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Id and development

Abstract

During development, it is obvious that enormous multiplication and diversification of cells is required to build a body plan from a single fertilized egg and that these two processes, proliferation and differentiation, must be coordinated properly. Id proteins, negative regulators of basic helix–loop–helix transcription factors, possess the ability to inhibit differentiation and to stimulate proliferation, and are useful molecules for investigating the mechanisms regulating development. In the past few years, our understanding of the roles of Id proteins has been substantially enhanced by the detailed investigation of genetically modified animals. The data have indicated that the functions of Id proteins in vivo are functionally related to those revealed by earlier work in cell culture systems. However, unexpected organs and cell types have also been found to require Id proteins for their normal development. This review looks at the advances made in our understanding of the in vivo functions of Id proteins. The topics discussed include neurogenesis, natural killer cell development, lymphoid organogenesis, mammary gland development and spermatogenesis.

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References

  • Andres-Barquin PJ, Hernandez MC, Israel MA . 2000 Histol. Histopathol. 15: 603–618

  • Bain G, Cravatt CB, Loomans C, Alberola-Ila J, Hedrick SM, Murre C . 1997 Nat. Immunol. 2: 165–171

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

  • Barres BA, Lazar MA, Raff MC . 1994 Development 120: 1097–1108

  • Barton K, Muthusamy N, Fischer C, Ting CN, Walunas TL, Lanier L, Leiden JM . 1998 Immunity 9: 555–563

  • Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H . 1990 Cell 61: 49–59

  • Blom B, Heemskerk MHM, Verschuren MCM, van Dongen JJM, Stegman APA, Bakker AQ, Couwenberg F, Res PCM, Spits H . 1999 EMBO J. 18: 2793–2802

  • Cai L, Morrow EM, Cepko CL . 2000 Development 127: 3021–3030

  • Carlyle JR, Zuniga-Pflucker JC . 1998 Immunol. Rev. 165: 63–74

  • Carson WE, Giri JG, Lindemann MJ, Linett ML, Ahdieh M, Paxton R, Anderson D, Eisenmann J, Grabstein K, Caligiuri MA . 1994 J. Exp. Med. 180: 1395–1403

  • Christy BA, Sanders LK, Lau LF, Copeland NG, Jenkins NA, Nathans D . 1991 Proc. Natl. Acad. Sci. USA 88: 1815–1819

  • De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, Mariathasan S, Smith SC, Carlson R, Shornick LP, Strauss Schoenberger J, Russell JH, Karr R, Chaplin DD . 1994 Science 264: 703–707

  • Duncan M, DiCicco Bloom EM, Xiang X, Benezra R, Chada K . 1992 Dev. Biol. 154: 1–10

  • Duncan MK, Bordas L, Dicicco Bloom E, Chada KK . 1997 Dev. Dyn. 208: 107–114

  • Durand B, Raff M . 2000 Bioessays 22: 64–71

  • Evans SM, O'Brien TX . 1993 Dev. Biol. 159: 485–499

  • Fantl V, Stamp G, Andrews A, Rosewell I, Dickson C . 1995 Genes Dev. 9: 2364–2372

  • Fu Y, Chaplin DD . 1999 Annu. Rev. Immunol. 17: 399–433

  • Futterer A, Mink K, Luz A, Kosco-Vilbois MH, Pfeffer K . 1998 Immunity 9: 59–70

  • Heemskerk MH, Blom B, Nolan G, Stegmann AP, Bakkar AQ, Weijer K, Res PC, Spits H . 1997 J. Exp. Med. 186: 1597–1602

  • Hennighausen L, Robinson GW . 1998 Genes Dev. 12: 449–455

  • Horseman ND, Zhao W, Montecino-Rodriguez E, Tanaka M, Nakashima K, Engle SJ, Smith F, Markoff E, Dorshkind K . 1997 EMBO J. 16: 6926–6935

  • Iavarone A, Garg P, Lasorella A, Hsu J, Israel MA . 1994 Genes Dev. 8: 1270–1284

  • Ikawa T, Kawamoto H, Fujimoto S, Katsura Y . 1999 J. Exp. Med. 190: 1617–1626

  • Ikawa T, Fujimoto S, Kawamoto H, Katsura Y, Yokota Y . 2001 Proc. Natl. Acad. Sci. USA 98: 5164–5169

  • Imada K, Bloom ET, Nakajima H, Horvath-Arcidiacono JA, Udy GB, Davey HW, Leonard WJ . 1998 J. Exp. Med. 188: 2067–2074

  • Inoue T, Shoji W, Obinata M . 1999 Biochem. Biophys. Res. Commun. 266: 147–151

  • Inoue T, Shoji W, Obinata M . 2000 Genes Cells 5: 699–709

  • Jen Y, Weintraub H, Benezra R . 1992 Genes Dev. 6: 1466–1479

  • Jen Y, Manova K, Benezra R . 1996 Dev. Dyn. 207: 235–252

  • Jen Y, Manova K, Benezra R . 1997 Dev. Dyn. 208: 92–106

  • Kim D, Peng XC, Sun XH . 1999 Mol. Cell. Biol. 19: 8240–8253

  • Kondo T, Raff M . 2000a EMBO J. 19: 1998–2007

  • Kondo T, Raff M . 2000b Development 127: 2989–2998

  • Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, Flavell RA . 1997 Immunity 6: 491–500

  • Lasorella A, Iavarone A, Israel MA . 1996 Mol. Cell. Biol. 16: 2570–2578

  • Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A . 2000 Nature 407: 592–598

  • Lee JE . 1997 Curr. Opin. Neurobiol. 7: 13–20

  • Liu X RG, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L . 1997 Genes Dev. 11: 179–186

  • Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH . 2000 Neuron 317–329

  • Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R . 1999 Nature 401: 670–677

  • Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CAJ, Shyamala G, Conneely OM, O'Malley BW . 1995 Genes Dev. 15: 2266–2278

  • Martinsen BJ, Bronner Fraser M . 1998 Science 281: 988–991

  • Massari ME, Murre C . 2000 Mol. Cell. Biol. 20: 429–440

  • Mebius RE, Rennert P, Weissman IL . 1997 Immunity 7: 493–504

  • Mebius RE, Miyamoto T, Christensen J, Domen J, Cupedo T, Weissman IL, Akashi K . 2001 J. Immunol. 166: 6593–6601

  • Mori S, Nishikawa S-I, Yokota Y . 2000 EMBO J. 19: 5772–5781

  • Morrow MA, Mayer EW, Perez CA, Adlam M, Siu G . 1999 Mol. Immunol. 36: 491–503

  • Neuman T, Keen A, Zuber MX, Kristjansson GI, Gruss P, Nornes HO . 1993 Dev. Biol. 160: 186–195

  • Neville MC, Daniel CW . 1987 The mammary gland: development, regulation, and function Plenum Press: New York

    Book  Google Scholar 

  • Norton JD, Deed RW, Craggs G, Sablitzky F . 1998 Trends Cell Biol. 8: 58–65

  • Oakberg EF . 1956 Am. J. Anat. 99: 507–516

  • Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E . 2001 Nature 409: 1067–1070

  • Olson EN, Klein WH . 1994 Genes Dev. 8: 1–8

  • Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, Edery M, Brousse N, Babinet C, Binart N, Kelly P.A . 1997 Genes Dev. 15: 167–178

  • Riechmann V, van Cruchten I, Sablitzky F . 1994 Nucleic Acids Res. 22: 749–755

  • Riechmann V, Sablitzky F . 1995 Cell Growth Differ. 6: 837–843

  • Rivera RR, Johns CP, Quan J, Johnson RS, Murre C . 2000 Immunity 12: 17–26

  • Roberts EC, Deed RW, Inoue T, Norton JD, Sharrocks AD . 2001 Mol. Cell. Biol. 21: 524–533

  • Robinson L, Panayiotakis A, Papas TS, Kola I, Seth A . 1997 Proc. Natl. Acad. Sci. USA 94: 7170–7175

  • Russell LD, Ettlin RA, Hickim APS, Clegg ED . 1990 Histological and histopathological evaluation of the testis Cache River Press

  • Sablitzky F, Moore A, Bromley M, Deed RW, Newton JS, Norton JD . 1998 Cell Growth Differ. 9: 1015–1024

  • Seagroves TN, Krnacik S, Raught B, Gay J, Burgess-Beusse B, Darlington GJ, Rosen JM . 1998 Genes Dev. 15: 1917–1928

  • Sharpe RM . 1994 Physiology of Reproduction Vol. 1: Knobil E and Neil, JD (eds) Raven Press: New York pp. 1363–1434

    Google Scholar 

  • Shinkura R, Kitada K, Matsuda F, Tashiro K, Ikuta K, Suzuki M, Kogishi K, Serikawa T, Honjo T . 1999 Nat. Genet. 22: 74–77

  • Shoji W, Inoue T, Yamamoto T, Obinata M . 1995 J. Biol. Chem. 270: 24818–24825

  • Shortman K, Wu L . 1996 Ann. Rev. Immunol. 14: 29–47

  • Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam S, Bronson RT, Elledge SJ, Weinberg RA . 1995 Cell 82: 621–630

  • Spits H, Blom B, Jaleco AC, Weijer K, Verschuren MCM, van Dongen JJM, Heemskerk MHM, Res PCM . 1998 Immunol. Rev. 165: 75–86

  • Sun XH, Copeland NG, Jenkins NA, Baltimore D . 1991 Mol. Cell. Biol. 11: 5603–5611

  • Sun XH . 1994 Cell 79: 893–900

  • Sun Z, Unutmaz D, Zou YR, Sunshine MJ, Pierani A, Brenner-Morton S, Mebius RE, Littman DR . 2000 Science 288: 2369–2373

  • Temple S, Raff MC . 1986 Cell 14: 773–779

  • Toscani A, Mettus RV, Coupland R, Simpkins H, Litvin J, Orth J, Hatton KS, Reddy EP . 1997 Nature 386: 713–717

  • Tournay O, Benezra R . 1966 Mol. Cell. Biol. 16: 2418–2430

  • Tzeng SF, de Vellis J . 1998 Glia 24: 372–381

  • Wang S, Sdrulla A, Johnson JE, Yokota Y, Barres BA . 2001 Neuron 29: 603–614

  • Wice BM, Gordon JI . 1998 J. Biol. Chem. 273: 25310–25319

  • Williams NS, Klem J, Puzanov IJ, Sivakumar PV, Schatzle JD, Bennett M, Kumar V . 1998 Immunol. Rev. 165: 47–61

  • Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y . 1997 Mol. Cell. Biol. 17: 7317–7327

  • Yates PR, Atherton GT, Deed RW, Norton JD, Sharrocks AD . 1999 EMBO J. 18: 968–976

  • Yin L, Wu L, Wesch H, Arthur CD, White JM, Goeddel DV, Schreiber RD . 2001 Science 291: 2162–2165

  • Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S, Nishikawa S-I, Gruss P . 1999 Nature 397: 702–706

  • Yoshida H, Honda K, Shinkura R, Adachi S, Nishikawa S, Maki K, Ikuta K, Nishikawa S-I . 1999 Int. Immunol. 11: 643–655

  • Zhou Q, Wang S, Anderson DJ . 2000 Neuron 25: 331–343

  • Zhu W, Dahmen J, Bulfone A, Rigolet M, Hernandez MC, Kuo WL, Puelles L, Rubenstein JL, Israel MA . 1995 Brain Res. Mol. Brain Res. 30: 312–326

  • Zhuang Y, Cheng P, Weintraub H . 1996 Mol. Cell. Biol. 16: 2898–2905

  • Zhuang Y, Barndt RJ, Pan L, Kelley R, Dai M . 1998 Mol. Cell. Biol. 18: 3340–3349

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Acknowledgements

I am grateful to Fred Sablitzky, Dan Littman and Yuan Zhuang for sharing their unpublished observations and to all members of my laboratory at the Department of Biochemistry, Fukui Medical University, for helpful discussions and comments on the manuscript. I also thank Y Matsui for her secretarial assistance.

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Correspondence to Yoshifumi Yokota.

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Yokota, Y. Id and development. Oncogene 20, 8290–8298 (2001). https://doi.org/10.1038/sj.onc.1205090

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