Regulation of Itch and Nedd4 E3 Ligase Activity and Degradation by LRAD3

Biochemistry

Volumn 55, Issue 8, 2016, Pages 1204-1213

  Noyes, Nathaniel C ^a   Hampton, Brian ^a   Migliorini, Mary ^a   Strickland, Dudley K ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; ENZYME ACTIVITY;

BIOLOGICAL PROCESS; E3 UBIQUITIN LIGASES; ENZYMATIC ACTIVITIES; INTRACELLULAR DOMAIN; INTRAMOLECULAR INTERACTIONS; LOW DENSITY LIPOPROTEIN RECEPTORS; MUTATIONAL ANALYSIS; PHYSIOLOGICAL FUNCTIONS;

ENZYMES;

ITCH PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR CLASS A DOMAIN CONTAINING 3; PROTEASOME; PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; ESCRT PROTEIN; ITCH PROTEIN, HUMAN; LRAD3 PROTEIN, HUMAN; NEDD4 UBIQUITIN PROTEIN LIGASES; PROTEIN BINDING; REPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; UBIQUITINATION; ANIMAL; CHEMISTRY; HEK293 CELL LINE; METABOLISM; MOUSE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; ANIMALS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HEK293 CELLS; HUMANS; MICE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPS; PROTEOLYSIS; RECEPTORS, LDL; REPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84960080203     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01218     Document Type: Article

References (41)

1. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system Annu. Rev. Biochem. 67, 425-479 10.1146/annurev.biochem.67.1.425
2. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway Cell 79, 13-21 10.1016/0092-8674(94)90396-4
3. Bernassola, F., Karin, M., Ciechanover, A., and Melino, G. (2008) The HECT family of E3 ubiquitin ligases: multiple players in cancer development Cancer Cell 14, 10-21 10.1016/j.ccr.2008.06.001
4. Harvey, K. F. and Kumar, S. (1999) Nedd4-like proteins: an emerging family of ubiquitin-protein ligases implicated in diverse cellular functions Trends Cell Biol. 9, 166-169 10.1016/S0962-8924(99)01541-X
5. Rotin, D. and Kumar, S. (2009) Physiological functions of the HECT family of ubiquitin ligases Nat. Rev. Mol. Cell Biol. 10, 398-409 10.1038/nrm2690
6. Perry, W. L., Hustad, C. M., Swing, D. A., O'Sullivan, T. N., Jenkins, N. A., and Copeland, N. G. (1998) The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice Nat. Genet. 18, 143-146 10.1038/ng0298-143
7. Fang, D., Elly, C., Gao, B., Fang, N., Altman, Y., Joazeiro, C., Hunter, T., Copeland, N., Jenkins, N., and Liu, Y. C. (2002) Dysregulation of T lymphocyte function in itchy mice: a role for Itch in TH2 differentiation Nat. Immunol. 3, 281-287 10.1038/ni763
8. Heissmeyer, V., Macian, F., Im, S. H., Varma, R., Feske, S., Venuprasad, K., Gu, H., Liu, Y. C., Dustin, M. L., and Rao, A. (2004) Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins Nat. Immunol. 5, 255-265 10.1038/ni1047
9. Gao, M., Labuda, T., Xia, Y., Gallagher, E., Fang, D., Liu, Y. C., and Karin, M. (2004) Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch Science 306, 271-275 10.1126/science.1099414
10. Gallagher, E., Gao, M., Liu, Y. C., and Karin, M. (2006) Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change Proc. Natl. Acad. Sci. U. S. A. 103, 1717-1722 10.1073/pnas.0510664103
11. Di Marcotullio, L., Ferretti, E., Greco, A., De Smaele, E., Po, A., Sico, M. A., Alimandi, M., Giannini, G., Maroder, M., Screpanti, I., and Gulino, A. (2006) Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination Nat. Cell Biol. 8, 1415-1423 10.1038/ncb1510
12. Bai, Y., Yang, C., Hu, K., Elly, C., and Liu, Y. C. (2004) Itch E3 ligase-mediated regulation of TGF-beta signaling by modulating smad2 phosphorylation Mol. Cell 15, 825-831 10.1016/j.molcel.2004.07.021
13. Stohr, R., Mavilio, M., Marino, A., Casagrande, V., Kappel, B., Mollmann, J., Menghini, R., Melino, G., and Federici, M. (2015) ITCH modulates SIRT6 and SREBP2 to influence lipid metabolism and atherosclerosis in ApoE null mice. Sci. Rep. 5, 9023 10.1038/srep09023
14. Angers, A., Ramjaun, A. R., and McPherson, P. S. (2004) The HECT domain ligase itch ubiquitinates endophilin and localizes to the trans-Golgi network and endosomal system J. Biol. Chem. 279, 11471-11479 10.1074/jbc.M309934200
15. Ranganathan, S., Noyes, N. C., Migliorini, M., Winkles, J. A., Battey, F. D., Hyman, B. T., Smith, E., Yepes, M., Mikhailenko, I., and Strickland, D. K. (2011) LRAD3, A Novel Low-Density Lipoprotein Receptor Family Member That Modulates Amyloid Precursor Protein Trafficking J. Neurosci. 31, 10836-10846 10.1523/JNEUROSCI.5065-10.2011
16. Hunziker, W. and Fumey, C. (1994) A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells EMBO J. 13, 2963-2967
17. Sudol, M. (1996) Structure and function of the WW domain Prog. Biophys. Mol. Biol. 65, 113-132 10.1016/S0079-6107(96)00008-9
18. Pawson, T. and Scott, J. D. (1997) Signaling through scaffold, anchoring, and adaptor proteins Science 278, 2075-2080 10.1126/science.278.5346.2075
19. Bacskai, B. J., Xia, M. Q., Strickland, D. K., Rebeck, G. W., and Hyman, B. T. (2000) The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-D-aspartate receptors Proc. Natl. Acad. Sci. U. S. A. 97, 11551-11556 10.1073/pnas.200238297
20. 2-macroglobulin receptor J. Biol. Chem. 266, 21232-21238
21. Ranganathan, S., Liu, C. X., Migliorini, M. M., Von Arnim, C. A., Peltan, I. D., Mikhailenko, I., Hyman, B. T., and Strickland, D. K. (2004) Serine and threonine phosphorylation of the low density lipoprotein receptor-related protein by protein kinase Calpha regulates endocytosis and association with adaptor molecules J. Biol. Chem. 279, 40536-40544 10.1074/jbc.M407592200
22. Craig, J., Mikhailenko, I., Noyes, N., Migliorini, M., and Strickland, D. K. (2013) The LDL Receptor-Related Protein 1 (LRP1) Regulates the PDGF Signaling Pathway by Binding the Protein Phosphatase SHP-2 and Modulating SHP-2- Mediated PDGF Signaling Events PLoS One 8, e70432 10.1371/journal.pone.0070432
23. Saenko, E. L., Yakhyaev, A. V., Mikhailenko, I., Strickland, D. K., and Sarafanov, A. G. (1999) Role of the low density lipoprotein-related protein receptor in mediation of factor VIII catabolism J. Biol. Chem. 274, 37685-37692 10.1074/jbc.274.53.37685
24. Choo, Y. S. and Zhang, Z. (2009) Detection of protein ubiquitination J. Visualized Exp. 10.3791/1293
25. Pranski, E. L., Van Sanford, C. D., Dalal, N. V., Orr, A. L., Karmali, D., Cooper, D. S., Costa, N., Heilman, C. J., Gearing, M., Lah, J. J., Levey, A. I., and Betarbet, R. S. (2012) Comparative distribution of protein components of the A20 ubiquitin-editing complex in normal human brain Neurosci. Lett. 520, 104-109 10.1016/j.neulet.2012.05.043
26. Mund, T. and Pelham, H. R. (2009) Control of the activity of WW-HECT domain E3 ubiquitin ligases by NDFIP proteins EMBO Rep. 10, 501-507 10.1038/embor.2009.30
27. Hooper, C., Puttamadappa, S. S., Loring, Z., Shekhtman, A., and Bakowska, J. C. (2010) Spartin activates atrophin-1-interacting protein 4 (AIP4) E3 ubiquitin ligase and promotes ubiquitination of adipophilin on lipid droplets BMC Biol. 8, 72 10.1186/1741-7007-8-72
28. Winberg, G., Matskova, L., Chen, F., Plant, P., Rotin, D., Gish, G., Ingham, R., Ernberg, I., and Pawson, T. (2000) Latent membrane protein 2A of Epstein-Barr virus binds WW domain E3 protein-ubiquitin ligases that ubiquitinate B-cell tyrosine kinases Mol. Cell. Biol. 20, 8526-8535 10.1128/MCB.20.22.8526-8535.2000
29. Mouchantaf, R., Azakir, B. A., McPherson, P. S., Millard, S. M., Wood, S. A., and Angers, A. (2006) The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X J. Biol. Chem. 281, 38738-38747 10.1074/jbc.M605959200
30. Matesic, L. E., Copeland, N. G., and Jenkins, N. A. (2008) Itchy mice: the identification of a new pathway for the development of autoimmunity Curr. Top. Microbiol. Immunol. 321, 185-200 10.1007/978-3-540-75203-5-9
31. Melino, G., Gallagher, E., Aqeilan, R. I., Knight, R., Peschiaroli, A., Rossi, M., Scialpi, F., Malatesta, M., Zocchi, L., Browne, G., Ciechanover, A., and Bernassola, F. (2008) Itch: a HECT-type E3 ligase regulating immunity, skin and cancer Cell Death Differ. 15, 1103-1112 10.1038/cdd.2008.60
32. Lohr, N. J., Molleston, J. P., Strauss, K. A., Torres-Martinez, W., Sherman, E. A., Squires, R. H., Rider, N. L., Chikwava, K. R., Cummings, O. W., Morton, D. H., and Puffenberger, E. G. (2010) Human ITCH E3 ubiquitin ligase deficiency causes syndromic multisystem autoimmune disease Am. J. Hum. Genet. 86, 447-453 10.1016/j.ajhg.2010.01.028
33. Rathinam, C., Matesic, L. E., and Flavell, R. A. (2011) The E3 ligase Itch is a negative regulator of the homeostasis and function of hematopoietic stem cells Nat. Immunol. 12, 399-407 10.1038/ni.2021
34. Azakir, B. A. and Angers, A. (2009) Reciprocal regulation of the ubiquitin ligase Itch and the epidermal growth factor receptor signaling Cell. Signalling 21, 1326-1336 10.1016/j.cellsig.2009.03.020
35. Chastagner, P., Israel, A., and Brou, C. (2008) AIP4/Itch regulates Notch receptor degradation in the absence of ligand PLoS One 3, e2735 10.1371/journal.pone.0002735
36. McGill, M. A. and McGlade, C. J. (2003) Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain J. Biol. Chem. 278, 23196-23203 10.1074/jbc.M302827200
37. Qiu, L., Joazeiro, C., Fang, N., Wang, H. Y., Elly, C., Altman, Y., Fang, D., Hunter, T., and Liu, Y. C. (2000) Recognition and ubiquitination of Notch by Itch, a hect-type E3 ubiquitin ligase J. Biol. Chem. 275, 35734-35737 10.1074/jbc.M007300200
38. Wiesner, S., Ogunjimi, A. A., Wang, H. R., Rotin, D., Sicheri, F., Wrana, J. L., and Forman-Kay, J. D. (2007) Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain Cell 130, 651-662 10.1016/j.cell.2007.06.050
39. Di Marcotullio, M. L., Greco, A., Mazza, D., Canettieri, G., Pietrosanti, L., Infante, P., Coni, S., Moretti, M., De Smaele, S. E., Ferretti, E., Screpanti, I., and Gulino, A. (2011) Numb activates the E3 ligase Itch to control Gli1 function through a novel degradation signal Oncogene 30, 65-76 10.1038/onc.2010.394
40. Riling, C., Kamadurai, H., Kumar, S., O'Leary, C. E., Wu, K. P., Manion, E. E., Ying, M., Schulman, B. A., and Oliver, P. M. (2015) Itch WW Domains Inhibit Its E3 Ubiquitin Ligase Activity by Blocking E2-E3 Ligase Trans-thiolation J. Biol. Chem. 290, 23875-23887 10.1074/jbc.M115.649269
41. Scialpi, F., Malatesta, M., Peschiaroli, A., Rossi, M., Melino, G., and Bernassola, F. (2008) Itch self-polyubiquitylation occurs through lysine-63 linkages Biochem. Pharmacol. 76, 1515-1521 10.1016/j.bcp.2008.07.028