Abstract
In recent years, studies in the model organism Drosophila melanogaster have contributed significant insights into the molecular and developmental biology of the AP-1 transcription factors Jun and Fos. Powerful genetic and biochemical approaches uncovered a baffling complexity and variability of the signaling connections to and from AP-1. The range of biological processes that Jun and Fos regulate in this organism is equally multi-faceted. Regulatory interactions between AP-1 and JNK, ERK, TGFβ, Notch or other signaling systems have been implicated in the control of a multitude of embryonic and adult events, including tissue closure processes, patterning of eye, gut and wing, as well as apoptosis. Here we review the information that has been gathered on Drosophila AP-1 in signal transduction and on the developmental and cellular functions controlled by AP-1-mediated signals in the fly. Lessons learned from the studies on AP-1 in Drosophila may contribute to our general understanding, beyond species boundaries, ofthis fundamental class of transcriptional regulators.
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
Adachi-Yamada T, Fujimura-Kamada K, Nishida Y, Matsumoto K . 1999 Nature 400: 166–169
Agnes F, Suzanne M, Noselli S . 1999 Development 126: 5453–5462
Andrew DJ, Baig A, Bhanot P, Smolik SM, Henderson KD . 1997 Development 124: 181–193
Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N . 1998 Genes Dev. 12: 2610–2622
Barila D, Mangano R, Gonfloni S, Kretzschmar J, Moro M, Bohmann D, Superti-Furga G . 2000 EMBO J 19: 273–281
Basdra EK, Huber LA, Komposch G, Papavassiliou AG . 1994 Biochim. Biophys. Acta. 1222: 315–322
Belvin MP, Zhou H, Yin JC . 1999 Neuron. 22: 777–787
Bergmann A, Agapite J, McCall K, Steller H . 1998 Cell 95: 331–341
Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R . 1996 Nature 382: 225–230
Bhat KM . 1998 Cell 95: 1027–1036
Bienz M . 1997 Curr. Opin. Genet. Dev. 7: 683–688
Biggs WHI, Zavitz KH, Dickson B, van der Straten A, Brunner D, Hafen E, Zipursky SL . 1994 EMBO J. 13: 1628–1635
Blair SS . 1995 Bioessays 17: 299–309
Blair SS . 1999 Curr. Biol. 9: R356–R360
Bohmann D, Ellis MC, Staszewski LM, Mlodzik M . 1994 Cell 78: 973–986
Boutros M, Mlodzik M . 1999 Mech. Dev. 83: 27–37
Boutros M, Paricio N, Strutt DI, Mlodzik M . 1998 Cell 94: 109–118
Brand AH, Perrimon N . 1993 Development 118: 401–415
Bray S . 2000 Curr Biol 10: R155–R158
Brook WJ, Diaz-Benjumea FJ, Cohen SM . 1996 Ann. Rev. Cell. Dev. Biol. 12: 161–180
Brunner D, Dücker K, Oellers N, Hafen E, Scholz H, Klämbt C . 1994a Nature 370: 386–389
Brunner D, Oellers N, Szabad J, Biggs WHI, Zipursky LH, Hafen E . 1994b Cell 76: 875–888
Brunner E, Peter O, Schweizer L, Basler K . 1997 Nature 385: 829–833
Byars CL, Bates KL, Letsou A . 1999 Development 126: 4913–4923
Cadigan KM, Fish MP, Rulifson EJ, Nusse R . 1998 Cell 93: 767–777
Chen Y, Riese MJ, Killinger MA, Hoffmann FM . 1998 Development 125: 1759–1768
Cho KO, Choi KW . 1998 Nature 396: 272–276
Cooper MT, Bray SJ . 1999 Nature 397: 526–530
Davis RJ . 2000 Cell 103: 239–252
Dominguez M, de Celis JF . 1998 Nature 396: 276–278
Eresh S, Riese J, Jackson DB, Bohmann D, Bienz M . 1997 EMBO J 16: 2014–2022
Erickson MR, Galletta BJ, Abmayr SM . 1997 J. Cell. Biol. 138: 589–603
Fanger GR, Gerwins P, Widmann C, Jarpe MB, Johnson GL . 1997 Curr. Opin. Genet. Dev. 7: 67–74
Fanto M, Mlodzik M . 1999 Nature 397: 523–526
Fanto M, Weber U, Strutt DI, Mlodzik M . 2000 Curr. Biol 10: 979–988
Fernandez R, Tabarini D, Azpiazu N, Frasch M, Schlessinger J . 1995 EMBO J 14: 3373–3384
Fernandez R, Takahashi F, Liu Z, Steward R, Stein D, Stanley ER . 2000 Genes Dev. 14: 604–614
Freeman M . 2000 Nature 408: 313–319
Genova JL, Jong S, Camp JT, Fehon RG . 2000 Dev. Biol. 221: 181–194
Glise B, Bourbon H, Noselli S . 1995 Cell 83: 451–461
Glise B, Noselli S . 1997 Genes Dev. 11: 1738–1747
Goyal L, McCall K, Agapite J, Hartwieg E, Steller H . 2000 EMBO J. 19: 589–597
Gubb D . 1993 Dev. Suppl 269–277
Hafezi F, Steinbach JP, Marti A, Munz K, Wang ZQ, Wagner EF, Aguzzi A, Reme CE . 1997 Nat. Med. 3: 346–349
Harden N, Lee J, Loh HY, Ong YM, Tan I, Leung T, Manser E, Lim L . 1996 Mol. Cell. Biol. 16: 1896–1908
Harden N, Loh HY, Chia W, Lim L . 1995 Development 121: 903–914
Herskowitz I . 1995 Cell 80: 187–197
Hewes RS, Schaefer AM, Taghert PH . 2000 Genetics 155: 1711–1723
Holland PM, Suzanne M, Campbell JS, Noselli S, Cooper JA . 1997 J. Biol. Chem. 272: 24994–24998
Hou XS, Goldstein ES, Perrimon N . 1997 Genes Dev. 11: 1728–1737
Hudson JB, Podos SD, Keith K, Simpson SL, Ferguson EL . 1998 Development 125: 1407–1420
Immerglück K, Lawrence PA, Bienz M . 1990 Cell 62: 261–268
Ip YT, Davis RJ . 1998 Curr. Opin. Cell. Biol. 10: 205–219
Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, Martin P . 2000 Curr. Biol. 10: 1420–1426
Kennerdell JR, Carthew RW . 1998 Cell 95: 1017–1026
Keyse SM . 1998 Semin. Cell. Dev. Biol. 9: 143–152
Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA . 2000 J. Cell. Biol. 149: 471–490
Knust E . 1996 Curr. Biol. 6: 379–381
Kockel L, Zeitlinger J, Staszewski LM, Mlodzik M, Bohmann D . 1997 Genes Dev. 11: 1748–1758
Lawrence PA . 1992 The Making of the Fly: The Genetics of Animal Design, Oxford and Boston
Li YS, Shyy JY, Li S, Lee J, Su B, Karin M, Chien S . 1996 Mol. Cell. Biol. 16: 5947–5954
Lisi S, Mazzon I, White K . 2000 Genetics 154: 669–678
Lu Y, Settleman J . 1999 Genes Dev. 13: 1168–1180
Martin-Blanco E . 2000 Bioessays 22: 637–645
Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky AM, Martinez-Arias A . 1998 Genes Dev. 12: 557–570
Martin-Blanco E, Pastor-Pareja JC, Garcia-Bellido A . 2000 Proc. Natl. Acad. Sci. USA 97: 7888–7893
McEwen DG, Cox RT, Peifer M . 2000 Development 127: 3607–3617
Mihaly J, Kockel L, Gaengel K, Weber U, Bohmann D, Mlodzik D . 2001 Mech. Development (in press.)
Mlodzik M . 1999 EMBO J. 18: 6873–6879
Morimura S, Maves L, Chen Y, Hoffmann FM . 1996 Dev. Biol. 177: 136–151
Muller H, Samanta R, Wieschaus E . 1999 Development 126: 577–586
Nolan KM, Barrett K, Lu Y, Hu KQ, Vincent S, Settleman J . 1998 Genes Dev. 12: 3337–3342
O'Neill EM, Rebay I, Tjian R, Rubin GM . 1994 Cell 78: 137–147
Panganiban GE, Reuter R, Scott MP, Hoffmann FM . 1990 Development 110: 1041–1050
Papavassiliou AG, Treier M, Bohmann D . 1995 EMBO J. 14: 2014–2019
Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD . 1998 Science 281: 2031–2034
Paricio N, Feiguin F, Boutros M, Eaton S, Mlodzik M . 1999 EMBO J. 18: 4669–4678
Peifer M, Rauskolb C, Williams M, Riggleman B, Wieschaus E . 1991 Development 111: 1029–1043
Perkins KK, Admon A, Patel N, Tjian R . 1990 Genes Dev. 4: 822–834
Perkins KK, Dailey GM, Tjian R . 1988 EMBO J. 7: 4265–4273
Perrimon N, McMahon AP . 1999 Cell 97: 13–16
Peverali FA, Isaksson A, Papavassiliou AG, Staszewski LM, Mlodzik M, Bohmann D . 1996 EMBO J. 15: 3943–3950
Raabe T . 2000 Biochim. Biophys. Acta. 1496: 151–163
Rebay I, Rubin GM . 1995 Cell 81: 857–866
Ricos MG, Harden N, Sem KP, Lim L, Chia W . 1999 J. Cell. Sci. 112: 1225–1235
Riese J, Tremml G, Bienz M . 1997 Development 124: 3353–3361
Riesgo-Escovar JR, Hafen E . 1997a Science 278: 669–672
Riesgo-Escovar JR, Hafen E . 1997b Genes Dev. 11: 1717–1727
Riesgo-Escovar JR, Jenni M, Fritz A, Hafen E . 1996 Genes Dev. 10: 2759–2768
Ring JM, Martinez-Arias A . 1993 Development 119: 251–259
Roulier EM, Panzer S, Beckendorf SK . 1998 Mol. Cell 1: 819–829
Sawamoto K, Winge P, Koyama S, Hirota Y, Yamada C, Miyao S, Yoshikawa S, Jin MH, Kikuchi A, Okano H . 1999 J. Cell. Biol. 146: 361–372
Shulman JM, Perrimon N, Axelrod JD . 1998 Trends Genet. 14: 452–458
Simin K, Bates EA, Horner MA, Letsou A . 1998 Genetics 148: 801–813
Sluss HK, Davis RJ . 1997 J. Cell. Biochem. 67: 1–12
Sluss HK, Han Z, Barrett T, Davis RJ, Ip YT . 1996 Genes Dev. 10: 2745–2758
St Johnston RD, Gelbart WM . 1987 EMBO J. 6: 2785–2791
Strutt DI, Weber U, Mlodzik M . 1997 Nature 387: 292–295
Strutt H, Strutt D . 1999 Curr. Opin. Genet. Dev. 9: 442–446
Su YC, Treisman JE, Skolnik EY . 1998 Genes Dev. 12: 2371–2380
Szüts D, Bienz M . 2000a Proc. Natl. Acad. Sci. USA 97: 5351–5356
Szüts D, Bienz M . 2000b Mech. Dev. 98: 71–76
Szüts D, Eresh S, Bienz M . 1998 Genes Dev. 12: 2022–2035
Takatsu Y, Nakamura M, Stapleton M, Danos MC, Matsumoto K, O'Connor MB, Shibuya H, Ueno N . 2000 Mol. Cell. Biol. 20: 3015–3026
Tateno M, Nishida Y, Adachi-Yamada T . 2000 Science 287: 324–327
Theisen H, Purcell J, Bennett M, Kansagara D, Syed A, Marsh JL . 1994 Development 120: 347–360
Tomlinson A, Struhl G . 1999 Development 126: 5725–5738
Treier M, Bohmann D, Mlodzik M . 1995 Cell 83: 753–760
Tremml G, Bienz M . 1992 Development 116: 447–456
Usui K, Simpson P . 2000 Dev. Biol. 225: 13–25
Wang SL, Hawkins CJ, Yoo SJ, Muller HA, Hay BA . 1999 Cell 98: 453–463
Watson L, Herdegen T, Buschmann T, Denger S, Wende P, Jahn L, Kreuzer J . 2000 Eur. J. Clin. Invest. 30: 11–17
Weber U, Paricio N, Mlodzik M . 2000 Development 127: 3619–3629
Wehrli M, Tomlinson A . 1998 Development 125: 1421–1432
Wolff T, Ready DF . 1993 The Biology of Drosophila melanogaster Bate, M. & Martinez-Arias, A. (eds) CSHL Press
Yin JC, Del Vecchio M, Zhou H, Tully T . 1995 Cell 81: 107–115
Young PE, Richman AM, Ketchum AS, Kiehart DP . 1993 Genes Dev. 7: 29–41
Zeidler MP, Bach EA, Perrimon N . 2000a Oncogene 19: 2598–2606
Zeidler MP, Perrimon N, Strutt DI . 1999a Curr. Biol. 9: 1363–1372
Zeidler MP, Perrimon N, Strutt DI . 1999b Genes Dev. 13: 1342–1353
Zeidler MP, Perrimon N, Strutt DI . 2000b Dev. Biol. 228: 181–196
Zeitlinger J, Bohmann D . 1999 Development 126: 3947–3956
Zeitlinger J, Kockel L, Peverali FA, Jackson DB, Mlodzik M, Bohmann D . 1997 EMBO J. 16: 7393–7401
Zhang K, Chaillet R, Perkins LA, Halazonetis TD, Perrimon N . 1990 Proc. Natl. Acad. Sci. USA 87: 6281–6285
Zheng L, Zhang J, Carthew RW . 1995 Development 121: 3045–3055
Acknowledgements
The authors thank Lena M Staszewski for technical help, Julia Zeitlinger for contributing Figure 6, Beth Stronach for discussion and Erwin Wagner for initiating this review and for his patience with delayed contributions.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kockel, L., Homsy, J. & Bohmann, D. Drosophila AP-1: lessons from an invertebrate. Oncogene 20, 2347–2364 (2001). https://doi.org/10.1038/sj.onc.1204300
Issue Date:
DOI: https://doi.org/10.1038/sj.onc.1204300