Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro

References

• Schaffler A, Buchler C, . Concise review. Adipose tissue-derived stromal cells: basic and clinical implications for novel cell-based therapies. Stem Cells 2007;25:818–27.
   PubMed Web of Science ®Google Scholar
• Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, . Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279–95.
   PubMed Web of Science ®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
• Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, . Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 2003;48:418–29.
   PubMed Web of Science ®Google Scholar
• Timper K, Seboek D, Eberhardt M, Linscheid P, Christ-Crain M, Keller U, . Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 2006;341:1135–40.
   PubMed Web of Science ®Google Scholar
• Seo MJ, Suh SY, Bae YC, Jung JS. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun 2005;328:258–64.
   PubMed Web of Science ®Google Scholar
• Safford KM, Hicok KC, Safford SD, Halvorsen YD, Wilkison WO, Gimble JM, . Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun 2002;294:371–9.
   PubMed Web of Science ®Google Scholar
• Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, . Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004;109:656–63.
   PubMed Web of Science ®Google Scholar
• Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, . Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 2004;113:585–94.
   PubMed Web of Science ®Google Scholar
• Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 2003;5:362–9.
   PubMed Web of Science ®Google Scholar
• Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249–60.
   PubMed Web of Science ®Google Scholar
• Niemeyer P, Vohrer J, Schmal H, Kasten P, Fellenberg J, Suedkamp N, . Survival of human mesenchymal stromal cells from bone marrow and adipose tissue after xenogenic transplantation in immunocompetent mice. Cytotherapy 2008;108:784–95.
   PubMed Web of Science ®Google Scholar
• Shahdadfar A, Fronsdal K, Haug T, Reinholt FP, Brinchmann JE. In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells 2005;23:1357–66.
   PubMed Web of Science ®Google Scholar
• McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, . The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 2006;24:1246–53.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rey E, Gonzalez MA, Rico L, Buscher D, Delgado M. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 2009;587:929–39.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rey E, Gonzalez MA, Varela N, O'Valle F, Hernandez-Cortes P, Rico L, . Human adipose-derived mesenchymal stem cells reduce inflammatory and T-cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis. September 21st2009.
   Google Scholar
• Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006;24:2582–91.
   PubMed Web of Science ®Google Scholar
• Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 2006;8:559–61.
   PubMed Web of Science ®Google Scholar
• Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, . Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129:118–29.
   PubMed Web of Science ®Google Scholar
• Lazarus HCP, Devine S, McCarthy P, Holland K, Moseley A, Bacigalupo A. Role of mesenchymal stem cells (MSC) in allogeneic transplantation: early phase I clinical results. Blood 2000;96:392A
   Google Scholar
• Spees JL, Gregory CA, Singh H, Tucker HA, Peister A, Lynch PJ, . Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol Ther 2004;9:747–56.
   PubMed Web of Science ®Google Scholar
• Heiskanen A, Satomaa T, Tiitinen S, Laitinen A, Mannelin S, Impola U, . N-glycolylneuraminic acid xenoantigen contamination of human embryonic and mesenchymal stem cells is substantially reversible. Stem Cells 2007;25:197–202.
   PubMed Web of Science ®Google Scholar
• Martin MJ, Muotri A, Gage F, Varki A. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 2005;11:228–32.
   PubMed Web of Science ®Google Scholar
• Mackensen A, Drager R, Schlesier M, Mertelsmann R, Lindemann A. Presence of IgE antibodies to bovine serum albumin in a patient developing anaphylaxis after vaccination with human peptide-pulsed dendritic cells. Cancer Immunol Immunother 2000;49:152–6.
   PubMed Web of Science ®Google Scholar
• Selvaggi TA, Walker RE, Fleisher TA. Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 1997;89:776–9.
   PubMed Web of Science ®Google Scholar
• Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, . A new variant of Creutzfeldt–Jakob disease in the UK. Lancet 1996;347:921–5.
   PubMed Web of Science ®Google Scholar
• Kocaoemer A, Kern S, Kluter H, Bieback K. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 2007;25:1270–8.
   PubMed Web of Science ®Google Scholar
• Nimura A, Muneta T, Koga H, Mochizuki T, Suzuki K, Makino H, . Increased proliferation of human synovial mesenchymal stem cells with autologous human serum: comparisons with bone marrow mesenchymal stem cells and with fetal bovine serum. Arthritis Rheum 2008;58:501–10.
   PubMed Web of Science ®Google Scholar
• Schallmoser K, Bartmann C, Rohde E, Reinisch A, Kashofer K, Stadelmeyer E, . Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 2007;47:1436–46.
   PubMed Web of Science ®Google Scholar
• Luttun A, Ross JJ, Verfaillie C, Aranguren XL, Prosper F. Differentiation of multipotent adult progenitor cells into functional endothelial and smooth muscle cells. Curr Protoc Immunol 2000;22:–Unit 22F 29.
   Google Scholar
• Caterson EJ, Nesti LJ, Danielson KG, Tuan RS. Human marrow-derived mesenchymal progenitor cells: isolation, culture expansion, and analysis of differentiation. Mol Biotechnol 2002;20:245–56.
   Google Scholar
• Tholpady SS, Llull R, Ogle RC, Rubin JP, Futrell JW, Katz AJ. Adipose tissue: stem cells and beyond. Clin Plast Surg 2006;33:55–62,vi.
   PubMed Web of Science ®Google Scholar
• Parker AM, Shang H, Khurgel M, Katz AJ. Low serum and serum-free culture of multipotential human adipose stem cells. Cytotherapy 2007;9:637–46.
   PubMed Web of Science ®Google Scholar
• Dahl JA, Duggal S, Coulston N, Millar D, Melki J, Shahdadfar A, . Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int J Dev Biol 2008;52:1033–42.
   PubMed Web of Science ®Google Scholar
• Lendeckel S, Jodicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, . Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg 2004;32:370–3.
   PubMed Web of Science ®Google Scholar
• Mesimaki K, Lindroos B, Tornwall J, Mauno J, Lindqvist C, Kontio R, . Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg 2009;38:201–9.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Samuelsson H, Lonnies L, Sundin M, Ringden O. Generation of immunosuppressive mesenchymal stem cells in allogeneic human serum. Transplantation 2007;84:1055–9.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Cho HH, Kim YJ, Seo SY, Kim HN, Lee JB, . Human adipose stromal cells expanded in human serum promote engraftment of human peripheral blood hematopoietic stem cells in NOD/SCID mice. Biochem Biophys Res Commun 2005;329:25–31.
   PubMed Web of Science ®Google Scholar
• . DIRECTIVE 2001/83/EC of the European Parliament and of the Council on the Community Code Relating to Medicinal Products for Human Use. The European Parliament and of the Council of the Community 2001.
   Google Scholar
• . Guideline on Human Cell-Based Medicinal Products. EMEA, Committee for Human Medicinal Products 2007.
   Google Scholar
• Regulation (EC) No. 726/2004 of the European Parliament and of the Council. Official Journal of the European Union 2004;L136:1–33.
   Google Scholar
• Meuleman N, Tondreau T, Delforge A, Dejeneffe M, Massy M, Libertalis M, . Human marrow mesenchymal stem cell culture: serum-free medium allows better expansion than classical alpha-MEM medium. Eur J Haematol 2006;76:309–16.
   PubMed Web of Science ®Google Scholar
• Mirabet V, Solves P, Minana MD, Encabo A, Carbonell-Uberos F, Blanquer A, . Human platelet lysate enhances the proliferative activity of cultured human fibroblast-like cells from different tissues. Cell Tissue Bank 2008;9:1–10.
   PubMed Web of Science ®Google Scholar
• Niemela SM, Miettinen S, Konttinen Y, Waris T, Kellomaki M, Ashammakhi NA, . Fat tissue: views on reconstruction and exploitation. J Craniofac Surg 2007;18:325–35.
   Google Scholar
• Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC. Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. Proc Natl Acad Sci USA 1998;95:10614–9.
   PubMed Web of Science ®Google Scholar
• Haimi S, Suuriniemi N, Haaparanta AM, Ella V, Lindroos B, Huhtala H, . Growth and osteogenic differentiation of adipose stem cells on PLA/bioactive glass and PLA/beta-TCP scaffolds. Tissue Eng Part A 2009;157:1473–80.
   PubMed Web of Science ®Google Scholar
• Lindroos B, Maenpaa K, Ylikomi T, Oja H, Suuronen R, Miettinen S. Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 2008;368:329–35.
   PubMed Web of Science ®Google Scholar
• Haimi S, Moimas L, Pirhonen E, Lindroos B, Huhtala H, Räty S, . Calcium phosphate surface treatment of bioactive glass causes a delay in early osteogenic differentiation of adipose stem cells. J Biomed Mater Res Part A. ; 91A2:540–547.
   Google Scholar
• Denker AE, Nicoll SB, Tuan RS. Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with transforming growth factor-beta 1. Differentiation 1995;59:25–34.
   PubMed Web of Science ®Google Scholar
• Muller I, Kordowich S, Holzwarth C, Spano C, Isensee G, Staiber A, . Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM. Cytotherapy 2006;8:437–44.
   PubMed Web of Science ®Google Scholar
• Jung J, Moon N, Ahn J, Oh EJ, Kim M, Cho CS, . Mesenchymal stromal cells expanded in human allogenic cord blood serum display higher self-renewal and enhanced osteogenic potential. Stem Cells Dev 2009;184:559–71.
   Google Scholar
• Bieback K, Hecker A, Kocaomer A, Lannert H, Schallmoser K, Strunk D, . Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 2009.
   Google Scholar
• Gstraunthaler G. Alternatives to the use of fetal bovine serum: serum-free cell culture. Altex 2003;20:275–81.
   PubMedGoogle Scholar
• Izadpanah R, Kaushal D, Kriedt C, Tsien F, Patel B, Dufour J, . Long-term in vitro expansion alters the biology of adult mesenchymal stem cells. Cancer Res 2008;68:4229–38.
   PubMed Web of Science ®Google Scholar
• Boquest AC, Shahdadfar A, Fronsdal K, Sigurjonsson O, Tunheim SH, Collas P, . Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell 2005;16:1131–41.
   PubMed Web of Science ®Google Scholar
• Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001;189:54–63.
   PubMed Web of Science ®Google Scholar
• Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, . Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 2005;54:132–41.
   PubMed Web of Science ®Google Scholar
• Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, . Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008;214:413–21.
   PubMed Web of Science ®Google Scholar
• Schilling T, Noth U, Klein-Hitpass L, Jakob F, Schutze N. Plasticity in adipogenesis and osteogenesis of human mesenchymal stem cells. Mol Cell Endocrinol 2007;271:1–17.
   PubMed Web of Science ®Google Scholar
• Liu TM, Martina M, Hutmacher DW, Hui JH, Lee EH, Lim B. Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells 2007;25:750–60.
   PubMed Web of Science ®Google Scholar
• de Girolamo L, Sartori MF, Albisetti W, Brini AT. Osteogenic differentiation of human adipose-derived stem cells: comparison of two different inductive media. J Tissue Eng Regen Med 2007;1s:154–7.
   PubMedGoogle Scholar