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Characterization of human embryonic stem cell lines by the International Stem Cell Initiative

Nature Biotechnology volume 25, pages 803816 (2007) | Download Citation

Abstract

The International Stem Cell Initiative characterized 59 human embryonic stem cell lines from 17 laboratories worldwide. Despite diverse genotypes and different techniques used for derivation and maintenance, all lines exhibited similar expression patterns for several markers of human embryonic stem cells. They expressed the glycolipid antigens SSEA3 and SSEA4, the keratan sulfate antigens TRA-1-60, TRA-1-81, GCTM2 and GCT343, and the protein antigens CD9, Thy1 (also known as CD90), tissue-nonspecific alkaline phosphatase and class 1 HLA, as well as the strongly developmentally regulated genes NANOG, POU5F1 (formerly known as OCT4), TDGF1, DNMT3B, GABRB3 and GDF3. Nevertheless, the lines were not identical: differences in expression of several lineage markers were evident, and several imprinted genes showed generally similar allele-specific expression patterns, but some gene-dependent variation was observed. Also, some female lines expressed readily detectable levels of XIST whereas others did not. No significant contamination of the lines with mycoplasma, bacteria or cytopathic viruses was detected.

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Acknowledgements

The International Stem Cell Initiative was sponsored and supported by the International Stem Cell Forum. Additional support from individual participants, and for elements of the project, was also provided by: A*STAR; Academy of Sciences of the Czech Republic; The Academy of Finland; Applied Biosystems; Axordia Ltd.; Bayer; Biotechnology and Biological Sciences Research Council, Centre for Cell Therapy and Tissue Repair, Charles University, Prague, Czech Republic; Chemicon now part of Millipore; Dutch Platform for Tissue Engineering; The Ellison Medical Foundation; Engineering and Physical Sciences Research Council; Embryonic Stem Cell International; GE Healthcare; The Helsinki University Central Hospital Research; Invitrogen Corporation; The Juvenile Diabetes Research Foundation; The Medical Research Council; The Ministry of Education, Culture, Sports, Science, & Technology of Japan; The National Institute for Biological Standards & Control; National Institutes of Health grants 9R24RR021314-04, 5R24RR018405, 5R24RR017498-04; One North East Regional Developmental Agency; The Shelby Cullom Davis Foundation; Stem Cell Network Canada; Stem Cells in Development and Disease; Swedish Research Council. We would like to thank the following for their invaluable assistance with the project: Marga van Rooijen, Hubrecht Laboratory; Christine Pigott, University of Sheffield; Ludmila Ruban, University of Sheffield; Katie Amps, University of Sheffield; Nicholas Jenkins, University of Sheffield; Jeff Jones, WiCell Research Institute; Nancy Block, WiCell Research Institute. We are also grateful to D. Melton and C. Cowan, Harvard University/Howard Hughes Medical Institute, respectively, for making available the human ES cell lines HUES1-17 and to the ES Cell International Pte Ltd. for human ES cell lines HES1-6.

Author information

Affiliations

  1. UK Stem Cell Bank, Division of Cell Biology and Imaging, National Institute for Biological Standards and Control, South Mimms, Herts., EN6 3QG, UK.

    • Oluseun Adewumi
    • , Lorraine S Berry
    • , Roland A Fleck
    • , Lyn E Healy
    • , Hema Patel
    • , Glyn N Stacey
    •  & Lesley A Young
  2. Centre for Stem Cell Biology, Department of Molecular Biology and Biotechnology, The University of Sheffield, Sheffield S10 2TN, UK.

    • Behrouz Aflatoonian
    •  & Harry D Moore
  3. Unit for Molecular Embryology, Department for Laboratory Medicine, Karolinska Institutet, 141 57 Stockholm, Sweden.

    • Lars Ahrlund-Richter
    •  & Karin Gertow
  4. Rambam Medical Center, Technion–Israel Institute of Technology, POB 9602, Haifa 31096, Israel.

    • Michal Amit
    •  & Joseph Itskovitz-Eldor
  5. Centre for Stem Cell Biology, Department of Biomedical Science, The University of Sheffield, Sheffield S10 2TN, UK.

    • Peter W Andrews
    • , Angela Ford
    • , Paul J Gokhale
    • , Jamie Jackson
    •  & Mark Jones
  6. Geneservice Limited, No.2 Cambridge Science Park, Cambridge, CB3 0FE, UK.

    • Gemma Beighton
    • , Simon Bevan
    • , Justin Brooking
    •  & Thomas A Weaver
  7. Cancer Research UK Genotyping Facility, St James's University Hospital, Leeds, LS9 3LP, UK.

    • Gemma Beighton
  8. Stem Cell Sciences Ltd., Building 75, Monash University, Wellington Rd., Clayton, Victoria 3800, Australia.

    • Paul A Bello
    • , Jacqueline L Johnson
    •  & Carmel M O'Brien
  9. The Hebrew University of Jerusalem, Institute of Life Sciences, Department of Genetics, Edmond J. Safra Campus, Givat Ram, Jerusalem 91904, Israel.

    • Nissim Benvenisty
    • , Barak Blum
    •  & Yoav Mayshar
  10. Matrix Technologies, Thermo Fisher Scientific, Unit 2 Lower Meadow Road, Handforth, SK9 3LP, UK.

    • Justin Brooking
  11. NIH Stem Cell Unit, Bldg 35/2B-213, MSC 3703, National Institutes of Health, 9000 Rockville Pike, Bethesda, Maryland 20892, USA.

    • Kevin G Chen
    • , Rebecca S Hamilton
    • , Barbara S Mallon
    • , Ronald D G Mckay
    •  & Kye-Yoon Park
  12. Bioprocessing Technology Institute, 20 Biopolis Way, #06-01 Centros, Singapore 138668.

    • Andre B H Choo
    •  & Steve K W Oh
  13. The Jackson Laboratory, 600 Main Street, Bar Harbor, Maine 04609, USA.

    • Gary A Churchill
    • , Benjamin L King
    • , Jin Szatkiewicz
    •  & Weidong Zhang
  14. Department of Surgery, University of Cambridge, Addenbrookes Hospital, Hills Road, Cambridge, CB2 2XY, UK.

    • Marie Corbel
    • , Roger Pedersen
    •  & Peter Rugg-Gunn
  15. Department of Pathology, The University of Kansas, School of Medicine, 3901 Rainbow Blvd., Kansas City, Kansas 66160, USA.

    • Ivan Damjanov
  16. Samuel Lunenfeld Research Institute, Room 881, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario, Canada, M5G 1X5.

    • Jon S Draper
    • , Marina Gertsenstein
    • , Masha Mileikovsky
    • , Andras Nagy
    •  & Kristina Vintersten
  17. Department of Biology, Faculty of Medicine, Masaryk University, Brno, Czech Republic, and Department of Molecular Embryology, Institute of Experimental Medicine, Academy of Sciences of the Czech Republic, Brno, Czech Republic.

    • Petr Dvorak
    •  & Ales Hampl
  18. Cellartis AB, Arvid Wallgrens Backe 20, 413 46, Göteborg, Sweden.

    • Katarina Emanuelsson
    •  & Johan Hyllner
  19. Monash Immunology and Stem Cell Laboratories (MISCL), Level 3, STRIP–Building 75, Monash University, Clayton, Victoria, 3800 Australia.

    • Karin Gertow
  20. Karolinska Institutet, Dept. of Clinical Science, Intervention and Technology, Div. of Obstetrics/Gynecology, Karolinska University Hospital, Huddinge, SE-141 86 Stockholm, Sweden.

    • Outi Hovatta
  21. Department of Laboratory Medicine, Clinical Research Centre, Karolinska Institutet, 141 57 Stockholm, Sweden.

    • Marta P Imreh
  22. Uppsala University, Department of Development and Genetics, SE-7523236, Sweden.

    • Marta P Imreh
  23. Center for Human Embryonic Stem Cell Research and Education, Institute for Stem Cell Biology & Regenerative Medicine, Department of Obstetrics and Gynecology, Stanford University, Palo Alto, California USA.

    • Kehkooi Kee
    • , Renee A Reijo Pera
    •  & Henrike Siemen
  24. The Jackson Laboratory & the Institute for Molecular Biophysics, 600 Main Street, Bar Harbor, Maine 04609, USA.

    • Barbara B Knowles
  25. Institute of Human Genetics, International Centre for Life, Central Parkway, University of Newcastle, Newcastle upon Tyne, NE1 3BZ, UK.

    • Majlinda Lako
    •  & Miodrag Stojkovic
  26. Hubrecht Laboratory, Uppsalalaan 8, 3584CT Utrecht, The Netherlands.

    • Franck Lebrin
    • , Christine L Mummery
    • , Robert Passier
    • , Steineke van den Brink
    •  & Dorien Ward
  27. INSERM UR 525, Faculté de Médecine Pitié-Salpêtrière, Paris, France.

    • Franck Lebrin
  28. WiCell Research Institute, PO Box 7365, Madison, WI 53707-7365, USA.

    • Daisy Manning
    •  & Marian S Piekarczyk
  29. WiCell Research Institute, 1298 S Mason Road, St. Louis, Missouri 63131, USA.

    • Daisy Manning
  30. Laboratory of Embryonic Stem Cell Biology, Monash Institute of Medical Research, Monash University & the Australian Stem Cell Centre, Wellington Road, Clayton 3800, Victoria, Australia.

    • Anna E Michalska
  31. Biomedicum Stem Cell Center, Biomedicum Helsinki, PO Box 63 FIN-00014, University of Helsinki, Helsinki, Finland.

    • Milla Mikkola
    • , Cia Olsson
    • , Timo Otonkoski
    • , Timo Tuuri
    •  & Sanna Vuoristo
  32. Wolfson Centre for Age-Related Diseases, King's College London, London SE1 1UL, UK.

    • Stephen L Minger
  33. Institute for Frontier Medical Sciences, Kyoto University, Kyoto 606-8507, Japan.

    • Norio Nakatsuji
    •  & Hirofumi Suemori
  34. King's College London/University College London, Regenerative Medicine Bioprocessing Unit, The Advanced Centre for Biochemical Engineering, Department of Biochemical Engineering, University College London, Torrington Place, London, WC1E 7JE, UK.

    • Minal Patel
  35. Centre for Reproduction and Development, Monash Institute of Medical Research, Monash University & the Australian Stem Cell Centre, Wellington Road, Clayton 3800, Victoria, Australia.

    • Martin F Pera
  36. Center for Stem Cell and Regenerative Medicine, Keck School of Medicine, University of Southern California, c/o Zilkha Neurogenetic Institute, Room 543, 1501 San Pablo Street, Los Angeles, California 90089-282, USA.

    • Martin F Pera
  37. Hadassah Human Embryonic Stem Cell Research Center, The Goldyne Savad Institute of Gene Therapy & The Department of Obstetrics and Gynecology, Hadassah University Medical Center, Ein Kerem POB 12000 Jerusalem 91120, Israel.

    • Benjamin E Reubinoff
    •  & Tikva Turetsky
  38. Novocell, 111 Riverbend Rd., Athens, Georgia 30606, USA.

    • Allan J Robins
    • , Thomas C Schulz
    •  & Eric S Sherrer
  39. Developmental Biology Program, The Hospital for Sick Children, TMDT Building, Room 13-305, 101 College Street, Toronto, Ontario, M5G 1L7, Canada.

    • Janet Rossant
  40. Program for Developmental Biology. The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada.

    • Peter Rugg-Gunn
  41. Stem Cell Center, Lund University, BMC, B10, Klinikgatan 26, SE-221-84 Lund, Sweden.

    • Henrik Semb
  42. Centro de Investigación Príncipe Felipe, Valencia, Spain.

    • Miodrag Stojkovic

Consortia

  1. The International Stem Cell Initiative

    Project coordination

    Coordination of data collection and analysis

    Coordination of material distribution and sample collection

    The scientific management of the ISCI project was provided by a steering committee comprising

Authors

    Competing interests

    P.W.A. and B.B.K. receive royalty payments from the Wistar Institute in connection with the nonexclusive commercial licenses issued by the Institute for several of its monoclonal antibodies used in the present study (B.B.K.: SSEA1, SSEA3, SSEA4; P.W.A.: TRA antibodies). A.J.R., T.S. and E.S. are employees of Novocell, Inc., which is a for-profit company involved in commercializing human ES cell–derived products.

    Corresponding author

    Correspondence to Peter W Andrews.

    Supplementary information

    PDF files

    1. 1.

      Supplementary Fig. 1

      Representative flow cytometry data for antigens expressed in the undifferentiated hES cells.

    2. 2.

      Supplementary Fig. 2

      Histological Review - examples of histological sections from xenograft tumours submitted for analysis in the ISCI study.

    3. 3.

      Supplementary Table 1

      Antibodies used in the FACS study.

    4. 4.

      Supplementary Table 3

      Gene assayed by Low Density Array based Q-PCR.

    5. 5.

      Supplementary Table 7

      hES Cell Line availability.

    6. 6.

      Supplementary Methods

    7. 7.

      Supplementary Note

    Excel files

    1. 1.

      Supplementary Table 2

      Flow Cytometry Data.

    2. 2.

      Supplementary Table 4

      Summary of gene expression results determined by quantitative PCR using Taqman Low-density arrays.

    3. 3.

      Supplementary Table 5

      Imprinting Data Summary.

    4. 4.

      Supplementary Table 6

      Cell lines and sample codes used in the ISCI study.

    5. 5.

      Supplementary Table 8

      Imprinted gene expression primers.

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    DOI

    https://doi.org/10.1038/nbt1318

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