Differential expression of biofunctional GM1 and GM3 gangliosides within the plastic-adherent multipotent mesenchymal stromal cell population

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
• 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
• Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation. 1974;17:331–40.
   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
• Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31:890–6.
   PubMed Web of Science ®Google Scholar
• Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol. 2002;30:783–91.
   PubMed Web of Science ®Google Scholar
• Tondreau T, Meuleman N, Delforge A, Dejeneffe M, Leroy R, Massy M, . 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
• Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res. 2005;306:330–5.
   PubMed Web of Science ®Google Scholar
• Pozzobon M, Piccoli M, Ditadi A, Bollini S, Destro R, Andre-Schmutz I, . Mesenchymal stromal cells can be derived from bone marrow CD133+ cells: implications for therapy. Stem Cells Dev. 2009;18:497–510.
   Google Scholar
• Delorme B, Ringe J, Gallay N, Le Vern Y, Kerboeuf D, Jorgensen C, . Specific plasma membrane protein pheno-type of culture-amplified and native human bone marrow mesenchymal stem cells. Blood. 2008;111:2631–5.
   PubMed Web of Science ®Google Scholar
• Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM. Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood. 2007;109:4245–8.
   PubMed Web of Science ®Google Scholar
• McNiece I. Subsets of mesenchymal stromal cells. Cytotherapy. 2007;9:301–2.
   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
• Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 2001;19:180–92.
   PubMed Web of Science ®Google Scholar
• Tormin A, Brune JC, Olsson E, Valcich J, Neuman U, Olofsson T, . Characterization of bone marrow-derived mesenchymal stromal cells (MSC) based on gene expression profiling of functionally defined MSC subsets. Cytotherapy. 2009;11:114–28.
   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
• Egana JT, Fierro FA, Krüger S, Bornhäuser M, Huss R, Lavandero S, . Use of human mesenchymal cells to improve vascularization in a mouse model for scaffold-based dermal regeneration. Tissue Eng Part A. 2009;15:1191–200.
   Google Scholar
• Ryser MF, Ugarte F, Thieme S, Bornhäuser M, Roesen-Wolff A, Brenner S. mRNA transfection of CXCR4-GFP fusion simply generated by PCR results in efficient migration of primary human mesenchymal stem cells. Tissue Eng Part C Methods. 2008;14:179–84.
   Google Scholar
• Alberti K, Davey RE, Onishi K, George S, Salchert K, Seib FP, . Functional immobilization of signaling proteins enables control of stem cell fate. Nat Methods. 2008;5:645–50.
   PubMed Web of Science ®Google Scholar
• Kwak DH, Yu K, Kim SM, Lee DH, Kim SM, Jung JU, . Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells. Exp Mol Med. 2006;38:668–76.
   Google Scholar
• Gomez-Mouton C, Abad JL, Mira E, Lacalle RA, Gallardo E, Jimenez-Baranda S, . Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA. 2001;98:9642–7.
   PubMed Web of Science ®Google Scholar
• Pike LJ. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J Lipid Res. 2006;47:1597–8.
   PubMed Web of Science ®Google Scholar
• Fujita A, Cheng J, Hirakawa M, Furukawa K, Kusunoki S, Fujimoto T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol Biol Cell. 2007;18:2112–22.
   PubMed Web of Science ®Google Scholar
• Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1:31–9.
   PubMed Web of Science ®Google Scholar
• Sharma P, Sabharanjak S, Mayor S. Endocytosis of lipid rafts: an identity crisis. Semin Cell Dev Biol. 2002;13:205–14.
   PubMedGoogle 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
• Jeong JA, Ko KM, Park HS, Lee J, Jang C, Jeon CJ, . Membrane proteomic analysis of human mesenchymal stromal cells during adipogenesis. Proteomics. 2007;7:4181–91.
   PubMed Web of Science ®Google Scholar
• Roche S, Delorme B, Oostendorp RA, Barbet R, Caton D, Noel D, . Comparative proteomic analysis of human mesenchymal and embryonic stem cells: towards the definition of a mesenchymal stem cell proteomic signature. Proteomics. 2009;9:223–32.
   PubMed Web of Science ®Google Scholar
• Cantu L, Corti M, Brocca P, Del Favero E. Structural aspects of ganglioside-containing membranes. Biochim Biophys Acta. 2009;1788:202–8.
   Google Scholar
• Freund D, Bauer N, Boxberger S, Feldmann S, Streller U, Ehninger G, . Polarization of human hematopoietic progenitors during contact with multipotent mesenchymal stromal cells: effects on proliferation and clonogenicity. Stem Cells Dev. 2006;15:815–29.
   PubMed Web of Science ®Google Scholar
• Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhäuser M, . Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells. 2004;22:377–84.
   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
• Weigmann A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA. 1997;94:12425–30.
   PubMed Web of Science ®Google Scholar
• Holmgren J, Lonnroth I. Oligomeric structure of cholera toxin: characteristics of the H and L subunits. J Gen Micro-biol. 1975;86:49–65.
   PubMedGoogle Scholar
• Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, . Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun. 2001;288:413–9.
   PubMed Web of Science ®Google Scholar
• Vyas KA, Patel HV, Vyas AA, Schnaar RL. Segregation of gangliosides GM1 and GD3 on cell membranes, isolated membrane rafts, and defined supported lipid monolayers. Biol Chem. 2001;382:241–50.
   Google Scholar
• Röper K, Corbeil D, Huttner WB. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol. 2000;2:582–92.
   PubMed Web of Science ®Google Scholar
• Corbeil D, Röper K, Fargeas CA, Joester A, Huttner WB. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2001;2:82–91.
   PubMed Web of Science ®Google Scholar
• Fargeas CA, Joester A, Missol-Kolka E, Hellwig A, Huttner WB, Corbeil D. Identification of novel Prominin-1/ CD133 splice variants with alternative C-termini and their expression in epididymis and testis. J Cell Sci. 2004;117:4301–11.
   PubMed Web of Science ®Google Scholar
• Fargeas CA, Fonseca A-V, Huttner WB, Corbeil D. Prominin-1 (CD133): from progenitor cells to human diseases. Future Lipidol. 2006;1:213–25.
   Web of Science ®Google Scholar
• Karbanova J, Missol-Kolka E, Fonseca AV, Lorra C, Janich P, Hollerova H, . The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J Histochem Cytochem. 2008;56:977–93.
   PubMed Web of Science ®Google Scholar
• Hakomori S. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J Biol Chem. 1990;265:18713–6.
   PubMed Web of Science ®Google Scholar
• Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Ko K, . Effects of gangliosides on the differentiation of human mesenchymal stem cells into osteoblasts by modulating epidermal growth factor receptors. Biochem Biophys Res Commun. 2008;371:866–71.
   Google Scholar
• Hardy RR, Kishimoto T, Hayakawa K. Differentiation of B cell progenitors in vitro: generation of surface IgM+ B cells, including Ly-1 B cells, from Thy-1- asialoGMl+ cells in newborn liver. Eur J Immunol. 1987;17:1769–74.
   Google Scholar
• Freund D, Oswald J, Feldmann S, Ehninger G, Corbeil D, Bornhäuser M. Comparative analysis of proliferative potential and clonogenicity of MACS-immunomagnetic isolated CD34+ and CD133+ blood stem cells derived from a single donor. Cell Prolif. 2006;39:325–32.
   PubMed Web of Science ®Google Scholar
• Janich P, Corbeil D. GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett. 2007;581:1783–7.
   PubMed Web of Science ®Google Scholar
• Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–89.
   PubMed Web of Science ®Google Scholar
• Ruiz SA, Chen CS. Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells. 2008;26:2921–7.
   PubMed Web of Science ®Google Scholar
• Bauer N, Fonseca AV, Florek M, Freund D, Jaszai J, Bornhäuser M, . New insights into the cell biology of hematopoietic progenitors by studying Prominin-1 (CD133). Cells Tissues Organs. 2008;188:127–38.
   PubMed Web of Science ®Google Scholar
• Fonseca AV, Bauer N, Corbeil D. The stem cell marker CD133 meets the endosomal compartment: new insights into the cell division of hematopoietic stem cells. Blood Cells Mol Dis. 2008;41:194–5.
   Google Scholar
• Ziulkoski AL, Andrade CM, Crespo PM, Sisti E, Trindade VM, Daniotti JL, . Gangliosides of myelosupportive stroma cells are transferred to myeloid progenitors and are required for their survival and proliferation. Biochem J. 2006;394:1–9.
   Google Scholar
• Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol. 2009;11:303–11.
   PubMed Web of Science ®Google Scholar
• Mora JR, von Andrian UH. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 2006;27:235–43.
   PubMed Web of Science ®Google Scholar
• Barreiro O, de la Fuente H, Mittelbrunn M, Sanchez-Madrid F. Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol Rev. 2007;218:147–64.
   PubMedGoogle Scholar
• Rusnati M, Urbinati C, Tanghetti E, Dell’Era P, Lortat-Jacob H, Presta M. Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc Natl Acad Sci USA. 2002;99:4367–72.
   PubMed Web of Science ®Google Scholar
• Miljan EA, Bremer EG. Regulation of growth factor receptors by gangliosides. Sci STKE. 2002;2002:re15.
   Google Scholar
• Sorice M, Longo A, Garofalo T, Mattei V, Misasi R, Pavan A. Role of GM3-enriched microdomains in signal transduction regulation in T lymphocytes. Glycoconj J. 2004;20:63–70.
   PubMed Web of Science ®Google Scholar