:2716–26.
   Google Scholar
• Wagner W. Senescence is heterogeneous in mesenchymal stromal cells: kaleidoscopes for cellular aging. Cell Cycle. 2010;9:2923–4.
   PubMed Web of Science ®Google Scholar
• Hayflick L, Moorhead P.S. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25:585–621.
   PubMed Web of Science ®Google Scholar
• Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp Hematol. 2000;28:707–15.
   PubMed Web of Science ®Google Scholar
• Noer A, Boquest AC, Collas P. Dynamics of adipogenic promoter DNA methylation during clonal culture of human adipose stem cells to senescence. BMC Cell Biol. 2007;8:18–22.
   PubMed Web of Science ®Google Scholar
• Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, . Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS ONE. 2008;5:e2213.
   Google Scholar
• Cholewa D, Stiehl T, Schellenberg A, Bokermann G, Joussen S, Koch C, . Expansion of adipose mesenchymal stromal cells is affected by human platelet lysate and plating density. Cell Transplant. 2011;20:1409–22.
   PubMed Web of Science ®Google Scholar
• Horn P, Bokermann G, Cholewa D, Bork S, Walenda T, Koch C, . Comparison of individual platelet lysates for isolation of human mesenchymal stromal cells. Cytotherapy. 2010;12:888–98.
   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
• Staszewski R. Murphy's law of limiting dilution cloning. Stat Med 1990;9:457–61.
   Google Scholar
• Underwood PA, Bean PA. Hazards of the limiting-dilution method of cloning hybridomas. J Immunol Methods. 1988;107:119–28.
   PubMedGoogle Scholar
• Lietzke R, Unsicker K. A statistical approach to determine monoclonality after limiting cell plating of a hybridoma clone. J Immunol Methods. 1985;76:223–8.
   Google Scholar
• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, . Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.
   PubMed Web of Science ®Google Scholar
• Fraser JK, Wulur I, Alfonso Z, Zhu M, Wheeler ES. Differences in stem and progenitor cell yield in different subcutaneous adipose tissue depots. Cytotherapy. 2007;9:459–67.
   PubMed Web of Science ®Google Scholar
• Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, . 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
• Wagner W, Feldmann RE Jr, Seckinger A, Maurer MH, Wein F, Blake J, . The heterogeneity of human mesenchymal stem cell preparations. Evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol. 2006;34:536–48.
   PubMed Web of Science ®Google Scholar
• Wagner W, Roderburg C, Wein F, Diehlmann A, Frankhauser M, Schubert R, . Molecular and secretory profiles of human mesenchymal stromal cells and their abilities to maintain primitive hematopoietic progenitors. Stem Cells. 2007;10:2638–57.
   Google Scholar
• Wagner W, Wein F, Roderburg C, Saffrich R, Faber A, Krause U, . Adhesion of hematopoietic progenitor cells to human mesenchymal stem cells as a model for cell–cell interaction. Exp Hematol. 2007;35:314–25.
   PubMed Web of Science ®Google Scholar
• Schellenberg A, Lin Q, Schueler H, Koch C, Joussen S, Denecke B, . Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging (Albany NY). 2011;3:873–88.
   PubMedGoogle Scholar
• Koch C, Suschek CV, Lin Q, Bork S, Goergens M, Joussen S, . Specific age-associated DNA methylation changes in human dermal fibroblasts. PLoS ONE. 2011;6:e16679.
   Google Scholar
• Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, . Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–28.
   PubMedGoogle Scholar
• Noel D, Caton D, Roche S, Bony C, Lehmann S, Casteilla L, . Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res. 2008;314:1575–84.
   PubMed Web of Science ®Google Scholar
• Orriss IR, Utting JC, Brandao-Burch A, Colston K, Grubb BR, Burnstock G, . Extracellular nucleotides block bone mineralization in vitro: evidence for dual inhibitory mechanisms involving both P2Y2 receptors and pyrophosphate. Endocrinology. 2007;148:4208–16.
   PubMed Web of Science ®Google Scholar
• Fischer-Valuck BW, Barrilleaux BL, Phinney DG, Russell KC, Prockop DJ, O'Connor KC. Migratory response of mesenchymal stem cells to macrophage migration inhibitory factor and its antagonist as a function of colony-forming efficiency. Biotechnol Lett. 2010;32:19–27.
   Google Scholar
• Sarugaser R, Hanoun L, Keating A, Stanford WL, Davies JE. Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PLoS ONE. 2009; 4:e6498.
   PubMed Web of Science ®Google Scholar
• Peters R, Wolf MJ, van den Broek M, Nuvolone M, Dannenmann S, Stieger B, . Efficient generation of multipotent mesenchymal stem cells from umbilical cord blood in stroma-free liquid culture. PLoS ONE. 2010;5:e15689.
   PubMedGoogle Scholar
• Wagner W, Bork S, Lepperdinger G, Joussen S, Ma N, Strunk D, . How to track cellular aging of mesenchymal stromal cells. Aging (Albany NY). 2010;2:224–30.
   PubMedGoogle Scholar
• Smith JR, Braunschweiger KI. Growth of human embryonic fibroblasts at clonal density: concordance with results from mass cultures. J Cell Physiol. 1979;98:597–601.
   Google Scholar
• Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS, . Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell. 2008;7:335–43.
   PubMed Web of Science ®Google Scholar
• Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 2006;7:14.
   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
• Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Exp Gerontol. 2005;40:926–30.
   PubMed Web of Science ®Google Scholar
• Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells. 2004;22:675–82.
   PubMed Web of Science ®Google Scholar
• Lee S, Park JR, Seo MS, Roh KH, Park SB, Hwang JW, . Histone deacetylase inhibitors decrease proliferation potential and multilineage differentiation capability of human mesenchymal stem cells. Cell Prolif. 2009;42:711–20.
   PubMed Web of Science ®Google Scholar
• Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, . Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell. 2007;6:745–57.
   PubMed Web of Science ®Google Scholar
• Holzwarth C, Vaegler M, Gieseke F, Pfister SM, Handgretinger R, Kerst G, . Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol. 2010;11:11.
   PubMed Web of Science ®Google Scholar
• Lindner U, Kramer J, Behrends J, Driller B, Wendler NO, Boehrnsen F, . Improved proliferation and differentiation capacity of human mesenchymal stromal cells cultured with basement-membrane extracellular matrix proteins. Cytotherapy. 2010;12:992–1005.
   PubMed Web of Science ®Google Scholar
• Bork S, Pfister S, Witt H, Horn P, Korn B, Ho AD, . DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell. 2010;9:54–63.
   PubMed Web of Science ®Google Scholar
• Wright WE, Shay JW. Historical claims and current interpretations of replicative aging. Nat Biotechnol. 2002;20:682–8.
   PubMed Web of Science ®Google Scholar
• Blackburn EH. Telomere states and cell fates. Nature. 2000;408:53–6.
   PubMed Web of Science ®Google Scholar