Abstract
Helix–loop–helix (HLH) proteins are essential factors for lymphocyte development and function. One class of HLH proteins, the E-proteins, regulate many aspects of lymphocyte maturation, survival, proliferation, and differentiation. E-proteins are negatively regulated by another class of HLH proteins known as the Id proteins. The Id proteins function as dominant negative inhibitors of E-proteins by inhibiting their ability to bind DNA. Here we discuss the function and regulation of the Id proteins in lymphocyte development.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 50 print issues and online access
$259.00 per year
only $5.18 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Abraham K, Levin S, Marth J, Forbush K, Perlmutter R . 1991 Proc. Natl. Acad. Sci. USA 88: 3977–3981
Alberola-Ila J, Forbush K, Seger R, Krebs E, Perlmutter R . 1995 Nature 373: 620–623
Ardavin C, Wu L, Shortman K . 1993 Nature 362: 761–763
Bain G, Cravatt C, Loomans C, Algerola-Ila J, Hedrick S, Murre C . 2001 Nature Immunol. 2: 165–171
Bain G, Engel I, Maandag ER, te Riele H, Voland J, Sharp L, Chun J, Huey B, Pinkel D, Murre C . 1997a Mol. Cell. Biol. 17: 4782–4791
Bain G, Gruenwald S, Murre C . 1993 Mol. Cell. Biol. 13: 3522–3529
Bain G, Maandag E, Izon D, Amsen D, Kruisbeek A, Weintraub B, Krop I, Schlissel M, Feeney A, van Roon M, van der Valk M, te Riele H, Berns A, Murre C . 1994 Cell 79: 885–892
Bain G, Maandag ER, te Riele H, Feeney A, Sheehy A, Schlissel M, Shinton S, Hardy R, Murre C . 1997b Immunity 6: 145–154
Bain G, Quong M, Soloff R, Hedrick S, Murre C . 1999a J. Exp. Med. 190: 1605–1616
Bain G, Romanow, WJ, Albers K, Havran WL, Murre C . 1999b J. Exp. Med. 189: 289–300
Baker J, Harland R . 1997 Curr. Opin. Gen. Dev. 7: 467–473
Barndt R, Dai M, Zhuang Y . 1999 J. Immunol. 163: 3331–3343
Benezra R, Davis R, Lockshon D, Turner D, Weintraub H . 1990 Cell 61: 49–59
Brunet A, Pouyssegur J . 1997 Essays Biochem. 32: 1–16
Carlyle J, Michie A, Furlonger C, Nakano T, Lenardo M, Paige C, Zuniga-Pflucker J . 1997 J. Exp. Med. 186: 173–182
Chantry D, Turner M, Felmann M . 1989 Eur. J. Immunol. 19: 783–786
Chen B, Han BH, Sun X, Lim RW . 1997 Nucl. Acids Res. 25: 423–430
Christy B, Sanders L, Lau L, Copeland N, Jenkins N, Nathans D . 1991 Proc. Natl. Acad. Sci. USA 88: 1815–1819
Clements J, Boerth N, Lee J, Koretzky G . 1999 Annu. Rev. Immunol. 17: 89–108
Deed RW, Bianchi SM, Atherton GT, Johnston D, Santibanez-Koref M, Murphy JJ, Norton JD . 1992 Oncogene 8: 599–607
Desprez P, Hara E, Bissell MJ, Campisi J . 1995 Mol. Cell. Biol. 15: 3398–3404
Ellis HM, Spann DR, Posakony JW . 1990 Cell 61: 27–38
Engel I, Murre C . 2000 Proc. Natl. Acad. Sci. USA 96: 966–1001
Garrell J, Modolel J . 1990 Cell 61: 39–48
Gartner F, Alt F, Monroe R, Chu M, Sleckman B, Davidson L, Swat W . 1999 Immunity 10: 537–546
Godfrey D, Zlotnik A . 1993 Immunol. Today 14: 547–553
Goldfarb AN, Flores JP, Lewandowska K . 1996 Mol. Immunol 33: 947–956
Gorelik L, Flavell R . 2000 Immunity 12: 171–181
Hagemann D, Troppmair J, Rapp U . 1999 Oncogene 18: 1391–1400
Hardy RR, Carmack CE, Shinton SA, Kemp JD, Hayakawa K . 1991 J. Exp. Med. 173: 1213–1225
Hayashi H, Abdollah S, Qiu Y, Cai J, Xu Y, Grinnell B, Richardson M, Topper J, Gimbrone MJ, Wrana J, Falb D . 1997 Cell 89: 1165–1173
Heemskerk MHM, Blom B, Nolan G, Stegmann APA, Bakker AQ, Weijer K, Res PCM, Spits H . 1997 J. Exp. Med. 186: 1597–1602
Henthorn P, Kiledjian M, Kadesch T . 1990 Science 247: 467–470
Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A . 1999 J. Biol. Chem. 274: 19838–19845
Hu J-S, Olson EN, Kingston RE . 1992 Mol. Cell. Biol. 12: 1031–1042
Ikawa T, Fujimoto S, Kawamoto H, Katsura Y, Yokota Y . 2001 Proc. Natl. Acad. Sci. USA 98: 5164–5169
Ikawa T, Kawamoto H, Fujimoto S, Katsura Y . 1999 J. Exp. Med. 190: 1617–1626
Jacobs Y, Vierra C, Nelson C . 1993 Mol. Cell. Biol. 13: 7321–7333
Jen Y, Weintraub H, Benezra R . 1992 Genes Dev. 6: 1466–1479
Kee B, Murre C . 1998 J. Exp. Med. 188: 699–713
Kee B, Paige C . 1995 Int. Rev. Cytol. 157: 129–179
Kee B, Rivera R, Murre C . 2001 Nature Immunol. 2: 242–247
Kim D, Peng X-C, Sun X-H . 1999 Mol. Cell. Biol. 19: 8240–8253
Kisielow P, Bluthmann J, Staerz UD, Steinmetz M, von Boehmer H . 1988 Nature 333: 742–745
Kleeff J, Ishiwata T, Friess H, Buchler M, Israel M, Korc M . 1998 Cancer Res. 58: 3769–3772
Kondo M, Weissman I, Akashi K . 1997 Cell 91: 661–672
Koni P, Sacca R, Lawton P, Browning J, Ruddle N, Flavell R . 1997 Immunity 6: 491–500
Kreider B, Benezra R, Rovera G, Kadesch T . 1992 Science 255: 1700–1702
Kulkarni A, Connors M, Firestone C, Morse H, Murphy B . 1993 Proc. Natl. Acad. Sci. USA 90: 770–774
Lasorella A, Noseda M, Beyna M, Iavarone A . 2000 Nature 407: 592–598
Lilja H, Kamohara Y, Neuman, T, Demetriou AA, Rozga J . 1999 Mol. Cell Biol. Res. Com. 1: 188–195
Leclercq G, Debacker V, Smedt MD, Plum J . 1996 J. Exp. Med. 184: 325–336
Lee G, Namen A, Gillis S, Ellingsworth L, Kincade P . 1989 J. Immunol. 142: 3875–3883
MacLennan I . 1994 Annu. Rev. Immunol. 12: 117–139
Makris A, Patriotis C, Bear S, Tsichlis P . 1993 J. Virol. 67: 4283–4289
Marshall C . 1995 Cell 80: 179–185
Massague J . 1998 Annu. Rev. Biochem. 67: 753–791
Massari M, Jennings P, Murre C . 1996 Mol. Cell. Biol. 16: 121–129
Matsuzaki Y, Gyotuku J, Ogawa M, Nishikawa G, Katsura Y, Gachelin G, Nakauchi H . 1993 J. Exp. Med. 178: 1283–1292
Mebius R, Rennert P, Weissman I . 1997 Immunity 7: 493–504
Miyazaki T, Lemonnier F . 1998 J. Exp. Med. 188: 715–723
Moldes M, Lasnier F, Feve B, Pairault J, Djian P . 1997 Mol. Cell. Biol. 17: 1796–1804
Morrow M, Mayer E, Perez C, Adlam M, Siu G . 1999 Mol. Immunol. 36: 491–503
Murre C, McCaw PS, Baltimore D . 1989 Cell 56: 777–783
Nakao A, Afrakhte M, Moren A, Nakayama T, Christian J, Heuchel R, Itoh S, Kawabata M, Heldin N, Heldin C, Dijke PT . 1997 Nature 389: 631–635
Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T . 2001 Proc. Natl. Acad. Sci. USA 98: 5868–5873
Nishida E, Gotoh Y . 1993 Trends. Biochem. Sci. 18: 128–131
Nossal GJV . 1994 Cell 76: 229–239
Pages G, Guerin S, Grall D, Bonino F, Smith A, Anjuere F, Auberger P, Pouyssegur J . 1999 Science 286: 1374–1377
Pan L, Sato S, Frederick J, Sun X-H, Zhuang Y . 1999 Mol. Cell. Biol. 19: 5969–5980
Park S, Nolan G, Sun X-H . 1999 J. Exp. Med. 189: 501–508
Patriotis C, Makris A, Bear S, Tsichlis P . 1993 Proc. Natl. Acad. Sci. USA 90: 2251–2255
Patriotis C, Makris A, Chernoff J, Tsichlis, P . 1994 Proc. Natl. Acad. Sci. USA 91: 9755–9759
Pongubala J, Atchison M . 1991 Mol. Cell. Biol. 11: 1040–1047
Quong M, Harris D, Swain S, Murre C . 1999 EMBO J. 18: 6307–6318
Quong MW, Massari ME, Zwart R, Murre C . 1993 Mol. Cell. Biol. 13: 792–800
Res P, Couwenberg F, Vyth-Dreese F, Spits H . 1999 Blood 94: 2647–2657
Riechmann V, Cruchten IV, Sablitzky F . 1994 Nuc. Acids Res. 22: 749–755
Rissoan M, Soumelis V, Kadowaki N, Grouard G, Briere F, Malefty RDW, Liu Y . 1999 Science 283: 1183–1186
Rivera R, Johns C, Quan J, Johnson R, Murre C . 2000 Immunity 12: 17–26
Roberts VJ, Steenbergen R, Murre C . 1993 Proc. Natl. Acad. Sci. USA 90: 7583–7587
Rodewald H, Moingeon P, Lucich J, Dosiou C, Lopez P, Reinherz E . 1992 Cell 69: 139–150
Romanow W, Langerak A, Goebel P, Wolvers-Tettero I, van Dongen J, Feeney A, Murre C . 2000 Mol. Cell 5: 343–353
Salmeron A . 1996 EMBO J. 15: 817–826
Sanchez M, Muench M, Roncarolo M, Lanier L, Phillips J . 1994 J. Exp. Med. 180: 569–576
Sawada S, Littman DR . 1993 Mol. Cell Biol. 13: 5620–5628
Schlissel M, Voronova A, Baltimore D . 1991 Genes Dev. 5: 1367–1376
Seger R, Krebs E . 1995 FASEB J. 9: 726–735
Shen CP, Kadesch T . 1995 Mol. Cell. Biol. 15: 4518–4524
Shoji W, Yamamoto T, Obinata M . 1994 J. Biol. Chem. 269: 5078–5084
Shortman K, Wu L . 1996 Ann. Rev. Immunol. 14: 29–47
Shull M, Ormsby I, Kier A, Powlowski S, Diebold R, Yin M, Allen R, Sidman C, Proetzel G, Calvin D . 1992 Nature 359: 693–699
Spits H, Couwenberg F, Bakker A, Weijer K, Uittenbogaart C . 2000 J. Exp. Med. 192: 1775–1783
Sun X, Copeland N, Jenkins N, Baltimore D . 1991 Mol. Cell. Biol. 11: 5603–5611
Togni PD, Goellner J, Ruddle N, Streeter P, Fick A, Mariathasan S, Smith S, Carlson R, Shornick L, Strauss-Schoenberger J . 1994 Science 264: 703–707
Topiliko P, Schneider-Maunoury S, Levi G, Trembleau A, Gourdji D, Draincourt M, Rao C, Charnay P . 1997 Mol. Endocrin. 12: 107–122
Tournay O, Benezra R . 1996 Mol. Cell. Biol. 16: 2418–2430
von Boehmer H . 1994 Cell 76: 219–228
Wilson R, Kiledjian M, Shen C, Benezra R, Zwollo P, Dymecki S, Desiderio S, Kadesch T . 1991 Mol. Cell. Biol. 11: 6185–6191
Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y . 1997 Mol. Cell. Biol. 17: 7317–7327
Yaswen L, Kulkarni A, Fredrickson T, Mittleman B, Schiffman B, Payne S, Longenecker G, Mozes E, Karlsson S . 1996 Blood 87: 1439–1445
Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S, Nishkawa S, Gruss P . 1999 Nature 397: 702–706
Zhuang Y, Cheng P, Weintraub H . 1996 Mol. Cell. Biol. 16: 2898–2905
Zhuang Y, Soriano P, Weintraub H . 1994 Cell 79: 875–884
Zuniga-Pflucker J, Lenardo M . 1996 Curr. Opin. Immunol. 8: 215–224
Acknowledgements
We would like to thank Drs Barbara Kee, Melanie Quong and Billy Romanow for critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rivera, R., Murre, C. The regulation and function of the Id proteins in lymphocyte development. Oncogene 20, 8308–8316 (2001). https://doi.org/10.1038/sj.onc.1205091
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.onc.1205091
Keywords
This article is cited by
-
Single-cell RNA-sequencing identifies the developmental trajectory of C-Myc-dependent NK1.1− T-bet+ intraepithelial lymphocyte precursors
Mucosal Immunology (2020)
-
A genome-wide regulatory network identifies key transcription factors for memory CD8+ T-cell development
Nature Communications (2013)
-
Stage-specific functions of E-proteins at the β-selection and T-cell receptor checkpoints during thymocyte development
Immunologic Research (2011)
-
Intrinsic inhibition of transcription factor E2A by HLH proteins ABF-1 and Id2 mediates reprogramming of neoplastic B cells in Hodgkin lymphoma
Nature Immunology (2006)
-
Id4
AfCS-Nature Molecule Pages (2006)