COP9 signalosome subunits protect capicua from MAPK-dependent and -independent mechanisms of degradation

Development (Cambridge)

Volumn 144, Issue 14, 2017, Pages 2673-2682

  Suisse, Annabelle ^a   He, DanQing ^a   Legent, Kevin ^a,b   Treisman, Jessica E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Teoxane Laboratories   (France)

Author keywords

Capicua; COP9 signalosome; Drosophila melanogaster; EGFR; Nedd8; Ubiquitin ligase; Wing disc

Indexed keywords

COP9 SIGNALOSOME; CULLIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; PROTEIN CAPICUA; REPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CIC PROTEIN, DROSOPHILA; CULLIN 1; DROSOPHILA PROTEIN; EGFR PROTEIN, DROSOPHILA; HIGH MOBILITY GROUP B PROTEIN; MULTIPROTEIN COMPLEX; PEPTIDE HYDROLASE; PROTEIN SUBUNIT; RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EYE DEVELOPMENT; GENE MUTATION; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SUBUNIT; UBIQUITINATION; WING; ANIMAL; BIOLOGICAL MODEL; DROSOPHILA MELANOGASTER; EYE; FEMALE; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MAPK SIGNALING; METABOLISM; MUTATION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CULLIN PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; FEMALE; GENES, INSECT; HMGB PROTEINS; MALE; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; MUTATION; PEPTIDE HYDROLASES; PROTEIN SUBUNITS; PROTEOLYSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; REPRESSOR PROTEINS; UBIQUITINATION; WINGS, ANIMAL;

EID: 85025167539     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.148767     Document Type: Article

References (80)

1. Ajuria, L., Nieva, C., Winkler, C., Kuo, D., Samper, N., Andreu, M. J., Helman, A., Gonzalez-Crespo, S., Paroush, Z., Courey, A. J. et al. (2011). Capicua DNA-binding sites are general response elements for RTK signaling in Drosophila. Development 138, 915-924.
2. Andreu, M. J., Ajuria, L., Samper, N., Gonzalez-Perez, E., Campuzano, S., Gonzalez-Crespo, S. and Jimenez, G. (2012). EGFR-dependent downregulation of Capicua and the establishment of Drosophila dorsoventral polarity. Fly 6, 234-239.
3. Appert-Collin, A., Hubert, P., Cremel, G. and Bennasroune, A. (2015). Role of ErbB receptors in cancer cell migration and invasion. Front. Pharmacol. 6, 283.
4. Astigarraga, S., Grossman, R., Diaz-Delfin, J., Caelles, C., Paroush, Z. and Jimenez, G. (2007). A MAPK docking site is critical for downregulation of Capicua by Torso and EGFR RTK signaling. EMBO J. 26, 668-677.
5. Beckmann, E. A., Kohler, A. M., Meister, C., Christmann, M., Draht, O. W., Rakebrandt, N., Valerius, O. and Braus, G. H. (2015). Integration of the catalytic subunit activates deneddylase activity in vivo as final step in fungal COP9 signalosome assembly. Mol. Microbiol. 97, 110-124.
6. Bettegowda, C., Agrawal, N., Jiao, Y., Sausen, M., Wood, L. D., Hruban, R. H., Rodriguez, F. J., Cahill, D. P., McLendon, R., Riggins, G. et al. (2011). Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333, 1453-1455.
7. Bocca, S. N., Muzzopappa, M., Silberstein, S. and Wappner, P. (2001). Occurrence of a putative SCF ubiquitin ligase complex in Drosophila. Biochem. Biophys. Res. Commun. 286, 357-364.
8. Boh, B. K., Smith, P. G. and Hagen, T. (2011). Neddylation-induced conformational control regulates cullin RING ligase activity in vivo. J. Mol. Biol. 409, 136-145.
9. Cavadini, S., Fischer, E. S., Bunker, R. D., Potenza, A., Lingaraju, G. M., Goldie, K. N., Mohamed, W. I., Faty, M., Petzold, G., Beckwith, R. E. et al. (2016). Cullin-RING ubiquitin E3 ligase regulation by the COP9 signalosome. Nature 531, 598-603.
10. Chamovitz, D. A. (2009). Revisiting the COP9 signalosome as a transcriptional regulator. EMBO Rep. 10, 352-358.
11. Choi, N., Park, J., Lee, J.-S., Yoe, J., Park, G. Y., Kim, E., Jeon, H., Cho, Y. M., Roh, T.-Y. and Lee, Y. (2015). miR-93/miR-106b/miR-375-CIC-CRABP1: a novel regulatory axis in prostate cancer progression. Oncotarget 6, 23533-23547.
12. Cope, G. A. and Deshaies, R. J. (2003). COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell 114, 663-671.
13. Cope, G. A., Suh, G. S., Aravind, L., Schwarz, S. E., Zipursky, S. L., Koonin, E. V. and Deshaies, R. J. (2002). Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298, 608-611.
14. Diaz-Benjumea, F. J. and Hafen, E. (1994). The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development 120, 569-578.
15. Dissanayake, K., Toth, R., Blakey, J., Olsson, O., Campbell, D. G., Prescott, A. R. and MacKintosh, C. (2011). ERK/p90(RSK)/14-3-3 signalling has an impact on expression of PEA3 Ets transcription factors via the transcriptional repressor Capicua. Biochem. J. 433, 515-525.
16. Dressel, U., Thormeyer, D., Altincicek, B., Paululat, A., Eggert, M., Schneider, S., Tenbaum, S. P., Renkawitz, R. and Baniahmad, A. (1999). Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol. Cell. Biol. 19, 3383-3394.
17. Dubiel, D., Rockel, B., Naumann, M. and Dubiel, W. (2015). Diversity of COP9 signalosome structures and functional consequences. FEBS Lett. 589, 2507-2513.
18. Enchev, R. I., Scott, D. C., da Fonseca, P. C., Schreiber, A., Monda, J. K., Schulman, B. A., Peter, M. and Morris, E. P. (2012). Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep. 2, 616-627.
19. Fang, L., Wang, X., Yamoah, K., Chen, P.-L., Pan, Z.-Q. and Huang, L. (2008). Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J. Proteome Res. 7, 4914-4925.
20. Fores, M., Ajuria, L., Samper, N., Astigarraga, S., Nieva, C., Grossman, R., Gonzalez-Crespo, S., Paroush, Z. and Jimenez, G. (2015). Origins of context-dependent gene repression by capicua. PLoS Genet. 11, e1004902.
21. Futran, A. S., Kyin, S., Shvartsman, S. Y. and Link, A. J. (2015). Mapping the binding interface of ERK and transcriptional repressor Capicua using photocrosslinking. Proc. Natl. Acad. Sci. USA 112, 8590-8595.
22. Fuzesi-Levi, M. G., Ben-Nissan, G., Bianchi, E., Zhou, H., Deery, M. J., Lilley, K. S., Levin, Y. and Sharon, M. (2014). Dynamic regulation of the COP9 signalosome in response to DNA damage. Mol. Cell. Biol. 34, 1066-1076.
23. Grimm, O., Sanchez Zini, V., Kim, Y., Casanova, J., Shvartsman, S. Y. and Wieschaus, E. (2012). Torso RTK controls Capicua degradation by changing its subcellular localization. Development 139, 3962-3968.
24. Guruharsha, K. G., Rual, J.-F., Zhai, B., Mintseris, J., Vaidya, P., Vaidya, N., Beekman, C., Wong, C., Rhee, D. Y., Cenaj, O. et al. (2011). A protein complex network of Drosophila melanogaster. Cell 147, 690-703.
25. Hazelett, D. J., Bourouis, M., Walldorf, U. and Treisman, J. E. (1998). decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125, 3741-3751.
26. Hunter, T. (2007). The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738.
27. Janody, F., Lee, J. D., Jahren, N., Hazelett, D. J., Benlali, A., Miura, G. I., Draskovic, I. and Treisman, J. E. (2004). A mosaic genetic screen reveals distinct roles for trithorax and Polycomb group genes in Drosophila eye development. Genetics 166, 187-200.
28. Jarman, A. P., Sun, Y., Jan, L. Y. and Jan, Y. N. (1995). Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121, 2019-2030.
29. Jiang, J. and Struhl, G. (1998). Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493-496.
30. Jimenez, G., Shvartsman, S. Y. and Paroush, Z. (2012). The Capicua repressor–a general sensor of RTK signaling in development and disease. J. Cell Sci. 125, 1383-1391.
31. Lam, Y. C., Bowman, A. B., Jafar-Nejad, P., Lim, J., Richman, R., Fryer, J. D., Hyun, E. D., Duvick, L. A., Orr, H. T., Botas, J. et al. (2006). ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neuropathology. Cell 127, 1335-1347.
32. Lasagna-Reeves, C. A., Rousseaux, M. W., Guerrero-Munoz, M. J., Park, J., Jafar-Nejad, P., Richman, R., Lu, N., Sengupta, U., Litvinchuk, A., Orr, H. T. et al. (2015). A native interactor scaffolds and stabilizes toxic ATAXIN-1 oligomers in SCA1. Elife 4.
33. Lee, D. H. and Goldberg, A. L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403.
34. Lee, J.-H., Yi, L., Li, J., Schweitzer, K., Borgmann, M., Naumann, M. and Wu, H. (2013). Crystal structure and versatile functional roles of the COP9 signalosome subunit 1. Proc. Natl. Acad. Sci. USA 110, 11845-11850.
35. Legent, K., Steinhauer, J., Richard, M. and Treisman, J. E. (2012). A screen for X-linked mutations affecting Drosophila photoreceptor differentiation identifies Casein kinase 1 alpha as an essential negative regulator of Wingless signaling. Genetics 190, 601-616.
36. Li, J.-Y., Chai, B.-X., Zhang, W., Liu, Y.-Q., Ammori, J. B. and Mulholland, M. W. (2007). Ankyrin repeat and SOCS box containing protein 4 (Asb-4) interacts with GPS1 (CSN1) and inhibits c-Jun NH2-terminal kinase activity. Cell. Signal. 19, 1185-1192.
37. Li, W., Zang, B., Liu, C., Lu, L., Wei, N., Cao, K., Deng, X. W. and Wang, X. (2011). TSA1 interacts with CSN1/CSN and may be functionally involved in Arabidopsis seedling development in darkness. J. Genet. Genomics 38, 539-546.
38. Lim, B., Samper, N., Lu, H., Rushlow, C., Jimenez, G. and Shvartsman, S. Y. (2013). Kinetics of gene derepression by ERK signaling. Proc. Natl. Acad. Sci. USA 110, 10330-10335.
39. Lingaraju, G. M., Bunker, R. D., Cavadini, S., Hess, D., Hassiepen, U., Renatus, M., Fischer, E. S. and Thoma, N. H. (2014). Crystal structure of the human COP9 signalosome. Nature 512, 161-165.
40. Lyapina, S., Cope, G., Shevchenko, A., Serino, G., Tsuge, T., Zhou, C., Wolf, D. A., Wei, N., Shevchenko, A. and Deshaies, R. J. (2001). Promotion of NEDD8-CUL1 conjugate cleavage by COP9 signalosome. Science 292, 1382-1385.
41. McKay, M. M. and Morrison, D. K. (2007). Integrating signals from RTKs to ERK/ MAPK. Oncogene 26, 3113-3121.
42. Merlet, J., Burger, J., Gomes, J.-E. and Pintard, L. (2009). Regulation of cullin-RING E3 ubiquitin-ligases by neddylation and dimerization. Cell. Mol. Life Sci. 66, 1924-1938.
43. Miura, G. I., Buglino, J., Alvarado, D., Lemmon, M. A., Resh, M. D. and Treisman, J. E. (2006). Palmitoylation of the EGFR ligand Spitz by Rasp increases Spitz activity by restricting its diffusion. Dev. Cell 10, 167-176.
44. Moberg, K. H., Bell, D. W., Wahrer, D. C., Haber, D. A. and Hariharan, I. K. (2001). Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413, 311-316.
45. Mosadeghi, R., Reichermeier, K. M., Winkler, M., Schreiber, A., Reitsma, J. M., Zhang, Y., Stengel, F., Cao, J., Kim, M., Sweredoski, M. J. et al. (2016). Structural and kinetic analysis of the COP9-Signalosome activation and the cullin-RING ubiquitin ligase deneddylation cycle. Elife 5.
46. Motzny, C. K. and Holmgren, R. (1995). The Drosophila Cubitus interruptus protein and its role in the Wingless and Hedgehog signal transduction pathways. Mech. Dev. 52, 137-150.
47. Mummery-Widmer, J. L., Yamazaki, M., Stoeger, T., Novatchkova, M., Bhalerao, S., Chen, D., Dietzl, G., Dickson, B. J. and Knoblich, J. A. (2009). Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 458, 987-992.
48. Nawrocki, S. T., Griffin, P., Kelly, K. R. and Carew, J. S. (2012). MLN4924: a novel first-in-class inhibitor of NEDD8-activating enzyme for cancer therapy. Expert Opin. Investig. Drugs 21, 1563-1573.
49. Okimoto, R. A., Breitenbuecher, F., Olivas, V. R., Wu, W., Gini, B., Hofree, M., Asthana, S., Hrustanovic, G., Flanagan, J., Tulpule, A. et al. (2016). Inactivation of Capicua drives cancer metastasis. Nat. Genet. 49, 87-96.
50. O’Neill, E. M., Rebay, I., Tjian, R. and Rubin, G. M. (1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137-147.
51. Oren-Giladi, P., Krieger, O., Edgar, B. A., Chamovitz, D. A. and Segal, D. (2008). Cop9 signalosome subunit 8 (CSN8) is essential for Drosophila development. Genes Cells 13, 221-231.
52. Oron, E., Mannervik, M., Rencus, S., Harari-Steinberg, O., Neuman-Silberberg, S., Segal, D. and Chamovitz, D. A. (2002). COP9 signalosome subunits 4 and 5 regulate multiple pleiotropic pathways in Drosophila melanogaster. Development 129, 4399-4409.
53. Oron, E., Tuller, T., Li, L., Rozovsky, N., Yekutieli, D., Rencus-Lazar, S., Segal, D., Chor, B., Edgar, B. A. and Chamovitz, D. A. (2007). Genomic analysis of COP9 signalosome function in Drosophila melanogaster reveals a role in temporal regulation of gene expression. Mol. Syst. Biol. 3, 108.
54. Ou, C.-Y., Lin, Y. F., Chen, Y. J. and Chien, C. T. (2002). Distinct protein degradation mechanisms mediated by Cul1 and Cul3 controlling Ci stability in Drosophila eye development. Genes Dev. 16, 2403-2414.
55. Pan, L., Wang, S., Lu, T., Weng, C., Song, X., Park, J. K., Sun, J., Yang, Z. H., Yu, J., Tang, H. et al. (2014). Protein competition switches the function of COP9 from self-renewal to differentiation. Nature 514, 233-236.
56. Pick, E. and Bramasole, L. (2014). Moonlighting and pleiotropy within two regulators of the degradation machinery: the proteasome lid and the CSN. Biochem. Soc. Trans. 42, 1786-1791.
57. Pierce, N. W., Lee, J. E., Liu, X., Sweredoski, M. J., Graham, R. L., Larimore, E. A., Rome, M., Zheng, N., Clurman, B. E., Hess, S. et al. (2013). Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins. Cell 153, 206-215.
58. Richardson, H., O’Keefe, L. V., Marty, T. and Saint, R. (1995). Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121, 3371-3379.
59. Roch, F., Jimenez, G. and Casanova, J. (2002). EGFR signalling inhibits Capicua-dependent repression during specification of Drosophila wing veins. Development 129, 993-1002.
60. Rozen, S., Fuzesi-Levi, M. G., Ben-Nissan, G., Mizrachi, L., Gabashvili, A., Levin, Y., Ben-Dor, S., Eisenstein, M. and Sharon, M. (2015). CSNAP is a stoichiometric subunit of the COP9 signalosome. Cell Rep. 13, 585-598.
61. Saha, A. and Deshaies, R. J. (2008). Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell 32, 21-31.
62. Schutz, A. K., Hennes, T., Jumpertz, S., Fuchs, S. and Bernhagen, J. (2012). Role of CSN5/JAB1 in Wnt/beta-catenin activation in colorectal cancer cells. FEBS Lett. 586, 1645-1651.
63. Schweitzer, R., Shaharabany, M., Seger, R. and Shilo, B. Z. (1995). Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 9, 1518-1529.
64. Singer, R., Atar, S., Atias, O., Oron, E., Segal, D., Hirsch, J. A., Tuller, T., Orian, A. and Chamovitz, D. A. (2014). Drosophila COP9 signalosome subunit 7 interacts with multiple genomic loci to regulate development. Nucleic Acids Res. 42, 9761-9770.
65. Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S. et al. (2009). An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736.
66. Suh, G. S., Poeck, B., Chouard, T., Oron, E., Segal, D., Chamovitz, D. A. and Zipursky, S. L. (2002). Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33, 35-46.
67. Sun, Y., Wilson, M. P. and Majerus, P. W. (2002). Inositol 1,3,4-trisphosphate 5/6-kinase associates with the COP9 signalosome by binding to CSN1. J. Biol. Chem. 277, 45759-45764.
68. Tseng, A. S., Tapon, N., Kanda, H., Cigizoglu, S., Edelmann, L., Pellock, B., White, K. and Hariharan, I. K. (2007). Capicua regulates cell proliferation downstream of the receptor tyrosine kinase/ras signaling pathway. Curr. Biol. 17, 728-733.
69. Tsuge, T., Matsui, M. and Wei, N. (2001). The subunit 1 of the COP9 signalosome suppresses gene expression through its N-terminal domain and incorporates into the complex through the PCI domain. J. Mol. Biol. 305, 1-9.
70. Tsuge, T., Menon, S., Tong, Y. and Wei, N. (2011). CSN1 inhibits c-Jun phosphorylation and down-regulates ectopic expression of JNK1. Protein Cell 2, 423-432.
71. Wang, X., Kang, D., Feng, S., Serino, G., Schwechheimer, C. and Wei, N. (2002). CSN1 N-terminal-dependent activity is required for Arabidopsis development but not for Rub1/Nedd8 deconjugation of cullins: a structure-function study of CSN1 subunit of COP9 signalosome. Mol. Biol. Cell 13, 646-655.
72. Wei, N. and Deng, X. W. (2003). The COP9 signalosome. Annu. Rev. Cell Dev. Biol. 19, 261-286.
73. Welcker, M. and Clurman, B. E. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83-93.
74. Worby, C. A., Simonson-Leff, N. and Dixon, J. E. (2001). RNA interference of gene expression (RNAi) in cultured Drosophila cells. Sci. STKE 2001, pl1.
75. Wu, J. T., Lin, H. C., Hu, Y. C. and Chien, C. T. (2005). Neddylation and deneddylation regulate Cul1 and Cul3 protein accumulation. Nat. Cell Biol. 7, 1014-1020.
76. Wu, J.-T., Lin, W.-H., Chen, W.-Y., Huang, Y.-C., Tang, C.-Y., Ho, M. S., Pi, H. and Chien, C.-T. (2011). CSN-mediated deneddylation differentially modulates Ci (155) proteolysis to promote Hedgehog signalling responses. Nat. Commun. 2, 182.
77. Wu, K., Chong, R. A., Yu, Q., Bai, J., Spratt, D. E., Ching, K., Lee, C., Miao, H., Tappin, I., Hurwitz, J. et al. (2016). Suramin inhibits cullin-RING E3 ubiquitin ligases. Proc. Natl. Acad. Sci. USA 113, E2011-E2018.
78. Yang, L. and Baker, N. E. (2003). Cell cycle withdrawal, progression, and cell survival regulation by EGFR and its effectors in the differentiating Drosophila eye. Dev. Cell 4, 359-369.
79. Yang, L., Paul, S., Trieu, K. G., Dent, L. G., Froldi, F., Fores, M., Webster, K., Siegfried, K. R., Kondo, S., Harvey, K. et al. (2016). Minibrain and Wings apart control organ growth and tissue patterning through down-regulation of Capicua. Proc. Natl. Acad. Sci. USA 113, 10583-10588.
80. Zhou, C., Wee, S., Rhee, E., Naumann, M., Dubiel, W. and Wolf, D. A. (2003). Fission yeast COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p. Mol. Cell 11, 927-938.