5,037
Views
56
CrossRef citations to date
0
Altmetric
Basic Research Papers

The E3 ubiquitin ligase NEDD4 is an LC3-interactive protein and regulates autophagy

, , , , , , & show all
Pages 522-537 | Received 01 Apr 2016, Accepted 30 Nov 2016, Published online: 13 Jan 2017

References

  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-1721; PMID:11099404; http://dx.doi.org/10.1126/science.290.5497.1717
  • Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ 2005; 2(12 Suppl):1542-1552; http://dx.doi.org/10.1038/sj.cdd.4401765
  • Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4(2):151-75; PMID:18188003; http://dx.doi.org/10.4161/auto.5338
  • Mortimore GE, Pösö AR. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu Rev Nutr 1987; 7:539-64; PMID:3300746; http://dx.doi.org/10.1146/annurev.nu.07.070187.002543
  • Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M. Autophagy-physiology and pathophysiology. Histochem Cell Biol 2008; 129(4):407-20; PMID:18320203; http://dx.doi.org/10.1007/s00418-008-0406-y
  • Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306:990-995; PMID:15528435; http://dx.doi.org/10.1126/science.1099993
  • Hippert MM, O'Toole PS, Thorburn A. Autophagy in cancer: good, bad, or both?. Cancer Res 2006; 66:9349-9351; PMID:17018585; http://dx.doi.org/10.1158/0008-5472.CAN-06-1597
  • Guo JY, Xia B, White E. Autophagy-mediated tumor promotion. Cell 2013; 155(6):1216-9; PMID:24315093; http://dx.doi.org/10.1016/j.cell.2013.11.019
  • Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, Nelson DA, Jin S, White E. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10:51-64; PMID:16843265; http://dx.doi.org/10.1016/j.ccr.2006.06.001
  • Edinger AL, Thompson CB. Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004; 16(6):663-9; PMID:15530778; http://dx.doi.org/10.1016/j.ceb.2004.09.011
  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19(21):5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
  • Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH, Thumm M. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J 1998; 17(13):3597-607; PMID:9649430; http://dx.doi.org/10.1093/emboj/17.13.3597
  • Shpilka T, Weidberg H, Pietrokovski S, Elazar Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol 2011; 12(7):226; PMID:21867568; http://dx.doi.org/10.1186/gb-2011-12-7-226
  • Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004; 36(12):2503-18; PMID:15325588; http://dx.doi.org/10.1016/j.biocel.2004.05.009
  • Nakatogawa H. Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy. Essays Biochem 2013; 55:39-50; PMID:24070470; http://dx.doi.org/10.1042/bse0550039
  • Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15(3):1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
  • Klionsky DJ, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8(4):445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • Birgisdottir ÅB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci 2013; 126(Pt 15):3237-47.
  • Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci 2014; 127(Pt 1):3-9; PMID:24345374; http://dx.doi.org/10.1242/jcs.140426
  • Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 2010; 12(3):213-23; PMID:20173742
  • Lau A, Wang XJ, Zhao F, Villeneuve NF, Wu T, Jiang T, Sun Z, White E, Zhang DD. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell Biol 2010; 30(13):3275-85; PMID:20421418; http://dx.doi.org/10.1128/MCB.00248-10
  • Linares JF, Duran A, Yajima T, Pasparakis M, Moscat J, Diaz-Meco MT. K63 polyubiquitination and activation of mTOR by the p62-TRAF6 complex in nutrient-activated cells. Mol Cell 2013; 51(3):283-96; PMID:23911927; http://dx.doi.org/10.1016/j.molcel.2013.06.020
  • Isakson P, Lystad AH, Breen K, Koster G, Stenmark H, Simonsen A. TRAF6 mediates ubiquitination of KIF23/MKLP1 and is required for midbody ring degradation by selective autophagy. Autophagy 2013; 9(12):1955-64; PMID:24128730; http://dx.doi.org/10.4161/auto.26085
  • Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 2009; 34(3):259-69; PMID:19450525; http://dx.doi.org/10.1016/j.molcel.2009.04.026
  • Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7(3):279-96; PMID:21189453; http://dx.doi.org/10.4161/auto.7.3.14487
  • Staub O, Dho S, Henry P, Correa J, Ishikawa T, McGlade J, Rotin D. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J 1996; 15(10):2371-80; PMID:8665844
  • Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, Schild L, Rotin D. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 1997; 16(21):6325-36; PMID:9351815; http://dx.doi.org/10.1093/emboj/16.21.6325
  • Lu C, Pribanic S, Debonneville A, Jiang C, Rotin D. The PY motif of ENaC, mutated in Liddle syndrome, regulates channel internalization, sorting and mobilization from subapical pool. Traffic 2007; 8(9):1246-64; PMID:17605762; http://dx.doi.org/10.1111/j.1600-0854.2007.00602.x
  • Katzmann DJ, Sarkar S, Chu T, Audhya A, Emr SD. Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol Biol Cell 2004; 15(2):468-80; PMID:14657247; http://dx.doi.org/10.1091/mbc.E03-07-0473
  • Blot V, Perugi F, Gay B, Prévost MC, Briant L, Tangy F, Abriel H, Staub O, Dokhélar MC, Pique C. Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. J Cell Sci 2004; 117(Pt 11):2357-67; PMID:15126635; http://dx.doi.org/10.1242/jcs.01095
  • Okumura A, Pitha PM, Harty RN. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc Natl Acad Sci U S A 2008; 105(10):3974-9; PMID:18305167; http://dx.doi.org/10.1073/pnas.0710629105
  • Magnifico A, Ettenberg S, Yang C, Mariano J, Tiwari S, Fang S, Lipkowitz S, Weissman AM. WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. J Biol Chem 2003; 278:43169-77; PMID:12907674; http://dx.doi.org/10.1074/jbc.M308009200
  • Katz M, Shtiegman K, Tal-Or P, Yakir L, Mosesson Y, Harari D, Machluf Y, Asao H, Jovin T, Sugamura K, Yarden Y. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 2002; 3(10):740-51; PMID:12230472; http://dx.doi.org/10.1034/j.1600-0854.2002.31006.x
  • Woelk T, Oldrini B, Maspero E, Confalonieri S, Cavallaro E, Di Fiore PP, Polo S. Molecular mechanisms of coupled monoubiquitination. Nat Cell Biol 2006; 8:1246-54; PMID:17013377; http://dx.doi.org/10.1038/ncb1484
  • Segura-Morales C, Pescia C, Chatellard-Causse C, Sadoul R, Bertrand E, Basyuk E. Tsg101 and Alix interact with murine leukemia virus Gag and cooperate with Nedd4 ubiquitin ligases during budding. J Biol Chem 2005; 280(29):27004-12; PMID:15908698; http://dx.doi.org/10.1074/jbc.M413735200
  • Aoh QL, Castle AM, Hubbard CH, Katsumata O, Castle JD. SCAMP3 negatively regulates epidermal growth factor receptor degradation and promotes receptor recycling. Mol Biol Cell 20(6):1816-32; PMID:19158374; http://dx.doi.org/10.1091/mbc.E08-09-0894
  • Lin Q, Wang J, Childress C, Sudol M, Carey DJ, Yang W. HECT E3 ubiquitin ligase NEDD4-1 ubiquitinates ACK and regulates EGF-induced degradation of EGFR and ACK. Mol Cell Biol 2010; 30:1541-1554; PMID:20086093; http://dx.doi.org/10.1128/MCB.00013-10
  • Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, Saadon Z, Fladd C, Parkinson J, Rotin D. Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol Syst Biol 2009; 5:333; PMID:19953087; http://dx.doi.org/10.1038/msb.2009.85
  • Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, Wang J, Erdjument-Bromage H, Tempst P, Cordon-Cardo C, Pandolfi PP, Jiang X. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 2007; 128:129-39; PMID:17218260; http://dx.doi.org/10.1016/j.cell.2006.11.039
  • Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature 2010; 466(7302):68-76; PMID:20562859; http://dx.doi.org/10.1038/nature09204
  • Li Y, Zhang L, Zhou J, Luo S, Huang R, Zhao C, Diao A. Nedd4 E3 ubiquitin ligase promotes cell proliferation and autophagy. Cell Prolif 2015; 48(3):338-47; PMID:25809873; http://dx.doi.org/10.1111/cpr.12184
  • Wang J, Peng Q, Lin Q, Childress C, Carey D, Yang W. Calcium activates Nedd4 E3 ubiquitin ligases by releasing the C2 domain-mediated auto-inhibition. J Biol Chem 2010; 285(16):12279-12288; PMID:20172859; http://dx.doi.org/10.1074/jbc.M109.086405
  • Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447(7148):1121-5; PMID:17589504
  • Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, Jung JU. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008; 10(7):776-87; PMID:18552835; http://dx.doi.org/10.1038/ncb1740
  • Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Fauré J, Blanc NS, Matile S, Dubochet J, Sadoul R, Parton RG, Vilbois F, Gruenberg J. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 2004; 303(5657):531-4; PMID:14739459; http://dx.doi.org/10.1126/science.1092425
  • Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 2012; 14(7):677-85; PMID:22660413; http://dx.doi.org/10.1038/ncb2502
  • Geng J, Klionsky DJ. The Golgi as a potential membrane source for autophagy. Autophagy 2010; 6(7):950-1; PMID:20729630; http://dx.doi.org/10.4161/auto.6.7.13009
  • Hamasaki M, Yoshimori T. Where do they come from? Insights into autophagosome formation. FEBS Lett 2010; 584(7):1296-301; PMID:20188731; http://dx.doi.org/10.1016/j.febslet.2010.02.061
  • Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 1995; 131(6 Pt 2):1715-26; PMID:8557739; http://dx.doi.org/10.1083/jcb.131.6.1715
  • Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ 2nd, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 1991; 266(29):19599-610; PMID:1918067
  • Padar S, van Breemen C, Thomas DW, Uchizono JA, Livesey JC, Rahimian R. Differential regulation of calcium homeostasis in adenocarcinoma cell line A549 and its Taxol-resistant subclone. Br J Pharmacol 2004; 142(2):305-16; PMID:15066902; http://dx.doi.org/10.1038/sj.bjp.0705755
  • Wang H, Sun RQ, Camera D, Zeng XY, Jo E, Chan SM, Herbert TP, Molero JC, Ye JM. Endoplasmic reticulum stress up-regulates Nedd4-2 to induce autophagy. FASEB J 2016; 30(7):2549-56; PMID:27022162; http://dx.doi.org/10.1096/fj.201500119
  • Platta HW, Abrahamsen H, Thoresen SB, Stenmark H. Nedd4-dependent lysine-11-linked polyubiquitination of the tumour suppressor Beclin 1. Biochem J 2012; 441(1):399-406; PMID:21936852; http://dx.doi.org/10.1042/BJ20111424
  • Metcalf D, Isaacs AM. The role of ESCRT proteins in fusion events involving lysosomes, endosomes and autophagosomes. Biochem Soc Trans 2010; 38(6):1469-73; PMID:21118109; http://dx.doi.org/10.1042/BST0381469
  • Lamark T, Kirkin V, Dikic I, Johansen T. NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 2009; 8(13):1986-90; PMID:19502794; http://dx.doi.org/10.4161/cc.8.13.8892
  • Park S, Choi SG, Yoo SM, Son JH, Jung YK. Choline dehydrogenase interacts with SQSTM1/p62 to recruit LC3 and stimulate mitophagy. Autophagy 2014; 10(11):1906-20; PMID:25483962; http://dx.doi.org/10.4161/auto.32177
  • Shen F, Lin Q, Gu Y, Childress C, Yang W. Activated Cdc42-associated Kinase 1 (ACK1) Is a Component of EGF Receptor Signaling Complex and Regulates EGF Receptor Degradation. Mol Biol Cell 2007; 18(3):732-42; PMID:17182860; http://dx.doi.org/10.1091/mbc.E06-02-0142
  • Mi W, Lin Q, Childress C, Sudol M, Robishaw J, Berlot CH, Shabahang M, Yang W. Geranylgeranylation signals to the Hippo pathway for breast cancer cell proliferation and migration. Oncogene 2015; 34(24):3095-106; PMID:25109332; http://dx.doi.org/10.1038/onc.2014.251

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.