Jab1 as a Mediator of Nuclear Export and Cytoplasmic Degradation of p53

  • Lee, Eun-Woo (Department of Food Science and Biotechnology, Faculty of Life Science and Technology, Sungkyunkwan University) ;
  • Oh, Wonkyung (Department of Food Science and Biotechnology, Faculty of Life Science and Technology, Sungkyunkwan University) ;
  • Song, Jaewhan (Department of Food Science and Biotechnology, Faculty of Life Science and Technology, Sungkyunkwan University)
  • Received : 2006.09.14
  • Accepted : 2006.09.27
  • Published : 2006.10.31

Abstract

Jun activation domain-binding protein 1 (Jab1) is involved in various cellular mechanisms including development in Drosophila and mouse, cell cycle control and signal transduction pathways. Recent studies also determined that Jab1 functions as a nuclear exporter and inducer of cytoplasmic degradation for several proteins including p53, p27, capsid of West Nile virus, and Smad4/7 proteins. In particular, p53 is shown to bind to and to be exported into the cytoplasm by Jab1, which helps to maintain low levels of p53 under normal conditions. This review was undertaken in an effort to understand the biological significance of the homeostasis of p53 as maintained in the presence of Jab1. Based on our observations, we have provided potential mechanistic hypotheses for the nuclear export of p53 in coordination with Jab1 and the role of other factors in these processes.

Keywords

Acknowledgement

Supported by : Ottogi Inc.

References

  1. Ambroggio, X. I., Rees, D. C., and Deshaies, R. J. (2004) JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol. 2, E2 https://doi.org/10.1371/journal.pbio.0020002
  2. Bae, M. K., Ahn, M. Y., Jeong, J. W., Bae, M. H., Lee, Y. M., et al. (2002) Jab1 interacts directly with HIF-1alpha and regulates its stability. J. Biol. Chem. 277, 9−12 https://doi.org/10.1074/jbc.C100442200
  3. Bech-Otschir, D., Kraft, R., Huang, X., Henklein, P., Kapelari, B., et al. (2001) COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J. 20, 1630−1639 https://doi.org/10.1093/emboj/20.7.1630
  4. Bernardi, R., Scaglioni, P. P., Bergmann, S., Horn, H. F., Vousden, K. H., et al. (2004) PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat. Cell. Biol. 6, 665− 672 https://doi.org/10.1038/ncb1147
  5. Bianchi, E., Denti, S., Granata, A., Bossi, G., Geginat, J., et al. (2000) Integrin LFA-1 interacts with the transcriptional coactivator JAB1 to modulate AP-1 activity. Nature 404, 617− 621 https://doi.org/10.1038/35007098
  6. Bode, A. M. and Dong, Z. (2004) Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 4, 793−805 https://doi.org/10.1038/nrc1455
  7. Boyd, S. D., Tsai, K. Y., and Jacks, T. (2000) An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell. Biol. 2, 563−568 https://doi.org/10.1038/35023500
  8. Brooks, C. L., Li, M., and Gu, W. (2004) Monoubiquitination: the signal for p53 nuclear export? Cell Cycle 3, 436−438
  9. Callige, M., Kieffer, I., and Richard-Foy, H. (2005) CSN5/Jab1 is involved in ligand-dependent degradation of estrogen receptor {alpha} by the proteasome. Mol. Cell. Biol. 25, 4349− 4358 https://doi.org/10.1128/MCB.25.11.4349-4358.2005
  10. Chamovitz, D. A., Wei, N., Osterlund, M. T., von Arnim, A. G., Staub, J. M., et al. (1996) The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 86, 115−121
  11. Chauchereau, A., Georgiakaki, M., Perrin-Wolff, M., Milgrom, E., and Loosfelt, H. (2000) JAB1 interacts with both the progesterone receptor and SRC-1. J Biol Chem, 275, 8540−8548 https://doi.org/10.1074/jbc.275.12.8540
  12. Claret, F. X., Hibi, M., Dhut, S., Toda, T., and Karin, M. (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383, 453−457 https://doi.org/10.1038/383453a0
  13. Cope, G. A. and Deshaies, R. J. (2006) Targeted silencing of Jab1/Csn5 in human cells downregulates SCF activity through reduction of F-box protein levels. BMC Biochem. 7, 1 https://doi.org/10.1186/1471-2091-7-1
  14. Cope, G. A., Suh, G. S., Aravind, L., Schwarz, S. E., Zipursky, S. L., et al. (2002) Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298, 608−611
  15. Dornan, D., Wertz, I., Shimizu, H., Arnott, D., Frantz, G. D., et al. (2004) The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 429, 86−92 https://doi.org/10.1038/nature02514
  16. Doronkin, S., Djagaeva, I., and Beckendorf, S. K. (2003) The COP9 signalosome promotes degradation of Cyclin E during early Drosophila oogenesis. Dev. Cell 4, 699−710 https://doi.org/10.1016/S1534-5807(03)00121-7
  17. Freedman, D. A. and Levine, A. J. (1998) Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18, 7288−7293
  18. Geyer, R. K., Yu, Z. K., and Maki, C. G. (2000) The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat. Cell. Biol. 2, 569−573 https://doi.org/10.1038/35023507
  19. Gronroos, E., Terentiev, A. A., Punga, T., and Ericsson, J. (2004) YY1 inhibits the activation of the p53 tumor suppressor in response to genotoxic stress. Proc. Natl. Acad. Sci. USA 101, 12165−12170
  20. Grossman, S. R., Deato, M. E., Brignone, C., Chan, H. M., Kung, A. L., et al. (2003) Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 300, 342−344 https://doi.org/10.1126/science.1080386
  21. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387, 296−299
  22. Kim, B. C., Lee, H. J., Park, S. H., Lee, S. R., Karpova, T. S., et al. (2004) Jab1/CSN5, a component of the COP9 signalosome, regulates transforming growth factor beta signaling by binding to Smad7 and promoting its degradation. Mol. Cell. Biol. 24, 2251−2262 https://doi.org/10.1128/MCB.24.6.2251-2262.2004
  23. Kleemann, R., Hausser, A., Geiger, G., Mischke, R., Burger- Kentischer, A., et al. (2000) Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408, 211−216 https://doi.org/10.1038/35041591
  24. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997) Regulation of p53 stability by Mdm2. Nature 387, 299−303
  25. Lane, D. P. (1992) Cancer. p53, guardian of the genome. Nature 358, 15−16
  26. Leng, R. P., Lin, Y., Ma, W., Wu, H., Lemmers, B., et al. (2003) Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell 112, 779−791 https://doi.org/10.1016/S0092-8674(03)00193-4
  27. Levine, A. J. (1997) p53, the cellular gatekeeper for growth and division. Cell 88, 323−331
  28. Levinson, H., Sil, A. K., Conwell, J. E., Hopper, J. E., and Ehrlich, H. P. (2004) Alpha V integrin prolongs collagenase production through Jun activation binding protein 1. Ann. Plast. Surg. 53, 155−161 https://doi.org/10.1097/01.sap.0000112281.97409.a6
  29. Li, M., Brooks, C. L., Wu-Baer, F., Chen, D., Baer, R., et al. (2003) Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302, 1972−1975 https://doi.org/10.1126/science.1091362
  30. Li, S., Liu, X., and Ascoli, M. (2000) p38JAB1 binds to the intracellular precursor of the lutropin/choriogonadotropin receptor and promotes its degradation. J. Biol. Chem. 275, 13386−13393
  31. Louria-Hayon, I., Grossman, T., Sionov, R. V., Alsheich, O., Pandolfi, P. P., et al. (2003) The promyelocytic leukemia protein protects p53 from Mdm2-mediated inhibition and degradation. J. Biol. Chem. 278, 33134−33141 https://doi.org/10.1074/jbc.M301264200
  32. Lu, C., Li, Y., Zhao, Y., Xing, G., Tang, F., et al. (2002) Intracrine hepatopoietin potentiates AP-1 activity through JAB1 independent of MAPK pathway. FASEB J. 16, 90−92
  33. Lyapina, S., Cope, G., Shevchenko, A., Serino, G., Tsuge, T., et al. (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292, 1382−1385 https://doi.org/10.1126/science.1059780
  34. O'Brate, A. and Giannakakou, P. (2003) The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist. Updat. 6, 313−322 https://doi.org/10.1016/j.drup.2003.10.004
  35. Oh, W., Lee, E. W., Sung, Y. H., Yang, M. R., Ghim, J., et al. (2006a) Jab1 induces the cytoplasmic localization and degradation of p53 in coordination with Hdm2. J. Biol. Chem. 281, 17457−17465 https://doi.org/10.1074/jbc.M601857200
  36. Oh, W., Yang, M. R., Lee, E. W., Park, K. M., Pyo, S., et al. (2006b) Jab1 mediates cytoplasmic localization and degradation of West Nile Virus capsid protein. J. Biol. Chem. (in press)
  37. Querido, E., Blanchette, P., Yan, Q., Kamura, T., Morrison, M., et al. (2001) Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15, 3104−3117 https://doi.org/10.1101/gad.926401
  38. Roth, J., Dobbelstein, M., Freedman, D. A., Shenk, T., and Levine, A. J. (1998) Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17, 554−564 https://doi.org/10.1093/emboj/17.2.554
  39. Sherr, C. J. and Weber, J. D. (2000) The ARF/p53 pathway. Curr. Opin. Genet. Dev. 10, 94−99
  40. Shirangi, T. R., Zaika, A., and Moll, U. M. (2002) Nuclear degradation of p53 occurs during down-regulation of the p53 response after DNA damage. FASEB J. 16, 420−422
  41. Shvarts, A., Steegenga, W. T., Riteco, N., van Laar, T., Dekker, P., et al. (1996) MDMX: a novel p53-binding protein with some functional properties of MDM2. EMBO J. 15, 5349− 5357
  42. Stommel, J. M., Marchenko, N. D., Jimenez, G. S., Moll, U. M., Hope, T. J., et al. (1999) A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18, 1660−1672 https://doi.org/10.1093/emboj/18.6.1660
  43. Sui, G., Affar el, B., Shi, Y., Brignone, C., Wall, N. R., et al. (2004) Yin Yang 1 is a negative regulator of p53. Cell 117, 859−872 https://doi.org/10.1016/j.cell.2004.06.004
  44. Tanaka, Y., Kanai, F., Ichimura, T., Tateishi, K., Asaoka, Y., et al. (2006) The hepatitis B virus X protein enhances AP-1 activation through interaction with Jab1. Oncogene 25, 633−642
  45. Tomoda, K., Kubota, Y., Arata, Y., Mori, S., Maeda, M., et al. (2002) The cytoplasmic shuttling and subsequent degradation of p27Kip1 mediated by Jab1/CSN5 and the COP9 signalosome complex. J. Biol. Chem. 277, 2302−2310
  46. Tomoda, K., Kubota, Y., and Kato, J. (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 398, 160−165 https://doi.org/10.1038/18230
  47. Tomoda, K., Yoneda-Kato, N., Fukumoto, A., Yamanaka, S., and Kato, J. Y. (2004) Multiple functions of Jab1 are required for early embryonic development and growth potential in mice. J. Biol. Chem. 279, 43013−43018 https://doi.org/10.1074/jbc.M406559200
  48. Verma, R., Aravind, L., Oania, R., McDonald, W. H., Yates, J. R., 3rd, et al. (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611−615
  49. Vousden, K. H. and Lu, X. (2002) Live or let die: the cell's response to p53. Nat. Rev. Cancer 2, 594−604
  50. Wan, M., Cao, X., Wu, Y., Bai, S., Wu, L., et al. (2002) Jab1 antagonizes TGF-beta signaling by inducing Smad4 degradation. EMBO Rep. 3, 171−176 https://doi.org/10.1093/embo-reports/kvf024
  51. Wang, Y., Lu, C., Wei, H., Wang, N., Chen, X., et al. (2004a) Hepatopoietin interacts directly with COP9 signalosome and regulates AP-1 activity. FEBS Lett. 572, 85−91 https://doi.org/10.1016/j.febslet.2004.07.012
  52. Wang, Z. Q., Wei, H. D., and He, F. C. (2004b) Protein product encoded by a human novel gene E9730 enhances AP-1 activity through interacting with Jab1. Acta Biochim. Biophys. Sin (Shanghai) 36, 11−15 https://doi.org/10.1093/abbs/36.1.11
  53. Weber, J. D., Taylor, L. J., Roussel, M. F., Sherr, C. J., and Bar- Sagi, D. (1999) Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell. Biol. 1, 20−26 https://doi.org/10.1038/8991
  54. Wei, N., Chamovitz, D. A., and Deng, X. W. (1994) Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development. Cell 78, 117−124
  55. Wei, N. and Deng, X. W. (1999) Making sense of the COP9 signalosome. A regulatory protein complex conserved from Arabidopsis to human. Trends Genet. 15, 98−103
  56. Woods, D. B. and Vousden, K. H. (2001) Regulation of p53 function. Exp. Cell. Res. 264, 56−66
  57. Yang, X., Menon, S., Lykke-Andersen, K., Tsuge, T., Di, X., et al. (2002) The COP9 signalosome inhibits p27(kip1) degradation and impedes G1-S phase progression via deneddylation of SCF Cul1. Curr. Biol. 12, 667−672 https://doi.org/10.1016/S0960-9822(02)00791-1
  58. Yang, Y., Li, C. C., and Weissman, A. M. (2004) Regulating the p53 system through ubiquitination. Oncogene 23, 2096−2106 https://doi.org/10.1038/sj.onc.1207411
  59. Yu, Z. K., Geyer, R. K., and Maki, C. G. (2000) MDM2-dependent ubiquitination of nuclear and cytoplasmic P53. Oncogene 19, 5892−5897 https://doi.org/10.1038/sj.onc.1203980