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The regulation and function of the Id proteins in lymphocyte development

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.

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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

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Acknowledgements

We would like to thank Drs Barbara Kee, Melanie Quong and Billy Romanow for critical reading of the manuscript.

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Correspondence to Richard Rivera.

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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

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