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.

  • Review
  • Published:

Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity

Abstract

Fos and Jun family proteins regulate the expression of a myriad of genes in a variety of tissues and cell types. This functional versatility emerges from their interactions with related bZIP proteins and with structurally unrelated transcription factors. These interactions at composite regulatory elements produce nucleoprotein complexes with high sequence-specificity and regulatory selectivity. Several general principles including binding cooperativity and conformational adaptability have emerged from studies of regulatory complexes containing Fos-Jun family proteins. The structural properties of Fos-Jun family proteins including opposite orientations of heterodimer binding and the ability to bend DNA can contribute to the assembly and functions of such complexes. The cooperative recruitment of transcription factors, coactivators and chromatin remodeling factors to promoter and enhancer regions generates multiprotein transcription regulatory complexes with cell- and stimulus-specific transcriptional activities. The gene-specific architecture of these complexes can mediate the selective control of transcriptional activity.

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

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D . 2000 Cell 103: 667–678

  • Agarwal SK, Guru SC, Heppner C, Erdos MR, Collins RM, Park SY, Saggar S, Chandrasekharappa SC, Collins FS, Spiegel AM, Marx SJ, Burns AL . 1999 Cell 96: 143–152

  • Aho S, Buisson M, Pajunen T, Ryoo YW, Giot JF, Gruffat H, Sergeant A, Uitto J . 2000 J. Cell. Biol. 148: 1165–1176

  • Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AM, Burow ME, Tou J . 2000 J. Biol. Chem. 275: 27694–27702

  • Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M . 1997 Mol. Cell. Biol. 17: 3094–3102

  • Bakin AV, Curran T . 1999 Science 283: 387–390

  • Bannister AJ, Kouzarides T . 1995 EMBO J. 14: 4758–4762

  • Baranger AM, Palmer CR, Hamm MK, Giebler HD, Brauweiler A, Nyborg JK and Schepartz A . 1995 Nature 376: 606–608

  • Bassuk AG, Leiden JM . 1995 Immunity 3: 223–237

  • Basuyaux JP, Ferreira E, Stehelin D, Buttice G . 1997 J. Biol. Chem. 272: 26188–26195

  • Benkhelifa S, Provot S, Lecoq O, Pouponnot C, Calothy G, Felder-Schmittbuhl MP . 1998 Oncogene 17: 247–254

  • Boehlk S, Fessele S, Mojaat A, Miyamoto NG, Werner T, Nelson EL, Schlondorff D, Nelson PJ . 2000 Eur. J. Immunol. 30: 1102–1112

  • Brodin G, Ahgren A, ten Dijke P, Heldin CH, Heuchel R . 2000 J. Biol. Chem. 275: 29023–29030

  • Buttice G, Duterque-Coquillaud M, Basuyaux JP, Carrere S, Kurkinen M, Stehelin D . 1996 Oncogene 13: 2297–2306

  • Caelles C, Gonzalez-Sancho JM, Munoz A . 1997 Genes Dev. 11: 3351–3364

  • Chen BK, Chang WC . 2000 Proc. Natl. Acad. Sci. USA 97: 10406–10411

  • Chen L, Glover JN, Hogan PG, Rao A, Harrison SC . 1998 Nature 392: 42–48

  • Chen L, Oakley MG, Glover JN, Jain J, Dervan PB, Hogan PG, Rao A, Verdine GL . 1995 Curr. Biol. 5: 882–889

  • Chen X, Rubock MJ, Whitman M . 1996 Nature 383: 691–696

  • Chytil M, Peterson BR, Erlanson DA, Verdine GL . 1998 Proc. Natl. Acad. Sci. USA 95: 14076–14081

  • Claret FX, Hibi M, Dhut S, Toda T, Karin M . 1996 Nature 383: 453–457

  • Curran T, Teich NM . 1982 J. Virol. 42: 114–122

  • Curran T, Franza BR . 1988 Cell 55: 395–397

  • De Cesare D, Palazzolo M, Berthelsen J, Blasi F . 1997 J. Biol. Chem. 272: 23921–23929

  • De Graeve F, Bahr A, Sabapathy KT, Hauss C, Wagner EF, Kedinger C, Chatton B . 1999 Oncogene 18: 3491–3500

  • Derynck R, Zhang Y, Feng XH . 1998 Cell 95: 737–740

  • Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR . 1990 Science 249: 1266–1272

  • Diebold RJ, Rajaram N, Leonard DA, Kerppola TK . 1998 Proc. Natl. Acad. Sci. USA 95: 7915–7920

  • Dlakic M, Grinberg AV, Leonard DA, Kerppola TK . 2001 EMBO J. 20: 1–14

  • D'Orazio D, Besser D, Marksitzer R, Kunz C, Hume DA, Kiefer B, Nagamine Y . 1997 Gene 201: 179–187

  • Du W, Thanos D, Maniatis T . 1993 Cell 74: 887–898

  • Duncliffe KN, Bert AG, Vadas MA, Cockerill PN . 1997 Immunity 6: 175–185

  • Echlin DR, Tae HJ, Mitin N, Taparowsky EJ . 2000 Oncogene 19: 1752–1763

  • Eckert RL, Crish JF, Banks EB, Welter JF . 1997 J. Invest. Dermatol. 109: 501–509

  • Ellenberger TE, Brandl CJ, Struhl K, Harrison SC . 1992 Cell 71: 1223–1237

  • Falvo JV, Brinkman BM, Tsytsykova AV, Tsai EY, Yao TP, Kung AL, Goldfeld AE . 2000a Proc. Natl. Acad. Sci. USA 97: 3925–3929

  • Falvo JV, Parekh BS, Lin CH, Fraenkel E, Maniatis T . 2000b Mol. Cell. Biol. 20: 4814–4825

  • Falvo JV, Uglialoro AM, Brinkman BM, Merika M, Parekh BS, Tsai EY, King HC, Morielli AD, Peralta EG, Maniatis T, Thanos D, Goldfeld AE . 2000c Mol. Cell. Biol. 20: 2239–2247

  • Fu SL, Waha A, Vogt PK . 2000 Oncogene 19: 3537–3545

  • Fujii Y, Shimizu T, Toda T, Yanagida M, Hakoshima T . 2000 Nat. Struct. Biol. 7: 889–893

  • Giese K, Kingsley C, Kirshner JR, Grosschedl R . 1995 Genes Dev. 9: 995–1008

  • Glover JN, Harrison SC . 1995 Nature 373: 257–261

  • Gottschalk LR, Giannola DM, Emerson SG . 1993 J. Exp. Med. 178: 1681–1692

  • Graves BJ, Petersen JM . 1998 Adv. Cancer Res. 75: 1–55

  • Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF . 1994 Science 266: 443–448

  • Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M, Boyd D . 1996 J. Biol. Chem. 271: 10672–10680

  • Gutman A, Wasylyk B . 1990 EMBO J. 9: 2241–2246

  • Hai T, Curran T . 1991 Proc. Natl. Acad. Sci. USA 88: 3720–3724

  • Hernandez-Munain C, Roberts JL, Krangel MS . 1998 Mol. Cell. Biol. 18: 3223–3233

  • Hilberg F, Aguzzi A, Howells N, Wagner EF . 1993 Nature 365: 179–181

  • Hoey T, Sun YL, Williamson K, Xu X . 1995 Immunity 2: 461–472

  • Hsu W, Kerppola TK, Chen PL, Curran T, Chen-Kiang S . 1994 Mol. Cell. Biol. 14: 268–276

  • Hua X, Liu X, Ansari DO, Lodish HF . 1998 Genes Dev. 12: 3084–3095

  • Iacobelli M, Wachsman W, McGuire KL . 2000 J. Immunol. 165: 860–868

  • Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A . 1993a Nature 365: 352–355

  • Jain J, Miner Z, Rao A . 1993b J. Immunol. 151: 837–848

  • Jaiswal AK . 2000 Free Radic. Biol. Med. 29: 254–262

  • Jang SI, Karaman-Jurukovska N, Morasso MI, Steinert PM, Markova NG . 2000 J. Biol. Chem. 275: 15295–15304

  • Johnson RS, Spiegelman BM, Papaioannou V . 1992 Cell 71: 577–586

  • Johnson RS, van Lingen B, Papaioannou VE, Spiegelman BM . 1993 Genes Dev. 7: 1309–1317

  • Jones JB, Kern SE . 2000 Nucleic Acids Res. 28: 2363–2368

  • Jonk LJ, Itoh S, Heldin CH, ten Dijke P, Kruijer W . 1998 J. Biol. Chem. 273: 21145–21152

  • Kataoka K, Fujiwara KT, Noda M, Nishizawa M . 1994a Mol. Cell. Biol. 14: 7581–7591

  • Kataoka K, Igarashi K, Itoh K, Fujiwara KT, Noda M, Yamamoto M, Nishizawa M . 1995 Mol. Cell. Biol. 15: 2180–2190

  • Kataoka K, Noda M, Nishizawa M . 1994b Mol. Cell. Biol. 14: 700–712

  • Kataoka K, Noda M, Nishizawa M . 1996 Oncogene 12: 53–62

  • Kawana M, Lee ME, Quertermous EE, Quertermous T . 1995 Mol. Cell. Biol. 15: 4225–4231

  • Kerppola TK . 1998 Structure 6: 549–554

  • Kerppola TK, Curran T . 1991 Cell 66: 317–326

  • Kerppola TK, Curran T . 1993 Mol. Cell. Biol. 13: 5479–5489

  • Kerppola TK, Curran T . 1994a Oncogene 9: 3149–3158

  • Kerppola TK, Curran T . 1994b Oncogene 9: 675–684

  • Kerppola TK, Luk D, Curran T . 1993 Mol. Cell. Biol. 13: 3782–3791

  • Kirstein M, Sanz L, Quinones S, Moscat J, Diaz-Meco MT, Saus J . 1996 J. Biol. Chem. 271: 18231–18236

  • Kodandapani R, Pio F, Ni CZ, Piccialli G, Klemsz M, McKercher S, Maki RA, Ely KR . 1996 Nature 380: 456–460

  • Konig H, Ponta H, Rahmsdorf HJ, Herrlich P . 1992 EMBO J. 11: 2241–2246

  • Kovary K, Bravo R . 1991 Mol. Cell. Biol. 11: 2451–2459

  • Kovary K, Bravo R . 1992 Mol. Cell. Biol. 12: 5015–5023

  • Kramer B, Wiegmann K, Kronke M . 1995 J. Biol. Chem. 270: 6577–6583

  • Lallemand D, Spyrou G, Yaniv M, Pfarr CM . 1997 Oncogene 14: 819–830

  • Landschulz WH, Johnson PF, McKnight SL . 1988 Science 240: 1759–1764

  • Lee SK, Kim HJ, Na SY, Kim TS, Choi HS, Im SY, Lee JW . 1998 J. Biol. Chem. 273: 16651–16654

  • Lee SK, Kim JH, Lee YC, Cheong J, Lee JW . 2000a J. Biol. Chem. 275: 12470–12474

  • Lee SK, Na SY, Jung SY, Choi JE, Jhun BH, Cheong J, Meltzer PS, Lee YC, Lee JW . 2000b Mol. Endocrinol. 14: 915–925

  • Lefstin JA, Yamamoto KR . 1998 Nature 392: 885–888

  • Leonard DA, Kerppola TK . 1998 Nat. Struct. Biol. 5: 877–881

  • Leonard DA, Rajaram N, Kerppola TK . 1997 Proc. Natl. Sci. USA 13: 4913–4918

  • Li B, Tournier C, Davis RJ, Flavell RA . 1999 EMBO J 18: 420–432

  • Li L, Chambard JC, Karin M, Olson EN . 1992 Genes Dev. 6: 676–689

  • Liberati NT, Datto MB, Frederick JP, Shen X, Wong C, Rougier-Chapman EM, Wang XF . 1999 Proc. Natl. Acad. Sci. USA 96: 4844–4849

  • Logan SK, Garabedian MJ, Campbell CE, Werb Z . 1996 J. Biol. Chem. 271: 774–782

  • Maki Y, Bos TJ, Davis C, Starbuck M, Vogt PK . 1987 Proc. Natl. Acad. Sci. USA 84: 2848–2852

  • Martin ME, Piette J, Yaniv M, Tang WJ, Folk WR . 1988 Proc. Natl. Acad. Sci. USA 85: 5839–5843

  • Mayall TP, Sheridan PL, Montminy MR, Jones KA . 1997 Genes Dev. 11: 887–899

  • McBride K, Nemer M . 1998 Mol. Cell. Biol. 18: 5073–5081

  • McCabe LR, Kockz M, Lian J, Stein G . 1995 Exp. Cell Res. 218: 255–262

  • McCabe LR, Banerjee C, Kundu R, Harrison RJ, Dobner PR, Stein JL, Lian JB, Stein GS . 1996 Endocrinology 137: 4398–4408

  • McCaffrey PG, Luo C, Kerppola TK, Jain J, Badalian TM, Ho AM, Burgeon E, Lane WS, Lambert JN, Curran T, Verdine GV, Rao A, Hogan PG . 1993 Science 262: 750–754

  • Merika M, Williams AJ, Chen G, Collins T, Thanos D . 1998 Mol. Cell. 1: 277–287

  • Metz R, Bannister AJ, Sutherland JA, Hagemeier C, O'Rourke EC, Cook A, Bravo R, Kouzarides T . 1994 Mol. Cell. Biol. 14: 6021–6029

  • Min W, Ghosh S, Lengyel P . 1996 Mol. Cell. Biol. 16: 359–368

  • Moinova HR, Mulcahy RT . 1999 Biochem. Biophys. Res. Commun. 261: 661–668

  • Monteclaro FS, Vogt PK . 1993 Proc. Natl. Acad. Sci. USA 90: 6726–6730

  • Moreau A, Yotov WV, Glorieux FH, St-Arnaud R . 1998 Mol. Cell. Biol. 18: 1312–1321

  • Moulton KS, Semple K, Wu H, Glass CK . 1994 Mol. Cell. Biol. 14: 4408–4418

  • Nakabeppu Y, Ryder K, Nathans D . 1988 Cell 55: 907–915

  • Nead MA, Baglia LA, Antinore MJ, Ludlow JW, McCance DJ . 1998 EMBO J. 17: 2342–2352

  • Nerlov C, De Cesare D, Pergola F, Caracciolo A, Blasi F, Johnsen M, Verde P . 1992 EMBO J. 11: 4573–4582

  • Nguyen T, Huang HC, Pickett CB . 2000 J. Biol. Chem. 275: 15466–15473

  • Noti JD, Reinemann C, Petrus MN . 1996 Mol. Immunol. 33: 115–127

  • Palazzolo M, Berthelsen J, De Cesare D, Blasi F . 2000 Eur. J. Biochem. 267: 5427–5437

  • Perini G, Oetjen E, Green MR . 1999 J. Biol. Chem. 274: 13970–13977

  • Perkins D, Wang Z, Donovan C, He H, Mark D, Guan G, Wang Y, Walunas T, Bluestone J, Listman J . 1996 J. Immunol. 156: 4154–4159

  • Peterson BR, Sun LJ, Verdine GL . 1996 Proc. Natl. Acad. Sci. USA 93: 13671–13676

  • Pognonec P, Boulukos KE, Aperlo C, Fujimoto M, Ariga H, Nomoto A, Kato H . 1997 Oncogene 14: 2091–2098

  • Qian Z, Brunovskis P, Lee L, Vogt PK, Kung HJ . 1996 J. Virol. 70: 7161–7170

  • Qing J, Zhang Y, Derynck R . 2000 J. Biol. Chem. 275: 38802–38812

  • Rajaram N, Kerppola TK . 1997 EMBO J. 16: 2917–2925

  • Ramirez-Carrozzi VR, Kerppola TK . 2001a Proc. Natl. Acad. Sci. USA 98: 4893–4898

  • Ramirez-Carrozzi VR, Kerppola TK . 2001b J. Mol. Biol. 305: 411–427

  • Rao A, Luo C, Hogan PG . 1997 Annu. Rev. Immunol. 15: 707–747

  • Rauscher FJD, Voulalas PJ, Franza Jr BR, Curran T . 1988 Genes Dev. 2: 1687–1699

  • Robertson LM, Kerppola TK, Vendrell M, Luk D, Smeyne RJ, Bocchiaro C, Morgan JI, Curran T . 1995 Neuron 14: 241–252

  • Rooney JW, Hoey T, Glimcher LH . 1995 Immunity 2: 473–483

  • Rushmore TH, Pickett CB . 1990 J. Biol. Chem. 265: 14648–14653

  • Sano Y, Harada J, Tashiro S, Gotoh-Mandeville R, Maekawa T, Ishii S . 1999 J. Biol. Chem. 274: 8949–8957

  • Sato M, Morii E, Takebayashi-Suzuki K, Yasui N, Ochi T, Kitamura Y, Nomura S . 1999 Biochem. Biophys. Res. Commun. 254: 384–387

  • Schorpp-Kistner M, Wang ZQ, Angel P, Wagner EF . 1999 EMBO J 18: 934–948

  • Schreiber M, Wang Z, Jochum W, Fetka I, Elliott C, Wagner EF . 2000 Development 127: 4937–4948

  • Schule R, Umesono K, Mangelsdorf DJ, Bolado J, Pike JW, Evans RM . 1990 Cell 61: 497–504

  • Schumacher MA, Goodman RH, Brennan RG . 2000 J. Biol. Chem. 275: 35242–35247

  • Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA, Crabtree GR . 1988 Science 241: 202–205

  • Shi Y, Wang YF, Jayaraman L, Yang H, Massague J, Pavletich NP . 1998 Cell 94: 585–594

  • Sieweke MH, Tekotte H, Frampton J, Graf T . 1996 Cell 85: 49–60

  • Sonnenberg JL, Macgregor-Leon PF, Curran T, Morgan JI . 1989 Neuron 3: 359–365

  • Spicuglia S, Payet D, Tripathi RK, Rameil P, Verthuy C, Imbert J, Ferrier P, Hempel WM . 2000 EMBO J. 19: 2034–2045

  • Stein B, Baldwin AS, Ballard DW, Greene WC, Angel P, Herrlich P . 1993 EMBO J. 12: 3897–3891

  • Stranick KS, Zambas DN, Uss AS, Egan RW, Billah MM, Umland SP . 1997 J. Biol. Chem. 272: 16453–16465

  • Tan S, Richmond TJ . 1998 Nature 391: 660–666

  • Thanos D, Maniatis T . 1995 Cell 83: 1091–1100

  • Thepot D, Weitzman JB, Barra J, Segretain D, Stinnakre MG, Babinet C, Yaniv M . 2000 Development 127: 143–153

  • Tsai EY, Jain J, Pesavento PA, Rao A, Goldfeld AE . 1996a Mol. Cell. Biol. 16: 459–467

  • Tsai EY, Yie J, Thanos D, Goldfeld AE . 1996b Mol. Cell. Biol. 16: 5232–5244

  • Tsai EY, Falvo JV, Tsytsykova AV, Barczak AK, Reimold AM, Glimcher LH, Fenton MJ, Gordon DC, Dunn IF, Goldfeld AE . 2000 Mol. Cell. Biol. 20: 6084–6094

  • Ubeda M, Vallejo M, Habener JF . 1999 Mol. Cell. Biol. 19: 7589–7599

  • Ullman KS, Northrop JP, Admon A, Crabtree GR . 1993 Genes. Dev. 7: 188–196

  • van Dam H, Duyndam M, Rottier R, Bosch A, de Vries-Smits L, Herrlich P, Zantema A, Angel P, van der Eb AJ . 1993 EMBO J. 12: 479–487

  • van Dam H, Huguier S, Kooistra K, Baguet J, Vial E, van der Eb AJ, Herrlich P, Angel P, Castellazzi M . 1998 Genes. Dev. 12: 1227–1239

  • Venugopal R, Jaiswal AK . 1998 Oncogene 17: 3145–3156

  • Virbasius CM, Wagner S, Green MR . 1999 Mol. Cell. 4: 219–228

  • Wang CY, Bassuk AG, Boise LH, Thompson CB, Bravo R, Leiden JM . 1994 Mol. Cell. Biol. 14: 1153–1159

  • Wang ZQ, Ovitt C, Grigoriadis AE, Mohle-Steinlein U, Ruther U, Wagner EF . 1992 Nature 360: 741–745

  • Wolfe SA, Zhou P, Dotsch V, Chen L, You A, Ho SN, Crabtree GR, Wagner G, Verdine GL . 1997 Nature 385: 172–176

  • Wong C, Rougier-Chapman EM, Frederick JP, Datto MB, Liberati NT, Li JM, Wang XF . 1999 Mol. Cell. Biol. 19: 1821–1830

  • Wu H, Moulton K, Horvai A, Parik S, Glass CK . 1994 Mol. Cell. Biol. 14: 2129–2139

  • Yie J, Merika M, Munshi N, Chen G, Thanos D . 1999 EMBO J. 18: 3074–3089

  • Zhang X, Wrzeszczynska MH, Horvath CM, Darnell Jr JE . 1999 Mol. Cell. Biol. 19: 7138–7146

  • Zhang Y, Derynck R . 2000 J. Biol. Chem. 275: 16979–16985

  • Zhang Y, Feng XH, Derynck R . 1998 Nature 394: 909–913

  • Zhou P, Sun LJ, Dotsch V, Wagner G, Verdine GL . 1998 Cell 92: 687–696

Download references

Acknowledgements

We apologize to the many people whose work could not be cited due to space limitations. We thank Mensur Dlakic, Asya Grinberg and Nirmala Rajaram for helpful discussions during preparation of the manuscript and Ann E Goldfeld (Harvard Medical School), Andy Sharroks (Manchester University), Laura McCabe (Michigan State University), Helen Moinova (Case Western Reserve University), Moshe Yaniv (Institute Pasteur) and Thomas Herdegen (University of Kiel) for comments.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chinenov, Y., Kerppola, T. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20, 2438–2452 (2001). https://doi.org/10.1038/sj.onc.1204385

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1204385

Keywords

This article is cited by

Search

Quick links