The arabidopsis COP9 SIGNALOSOME INTERACTING F-BOX KELCH 1 protein forms an SCF ubiquitin ligase and regu

Molecular Plant

Volumn 6, Issue 5, 2013, Pages 1616-1629

  Franciosini, Anna ^a   Lombardi, Benedetta ^a   Iafrate, Silvia ^a   Pecce, Valeria ^a   Mele, Giovanni ^b   Lupacchini, Leonardo ^a   Rinaldi, Gianmarco ^a   Kondou, Youichi ^c   Gusmaroli, Giuliana ^d,e   Aki, Shiori ^f   Tsuge, Tomohiko ^f   Deng, Xing Wang ^d   Matsui, Minami ^c   Vittorioso, Paola ^a   Costantino, Paolo ^a   Serino, Giovanna ^a,g  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CNR   (Italy)

^c Elements Chemistry Laboratory   (Japan)

^d YALE UNIVERSITY   (United States)

^e UNIVERSITY OF SOUTH CAROLINA BEAUFORT   (United States)

^f KYOTO UNIVERSITY   (Japan)

^g NEW YORK BOTANICAL GARDEN   (United States)

Author keywords

Arabidopsis thaliana; COP9 signalosome; F box protein; hypocotyl elongation; proteasome; seedling development; ubiquitin

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

ARABIDOPSIS PROTEIN; CFK1 PROTEIN, ARABIDOPSIS; COP9 SIGNALOSOME; F BOX PROTEIN; MESSENGER RNA; MULTIPROTEIN COMPLEX; PEPTIDE HYDROLASE; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CELL SIZE; CHEMISTRY; CYTOLOGY; DOWN REGULATION; ENZYMOLOGY; F-BOX PROTEIN; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPOCOTYL ELONGATION; LIGHT; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PLANT GENE; PLANT GROWTH; PROTEIN DEGRADATION; PROTEIN STABILITY; RADIATION EXPOSURE; SEEDLING DEVELOPMENT.; TRANSGENIC PLANT; UBIQUITINATION;

ARABIDOPSIS THALIANA; COP9 SIGNALOSOME; F-BOX PROTEIN; HYPOCOTYL ELONGATION; PROTEASOME; SEEDLING DEVELOPMENT.; UBIQUITIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL SIZE; DOWN-REGULATION; F-BOX PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYPOCOTYL; LIGHT; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PEPTIDE HYDROLASES; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; RNA, MESSENGER; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITINATION;

EID: 84885038670     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst045     Document Type: Article

References (64)

1. Adams, J., Kelso, R., and Cooley, L. (2000). The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 10, 17-24.
2. Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M., Harper, J.W., and Elledge, S.J. (1996). SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell. 86, 263-274.
3. Bennett, E.J., Rush, J., Gygi, S.P., and Harper, J.W. (2010). Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell. 143, 951-965.
4. Chamovitz, D.A., et al. (1996). The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell. 86, 115-121.
5. Chen, H., et al. (2010). Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1- SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell. 22, 108-123.
6. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
7. 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.
8. Cope, G.A., et al. (2002). Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science. 298, 608-611.
9. Denti, S., Fernandez-Sanchez, M.E., Rogge, L., and Bianchi, E. (2006). The COP9 signalosome regulates Skp2 levels and proliferation of human cells. J. Biol. Chem. 281, 32188-32196.
10. Dohmann, E.M., Kuhnle, C., and Schwechheimer, C. (2005). Loss of the CONSTITUTIVE PHOTOMORPHOGENIC9 signalosome subunit 5 is sufficient to cause the cop/det/fus mutant phenotype in Arabidopsis. Plant Cell. 17, 1967-1978.
11. Dohmann, E.M., Levesque, M.P., Isono, E., Schmid, M., and Schwechheimer, C. (2008). Auxin responses in mutants of the Arabidopsis CONSTITUTIVE PHOTOMORPHOGENIC9 signalosome. Plant Physiol. 147, 1369-1379.
12. Dohmann, E.M., Nill, C., and Schwechheimer, C. (2010). DELLA proteins restrain germination and elongation growth in Arabidopsis thaliana COP9 signalosome mutants. Eur. J. Cell Biol. 89, 163-168.
13. Duda, D.M., Borg, L.A., Scott, D.C., Hunt, H.W., Hammel, M., and Schulman, B.A. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell. 134, 995-1006.
14. Emberley, E.D., Mosadeghi, R., and Deshaies, R.J. (2012). Deconjugation of Nedd8 from Cul1 is directly regulated by Skp1-F-box and substrate, and the COP9 signalosome inhibits deneddylated SCF by a noncatalytic mechanism. J. Biol. Chem. 287, 29679-29689.
15. Enchev, R.I., et al. (2012). Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep. 2, 616-627.
16. Feldman, R.M., Correll, C.C., Kaplan, K.B., and Deshaies, R.J. (1997). A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell. 91, 221-230.
17. Feng, S., et al. (2003). The COP9 signalosome interacts physically with SCF COI1 and modulates jasmonate responses. Plant Cell. 15, 1083-1094.
18. Fischer, E.S., et al. (2011). The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell. 147, 1024-1039.
19. Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M., and Vierstra, R.D. (2002). The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl Acad. Sci. U S A. 99, 11519-11524.
20. Galan, J.M., and Peter, M. (1999). Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proc. Natl Acad. Sci. U S A. 96, 9124-9129.
21. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M., and Hofte, H. (1997). Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295-305.
22. Golemis, E. A., and Khazak, V. (1997). Alternative yeast two-hybrid systems. The interaction trap and interaction mating. Methods Mol. Biol. 63, 197-218.
23. Gray, W.M., et al. (1999). Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev. 13, 1678-1691.
24. Gusmaroli, G., Feng, S., and Deng, X.W. (2004). The Arabidopsis CSN5A and CSN5B subunits are present in distinct COP9 signalosome complexes, and mutations in their JAMM domains exhibit differential dominant negative effects on development. Plant Cell. 16, 2984-3001.
25. Gusmaroli, G., Figueroa, P., Serino, G., and Deng, X.W. (2007). Role of the MPN subunits in COP9 signalosome assembly and activity, and their regulatory interaction with Arabidopsis Cullin3- based E3 ligases. Plant Cell. 19, 564-581.
26. He, Q., Cheng, P., and Liu, Y. (2005). The COP9 signalosome regulates the Neurospora circadian clock by controlling the stability of the SCFFWD-1 complex. Genes Dev. 19, 1518-1531.
27. Heazlewood, J.L., Verboom, R.E., Tonti-Filippini, J., Small, I., and Millar, A.H. (2007). SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res. 35, D213-D218.
28. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
29. Hua, Z., and Vierstra, R.D. (2011). The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 62, 299-334.
30. Hudson, A.M., and Cooley, L. (2008). Phylogenetic, structural and functional relationships between WD- and Kelch-repeat proteins. Subcell. Biochem. 48, 6-19.
31. Kao, W.H., Beaudenon, S.L., Talis, A.L., Huibregtse, J.M., and Howley, P.M. (2000). Human papillomavirus type 16 E6 induces self-ubiquitination of the E6AP ubiquitin-protein ligase. J. Virol. 74, 6408-6417.
32. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
33. Kwok, S.F., Piekos, B., Misera, S., and Deng, X.W. (1996). A complement of ten essential and pleiotropic Arabidopsis COP/DET/ FUS genes is necessary for repression of photomorphogenesis in darkness. Plant Physiol. 110, 731-742.
34. Kwok, S.F., et al. (1998). Arabidopsis homologs of a c-Jun coactivator are present both in monomeric form and in the COP9 complex, and their abundance is differentially affected by the pleiotropic cop/det/fus mutations. Plant Cell. 10, 1779-1790.
35. Kwok, S.F., Staub, J.M., and Deng, X.W. (1999). Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex. J. Mol. Biol. 285, 85-95.
36. Lee, D.H., and Goldberg, A.L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403.
37. Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I., and Kim, W.T. (2009). Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell. 21, 622-641.
38. Letunic, I., Doerks, T., and Bork, P. (2009). SMART 6: recent updates and new developments. Nucleic Acids Res. 37, D229-D232.
39. Luke-Glaser, S., et al. (2007). CIF-1, a shared subunit of the COP9/ signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol. Cell. Biol. 27, 4526-4540.
40. Lyapina, S., et al. (2001). Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science. 292, 1382-1385.
41. Mathias, N., Johnson, S., Byers, B., and Goebl, M. (1999). The abundance of cell cycle regulatory protein Cdc4p is controlled by interactions between its F box and Skp1p. Mol. Cell. Biol. 19, 1759-1767.
42. Peng, Z., et al. (2001). The cellular level of PR500, a protein complex related to the 19S regulatory particle of the proteasome, is regulated in response to stresses in plants. Mol. Biol. Cell. 12, 383-392.
43. Rouillon, A., Barbey, R., Patton, E.E., Tyers, M., and Thomas, D. (2000). Feedback-regulated degradation of the transcriptional activator Met4 is triggered by the SCF(Met30)complex. EMBO J. 19, 282-294.
44. Saha, A., and Deshaies, R.J. (2008). Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell. 32, 21-31.
45. Schmidt, M.W., McQuary, P.R., Wee, S., Hofmann, K., and Wolf, D.A. (2009). F-box-directed CRL complex assembly and regulation by the CSN and CAND1. Mol. Cell. 35, 586-597.
46. Schwechheimer, C., et al. (2001). Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response. Science. 292, 1379-1382.
47. Serino, G., et al. (2003). Characterization of the last subunit of the Arabidopsis COP9 signalosome: implications for the overall structure and origin of the complex. Plant Cell. 15, 719-731.
48. Serino, G., Tsuge, T., Kwok, S., Matsui, M., Wei, N., and Deng, X.W. (1999). Arabidopsis cop8 and fus4 mutations define the same gene that encodes subunit 4 of the COP9 signalosome. Plant Cell. 11, 1967-1980.
49. Skowyra, D., Craig, K.L., Tyers, M., Elledge, S.J., and Harper, J.W. (1997). F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell. 91, 209-219.
50. Spoel, S.H., Mou, Z., Tada, Y., Spivey, N.W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell. 137, 860-872.
51. Tsukaya, H., Tsuge, T., and Uchimiya, H. (1994). The cotyledon: a superior system for studies of leaf development. Planta. 195, 309-312.
52. Vittorioso, P., Cowling, R., Faure, J.D., Caboche, M., and Bellini, C. (1998). Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol. Cell. Biol. 18, 3034-3043.
53. Wang, X., et al. (2003). The COP9 signalosome interacts with SCF UFO and participates in Arabidopsis flower development. Plant Cell. 15, 1071-1082.
54. Wee, S., Geyer, R.K., Toda, T., and Wolf, D.A. (2005). CSN facilitates Cullin-RING ubiquitin ligase function by counteracting autocatalytic adapter instability. Nat. Cell Biol. 7, 387-391.
55. Wei, N., Serino, G., and Deng, X.W. (2008). The COP9 signalosome: more than a protease. Trends Biochem. Sci. 33, 592-600.
56. Wesley, S.V., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581-590.
57. Woody, S.T., Austin-Phillips, S., Amasino, R.M., and Krysan, P.J. (2007). The WiscDsLox T-DNA collection: an Arabidopsis community resource generated by using an improved highthroughput T-DNA sequencing pipeline. J. Plant Res. 120, 157-165.
58. Yamoah, K., Oashi, T., Sarikas, A., Gazdoiu, S., Osman, R., and Pan, Z.Q. (2008). Autoinhibitory regulation of SCF-mediated ubiquitination by human cullin 1's C-terminal tail. Proc. Natl Acad. Sci. U S A. 105, 12230-12235.
59. Yan, J., et al. (2013). The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFC°I1 and degraded via the 26S proteasome pathway. Plant Cell. 5 Feb. [Epub ahead of print]
60. Zhou, C., et al. (2001). The fission yeast COP9/signalosome is involved in cullin modification by ubiquitin-related Ned8p. BMC Biochem. 2, 7.
61. 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.
62. Zhou, P., and Howley, P.M. (1998). Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. Mol. Cell. 2, 571-580.
63. Zhou, Z., Wang, Y., Cai, G., and He, Q. (2012). Neurospora COP9 signalosome integrity plays major roles for hyphal growth, conidial development, and circadian function. PLoS Genet. 8, e1002712.
64. Zuo, J., Niu, Q.W., and Chua, N.H. (2000). Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265-273.