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AP1 genes in Fugu indicate a divergent transcriptional control to that of mammals

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Abstract

The draft genomic sequence of the Japanese puffer fish, Fugu rubripes, has now been announced. This is the first complete sequence of a teleost fish and the second available vertebrate sequence, the first being that of human. For the first time, whole-genome comparisons between two vertebrates can be undertaken. Early analysis has suggested that there may be surprising differences in gene regulation between human and fish. In mammals, a gene commonly has several functions, and this may not always be the case in fish. Many gene families comprise more members in fish than they do in mammals, possibly because each fish gene has evolved an individual function. Complexities of gene regulation in mammals has hampered studies of all biological processes from cell proliferation to cell death. Determining the activities of the AP1 transcription factor proteins has been non-trivial. The AP1 complex typically comprises two proteins, a Jun (c-Jun, JunB, and JunD) and a Fos (c-Fos, FosB, Fra1, and Fra2). These proteins can form both homodimers and heterodimers among-themselves and can interact with additional proteins; thus, dissecting their individual roles has been difficult. We have determined that Fugu has more Jun and Fos genes than mammals, and if each proves to have a separate function, then addressing the roles of the individual AP1 proteins in Fugu may be simpler than in human.

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References

  1. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang et al. (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694

    PubMed  Google Scholar 

  2. S Aparicio J Chapman E Stupka N Putnam JM Chia et al. (2002) ArticleTitleWhole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297 1301–1310 Occurrence Handle10.1126/science.1072104 Occurrence Handle1:CAS:528:DC%2BD38Xms1ejtr8%3D Occurrence Handle12142439

    Article  CAS  PubMed  Google Scholar 

  3. VR Baichwal A Park R Tjian (1991) ArticleTitlev-Src and EJ Ras alleviate repression of c-Jun by a cell-specific inhibitor. Nature 352 165–168 Occurrence Handle10.1038/352165a0 Occurrence Handle1:CAS:528:DyaK3MXkvVOkurg%3D Occurrence Handle1906140

    Article  CAS  PubMed  Google Scholar 

  4. D Barila R Mangano S Gonfloni J Kretzschmar M Moro (2000) ArticleTitleA nuclear tyrosine phosphorylation circuit: c-Jun as an activator and substrate of c-Ab1 and JNK. EMBO J 19 273–281 Occurrence Handle10.1093/emboj/19.2.273 Occurrence Handle1:CAS:528:DC%2BD3cXotFejtw%3D%3D Occurrence Handle10637231

    Article  CAS  PubMed  Google Scholar 

  5. S Baxendale S Abdulla G Elgar D Buck M Berks et al. (1995) ArticleTitleComparative sequence analysis of the human and pufferfish Huntington's disease genes. Nat Genet 10 67–76 Occurrence Handle1:CAS:528:DyaK2MXlsVymtro%3D Occurrence Handle7647794

    CAS  PubMed  Google Scholar 

  6. G Bergers P Graninger S Braselmann C Wrighton M Busslinger (1995) ArticleTitleTranscriptional activation of the fra-1 gene by AP-1 is mediated by regulatory sequences in the first intron. Mol Cell Biol 15 3748–3758 Occurrence Handle1:CAS:528:DyaK2MXmsVClsL8%3D Occurrence Handle7791782

    CAS  PubMed  Google Scholar 

  7. J Blenis (1993) ArticleTitleSignal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci USA 90 5889–5892 Occurrence Handle1:CAS:528:DyaK3sXltFWnsL8%3D Occurrence Handle8392180

    CAS  PubMed  Google Scholar 

  8. S Brenner G Elgar R Sandford A Macrae B Venkatesh et al. (1993) ArticleTitleCharacterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature 366 265–268

    Google Scholar 

  9. HJ Brown JA Sutherland A Cook AJ Bannister T Kouzarides (1995) ArticleTitleAn inhibitor domain in c-Fos regulates activation domains containing the HOB1 motif. EMBO J 14 124–131 Occurrence Handle1:CAS:528:DyaK2MXjt1yqur4%3D Occurrence Handle7828584

    CAS  PubMed  Google Scholar 

  10. JR Brown H Ye RT Bronson P Dikkes ME Greenberg (1996) ArticleTitleA defect in nurturing in mice lacking the immediate early gene fosB. Cell 86 297–309 Occurrence Handle1:CAS:528:DyaK28Xks1Gns7Y%3D Occurrence Handle8706134

    CAS  PubMed  Google Scholar 

  11. YR Chen X Wang D Templeton RJ Davis TH Tan (1996) ArticleTitleThe role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem 271 31929–31936 Occurrence Handle10.1074/jbc.271.50.31929 Occurrence Handle1:CAS:528:DyaK2sXitFKitg%3D%3D Occurrence Handle8943238

    Article  CAS  PubMed  Google Scholar 

  12. Y Chinenov TK Kerppola (2001) ArticleTitleClose encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20 2438–2452 Occurrence Handle10.1038/sj.onc.1204385 Occurrence Handle1:STN:280:DC%2BD3Mzjt1Oisg%3D%3D Occurrence Handle11402339

    Article  CAS  PubMed  Google Scholar 

  13. R Chiu P Angel M Karin (1989) ArticleTitleJun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell 59 979–986 Occurrence Handle1:CAS:528:DyaK3cXntFCrsg%3D%3D Occurrence Handle2513128

    CAS  PubMed  Google Scholar 

  14. SY Chou V Baichwal JE Ferrell Jr (1992) ArticleTitleInhibition of c-Jun DNA binding by mitogen-activated protein kinase. Mol Biol Cell 3 1117–1130 Occurrence Handle1:CAS:528:DyaK3sXhs1emsb8%3D Occurrence Handle1421569

    CAS  PubMed  Google Scholar 

  15. B Derijard M Hibi IH Wu T Barrett B Su et al. (1994) ArticleTitleJNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76 1025–1037 Occurrence Handle8137421

    PubMed  Google Scholar 

  16. M Ekker MA Akimenko ML Allende R Smith G Drouin et al. (1997) ArticleTitleRelationships among msx gene structure and function in zebrafish and other vertebrates. Mol Biol Evol 14 1008–1022 Occurrence Handle1:CAS:528:DyaK2sXms1entrg%3D Occurrence Handle9335141

    CAS  PubMed  Google Scholar 

  17. F Fisher DH Crouch PS Jayaraman W Clark DA Gillespie et al. (1993) ArticleTitleTranscription activation by Myc and Max: flanking sequences target activation to a subset of CACGTG motifs in vivo. EMBO J 12 5075–5082 Occurrence Handle1:CAS:528:DyaK2cXpvVSqtA%3D%3D Occurrence Handle8262050

    CAS  PubMed  Google Scholar 

  18. RR Freter JC Irminger JA Porter SD Jones CD Stiles (1992) ArticleTitleA novel 7-nucleotide motif located in 3′ untranslated sequences of the immediate-early gene set mediates platelet-derived growth factor induction of the JE gene. Mol Cell Biol 12 5288–5300 Occurrence Handle1:CAS:528:DyaK3sXnsVKlsw%3D%3D Occurrence Handle1448065

    CAS  PubMed  Google Scholar 

  19. G Fritz B Kaina (1999) ArticleTitlePhosphorylation of the DNA repair protein APE/REF-1 by CKII affects redox regulation of AP-1. Oncogene 18 1033–1040 Occurrence Handle1:CAS:528:DyaK1MXhsVyitLg%3D Occurrence Handle10023679

    CAS  PubMed  Google Scholar 

  20. M Funk B Poensgen W Graulich V Jerome R Muller (1997) ArticleTitleA novel, transformation-relevant activation domain in Fos proteins. Mol Cell Biol 17 537–544 Occurrence Handle1:CAS:528:DyaK2sXmvVWjtQ%3D%3D Occurrence Handle9001206

    CAS  PubMed  Google Scholar 

  21. N Galtier M Gouy C Gautier (1996) ArticleTitleSEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12 543–548 Occurrence Handle1:CAS:528:DyaK2sXhtlWktLw%3D Occurrence Handle9021275

    CAS  PubMed  Google Scholar 

  22. MC Gruda K Kovary R Metz R Bravo (1994) ArticleTitleRegulation of Fra-1 and Fra-2 phosphorylation differs during the cell cycle of fibroblasts and phosphorylation in vitro by MAP kinase affects DNA binding activity. Oncogene 9 2537–2547 Occurrence Handle1:CAS:528:DyaK2cXlslKjtbo%3D Occurrence Handle8058317

    CAS  PubMed  Google Scholar 

  23. T Hai T Curran (1991) ArticleTitleCross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci USA 88 3720–3724 Occurrence Handle1:CAS:528:DyaK3MXktVahurw%3D Occurrence Handle1827203

    CAS  PubMed  Google Scholar 

  24. T Herdegen JD Leah (1998) ArticleTitleInducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 28 370–490 Occurrence Handle1:CAS:528:DyaK1cXotVKhsrc%3D Occurrence Handle9858769

    CAS  PubMed  Google Scholar 

  25. M Hibi A Lin T Smeal A Minden M Karin (1993) ArticleTitleIdentification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7 2135–2148 Occurrence Handle1:CAS:528:DyaK2cXisVyksQ%3D%3D Occurrence Handle8224842

    CAS  PubMed  Google Scholar 

  26. KU Jooss M Funk R Muller (1994) ArticleTitleAn autonomous N-terminal transactivation domain in Fos protein plays a crucial role in transformation. EMBO J 13 1467–1475 Occurrence Handle1:CAS:528:DyaK2cXjtFOqu7c%3D Occurrence Handle8137828

    CAS  PubMed  Google Scholar 

  27. T Kallunki T Deng M Hibi M Karin (1996) ArticleTitlec-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87 929–939 Occurrence Handle1:CAS:528:DyaK28Xntlyqur4%3D Occurrence Handle8945519

    CAS  PubMed  Google Scholar 

  28. S Karlin (1995) ArticleTitleStatistical significance of sequence patterns in proteins. Curr Opin Struct Biol 5 360–371 Occurrence Handle10.1016/0959-440X(95)80098-0 Occurrence Handle1:CAS:528:DyaK2MXntlamurY%3D Occurrence Handle7583634

    Article  CAS  PubMed  Google Scholar 

  29. TK Kerppola T Curran (1994) ArticleTitleA conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins. Oncogene 9 3149–3158 Occurrence Handle1:CAS:528:DyaK2cXmvFCgtb8%3D Occurrence Handle7936637

    CAS  PubMed  Google Scholar 

  30. EW Knapik A Goodman M Ekker M Chevrette J Delgado et al. (1998) ArticleTitleA microsatellite genetic linkage map for zebrafish. Nat Genet 18 338–343 Occurrence Handle1:CAS:528:DyaK1cXit1egsro%3D Occurrence Handle9537415

    CAS  PubMed  Google Scholar 

  31. B Li C Tournier RJ Davis RA Flavell (1999) ArticleTitleRegulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J 18 4204–4232

    Google Scholar 

  32. A Lin J Frost T Deng T Smeal (1992) ArticleTitleCasein kinase II is a negative regulator of c-Jun DNA binding and AP-1 activity. Cell 70 777–789 Occurrence Handle1:CAS:528:DyaK38XlvVKjsrc%3D Occurrence Handle1516134

    CAS  PubMed  Google Scholar 

  33. GH May M Funk EJ Black W Clark S Hussain et al. (1998) ArticleTitleAn oncogenic mutation uncouples the v-Jun oncoprotein from positive regulation by the SAPK/JNK pathway in vivo. Curr Biol 8 117–120 Occurrence Handle1:CAS:528:DyaK1cXltlSmtA%3D%3D Occurrence Handle9427647

    CAS  PubMed  Google Scholar 

  34. R Metz AJ Bannister JA Sutherland C Hagemeier EC O'Rourke et al. (1994a) ArticleTitlec-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein. Mol Cell Biol 14 6021–6029 Occurrence Handle1:CAS:528:DyaK2cXlslaitrk%3D

    CAS  Google Scholar 

  35. R Metz T Kouzarides R Bravo (1994b) ArticleTitleA C-terminal domain in FosB, absent in FosB/SF and Fra-1, which is able to interact with the TATA binding protein, is required for altered cell growth. EMBO J 13 3832–3842 Occurrence Handle1:CAS:528:DyaK2cXmtVWktrw%3D

    CAS  Google Scholar 

  36. A Meyer TD Kocher P Basasibwaki AC Wilson (1990) ArticleTitleMonophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347 550–553 Occurrence Handle10.1038/347550a0 Occurrence Handle1:CAS:528:DyaK3cXmt1yhs7w%3D Occurrence Handle2215680

    Article  CAS  PubMed  Google Scholar 

  37. M Murakami MH Sonobe M Ui Y Kabuyama H Watanabe et al. (1997) ArticleTitlePhosphorylation and high level expression of Fra-2 in v-src transformed cells: a pathway of activation of endogenous AP-1. Oncogene 14 2435–2444 Occurrence Handle10.1038/sj.onc.1201077 Occurrence Handle1:CAS:528:DyaK2sXjvVKiurk%3D Occurrence Handle9188858

    Article  CAS  PubMed  Google Scholar 

  38. R Ofir VJ Dwarki D Rashid IM Verma (1990) ArticleTitlePhosphorylation of the C terminus of Fos protein is required for transcriptional transrepression of the c-fos promoter. Nature 348 80–82 Occurrence Handle10.1038/348080a0 Occurrence Handle1:CAS:528:DyaK3MXls1KgsA%3D%3D Occurrence Handle2122257

    Article  CAS  PubMed  Google Scholar 

  39. E Passegue W Jochum M Schorpp-Kistner U Mohle-Steinlein EF Wagner (2001) ArticleTitleChronic myeloid leukemia with increased granulocyte progenitors in mice lacking junB expression in the myeloid lineage. Cell 104 21–32 Occurrence Handle1:CAS:528:DC%2BD3MXis1Oqsrs%3D Occurrence Handle11163237

    CAS  PubMed  Google Scholar 

  40. KK Perkins A Admon N Patel R Tjian (1990) ArticleTitleThe Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. Genes Dev 4 822–834 Occurrence Handle1:CAS:528:DyaK3cXkvFentLo%3D Occurrence Handle2116361

    CAS  PubMed  Google Scholar 

  41. JH Postlethwait YL Yan MA Gates S Horne A Amores et al. (1998) ArticleTitleVertebrate genome evolution and the zebrafish gene map. Nat Genet 18 345–349 Occurrence Handle1:CAS:528:DyaK1cXit1egsrs%3D Occurrence Handle9537416

    CAS  PubMed  Google Scholar 

  42. E Shaulian M Schreiber F Piu M Beeche EF Wagner et al. (2000) ArticleTitleThe mammalian UV response: c-Jun induction is required for exit from p53-imposed growth arrest. Cell 103 897–907 Occurrence Handle1:CAS:528:DC%2BD3cXovFCjtL4%3D Occurrence Handle11136975

    CAS  PubMed  Google Scholar 

  43. SF Smith P Snell F Gruetzner AJ Bench T Haaf et al. (2002) ArticleTitleAnalyses of the extent of shared synteny and conserved gene orders between the genome of Fugu rubripes and human 20q. Genome Res 12 776–784 Occurrence Handle11997344

    PubMed  Google Scholar 

  44. C Sturmbauer A Meyer (1992) ArticleTitleGenetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358 578–581 Occurrence Handle10.1038/358578a0 Occurrence Handle1:STN:280:By2A28rotFw%3D Occurrence Handle1501712

    Article  CAS  PubMed  Google Scholar 

  45. JA Sutherland A Cook AJ Bannister T Kouzarides (1992) ArticleTitleConserved motifs in Fos and Jun define a new class of activation domain. Genes Dev 6 1810–1819 Occurrence Handle1:CAS:528:DyaK38XmtVOntrk%3D Occurrence Handle1516835

    CAS  PubMed  Google Scholar 

  46. R Tjian T Maniatis (1994) ArticleTitleTranscriptional activation: a complex puzzle with few easy pieces. Cell 77 5–8 Occurrence Handle1:CAS:528:DyaK2cXjtFKktbk%3D Occurrence Handle8156597

    CAS  PubMed  Google Scholar 

  47. SJ Triezenberg (1995) ArticleTitleStructure and function of transcriptional activation domains. Curr Opin Genet Dev 5 190–196 Occurrence Handle10.1016/0959-437X(95)80007-7 Occurrence Handle1:CAS:528:DyaK2MXkvFWis7o%3D Occurrence Handle7613088

    Article  CAS  PubMed  Google Scholar 

  48. MK Trower SM Orton IJ Purvis P Sanseau J Riley et al. (1996) ArticleTitleConservation of synteny between the genome of the pufferfish (Fugu rubripes) and the region on human chromosome 14 (14q24.3) associated with familial Alzheimer disease (AD3 locus). Proc Natl Acad Sci USA 93 1366–1369 Occurrence Handle10.1073/pnas.93.4.1366 Occurrence Handle1:CAS:528:DyaK28Xht1ensrw%3D Occurrence Handle8643637

    Article  CAS  PubMed  Google Scholar 

  49. P Vogt (2001) ArticleTitleJun, the oncoprotein. Oncogene 20 2365–2377 Occurrence Handle10.1038/sj.onc.1204443 Occurrence Handle1:CAS:528:DC%2BD3MXjslyrsrw%3D Occurrence Handle11402333

    Article  CAS  PubMed  Google Scholar 

  50. JB Weitzman L Fiette K Matsuo M Yaniv (2000) ArticleTitleJunD protects cells from p53-dependent senescence and apoptosis. Mol Cell 6 1109–1119 Occurrence Handle1:CAS:528:DC%2BD3cXosV2mtrg%3D Occurrence Handle11106750

    CAS  PubMed  Google Scholar 

  51. J Wittbrodt A Meyer M Schartl (1998) ArticleTitleMore genes in fish? Bioessays 20 511–515 Occurrence Handle10.1002/(SICI)1521-1878(199806)20:6<511::AID-BIES10>3.0.CO;2-3

    Article  Google Scholar 

  52. J Yen RM Wisdom I Tratner IM Verma (1991) ArticleTitleAn alternative spliced form of FosB is a negative regulator of transcriptional activation and transformation by Fos proteins. Proc Natl Acad Sci USA 88 5077–5081 Occurrence Handle1:CAS:528:DyaK3MXlt1yrtLg%3D Occurrence Handle1905017

    CAS  PubMed  Google Scholar 

  53. K Zhang JR Chaillet LA Perkins TD Halazonetis N Perrimon (1990) ArticleTitleDrosophila homolog of the mammalian jun oncogene is expressed during embryonic development and activates transcription in mammalian cells. Proc Natl Acad Sci USA 87 6281–6285 Occurrence Handle1:CAS:528:DyaK3MXhvVCqtw%3D%3D Occurrence Handle1696724

    CAS  PubMed  Google Scholar 

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Acknowledgements

Thanks to Dr. Melody Clark for her comments.

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  1. Medical Research Council, UK Human Genome Mapping Project Resource Centre, Hinxton, Cambridge, CB 10 1SB, UK

    Amanda J. Cottage, Yvonne J. K. Edwards & Greg Elgar

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  1. Amanda J. Cottage
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  3. Greg Elgar
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Correspondence to Greg Elgar.

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Cottage, A.J., Edwards, Y.J. & Elgar, G. AP1 genes in Fugu indicate a divergent transcriptional control to that of mammals . Mamm Genome 14, 514–525 (2003). https://doi.org/10.1007/s00335-002-3067-5

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