Cell and Tissue Biology

, Volume 4, Issue 1, pp 1–13 | Cite as

Characteristics and specific features of new human embryonic stem cell lines

  • T. A. Krylova
  • A. M. Kol’tsova
  • V. V. Zenin
  • O. F. Gordeeva
  • A. S. Musorina
  • T. S. Goryachaya
  • S. A. Shlykova
  • Yu. K. Kamenetskaya
  • G. P. Pinaev
  • G. G. Poljanskaya


Four continuous human embryonic stem cell (ESC) lines (SC1, SC2, SC3, and SC4) isolated from preimplantational blastocysts obtained by artificial fertilization have been described. The cell lines were cultivated on mitotically inactivated human feeder cells. SC1 and SC2 cell lines passed through 150 population doublings, while the SC3 and SC4 cell lines passed through about 120 population doublings, which significantly exceeded Hayflick’s limit. All of these cell lines maintain the high activity of alkaline phosphatase and the expression of transcription factor OCT-4 and cell surface antigens (SSEA-4, TRA-1-60, TRA-1-81), which confirms the status of ESC and human specificity. An immunofluorescent analysis of the expression of antigens that characterize the ectoderm, endoderm, and mesoderm has confirmed the capacity of these cells for pluripotency in all four lines under in vitro conditions. Using PCR analysis, the expression of six genes specific to pluripotent cells, i.e., OCT-4, NANOG, DPPA3/STELLA, TDGF/CRIPTO, and LEFTYA, has been revealed. The correlation between the level of proliferative activity and the character of staining with DNA-bound fluorescent dyes has been found. Hoechst 33342 and PI dyes produced a diffuse staining of nuclei in slowly proliferating cells of the SC1 and SC2 lines. On the contrary, in actively proliferating cells of the SC3 and SC4 lines, a distinct staining of nuclei was observed. Upon changing the cultivation conditions, proliferative activity of the SC3 and SC4 lines decreased and the character of the fluorescent staining became similar to that of the SC1 and SC2 lines. The quality of the fluorescent staining with Hoechst 33342 and propidium iodide reflects the level of proliferation. Possible causes and mechanisms of this peculiarity of human ESCs are discussed.

Key words

continuous human embryonic stem cell lines immunofluorescent analysis expression of genes antibodies fluorescent dyes 


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  1. Addla, S.K., Brown, M.D., Hart, C.A., Ramani, V.A., and Clarke, N.W., Characterization of the Hoechst 33342 Side Population from Normal and Malignant Human Renal Epithelial Cells, Am. J. Physiol. Renal Physiol., 2008, vol. 295, pp. F680–F687.CrossRefPubMedGoogle Scholar
  2. Adewumi, O., Aflatoonian, B., and Ahrlund-Richter, L., Characterization of Human Embryonic Stem Cell Lines by the International Stem Cell Initiative, Nat. Biotech., 2007, vol. 25, pp. 803–806.CrossRefGoogle Scholar
  3. Amit, M., Carpenter, M.K., Inokina, M.S., Chiu, C., Harris, C.P., Waknitz, M.A., Itskovitz-Eldor, J., and Thomson, J.A., Clonally Derived Human Embryonic Stem Cell Lines Maintain Pluripotency and Proliferative Potential for Prolonged Periods of Culture, Dev. Biol., 2000, vol. 227, pp. 271–278.CrossRefPubMedGoogle Scholar
  4. Amit, M., Shariki, C., Margulets, V., and Itskovitz-Eldor, J., Feeder and Serum Free Culture of Human Embryonic Stem Cells, Biol. Reprod., 2004, vol. 70, pp. 837–845.CrossRefPubMedGoogle Scholar
  5. Apati, A., Orban, T.I., Varga, N., Nemeth, A., Schamberger, A., Krizsik, V., Erdelyi-Belle, B., Homolya, L., Varady, G., Padanyi, R., Karaszi, E., Kemna, E.W.M., Nemet, K., and Sarkadi, B., High Level Functional Expression of the ABCG2 Multidrug Transporter in Undifferentiated Human Embryonic Stem Cells, Biochim. Biophys. Acta, 2008, vol. 1778, no. 12, pp. 2700–2709.CrossRefPubMedGoogle Scholar
  6. Baharvand, H., Ashtiani, S.K., Taee, A., Massumi, M., Valojerdi, M.R., Yazdi, P.E., Moradi, S.Z., and Farrokhi, A., Generation of New Human Embryonic Stem Cell Lines with Diploid and Triploid Karyotypes, Develop. Growth Differ., 2006, vol. 48, pp. 117–128.CrossRefGoogle Scholar
  7. Baker, D.E.C., Harrison, N.J., Maltby, E., Smith, K., Moore, H.D., Shaw, P.J., Heath, P.R., Holden, H., and Andrews, P.W., Adaptation to Culture of Human Embryonic Stem Cells and Oncogenesis in Vitro, Nature Biotechnol., 2007, vol. 25, pp. 207–215.CrossRefGoogle Scholar
  8. Besser, D., Expression of Nodal, Lefty-a, and Lefty-B in Undifferentiated Human Embryonic Stem Cells Requires Activation of Smad2/3, J. Biol. Chem., 2004, vol. 279, pp. 45076–45084.CrossRefPubMedGoogle Scholar
  9. Bhattacharya, B., Miura, T., Brandenberger, R., Mejido, J., Luo, Y., Yang, A., Joshi, B., Ginis, I., Thies, R., Amit, M., Lyons, I., Condie, B., Itskovitz-Eldor, J., Rao, M., and Puri, R., Gene Expression in Human Embryonic Stem Cell Lines: Unique Molecular Signature, Blood, 2004, vol. 103, pp. 2956–2961.CrossRefPubMedGoogle Scholar
  10. Bigdeli, N., Andersson, M., Strehl, R., Emanuelsson, K., Kilmare, E., Hyllner, J., and Lindahl, A., Adaptation of Human Embryonic Stem Cells to Feeder-Free and Matrix-Free Culture Conditions Directly on Plastic Surfaces, J. Biotechnol., 2008, vol. 133, pp. 146–153.CrossRefPubMedGoogle Scholar
  11. Brandenberger, R., Wei, H., Zhang, S., Lei, S., Murage, J., Fisk, G., Li, Y., Xu, C., Fang, R., Giegler, K., Rao, M., Mandalm, R., Lebkowski, J., and Stanton, L., Transcriptome Characterization Elucidates Signaling Networks that Control Human ES Cell Growth and Differentiation, Nat. Biotechnol., 2004, vol. 22, pp. 707–716.CrossRefPubMedGoogle Scholar
  12. Calhoun, J.D., Rao, R.R., Warrenfeltz, S., Rekaya, R., Dalton, S., Mc Donald, J., and Stice, S., Transcriptional Profiling of Initial Differentiation Events in Human Embryonic Stem Cells, Biochem. Biophys. Res. Commun., 2004, vol. 323, pp. 453–464.CrossRefPubMedGoogle Scholar
  13. Carpenter, M.K., Rosler, E., and Rao, M.S., Characterization and Differentiation of Human Embryonic Stem Cells, Cloning Stem Cells, 2003, vol. 5, pp. 79–88.CrossRefPubMedGoogle Scholar
  14. Chavez, S.L., Meneses, J.J., Nguyen, N.M., Kim, S.K., and Pera, R.A., Characterization of Six New Human Embryonic Stem Cell Lines (HSF7, −8, −9, −10, −12, and −13) Derived under Minimal-Animal Component Conditions, Stem Cells Dev., 2008, vol. 17, pp. 535–546.CrossRefPubMedGoogle Scholar
  15. Cowan, C.A., Klimanskaya, I., McMahon, Jill, Atienza, J., Witmyer, J., Zucker, J.P., Wang, S., Morton, C.C., McMahon, A.P., Powers, D., and Melton, D.A., Derivation of Embryonic Stem-Cell Lines from Human Blastocysts, New Engl. J. Med., 2004, vol. 350, pp. 1353–1356.CrossRefPubMedGoogle Scholar
  16. Draper, J.S., Pigott, C., Thomson, J.A., Andrews, P.W., Surface Antigens of Human Embryonic Stem Cells: Changes upon Differentiation in Culture, J. Anat., 2002, vol. 200,pt. 3, pp. 249–258.CrossRefPubMedGoogle Scholar
  17. Draper, J.S., Smith, K., Gokhale, P., Moore, H.D., Maltby, E., Johnson, J., Meisner, L., Zwaka, T.P., Thomson, J.A., and Andrews, P.W., Recurrement Gain of Chromosomes 17q and 12 in Cultured Human Embryonic Stem Cells, Nat. Biotechnol., 2004, vol. 22, pp. 53–54.CrossRefPubMedGoogle Scholar
  18. Ellerstrom, C., Strehl, R., Moya, K., Andersson, K., Bergh, C., Lundin, K., Hyllner, J., and Semb, H., Derivation of a Xeno-Free Human ES Cell Line, Stem Cells, 2006, vol. 24, pp. 2170–2176.CrossRefPubMedGoogle Scholar
  19. Ezashi, T., Das, P., and Roberts, R.M., Low O2 Tensions and the Prevention of Differentiation of hES Cells, Proc. Natl. Acad. USA, 2006, vol. 102, pp. 4783–4788.CrossRefGoogle Scholar
  20. Forsyth, N.R., Musio, A., Vezzoni, P., Simpson, A.H.R.W., Noble, B.S., and McWhir, J.I.M., Physiologic Oxygen Enhances Human Embryonic Stem Cell Clonal Recovery and Reduces Chromosomal Abnormalities, Cloning Stem Cells, 2006, vol. 8, pp. 16–23.CrossRefPubMedGoogle Scholar
  21. Ginis, I., Luo, Y., Takumi, M., Thies, S., Brandenberger, R., Gerecht-Nir, S., Amit, M., Hoke, A., Carpenter, M.K., Itskovitz-Eldor, J., and Rao, M.S., Differences between Human and Mouse Embryonic Stem Cells, Dev. Biol., 2004, vol. 269, pp. 360–380.CrossRefPubMedGoogle Scholar
  22. Gordeeva, O.F., Krasnikova, N.Yu., Larionova, A.V., Krylova, T.A., Polyanskaya, G.G., Zinov’eva, R.D., Gulyaev, D.V., Pryzhkova, M.V., Nikolsky, N.N., and Khrushchov, N.G., Analysis of Expression of Genes Specific for Pluripotent and Primordial Germ Cells in Human and Mouse Embryonic Stem Cell Lines, Dokl. Ros. Akad. Nauk, 2006, vol. 406, pp. 835–839.Google Scholar
  23. Harrison, N.J., Baker, D., and Andrews, P.W., Culture Adaptation of Embryonic Stem Cells Echoes Germ Cell Malignancy, Int. J. Androl., 2007, vol. 30, pp. 275–281.CrossRefPubMedGoogle Scholar
  24. He, Z., Huang, S., Li, Y., and Zhang, Q., Human Embryonic Stem Cell Lines Preliminarily Established in China, Zhonghua Yi Xue Za Zhi, 2002, vol. 82, pp. 1314–1318.PubMedGoogle Scholar
  25. Heins, N., Englund, M.C., Sjoblom, C., Dahl, U., Tonning, A., Bergh, C., Lindahl, A., Hanson, C., and Semb, H., Derivation, Characterization, and Differentiation of Human Embryonic Stem Cells, Stem Cells, 2004, vol. 22: 367–376.CrossRefPubMedGoogle Scholar
  26. Heins, N., Lindahl, A., Karlsson, U., Rehnstrom, M., Caisander, G., Emanuelsson, K., Hanson, C., Semb, H., Bjorquist, P., Sartipy, P., and Hyllner, J., Clonal Derivation and Characterization of Human Embryonic Stem Cell Lines, J. Biotechnol., 2006, vol. 122, pp. 511–520.CrossRefPubMedGoogle Scholar
  27. Ho, M.M., Ng, A.V., Lam, S., and Hung, J.Y., Side Population in Human Lung Cancer Cell Lines and Tumors Is Enriched with Stem-Like Cancer Cells, Cancer Res., 2007, vol. 67, pp. 4827–4833.CrossRefPubMedGoogle Scholar
  28. Hovatta, O., Mikkola, M., Gertow, K., Stromberg, A., Inzunza, J., Hreinsson, J., Rozell, B., Blennow, E., Andang, M., and Ahrlund-Richter, L., A Culture System using Human Foreskin Fibroblasts as Feeder Cells Allows Production of Human Embryonic Stem Cells, Hum. Reprod., 2003, vol. 18, pp. 1404–1409.CrossRefPubMedGoogle Scholar
  29. Huang, G., Li, W.Q., Chen, R., Chen, Z.G., Zhang, X.M., Mao, F.X., Huang, S.L., Li, S.N., Lahn, B.T., and Xiang, A.P., Establishment and Characterization of Two New Human Embryonic Stem Cell Lines, SYSU-1 and SYSU-2, Chin. Med. J., 2007, vol. 120, pp. 589–594.PubMedGoogle Scholar
  30. Imreh, M.P., Gertow, K., Cederwall, J., Unger, C., Holmberg, K., Szoke, K., Csoregh, L., Fried, G., Dilber, S., Blennow, E., and Ahrlund-Richter, L., In Vitro Culture Conditions Favoring Selection of Chromosomal Abnormalities in Human ES Cells, J. Cell. Biochem., 2006, vol. 99, pp. 508–516.CrossRefPubMedGoogle Scholar
  31. Inzunza, J., Gertow, K., Stromberg, M.A., Matilainen, E., Blennow, E., Skottman, H., Wolbank, S., Ahrlund-Richter., L., and Hovatta, O., Derivation of Human Embryonic Stem Cell Lines in Serum Replacement Medium using Postnatal Human Fibroblasts as Feeder Cells, Stem Cells, 2005, vol. 23, pp. 544–549.CrossRefPubMedGoogle Scholar
  32. Inzunza, J., Sahlen, S., Holmberg, K., Stromberg, A.M., Teerijoki, H., Blennow, E., Hovatta, O., and Malmgren, H., Comparative Genomic Hybridization and Karyotyping of Human Embryonic Stem Cells Reveals the Occurrence of an Isodicentric X Chromosome after Long-Term Cultivation, Mol. Hum. Reprod., 2004, vol. 10, pp. 461–466.CrossRefPubMedGoogle Scholar
  33. James, D., Levine, A.J., Besser, D., and Hemmati-Brivanlou, A., TGFbeta/Activin/Nodal Signaling Is Necessary for the Maintenance of Pluripotency in Human Embryonic Stem Cells, Development, 2005, vol. 132, pp. 1273–1282.CrossRefPubMedGoogle Scholar
  34. Kato, K., Yoshimoto, M., Kato, K., Adachi, S., Yamayoshi, A., Arima, T., Asanoma, K., Kyo, S., Nakahata, T., and Wake, N., Characterization of Side-Population Cells in Human Normal Endometrium, Hum. Reprod., 2007, vol. 22, pp. 1214–1223.CrossRefPubMedGoogle Scholar
  35. Kawanabe, N., Murakami, K., and Takano-Yamamoto, T., The Presence of ABCG2-Dependent Side Population Cells in Human Periodontal Ligaments, Biochem. Biophys. Res. Commun., 2006, vol. 344, pp. 1278–1283.CrossRefPubMedGoogle Scholar
  36. Klimanskaya, I., Chung, Y., Becker, S., Lu, S.J., and Lanza, R., Human Embryonic Stem Cell Lines Derived from Single Blastomeres, Nature, 2006, vol. 444, pp. 481–485.CrossRefPubMedGoogle Scholar
  37. Klimanskaya, I., Chung, Y., Meisner, L., Johnson, J., West, M.D., and Lanza, R., Human Embryonic Stem Cells Derived without Feeder Cells, Lancet, 2005, vol. 365, pp. 1636–1641.CrossRefPubMedGoogle Scholar
  38. Krylova, T.A., Zenin, V.V., Mikhailova, N.A., Pinaev, G.P., Nikolsky, N.N., and Poljanskaia, G.G., Continuous Human Embryonic Stem Cell Lines, Tsitologiia, 2005, vol. 47, no. 1, pp. 121–130.PubMedGoogle Scholar
  39. Krylova, T.A., Zenin, V.V., Musorina, N.S., Baranov, V.S., Bichevaya, N.K., Korsak, V.S., Nikol’skii, N.N., Pinaev, G.P., and Poljanskaya, G.G., Isolation and Characterisation of Continuous Human Embryonic Stem Cell Lines, Tsitologiia, 2003, vol. 5, no. 12, pp. 1172–1178.Google Scholar
  40. Kumar, N., Hinduja, I., Nagvenkar, P., Pillai, L., Jhavery, K., Mukadam, L., Telang, J., Desai, S., Mangoli, V., Mangoli, R., Padgaonkar, S., Kaur, G., Puri, C., and Bhartiya, D., Derivation and Characterization of Two Genetically Unique Human Embryonic Stem Cell Lines on In-house Derived Human Feeder, Stem Cells Dev., 2009, vol. 18, no. 3, pp. 435–445.CrossRefPubMedGoogle Scholar
  41. Liu, Y., Song, Z., Zhao, Y., Qin, H., Cai, J., Zhang, H., Tiaxin, Yu., Jiang, S., Wang, G., Ding, M., and Deng, H., A Novel Chemical-Defined Medium with bFGF and N2 B27 Supplements Supports Undifferentiated Growth in Human Embryonic Stem Cells, Biochem. Biophys. Res. Commun., 2006, vol. 346, pp. 131–139.CrossRefPubMedGoogle Scholar
  42. Loebinger, M.R., Giangreco, A., Groot, K.R., Prichard, L., Allen, K., Simpson, C., Bazley, L., Navani, N., Tibrewal, S., Davies, D., and Janes, S.M., Squamous Cell Cancers Contain a Side Population of Stem-Like Cells That Are Made Chemosensitive by ABC Transporter Blockade, Br. J. Cancer, 2008, vol. 98, pp. 380–387.CrossRefPubMedGoogle Scholar
  43. Lu, J., Hou, R., Booth, C.J., Yang, S-H., and Snyder, M., Defined Culture Conditions of Human Embryonic Stem Cells, Proc. Natl. Acad. USA, 2006, vol. 103, pp. 5688–5693.CrossRefGoogle Scholar
  44. Ludwig, T.E., Levenstein, M.E., Jones, M.J., Berggren, W.T., Mitchen, E.R., Frane, J.L., Crandall, L.J., Daigh, C.A., Conard, K.R., Piekarczyk, M.S., Llanas, R.A., and Thomson, J.A., Derivation of Human Embryonic Stem Cells in Defined Conditions, Nat. Biotechnol., 2006, vol. 24, pp. 185–187.CrossRefPubMedGoogle Scholar
  45. Miyazaki, T., Futaki, S., Hasegawa, K., Sanzen, N., Hayashi, M., Kawase, E., Sekiguchi, K., Nakatsuji, N., and Suemori, H., Recombinant Human Laminin Isoforms Can Support the Undifferentiated Growth of Human Embryonic Stem Cells, Biochem. Biophys. Res. Commun., 2008, vol. 375, pp. 27–32.CrossRefPubMedGoogle Scholar
  46. Nakamura, T., Arai, Y., Umehara, H., Masuhara, M., Kimura, T., Taniguchi, H., Sekimoto, T., Ikawa, M., Yoneda, Y., Okabe, M., Tanaka, S., Shiota, K., and Nakano, N., PGC7/Stella Protects against DNA Demethylation in Early Embryogenesis, Nat. Cell Biol., 2007, vol. 1, pp. 64–71.CrossRefGoogle Scholar
  47. Nikolsky, N.N., Gabai, I.A., and Somova, N.V., Human Embryonic Stem Cells: Problems and Perspectives, Tsitologiia, 2007, vol. 49, no. 7, pp. 529–537.Google Scholar
  48. Oh, S.K., Kim, H.S., Ahn, H.J., Seol, H.W., Kim, Y.Y., Park, Y.B., Yoon, C.J., Kim, D-W., Kim, S.H., and Moon, S.Y., Derivation and Characterization of New Human Embryonic Stem Cell Lines: SNUhES1, SNUhES2, and SNUhES3, Stem Cells, 2005, vol. 23, pp. 211–219.CrossRefPubMedGoogle Scholar
  49. Park, J.H., Kim, S.J., Oh, E.J., Moon, S.Y., Roh, S., Kim, C.G., and Yoon, H.S., Establishment and Maintenance of Human Embryonic Stem Cells on STO, a Permanently Growing Cell Line, Biol. Reprod., 2003, vol. 69, pp. 2007–2014.CrossRefPubMedGoogle Scholar
  50. Plaia, T.W., Josephson, R., Liu, Y., Zeng, X., Orbing, C., Toumadje, A., Brimble, S.N., Sherrer, E.S., Uhl, E.W., Freed, W.J., Schulz, T.C., Maitra, A., Rao, MS., and Auerbach, J.M., Characterization of a New NIH Registered Variant Human Embryonic Stem Cell Line BGO1V: A Tool for Human Embryonic Stem Cell Research, Stem Cells, 2006, vol. 24, pp. 531–546.CrossRefPubMedGoogle Scholar
  51. Pryzhkova, M.V., Lagarkova, M.A., Lyakisheva, A.V., Revazova, E.S., Gnuchev, N.V., and Kiselev, S.L., Isolation of Human Embryonic Stem Cell Lines, Their Analysis and Characterization by Specific Markers, Inform. Byull. Klet. Kult. 2004, vol. 19, pp. 22–25.Google Scholar
  52. Richards, M., Fong, C.Y., Chan, W.K., Wong, P.C., and Bongso, A., Human Feeders Support Prolonged Undifferentiated Growth of Human Inner Cell Masses and Embryonic Stem Cells, Nat. Biotechnol., 2002, vol. 20, pp. 933–936.CrossRefPubMedGoogle Scholar
  53. Richards, M., Tan, S., Fong, C.-Y., Biswas, A., Chan, W-K., and Bongso, A., Comparative Evaluation of Various Human Feeders for Prolonged Undifferentiated Growth of Human Embryonic Stem Cells, Stem Cells, 2003, vol. 21, pp. 546–556.CrossRefPubMedGoogle Scholar
  54. Rosler, E., Fisk, G.J., Ares, X., Irving, J., Miura, T., Rao, M.S., and Carpenter, M.K., Long-Term Culture of Human Embryonic Stem Cells in Feeder-Free Conditions, Dev. Dyn., 2004, vol. 229, pp. 259–274.CrossRefPubMedGoogle Scholar
  55. Sherr, C.J. and DePinho, R.A., Cellular Senescence: Mitotic Clock or Culture Shock?, Cell, 2000, vol. 102, pp. 407–410.CrossRefPubMedGoogle Scholar
  56. Shimano, K., Satake, M., Okaya, A., Kitanaka, J., Kitanaka, N., Takemura, M., Sakagami, M., Terada, N., and Tsujimura, T., Hepatic Oval Cells Have the Side Population Phenotype Defined by Expression of ATP-Binding Cassette Transporter ABCG/BCRP1, Am. J. Pathol., 2003, vol. 163, pp. 3–9.PubMedGoogle Scholar
  57. Skottman, H. and Hovatta, O., Culture Conditions for Human Embryonic Stem Cells, Reproduction, 2006, vol. 132, pp. 691–698.CrossRefPubMedGoogle Scholar
  58. Suda, T., Arai, F., and Hirao, A., Hematopoietic Stem Cells and Their Niche, Trends Immunol., 2005, vol. 26, pp. 426–433.CrossRefPubMedGoogle Scholar
  59. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., and Jones, J.M., Embryonic Stem Cell Lines Derived from Human Blastocysts, Science, 1998, vol. 282, pp. 1145–1147.CrossRefPubMedGoogle Scholar
  60. Tsyji, S., Yoshimoto, K., Takahashi, K., Noda, Y., Nakahata, T., and Heike, T., Side Population Cells Contributed to the Genesis of Human Endometrium, Fertil. Steril., 2008, vol. 90,Suppl. 4, pp. 1528–1537.CrossRefGoogle Scholar
  61. Vallier, L., Alexander, M., and Pedersen, R.A., Activin/Nodal and FGF Pathways Cooperate to Maintain Pluripotency of Human Embryonic Stem Cells, J. Cell. Sci., 2005, vol. 118, pp. 4495–4509.CrossRefPubMedGoogle Scholar
  62. Wang, G., Zhang, H., Zhao, Y., Li, J., Cai, J., Wang, P., Meng, S., Feng, J., Miao, C., Ding, M., Li, D., and Deng, H., Noggin and bFGF Cooperate to Maintain the Pluripotency of Human Embryonic Stem Cells in the Absence of Feeder Layers, Biochem. Biophys. Res. Commun., 2005, vol. 330, pp. 934–942.CrossRefPubMedGoogle Scholar
  63. Wu, C. and Alman, B.A., Side Population Cells in Human Cancer, Cancer Lett., 2008, vol. 268, pp. 1–9.CrossRefPubMedGoogle Scholar
  64. Xiao, L., Yuan, X., and Sharkis, J., Activin A Maintains Self-renewal and Regulates FGF, Wnt and BMP Pathways in Human Embryonic Stem Cells, Stem Cells, 2006, vol.. 24, pp. 1476–1486.CrossRefPubMedGoogle Scholar
  65. Xu, C., Inokuma, M.S., Denham, J., Golds, K., Kundu, P., Gold, J.D., and Carpenter, M.K., Feeder-Free Growth of Undifferentiated Human Embryonic Stem Cells, Nature Biotechnol., 2001, vol. 19, pp. 971–974.CrossRefGoogle Scholar
  66. Xu, R.H., Peck, R.M., Li, D.S., Feng, X., Ludwig, T., and Thomson, J.A., Basic FGF and Suppression of BMP Signaling Sustain Undifferentiated Proliferation of Human ES Cells, Nat. Methods, 2005, vol. 2, pp. 185–190.CrossRefPubMedGoogle Scholar
  67. Yang, S., Lin, G., Tan, Y.Q., Zhou, D., Deng, L.Y., Cheng, D.H., Luo, S.W., Liu, T.C., Zhou, X.Y., Sun, Z., Xiang, Y., Chen, T.J., Wen, J.F., and Lu, G.X., Tumor Progression of Culture-Adapted Human Embryonic Stem Cells during Long-Term Culture, Genes Chromosomes Cancer, 2008, vol. 47, pp. 665–679.CrossRefPubMedGoogle Scholar
  68. Yawazaki, T., Enosawa, S., Tsukiyama, T., and Tokiwa, T., Presence of Side-Population Cells in an Immortalized Nontumorigenic Human Liver Epithelial Cell Line, In Vitro Cell Dev. Biol. Anim., 2008, vol. 44, pp. 6–9.CrossRefGoogle Scholar
  69. Zeng, X., Miura, T., Luo, Y., Bhattacharya, B., Condie, B., Chen, J., Ginis, I., Lyons, I., Mejido, J., Puri, R.K., Rao, M.S., and Freed, W.J., Properties of Pluripotent Human Embryonic Stem Cells BG01 and BG02, Stem Cells, 2004, vol. 22, pp. 292–312.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • T. A. Krylova
    • 1
  • A. M. Kol’tsova
    • 1
  • V. V. Zenin
    • 1
  • O. F. Gordeeva
    • 2
  • A. S. Musorina
    • 1
  • T. S. Goryachaya
    • 1
  • S. A. Shlykova
    • 3
  • Yu. K. Kamenetskaya
    • 3
  • G. P. Pinaev
    • 1
  • G. G. Poljanskaya
    • 1
  1. 1.Institute of CytologyRussian Academy of SciencesSt. PetersburgRussia
  2. 2.Kol’tsov Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia
  3. 3.AVA-PETER CompanySt. PetersburgRussia

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