DOI: 10.1073/pnas.2235735100. Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors

Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors

10.1073/pnas.2235735100

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Remarkably little is known about the transcriptional profiles of human embryonic stem (ES) cells or the molecular mechanisms that underlie their pluripotency. To identify commonalties among the transcriptional profiles of different human pluripotent cells and to search for clues into the genesis of human germ cell tumors, we compared the expression profiles of human ES cell lines, human germ cell tumor cell lines and tumor samples, somatic cell lines, and testicular tissue samples by using cDNA microarray analysis. Hierarchical cluster analysis of gene expression profiles showed that the five independent human ES cell lines clustered tightly together, reflecting highly similar expression profiles. The gene expression patterns of human ES cell lines showed many similarities with the human embryonal carcinoma cell samples and more distantly with the seminoma samples. We identified 895 genes that were expressed at significantly greater levels in human ES and embryonal carcinoma cell lines than in control samples. These genes are candidates for involvement in the maintenance of a pluripotent, undifferentiated phenotype.

Bibliography

Sperger, J. M., Chen, X., Draper, J. S., Antosiewicz, J. E., Chon, C. H., Jones, S. B., Brooks, J. D., Andrews, P. W., Brown, P. O., & Thomson, J. A. (2003). Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proceedings of the National Academy of Sciences, 100(23), 13350â13355.

Authors 10

Jamie M. Sperger (first)
Xin Chen (additional)
Jonathan S. Draper (additional)
Jessica E. Antosiewicz (additional)
Chris H. Chon (additional)
Sunita B. Jones (additional)
James D. Brooks (additional)
Peter W. Andrews (additional)
Patrick O. Brown (additional)
James A. Thomson (additional)

References 55 Referenced 519

10.1038/292154a0
10.1073/pnas.78.12.7634
10.1002/j.1460-2075.1989.tb08393.x
10.1016/S0092-8674(00)81769-9
10.1101/gad.966002
10.1006/dbio.1997.8777
10.1002/(SICI)1520-6408(1996)19:1<51::AID-DVG6>3.0.CO;2-#
10.1101/gad.9.21.2635
10.1074/jbc.271.38.23126
10.1101/gad.1020502
10.1101/gad.224503
10.1016/S0092-8674(03)00393-3
10.1016/S0092-8674(03)00392-1
10.1016/0012-1606(92)90174-F
10.1101/gad.12.13.2048
10.1126/science.282.5391.1145
10.1126/science.1072530
10.1126/science.1073823
10.1016/S0012-1606(03)00256-2
Stevens, L. C. (1967) J. Natl. Cancer Inst. 38, 549-552.6025005 / J. Natl. Cancer Inst. (1967)
10.1016/B978-1-4831-9953-5.50005-6
10.1016/0092-8674(92)90317-6
Andrews, P. W. (1988) Biochim. Biophys. Acta 948, 17-36.3293662 / Biochim. Biophys. Acta (1988)
10.1159/000474691
Skakkebaek, N. E. (1972) Lancet 2, 516-517.4115573 / Lancet (1972)
Pierce, G. B. (1974) Am. J. Pathol. 77, 103-118.4447121 / Am. J. Pathol. (1974)
10.1634/stemcells.20-4-329
Andrews P. W. & Damjanov I. (1994) in Atlas of Human Tumor Cell Lines eds. Hay R. J. Park J.-G. & Gazdar A. (Academic London) pp. 443-476. (10.1016/B978-0-12-333530-2.50021-6)
Andrews, P. W., Damjanov, I., Simon, D., Banting, G., Carlin, C., Dracopoli, N. C. & Fogh, J. (1984) Lab. Invest. 50, 147-162.6694356 / Lab. Invest. (1984)
10.1002/ijc.2910400309
10.1111/j.1432-0436.1989.tb00602.x
Bronson, D. L., Andrews, P. W., Vessella, R. L. & Fralley, E. E. (1983) in Cold Spring Harbor Conferences on Cell Proliferation, eds. Silver, L. M., Martin, G. R. & Strickland, S. (Cold Spring Harbor Lab. Press, Plainview, NY), Vol. 10, pp. 597-605. / Cold Spring Harbor Conferences on Cell Proliferation (1983)
Teshima, S., Shimosato, Y., Hirohashi, S., Tome, Y., Hayashi, I., Kanazawa, H. & Kakizoe, T. (1988) Lab. Invest. 59, 328-336.2842544 / Lab. Invest. (1988)
10.1002/ijc.2910260304
10.1002/ijc.2910290507
Bronson, D. L., Andrews, P. W., Solter, D., Cervenka, J., Lange, P. H. & Fraley, E. E. (1980) Cancer Res. 40, 2500-2506.7388807 / Cancer Res. (1980)
10.1002/1097-0142(19850601)55:11<2584::AID-CNCR2820551110>3.0.CO;2-B
10.1006/dbio.2000.9912
10.1038/35021093
10.1038/35000501
10.1073/pnas.95.25.14863
10.1073/pnas.091062498
10.1002/(SICI)1521-1878(199809)20:9<722::AID-BIES5>3.0.CO;2-I
10.1038/74199
10.1016/S0925-4773(02)00242-3
10.1038/nature00927
10.1093/nar/gkg014
10.1038/ng1045
10.1038/nbt761
Atkin, N. B. & Baker, M. C. (1982) Lancet 2, 1349. / Lancet (1982)
10.1038/sj.onc.1203950
10.1038/sj.onc.1206302
10.1016/S0960-9822(01)00144-0
10.1634/stemcells.21-1-111
10.1038/nbt788

Dates

Type	When
Created	21 years, 9 months ago (Nov. 16, 2003, 3:42 p.m.)
Deposited	3 years, 4 months ago (April 25, 2022, 9:37 p.m.)
Indexed	1 month ago (Aug. 2, 2025, 1:09 a.m.)
Issued	21 years, 10 months ago (Oct. 31, 2003)
Published	21 years, 10 months ago (Oct. 31, 2003)
Published Online	21 years, 10 months ago (Oct. 31, 2003)
Published Print	21 years, 9 months ago (Nov. 11, 2003)

Funders 0

None

BibTeX

@article{Sperger_2003, title={Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors}, volume={100}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.2235735100}, DOI={10.1073/pnas.2235735100}, number={23}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Sperger, Jamie M. and Chen, Xin and Draper, Jonathan S. and Antosiewicz, Jessica E. and Chon, Chris H. and Jones, Sunita B. and Brooks, James D. and Andrews, Peter W. and Brown, Patrick O. and Thomson, James A.}, year={2003}, month=oct, pages={13350–13355} }

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