Primate-specific isoform of Nedd4-1 regulates substrate binding via Ser/Thr phosphorylation and 14-3-3 binding.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 10 2023
20 10 2023
Historique:
received:
06
07
2023
accepted:
12
10
2023
medline:
31
10
2023
pubmed:
21
10
2023
entrez:
20
10
2023
Statut:
epublish
Résumé
Nedd4 (Nedd4-1) is an E3 ubiquitin ligase involved in crucial biological processes such as growth factor receptor signaling. While canonical Nedd4-1 comprises a C2-WW
Identifiants
pubmed: 37863970
doi: 10.1038/s41598-023-44761-9
pii: 10.1038/s41598-023-44761-9
pmc: PMC10589272
doi:
Substances chimiques
14-3-3 Proteins
0
Endosomal Sorting Complexes Required for Transport
0
Nedd4 Ubiquitin Protein Ligases
EC 2.3.2.26
Protein Isoforms
0
Ubiquitin-Protein Ligases
EC 2.3.2.27
Nedd4 protein, human
EC 2.3.2.26
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
17903Subventions
Organisme : CIHR
ID : FDN-387969
Pays : Canada
Informations de copyright
© 2023. Springer Nature Limited.
Références
Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425–479. https://doi.org/10.1146/annurev.biochem.67.1.425 (1998).
doi: 10.1146/annurev.biochem.67.1.425
pubmed: 9759494
Rotin, D. & Kumar, S. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398–409. https://doi.org/10.1038/nrm2690 (2009).
doi: 10.1038/nrm2690
pubmed: 19436320
Cao, X. R. et al. Nedd4 controls animal growth by regulating IGF-1 signaling. Sci. Signal 1, ra5. https://doi.org/10.1126/scisignal.1160940 (2008).
doi: 10.1126/scisignal.1160940
pubmed: 18812566
pmcid: 2833362
Lin, Q. et al. HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Mol. Cell. Biol. 30, 1541–1554. https://doi.org/10.1128/mcb.00013-10 (2010).
doi: 10.1128/mcb.00013-10
pubmed: 20086093
pmcid: 2832494
Persaud, A. et al. Nedd4-1 binds and ubiquitylates activated FGFR1 to control its endocytosis and function. EMBO J. 30, 3259–3273. https://doi.org/10.1038/emboj.2011.234 (2011).
doi: 10.1038/emboj.2011.234
pubmed: 21765395
pmcid: 3160656
Sicari, D., Weber, J., Maspero, E. & Polo, S. The NEDD4 ubiquitin E3 ligase: A snapshot view of its functional activity and regulation. Biochem. Soc. Trans. 50, 473–485. https://doi.org/10.1042/bst20210731 (2022).
doi: 10.1042/bst20210731
pubmed: 35129615
Bernassola, F., Chillemi, G. & Melino, G. HECT-type E3 ubiquitin ligases in cancer. Trends Biochem. Sci. 44, 1057–1075. https://doi.org/10.1016/j.tibs.2019.08.004 (2019).
doi: 10.1016/j.tibs.2019.08.004
pubmed: 31610939
Plant, P. J., Yeger, H., Staub, O., Howard, P. & Rotin, D. The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2+-dependent plasma membrane localization. J. Biol. Chem. 272, 32329–32336. https://doi.org/10.1074/jbc.272.51.32329 (1997).
doi: 10.1074/jbc.272.51.32329
pubmed: 9405440
Wang, J. et al. Calcium activates Nedd4 E3 ubiquitin ligases by releasing the C2 domain-mediated auto-inhibition. J. Biol. Chem. 285, 12279–12288. https://doi.org/10.1074/jbc.M109.086405 (2010).
doi: 10.1074/jbc.M109.086405
pubmed: 20172859
pmcid: 2852967
Persaud, A. et al. Tyrosine phosphorylation of NEDD4 activates its ubiquitin ligase activity. Sci. Signal 7, ra95. https://doi.org/10.1126/scisignal.2005290 (2014).
doi: 10.1126/scisignal.2005290
pubmed: 25292214
Wiesner, S. et al. Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 130, 651–662. https://doi.org/10.1016/j.cell.2007.06.050 (2007).
doi: 10.1016/j.cell.2007.06.050
pubmed: 17719543
Staub, O. et al. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle’s syndrome. EMBO J. 15, 2371–2380 (1996).
doi: 10.1002/j.1460-2075.1996.tb00593.x
pubmed: 8665844
pmcid: 450167
Kanelis, V., Rotin, D. & Forman-Kay, J. D. Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat. Struct. Biol. 8, 407–412. https://doi.org/10.1038/87562 (2001).
doi: 10.1038/87562
pubmed: 11323714
Huibregtse, J. M., Scheffner, M., Beaudenon, S. & Howley, P. M. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. U. S. A. 92, 2563–2567. https://doi.org/10.1073/pnas.92.7.2563 (1995).
doi: 10.1073/pnas.92.7.2563
pubmed: 7708685
pmcid: 42258
Dunn, D. M. et al. Common variant of human NEDD4L activates a cryptic splice site to form a frameshifted transcript. J. Hum. Genet. 47, 665–676. https://doi.org/10.1007/s100380200102 (2002).
doi: 10.1007/s100380200102
pubmed: 12522688
Flasza, M., Gorman, P., Roylance, R., Canfield, A. E. & Baron, M. Alternative splicing determines the domain structure of WWP1, a Nedd4 family protein. Biochem. Biophys. Res. Commun. 290, 431–437. https://doi.org/10.1006/bbrc.2001.6206 (2002).
doi: 10.1006/bbrc.2001.6206
pubmed: 11779188
Soond, S. M. & Chantry, A. Selective targeting of activating and inhibitory Smads by distinct WWP2 ubiquitin ligase isoforms differentially modulates TGFbeta signalling and EMT. Oncogene 30, 2451–2462. https://doi.org/10.1038/onc.2010.617 (2011).
doi: 10.1038/onc.2010.617
pubmed: 21258410
pmcid: 4073228
Strausberg, R. L. et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc. Natl. Acad. Sci. U. S. A. 99, 16899–16903. https://doi.org/10.1073/pnas.242603899 (2002).
doi: 10.1073/pnas.242603899
pubmed: 12477932
Persaud, A. et al. Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol. Syst. Biol. 5, 333. https://doi.org/10.1038/msb.2009.85 (2009).
doi: 10.1038/msb.2009.85
pubmed: 19953087
pmcid: 2824488
Mari, S. et al. Structural and functional framework for the autoinhibition of Nedd4-family ubiquitin ligases. Structure 22, 1639–1649. https://doi.org/10.1016/j.str.2014.09.006 (2014).
doi: 10.1016/j.str.2014.09.006
pubmed: 25438670
Bridges, D. & Moorhead, G. B. 14-3-3 proteins: A number of functions for a numbered protein. Sci. STKE 2005, re10. https://doi.org/10.1126/stke.2962005re10 (2005).
doi: 10.1126/stke.2962005re10
pubmed: 16091624
Liu, D. et al. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376, 191–194. https://doi.org/10.1038/376191a0 (1995).
doi: 10.1038/376191a0
pubmed: 7603574
Xiao, B. et al. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376, 188–191. https://doi.org/10.1038/376188a0 (1995).
doi: 10.1038/376188a0
pubmed: 7603573
Muslin, A. J., Tanner, J. W., Allen, P. M. & Shaw, A. S. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889–897. https://doi.org/10.1016/s0092-8674(00)81067-3 (1996).
doi: 10.1016/s0092-8674(00)81067-3
pubmed: 8601312
Yaffe, M. B. et al. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961–971. https://doi.org/10.1016/s0092-8674(00)80487-0 (1997).
doi: 10.1016/s0092-8674(00)80487-0
pubmed: 9428519
Brunet, A. et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857–868. https://doi.org/10.1016/s0092-8674(00)80595-4 (1999).
doi: 10.1016/s0092-8674(00)80595-4
pubmed: 10102273
Madeira, F. et al. 14-3-3-Pred: Improved methods to predict 14-3-3-binding phosphopeptides. Bioinformatics 31, 2276–2283. https://doi.org/10.1093/bioinformatics/btv133 (2015).
doi: 10.1093/bioinformatics/btv133
pubmed: 25735772
pmcid: 4495292
Attali, I. et al. Ubiquitylation-dependent oligomerization regulates activity of Nedd4 ligases. EMBO J. 36, 425–440. https://doi.org/10.15252/embj.201694314 (2017).
doi: 10.15252/embj.201694314
pubmed: 28069708
pmcid: 5437815
Jiang, H., Thomas, S. N., Chen, Z., Chiang, C. Y. & Cole, P. A. Comparative analysis of the catalytic regulation of NEDD4-1 and WWP2 ubiquitin ligases. J. Biol. Chem. 294, 17421–17436. https://doi.org/10.1074/jbc.RA119.009211 (2019).
doi: 10.1074/jbc.RA119.009211
pubmed: 31578285
pmcid: 6873185
Escobedo, A. et al. Structural basis of the activation and degradation mechanisms of the E3 ubiquitin ligase Nedd4L. Structure 22, 1446–1457. https://doi.org/10.1016/j.str.2014.08.016 (2014).
doi: 10.1016/j.str.2014.08.016
pubmed: 25295397
Ichimura, T. et al. 14-3-3 proteins modulate the expression of epithelial Na+ channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J. Biol. Chem. 280, 13187–13194. https://doi.org/10.1074/jbc.M412884200 (2005).
doi: 10.1074/jbc.M412884200
pubmed: 15677482
Bhalla, V. et al. Serum- and glucocorticoid-regulated kinase 1 regulates ubiquitin ligase neural precursor cell-expressed, developmentally down-regulated protein 4–2 by inducing interaction with 14-3-3. Mol. Endocrinol. 19, 3073–3084. https://doi.org/10.1210/me.2005-0193 (2005).
doi: 10.1210/me.2005-0193
pubmed: 16099816
Chandran, S. et al. Neural precursor cell-expressed developmentally down-regulated protein 4–2 (Nedd4-2) regulation by 14-3-3 protein binding at canonical serum and glucocorticoid kinase 1 (SGK1) phosphorylation sites. J. Biol. Chem. 286, 37830–37840. https://doi.org/10.1074/jbc.M111.293233 (2011).
doi: 10.1074/jbc.M111.293233
pubmed: 21900244
pmcid: 3199524
Joshi, R. et al. Nedd4-2 binding to 14-3-3 modulates the accessibility of its catalytic site and WW domains. Biophys. J. 121, 1299–1311. https://doi.org/10.1016/j.bpj.2022.02.025 (2022).
doi: 10.1016/j.bpj.2022.02.025
pubmed: 35189105
pmcid: 9034186
Pohl, P., Joshi, R., Petrvalska, O., Obsil, T. & Obsilova, V. 14-3-3-protein regulates Nedd4-2 by modulating interactions between HECT and WW domains. Commun. Biol. 4, 899. https://doi.org/10.1038/s42003-021-02419-0 (2021).
doi: 10.1038/s42003-021-02419-0
pubmed: 34294877
pmcid: 8298602
Anindya, R., Aygün, O. & Svejstrup, J. Q. Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 28, 386–397. https://doi.org/10.1016/j.molcel.2007.10.008 (2007).
doi: 10.1016/j.molcel.2007.10.008
pubmed: 17996703
Huibregtse, J. M., Yang, J. C. & Beaudenon, S. L. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. U. S. A. 94, 3656–3661. https://doi.org/10.1073/pnas.94.8.3656 (1997).
doi: 10.1073/pnas.94.8.3656
pubmed: 9108033
pmcid: 20496
The ORFeome Collaboration. The ORFeome Collaboration: A genome-scale human ORF-clone resource. Nat. Methods 13, 191–192. https://doi.org/10.1038/nmeth.3776 (2016).
doi: 10.1038/nmeth.3776