Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Paper
  • Published:

The Polycomb-group gene eed regulates thymocyte differentiation and suppresses the development of carcinogen-induced T-cell lymphomas

Oncogene volume 21, pages 299–306 (2002)Cite this article

Abstract

The mouse Polycomb-group gene, embryonic ectoderm development (eed), appears to regulate cellular growth and differentiation in a developmental and tissue specific manner. During embryogenesis, eed regulates axial patterning, whereas in the adult eed represses proliferation of myeloid and B cell precursors. The present report demonstrates two novel functional activities of eed: alteration of thymocyte maturation and suppression of thymic lymphoma development. Mice that inherit the viable hypomorphic 17Rn51989SB eed allele sustain a partial developmental block at or before the CD4−CD8−CD44−CD25+ stage of thymocyte differentiation. Furthermore, mice that are homozygous or heterozygous for the hypomorphic eed allele have an increased incidence and decreased latency of N-methyl-N-nitrosourea-induced thymic lymphoma compared to wild-type littermates. These findings support the notion that Polycomb-group genes exert pleiotrophic effects dictated by developmental stage and cellular context.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Akasaka T, Kanno M, Balling R, Miesa MA, Taniguchi M, Koseki H . 1996 Development 122: 1513–1522

  • Alkema MJ, Bronk M, Verhoeven E, Otte AP, van't Veer LJ, Berns A, van Lohuizen M . 1997 Genes Dev. 11: 226–240

  • Angel JM, Morizot DC, Richie ER . 1989 J. Natl. Cancer Inst. 81: 1652–1655

  • Angel JM, Morizot DC, Richie ER . 1993 Mol. Carcinog. 7: 151–156

  • Bain G, Engel I, Robanus Maandag E, Hein PJ, te Riele HPJ, Voland JR, Sharp LL, Chun J, Huey B, Pinkel D, Murre C . 1997 Mol. Cell. Biol. 17: 4782–4791

  • Denisenko ON, Bomsztyk K . 1997 Mol. Cell. Biol. 17: 4707–4717

  • Denisenko ON, Shnyreva M, Suzuki H, Bomsztyk K . 1998 Mol. Cell. Biol. 18: 5634–5642

  • Faust C, Lawson KA, Schork NJ, Thiel B, Magnuson T . 1998 Development 125: 4495–4506

  • Faust C, Schumacher A, Holdener B, Magnuson T . 1995 Development 121: 273–285

  • Fehling HJ, Von Boehmer H . 1997 Curr. Opin. Immunol. 9: 263–275

  • Frei JV . 1980 Carcinogenesis 1: 721–723

  • Frei JV, Maitra SC . 1974 Chem. Biol. Interactions 9: 65–69

  • Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A . 1994 J. Immunol. 152: 4783–4792

  • Godfrey DI, Kennedy J, Suda T, Zlotnik A . 1993 J. Immunol. 150: 4244–4252

  • Gomez G, Clarkin KZ, Kraig E, Infante AJ, Richie ER . 2000 Int. Immunol. 12: 263–270

  • Gunster MJ, Staijn DPE, Hamer KM, den Blaauwen DL, de Bruijn D, Alkema JJ, van Lohuizen M, van Driel R, Otte AP . 1997 Mol. Cell. Biol. 17: 2326–2335

  • Gutjahr T, Frei E, Spicer C, Baumgartner S, White RAH, Noll M . 1995 EMBO J. 14: 4296–4306

  • Hunter T . 1991 Cell 64: 249–270

  • Jacobs JJL, Kieboom K, Marino S, DePinho RA, van Lohuizen M . 1999 Nature 397: 164–168

  • Kung AL, Rebel VI, Bronson RT, Ch'ng L-E, Sieff CA, Livingston DM, Yao T-P . 2000 Genes Dev. 14: 272–277

  • Lessard H, Schumacher A, Thorsteinsdottir U, van Lohuizen M, Magnuson T, Sauvageau G . 1999 Genes Dev. 13: 2691–2703

  • Malissen M, Minard K, Mjolsness S, Kronenberg M, Goverman J, Hunkapiller T, Prystowsky MB, Yoshikai Y, Fitch F, Mak TW, Hood L . 1984 Cell 37: 1101–1110

  • Newcomb EW, Steinber JJ, Pellicer A . 1988 Cancer Res. 48: 5514–5521

  • Ng J, Li R, Morgan K, Simon J . 1997 Mol. Cell. Biol. 17: 6663–6672

  • Richie E . 1988 Leukemia Res. 12: 233–242

  • Richie ER, Angel JM, Rinchik EM . 1996 Prog. Clin. Biol. Res. Slaga TJ (ed) Wiley-Liss, Inc.: New York, NY pp. 23–32

    Google Scholar 

  • Rinchik EM, Carpenter DA . 1993 Mamm. Genome 4: 349–353

  • Rinchik EM, Carpenter DA, Selby PB . 1990 Proc. Natl. Acad. Sci. USA 87: 896–900

  • Rodewald H-R, Fehling HJ . 1998 Adv. Immunol. 69: 1–112

  • Romach E, Moore JL, Rummel S, Richie ER . 1994 Carcinogenesis 15: 2275–2280

  • Sathe SS, Harte PJ . 1995 Mech. Dev. 52: 77–87

  • Satijn DPE, Gunster MJ, van der Vlag J, Hamer KM, Schul W, Alkema MJ, Saurin AJ, Freemont PS, van Driel R, Otte AP . 1999 Mol. Cell. Biol. 17: 4105–4113

  • Schumacher A, Faust C, Magnuson T . 1996 Nature 383: 250–253

  • Schumacher A, Lichtarge O, Schwartz S, Magnuson T . 1998 Genomics 54: 79–88

  • Sewalt RG, van der Vlag J, Gunster MJ, Hamer KM, den Blaauwen JL, Staijn DPE, Hendrix T, van Driel R, Otte AP . 1998 Mol. Cell. Biol. 18: 3586–3595

  • Simon J . 1995 Curr. Opin. Cell Biol. 7: 376–385

  • Simon J, Bornemann D, Lunde K, Schwartz C . 1995 Mech. Dev. 53: 197–208

  • Stettner SL, Rummel SA, Conti CJ, Richie ER . 1991 Cancer Res. 51: 737–740

  • Struhl G, Brower D . 1982 Cell 31: 285–292

  • van der Lugt NMT, Domen J, Linders K, van Roon M, Robanus-Maandag E, Riele H, van der Valk M, Deschamps J, Sofroniew M, van Lohuizen M, Berns A . 1994 Genes Dev. 8: 757–769

  • van der Vlag J, Otte AP . 1999 Nature Genet. 23: 474–478

  • van Lohuizen M, Tijms M, Vonchen JW, Schumacher A, Magnuson T, Wientjens E . 1998 Mol. Cell. Biol. 18: 3572–3579

  • Weinberg RA . 1991 Science 254: 1138

  • Winandy S, Wu P, Georgopoulos K . 1995 Cell 83: 289–299

  • Zaidi NH, Allay E, Ayi TC, Li BFL, Dumenco LL, Sy MS, Gerson SL . 1995 Carcinogenesis 16: 1047–1053

Download references

Acknowledgements

This work was supported in part by ACS grant RPG-93-002-04-CN, NIEHS Center Grant ES07784, M.D. Anderson Core Grant CA16672, and a Bruce McMillan, Jr., Fdn. grant to ER Richie; NHGRI grant HG00370 and The Department of Energy BER Program under contract DE-AC 05-96OR22464 with Lockheed Martin Energy Research Corp. to EM Rinchik; and HD24462 to T Magnuson. The authors are grateful to Dr Lezlee Coghlan and Dale Weiss for maintenance of the animal colony at SPRD. We also thank Dr John Repass for PCR analysis, Dr Dennis Johnston for performing the statistical analyses and Carrie McKinley for assistance with manuscript preparation.

Author information

Authors and Affiliations

  1. Department of Carcinogenesis, Science Park-Research Division, The University of Texas, M.D. Anderson Cancer Center, Smithville, 78957, Texas, USA

    Ellen R Richie, Joe M Angel & Marina Holloway

  2. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, 77030, Texas, USA

    Armin Schumacher

  3. Life Sciences Division, Oak Ridge National Laboratory, Oak Ridge, 37831, Tennessee, USA

    Eugene M Rinchik

  4. Department of Genetics, CB 7264, University of North Carolina, Chapel Hill, 27599, North Carolina, USA

    Terry Magnuson

Authors
  1. Ellen R Richie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Armin Schumacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joe M Angel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina Holloway
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eugene M Rinchik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Terry Magnuson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ellen R Richie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richie, E., Schumacher, A., Angel, J. et al. The Polycomb-group gene eed regulates thymocyte differentiation and suppresses the development of carcinogen-induced T-cell lymphomas. Oncogene 21, 299–306 (2002). https://doi.org/10.1038/sj.onc.1205051

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1205051

Keywords

This article is cited by

Search

Advanced search

Quick links