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

Nature Biotechnology volume 25, pages 803–816 (2007)Cite this article

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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Figure 1: Surface-antigen expression patterns of undifferentiated hES cells.
Figure 2: Expression profiles of the archetypal hES genes, NANOG, POU5F1(OCT4) and TDGF.
Figure 3: Pairwise correlation of expression of NANOG with that of all tested genes.
Figure 4: Two-way cluster analysis of hES cell lines with respect to gene expression.
Figure 5: Two-way cluster analysis of differentiated hES cell lines with respect to gene expression.
Figure 6: XIST expression in male and female hES cell lines.

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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

Authors and Affiliations

  1. Division of Cell Biology and Imaging, UK Stem Cell Bank, 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, Lyn E Healy & Glyn N Stacey

  2. Department of Molecular Biology and Biotechnology, Centre for Stem Cell Biology, The University of Sheffield, Sheffield, S10 2TN, UK

    Behrouz Aflatoonian & Harry D Moore

  3. Department for Laboratory Medicine, Unit for Molecular Embryology, Karolinska Institutet, Stockholm, 141 57, 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. Department of Biomedical Science, Centre for Stem Cell Biology, The University of Sheffield, Sheffield, S10 2TN, UK

    Peter W Andrews, Angela Ford, Paul J Gokhale, Jamie Jackson, Mark Jones, Peter W Andrews, Paul J Gokhale & Peter W Andrews

  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, 3800, Victoria, Australia

    Paul A Bello, Jacqueline L Johnson & Carmel M O'Brien

  9. Department of Genetics, The Hebrew University of Jerusalem, Institute of Life Sciences, Edmond J. Safra Campus, Givat Ram, Jerusalem, 91904, Israel

    Nissim Benvenisty, Barak Blum, Yoav Mayshar & Nissim Benvenisty

  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, 20892, Maryland, USA

    Kevin G Chen, Rebecca S Hamilton, Barbara S Mallon, Ronald D G Mckay, Kye-Yoon Park, Barbara S Mallon & Ronald D G Mckay

  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, 04609, Maine, 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, 66160, Kansas, USA

    Ivan Damjanov

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

    Jon S Draper, Marina Gertsenstein, Masha Mileikovsky, Andras Nagy & Kristina Vintersten

  17. Department of Biology, and Department of Molecular Embryology, Faculty of Medicine, Masaryk University, Brno, Czech Republic, 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, 3800, Victoria, Australia

    Karin Gertow

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

    Outi Hovatta

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

    Marta P Imreh

  22. Department of Development and Genetics, Uppsala University, SE-7523236, Sweden

    Marta P Imreh

  23. Department of Obstetrics and Gynecology, Center for Human Embryonic Stem Cell Research and Education, Institute for Stem Cell Biology & Regenerative Medicine, 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, 04609, Maine, 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, Utrecht, 3584CT, 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,

    Daisy Manning

  30. 1298 S Mason Road, St. Louis, 63131, Missouri, USA

    Daisy Manning & Daisy Manning

  31. 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

  32. 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

  33. Wolfson Centre for Age-Related Diseases, King's College London, London, SE1 1UL, UK

    Stephen L Minger

  34. Institute for Frontier Medical Sciences, Kyoto University, Kyoto, 606-8507, Japan

    Norio Nakatsuji & Hirofumi Suemori

  35. Department of Biochemical Engineering, King's College London/University College London, Regenerative Medicine Bioprocessing Unit, The Advanced Centre for Biochemical Engineering, University College London, Torrington Place, London, WC1E 7JE, UK

    Minal Patel

  36. 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 & Martin F Pera

  37. 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, 90089-282, California, USA

    Martin F Pera & Martin F Pera

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

    Benjamin E Reubinoff & Tikva Turetsky

  39. Novocell, 111 Riverbend Rd., Athens, 30606, Georgia, USA

    Allan J Robins, Thomas C Schulz & Eric S Sherrer

  40. Developmental Biology Program, The Hospital for Sick Children, TMDT Building, Room 13-305, 101 College Street, Toronto, M5G 1L7, Ontario, Canada

    Janet Rossant & Janet Rossant

  41. Program for Developmental Biology. The Hospital for Sick Children, 555 University Avenue, Toronto, M5G 1X8, Ontario, Canada

    Peter Rugg-Gunn

  42. Stem Cell Center, Lund University, BMC, B10, Klinikgatan 26, Lund, SE-221-84, Sweden

    Henrik Semb & Henrik Semb

  43. Centro de Investigación Príncipe Felipe, Valencia, Spain

    Miodrag Stojkovic

Consortia

The International Stem Cell Initiative

  • Oluseun Adewumi
  • , Behrouz Aflatoonian
  • , Lars Ahrlund-Richter
  • , Michal Amit
  • , Peter W Andrews
  • , Gemma Beighton
  • , Paul A Bello
  • , Nissim Benvenisty
  • , Lorraine S Berry
  • , Simon Bevan
  • , Barak Blum
  • , Justin Brooking
  • , Kevin G Chen
  • , Andre B H Choo
  • , Gary A Churchill
  • , Marie Corbel
  • , Ivan Damjanov
  • , Jon S Draper
  • , Petr Dvorak
  • , Katarina Emanuelsson
  • , Roland A Fleck
  • , Angela Ford
  • , Karin Gertow
  • , Marina Gertsenstein
  • , Paul J Gokhale
  • , Rebecca S Hamilton
  • , Ales Hampl
  • , Lyn E Healy
  • , Outi Hovatta
  • , Johan Hyllner
  • , Marta P Imreh
  • , Joseph Itskovitz-Eldor
  • , Jamie Jackson
  • , Jacqueline L Johnson
  • , Mark Jones
  • , Kehkooi Kee
  • , Benjamin L King
  • , Barbara B Knowles
  • , Majlinda Lako
  • , Franck Lebrin
  • , Barbara S Mallon
  • , Daisy Manning
  • , Yoav Mayshar
  • , Ronald D G Mckay
  • , Anna E Michalska
  • , Milla Mikkola
  • , Masha Mileikovsky
  • , Stephen L Minger
  • , Harry D Moore
  • , Christine L Mummery
  • , Andras Nagy
  • , Norio Nakatsuji
  • , Carmel M O'Brien
  • , Steve K W Oh
  • , Cia Olsson
  • , Timo Otonkoski
  • , Kye-Yoon Park
  • , Robert Passier
  • , Hema Patel
  • , Minal Patel
  • , Roger Pedersen
  • , Martin F Pera
  • , Marian S Piekarczyk
  • , Renee A Reijo Pera
  • , Benjamin E Reubinoff
  • , Allan J Robins
  • , Janet Rossant
  • , Peter Rugg-Gunn
  • , Thomas C Schulz
  • , Henrik Semb
  • , Eric S Sherrer
  • , Henrike Siemen
  • , Glyn N Stacey
  • , Miodrag Stojkovic
  • , Hirofumi Suemori
  • , Jin Szatkiewicz
  • , Tikva Turetsky
  • , Timo Tuuri
  • , Steineke van den Brink
  • , Kristina Vintersten
  • , Sanna Vuoristo
  • , Dorien Ward
  • , Thomas A Weaver
  • , Lesley A Young
  • , Weidong Zhang

  • Project coordination

    • Peter W Andrews

  • Coordination of data collection and analysis

    • Paul J Gokhale

  • Coordination of material distribution and sample collection

    • Lyn E Healy

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

    • Peter W Andrews
    • , Nissim Benvenisty
    • , Barbara S Mallon
    • , Ronald D G Mckay
    • , Martin F Pera
    • , Janet Rossant
    • , Henrik Semb
    •  & Glyn N Stacey

Corresponding author

Correspondence to Peter W Andrews.

Ethics declarations

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.

Supplementary information

Supplementary Fig. 1

Representative flow cytometry data for antigens expressed in the undifferentiated hES cells. (PDF 63 kb)

Supplementary Fig. 2

Histological Review - examples of histological sections from xenograft tumours submitted for analysis in the ISCI study. (PDF 260 kb)

Supplementary Table 1

Antibodies used in the FACS study. (PDF 80 kb)

Supplementary Table 2

Flow Cytometry Data. (XLS 601 kb)

Supplementary Table 3

Gene assayed by Low Density Array based Q-PCR. (PDF 80 kb)

Supplementary Table 4

Summary of gene expression results determined by quantitative PCR using Taqman Low-density arrays. (XLS 917 kb)

Supplementary Table 5

Imprinting Data Summary. (XLS 99 kb)

Supplementary Table 6

Cell lines and sample codes used in the ISCI study. (XLS 60 kb)

Supplementary Table 7

hES Cell Line availability. (PDF 76 kb)

Supplementary Table 8

Imprinted gene expression primers. (XLS 18 kb)

Supplementary Methods (PDF 230 kb)

Supplementary Note (PDF 827 kb)

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The International Stem Cell Initiative. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25, 803–816 (2007). https://doi.org/10.1038/nbt1318

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  • DOI: https://doi.org/10.1038/nbt1318

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