Growth Kinetics of Human Mesenchymal Stem Cells from Bone Marrow and Umbilical Cord Blood

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1 Brief Communication Acta Haematol 2004;112: DOI: / Received: December 16, 2002 Accepted after revision: May 12, 2004 Growth Kinetics of Human Mesenchymal Stem Cells from Bone Marrow and Umbilical Cord Blood Tae Jin Kang a Jung-Eun Yeom a Hye Jung Lee a Seung Hye Rho b Hoon Han c Gue-Tae Chae a Departments of a Pathology and b Microbiology, College of Medicine, The Catholic University of Korea, c Research Institute of Biotechnology, HistoStem Corporation, Seoul, Republic of Korea Bone marrow (BM) is a rich source of human mesenchymal stem cells (MSCs). MSCs were first identified by Friedenstein et al. [1], who demonstrated that when BM is plated in fetal bovine serum (FBS)-containing medium, colonies of adherent fibroblast-like cells develop that differentiate into bone and adipocytes. The cells were referred to as MSCs or mesenchymal progenitor cells, because of their ability to differentiate into a variety of nonhematopoietic cells. Since then, several investigators have shown that these cells can also differentiate into chondrocytes, adipocytes, osteocytes and myocytes [2 5]. MSCs have recently been shown to have the potential to serve as effective vehicles for cell therapy, gene therapy and immunotherapy [6, 7]. Umbilical cord blood (UCB) has been utilized for human hematopoietic stem cell transplantation as an alternative source to BM [8]. MSCs are adult stem cells, present in most tissues. Although the presence of hematopoietic stem cells in UCB is well known, that of MSCs has not been fully evaluated. However, recent research has shown that UCB is also a source of human MSCs [9]. Nevertheless, the presence of MSCs in UCB is a subject of debate among researchers [10, 11]. The goal of the current study was to determine the growth kinetics of purified human MSCs during subcultivation, and to compare the growth kinetics in cells from BM and UCB. All samples were obtained with the written, informed consent of the donors in accordance with the requirements of the hospital ethics committee. Cord blood harvests (n = 67) were a gift by HistoStem Corp. (Seoul, Korea), and BM samples (n = 7) were from the Catholic Hematopoietic Stem Cell Bank (Catholic Medical Center, Seoul, Korea). The age of cord blood donors ranged between 22 and 35 years, and the median gestational age was 29 years. Cord blood and BM were separated into a low-density fraction (Histo-Paque-1077, Amersham Pharmacia), and mononuclear cells were washed, suspended in culture medium [Dulbecco s modified Eagle s medium containing 20% FBS (Hyclone) and 10% streptomycin-penicillin (Gibco BRL, N.Y., USA)] and seeded at a concentration of 1! 10 8 cells/cm 2. Cultures were maintained at 37 C in a humidified atmosphere containing 5% CO 2 with a change of culture medium every 7 days until the fibroblast-like cells at the base of the flask reached confluence. On reaching confluence, the adherent cells were resuspended using 0.25% trypsin-edta and reseeded at 1! 10 6 cells/flask (first passage). These cells were incubated again until confluence, and were once again trypsinized and reseeded at 1! 10 6 cells/flask (second passage). At the end of the second passage, when the cells reached confluence, they were trypsinized and either cryopreserved or used immediately. ABC Fax karger@karger.ch S. Karger AG, Basel /04/ $21.00/0 Accessible online at: Dr. Gue-Tae Chae Department of Pathology, College of Medicine, The Catholic University of Korea 505 Banpo-Dong, Seocho-Gu Seoul, (Republic of Korea) Tel , Fax , guetae@catholic.ac.kr

2 Fig. 1. A Growth curves of human MSC cultures from UCB at passages 3, 4 and 5 (P3, P4 and P5, respectively). At each passage, cells were plated in 6-well plates at 4! 10 3 cells/well, and medium was changed twice weekly. Triplicate cultures were harvested for calculation of cell number. The results represent the mean cell number B SD of 3 preparations. * p! 0.05 compared to passage 3 culture. B Comparison of growth curves of human MSC cultures from UCB (n = 3) and BM (n = 3) at passage 3. MSCs from UCB and BM, respectively, were plated in 6-well plates at 4! 10 3 cells/well. Triplicate cultures were harvested for calculation of cell number. The results represent the mean cell number B SD from one representative experiment. * p! 0.05 compared to MSCs from UCB. Statistical analyses were performed using Student s t test. To determine growth kinetics of MSCs from UCB and BM, MSCs were seeded in 6-well plates at 4! 10 3 cells/ well. Every 2 days for 12 days, triplicate cultures were trypsinized and counted on a hemocytometer. For the measurement of growth kinetics of serially passaged cultures, at each passage, MSCs were harvested for calculation of cell number, by the same method. Growth kinetics of MSCs from UCB were measured at passages 3, 4 and 5, and compared with those of MSCs from BM. Cells were allowed to divide for 12 days, with medium changes occurring twice weekly. Figure 1 shows the growth curves obtained at passages 3, 4 and 5 and illustrates the similarities and differences of MSC growth characteristics between UCB and BM. At each passage, MSC growth curves show an initial lag phase of 2 4 days. This was followed by a log phase in which the MSCs divided at exponential rates for 6 10 days, depending on the passage from which the cells were derived. With increasing passage number, the MSC growth rates were slower and the number of cells generated by the end of 12 days in culture was reduced (fig. 1A). MSCs from BM show the same results (data not shown). MSC cultures from BM grew at faster rates and generated significantly more cells by the end of the 12-day growth period as compared to cultures from UCB (fig. 1B). In contrast to our finding that MSCs could be isolated from UCB, it was reported recently that it was not possible to isolate MSCs from UCB [10, 11]. It is likely that this discrepancy is due to factors such as the difference in culture conditions and the very low frequency of MSCs in UCB, among others. It might be significant that the number of total mononuclear cells varies in different cord blood units. The total number of mononuclear cells in the cord blood units that were used in this study ranged from 0.5! 10 8 to 5! MSCs were isolated in the cord blood units that averaged a total of 4! 10 8 mononuclear cells. However, the cord blood units with 1.2! 10 8 mononuclear cells showed poor colony formation, so we could not find MSCs in Growth Kinetics of Human Mesenchymal Stem Cells Acta Haematol 2004;112:

3 Fig. 2. Photomicrographs showing MSCs from UCB. A Primary cultures of MSCs contain a heterogeneous population. B Confluent UCB-derived MSCs, displaying homogeneous fibroblastoid cells. C, D Adipogenic differentiation is visually apparent by the accumulation of lipid vacuoles (C) that stained with oil red O (D) after 14 days of induction. Original magnification! Acta Haematol 2004;112: Kang/Yeom/Lee/Rho/Han/Chae

4 them. Therefore, we hypothesize that the total number of mononuclear cells in a cord blood unit is one of the important factors for the successful isolation of MSCs. We sought to establish the morphological differences of MSCs derived from cord blood in a time-dependent manner. Five of 67 cultured UCB harvests had fibroblastlike cells morphologically distinguishable from other adherent cells. However, in contrast to UCB, all our BM samples (n = 7) produced MSCs. MSCs were cultured from the Ficoll fraction of mononuclear cells from UCB in an enriched medium containing 20% FBS. UCBderived mononuclear cells, when in culture, gave rise to adherent cells which exhibited fibroblast-like morphology and remained as a monolayer in vitro. Primary cultures of MSCs contained a heterogeneous population (fig. 2A). After 28 days, MSC culture appeared morphologically as a homogenous population of fibroblastoid cells (fig. 2B). UCB-derived adherent cells expressed CD13, CD29, CD44, CD59, CD90 and CD105 (SH2), but did not express CD14, CD34 and CD45, found on hematopoietic precursors. The lack of expression of CD14, CD34 and CD45 suggested that cultures were depleted of hematopoietic cells. To confirm that the isolated cells were MSCs, they were cultured in adipogenic media and differentiated into adipocytes. At the end of passage 3, when UCB-derived MSCs were treated with adipogenic media, cells were differentiated into adipocytes, which was apparent by the accumulation of lipid-containing vacuoles (fig. 2C) as detected by microscopy after staining with oil red O (fig. 2D). Cells containing lipid vacuoles were gradually observed after 1 week. Our results suggest that although it is difficult to isolate MSCs from UCB and while MSCs from UCB proliferate slowly in vitro in comparison to those from BM, UCB could be regarded as a source of MSCs for experimental and clinical needs. Further studies are needed to establish rapid and easy methods for isolation of MSCs from UCB. Acknowledgment This study was supported by a grant of the Korea Health 21 R&D Project, Ministry of Health and Welfare, Republic of Korea (01- PJ10-PG8-01EC ). References 1 Friedenstein AJ, Gorskaja JF, Kalugina NN: Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976;4: Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP: Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997;64: 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: 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: Nakamura T, Shiojima S, Hirai Y, Iwama T, Tsuruzoe N, Hirasawa A, Katsuma S, Tsujimoto G: Temporal gene expression changes during adipogenesis in human mesenchymal stem cells. Biochem Biophys Res Commun 2003; 303: Prockop DJ: Marrow stromal cells as stem cells for nonhematopoietic tissue. Science 1997;276: Jorgensen C, Djouad F, Apparailly F, Noel D: Engineering mesenchymal stem cells for immunotherapy. Gene Ther 2003;10: Lewis ID, Almeida-Porada G, Du J, Lemischka IR, Moore KA, Zanjani ED, Verfaillie CM: Umbilical cord blood cells capable of engrafting in primary, secondary, and tertiary xenogeneic hosts are preserved after ex vivo culture in a noncontact system. Blood 2001;97: Erices A, Conget P, Minguell JJ: Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000;109: Mareschi K, Biasin E, Piacibello W, Aglietta M, Madon E, Fagioli F: Isolation of human mesenchymal stem cells: Bone marrow versus umbilical cord blood. Haematologica 2001;86: Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM: Adult bone marrow is a rich source of human mesenchymal stem cells but umbilical cord and mobilized adult blood are not. Br J Haematol 2003;121: Growth Kinetics of Human Mesenchymal Stem Cells Acta Haematol 2004;112:

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