Mesenchymal stem cells from bone marrow show a stronger stimulating effect on megakaryocyte progenitor expansion than those from non-hematopoietic tissues

References

• Han ZC, Bellucci S, Caen JP. Megakaryocytopoiesis: Characterization and regulation in normal and pathologic states. Int J Hematol 1991; 54: 3–14
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143–147
   PubMed Web of Science ®Google Scholar
• Conget PA, Minguell JJ. Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 1999; 181: 67–73
   PubMed Web of Science ®Google Scholar
• Chichester CO, Fernández M, Minguell JJ. Extracellular matrix gene expression by human bone marrow stroma and by marrow fibroblasts. Cell Adhes Commun 1993; 1: 93–99
   PubMed Web of Science ®Google Scholar
• Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts. Proc Natl Acad Sci USA 1998; 95: 3908–3913
   PubMed Web of Science ®Google Scholar
• Deans RJ, Moseley AB. Mesenchymal stem cells: Biology and potential clinical uses. Exp Hematol 2000; 28: 875–884
   PubMed Web of Science ®Google Scholar
• Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL. 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
• De Ugarte DA, Alfonso Z, Zuk PA, Elbarbary A, Zhu M, Ashjian P, Benhaim P, Hedrick MH, Fraser JK. Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol Lett 2003; 89: 267–270
   PubMed Web of Science ®Google Scholar
• Cheng L, Qasba P, Vanguri P, Thiede MA. Human mesenchymal stem cells support megakaryocyte and pro-platelet formation from CD34(+) hematopoietic progenitor cells. J Cell Physiol 2000; 184: 58–69
   PubMed Web of Science ®Google Scholar
• Haynesworth SE, Baber MA, Caplan AI. Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: Effects of dexamethasone and IL-1 alpha. J Cell Physiol 1996; 166: 585–592
   PubMed Web of Science ®Google Scholar
• Mbalaviele G, Jaiswal N, Meng A, Cheng L, Van Den Bos C, Thiede M. Human mesenchymal stem cells promote human osteoclast differentiation from CD34+ bone marrow hematopoietic progenitors. Endocrinology 1999; 140: 3736–3743
   PubMed Web of Science ®Google Scholar
• Fan CG, Tang FW, Zhang QJ, Lu SH, Liu HY, Zhao ZM, Liu B, Han ZB, Han ZC. Characterization and neural differentiation of fetal lung mesenchymal stem cells. Cell Transplant 2005; 14: 311–321
   PubMed Web of Science ®Google Scholar
• Lu LL, Liu YJ, Yang SG, Zhao QJ, Wang X, Gong W, Han ZB, Xu ZS, Lu YX, Liu D, Chen ZZ, Han ZC. Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 2006; 91: 1017–1026
   PubMed Web of Science ®Google Scholar
• Feng Y, Zhang L, Xiao ZJ, Li B, Liu B, Fan CG, Yuan XF, Han ZC. An effective and simple expansion system for megakaryocyte progenitor cells using a combination of heparin with thrombopoietin and interleukin-11. Exp Hematol 2005; 33: 1537–1543
   PubMed Web of Science ®Google Scholar
• Mattia G, Milazzo L, Vulcano F, Pascuccio M, Macioce G, Hassan HJ, Giampaolo A. Long-term platelet production assessed in NOD/SCID mice injected with cord blood CD34+ cells, thrombopoietin-amplified in clinical grade serum-free culture. Exp Hematol 2008; 36: 244–252
   PubMedGoogle Scholar
• Chen TW, Yao CL, Chu IM, Chuang TL, Hsieh TB, Hwang SM. Large generation of megakaryocytes from serum-free expanded human CD34+ cells. Biochem Biophys Res Commun 2009; 378: 112–117
   PubMed Web of Science ®Google Scholar
• Angelopoulou M, Novelli E, Grove JE, Rinder HM, Civin C, Cheng L, Krause DS. Cotransplantation of human mesenchymal stem cells enhances human myelopoiesis and megakaryocytopoiesis in NOD/SCID mice. Exp Hematol 2003; 31: 413–420
   PubMed Web of Science ®Google Scholar
• Guillot PV, Gotherstrom C, Chan J, Kurata H, Fisk NM. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007; 25: 646–654
   PubMed Web of Science ®Google Scholar
• Barlow S, Brooke G, Chatterjee K, Price G, Pelekanos R, Rossetti T, Doody M, Venter D, Pain S, Gilshenan K, Atkinson K. Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev 2008; 17: 1095–1107
   PubMed Web of Science ®Google Scholar
• in't Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003; 88: 845–852
   PubMed Web of Science ®Google Scholar
• Hu Y, Liao L, Wang Q, Ma L, Ma G, Jiang X, Zhao RC. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med 2003; 141: 342–349
   PubMed Web of Science ®Google Scholar
• Li G, Zhang XA, Wang H, Wang X, Meng CL, Chan CY, Yew DT, Tsang KS, Li K, Tsai SN, et al. Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: Implication in the migration. Proteomics 2009; 9: 20–30
   PubMed Web of Science ®Google Scholar
• Schöler HR, Dressler GR, Balling R, Rohdewohld H, Gruss P. Oct-4: A germline-specific transcription factor mapping to the mouse t-complex. EMBO J 1990; 9: 2185–2195
   PubMed Web of Science ®Google Scholar
• Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17: 126–140
   PubMed Web of Science ®Google Scholar
• Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113: 643–655
   PubMed Web of Science ®Google Scholar
• Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122: 947–956
   PubMed Web of Science ®Google Scholar
• Gonzalez R, Maki CB, Pacchiarotti J, Csontos S, Pham JK, Slepko N, Patel A, Silva F. Pluripotent marker expression and differentiation of human second trimester Mesenchymal Stem Cells. Biochem Biophys Res Commun 2007; 362: 491–497
   PubMedGoogle Scholar
• Jo CH, Kim OS, Park EY, Kim BJ, Lee JH, Kang SB, Lee JH, Han HS, Rhee SH, Yoon KS. Fetal mesenchymal stem cells derived from human umbilical cord sustain primitive characteristics during extensive expansion. Cell Tissue Res 2008; 334: 423–433
   PubMed Web of Science ®Google Scholar
• Greco SJ, Liu K, Rameshwar P. Functional similarities among genes regulated by OCT4 in human mesenchymal and embryonic stem cells. Stem Cells 2007; 25: 3143–3154
   PubMedGoogle Scholar
• Xie CG, Wang JF, Xiang Y, Jia BB, Qiu LY, Wang LJ, Wang GZ, Huang GP. Marrow mesenchymal stem cells transduced with TPO/FL genes as support for ex vivo expansion of hematopoietic stem/progenitor cells. Cell Mol Life Sci 2005; 62: 2495–2507
   PubMed Web of Science ®Google Scholar
• Zhou XY, Tan MQ. Effect of human thrombopoietin-modified bone marrow mesenchymal stem cells mediated by recombinant adeno-associated virus on megakaryocytopoiesis. Stem Cells Dev 2007; 16: 243–251
   PubMedGoogle Scholar
• Vainchenker W, Deschamps JF, Bastin JM, Guichard J, Titeux M, Breton-Gorius J, McMichael AJ. Two monoclonal antiplatelet antibodies as markers of human megakaryocyte maturation: Immunofluorescent staining and platelet peroxidase detection in megakaryocyte colonies and in in vivo cells from normal and leukemic patients. Blood 1982; 59: 514–521
   PubMed Web of Science ®Google Scholar
• Qiao X, Loudovaris M, Unverzagt K, Walker DE, Smith SL, Martinson J, Schilling M, Lee W, Williams SF, Van Epps DE, Cohen I, Bender JG. Immunocytochemistry and flow cytometry evaluation of human megakaryocytes in fresh samples and cultures of CD34+ cells. Cytometry 1996; 23: 250–259
   PubMedGoogle Scholar
• den Dekker E, van Abel M, van der Vuurst H, van Eys GJ, Akkerman JW, Heemskerk JW. Cell-to-cell variability in the differentiation program of human megakaryocytes. Biochim Biophys Acta 2003; 1643: 85–94
   PubMedGoogle Scholar
• Tomer A. Human marrow megakaryocyte differentiation: Multiparameter correlative analysis identifies von Willebrand factor as a sensitive and distinctive marker for early (2N and 4N) megakaryocytes. Blood 2004; 104: 2722–2727
   PubMed Web of Science ®Google Scholar
• Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 2004; 10: 64–71
   PubMed Web of Science ®Google Scholar
• Bruno E, Miller ME, Hoffman R. Interacting cytokines regulate in vitro human megakaryocytopoiesis. Blood 1989; 73: 671–677
   PubMed Web of Science ®Google Scholar
• Lu L, Briddell RA, Graham CD, Brandt JE, Bruno E, Hoffman R. Effect of recombinant and purified human haematopoietic growth factors on in vitro colony formation by enriched populations of human megakaryocyte progenitor cells. Br J Haematol 1988; 70: 149–156
   PubMed Web of Science ®Google Scholar
• Teramura M, Katahira J, Hoshino S, Motoji T, Oshimi K, Mizoguchi H. Effect of recombinant hemopoietic growth factors on human megakaryocyte colony formation in serum-free cultures. Exp Hematol 1989; 17: 1011–1016
   PubMed Web of Science ®Google Scholar
• Briddell RA, Hoffman R. Cytokine regulation of the human burst-forming unit-megakaryocyte. Blood 1990; 76: 516–522
   PubMedGoogle Scholar
• Kaushansky K, O'Hara PJ, Berkner K, Segal GM, Hagen FS, Adamson JW. Genomic cloning, characterization, and multilineage growth-promoting activity of human granulocyte-macrophage colony-stimulating factor. Proc Natl Acad Sci USA 1986; 83: 3101–3105
   PubMed Web of Science ®Google Scholar
• Mazur EM, Cohen JL, Wong GG, Clark SC. Modest stimulatory effect of recombinant human GM-CSF on colony growth from peripheral blood human megakaryocyte progenitor cells. Exp Hematol 1987; 15: 1128–1133
   PubMed Web of Science ®Google Scholar
• Bruno E, Hoffman R. Effect of interleukin 6 on in vitro human megakaryocytopoiesis: Its interaction with other cytokines. Exp Hematol 1989; 17: 1038–1043
   PubMed Web of Science ®Google Scholar
• Briddell RA, Bruno E, Cooper RJ, Brandt JE, Hoffman R. Effect of c-kit ligand on in vitro human megakaryocytopoiesis. Blood 1991; 78: 2854–2859
   PubMed Web of Science ®Google Scholar
• Broudy VC, Lin NL, Kaushansky K. Thrombopoietin (c-mpl ligand) acts synergistically with erythropoietin, stem cell factor, and interleukin-11 to enhance murine megakaryocyte colony growth and increases megakaryocyte ploidy in vitro. Blood 1995; 85: 1719–1726
   PubMed Web of Science ®Google Scholar
• Hagiwara T, Kodama I, Horie K, Kato T, Miyazaki H. Proliferative properties of human umbilical cord blood megakaryocyte progenitor cells to human thrombopoietin. Exp Hematol 1998; 26: 228–235
   PubMedGoogle Scholar
• Kie JH, Yang WI, Lee MK, Kwon TJ, Min YH, Kim HO, Ahn HS, Im SA, Kim HL, Park HY, et al. Decrease in apoptosis and increase in polyploidization of megakaryocytes by stem cell factor during ex vivo expansion of human cord blood CD34+ cells using thrombopoietin. Stem Cells 2002; 20: 73–79
   PubMedGoogle Scholar
• Bruno S, Gunetti M, Gammaitoni L, Danè A, Cavalloni G, Sanavio F, Fagioli F, Aglietta M, Piacibello W. In vitro and in vivo megakaryocyte differentiation of fresh and ex-vivo expanded cord blood cells: Rapid and transient megakaryocyte reconstitution. Haematologica 2003; 88: 379–387
   PubMed Web of Science ®Google Scholar
• Kaushansky K, Broudy VC, Lin N, Jorgensen MJ, McCarty J, Fox N, Zucker-Franklin D, Lofton-Day C. Thrombopoietin, the Mp1 ligand, is essential for full megakaryocyte development. Proc Natl Acad Sci USA 1995; 92: 3234–3238
   PubMed Web of Science ®Google Scholar
• Lazzari L, Henschler R, Lecchi L, Rebulla P, Mertelsmann R, Sirchia G. Interleukin-6 and interleukin-11 act synergistically with thrombopoietin and stem cell factor to modulate ex vivo expansion of human CD41+ and CD61+ megakaryocytic cells. Haematologica 2000; 85: 25–30
   PubMed Web of Science ®Google Scholar