RNF2 is recruited by WASH to ubiquitinate AMBRA1 leading to downregulation of autophagy

Cell Research

Volumn 24, Issue 8, 2014, Pages 943-958

  Xia, Pengyan ^a,b   Wang, Shuo ^a   Huang, Guanling ^a,b   Du, Ying ^a   Zhu, Pingping ^a   Li, Man ^a,b   Fan, Zusen ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

AMBRA1; polyubiquitination; RNF2; the BECN1 PIK3C3 complex; WASH

Indexed keywords

ACTIN BINDING PROTEIN; AMBRA1 PROTEIN, MOUSE; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, MOUSE; BMI1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RNF2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE; VESICULAR TRANSPORT PROTEIN; WASH PROTEIN, MOUSE;

ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; CELL LINE; CHEMISTRY; DOWN REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; RNA INTERFERENCE; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE; DOWN-REGULATION; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; POLYCOMB REPRESSIVE COMPLEX 1; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VESICULAR TRANSPORT PROTEINS;

EID: 84905582805     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.85     Document Type: Article

References (53)

1. Bodemann BO, Orvedahl A, Cheng TL, et al. RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 2011; 144:253-267.
2. Lee JH, Yu WH, Kumar A, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141:1146-1158.
3. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147:728-741.
4. Shintani T, Klionsky DJ. Autophagy in health and disease: A double-edged sword. Science 2004; 306:990-995.
5. Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182:685-701.
6. Hailey DW, Rambold AS, Satpute-Krishnan P, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 2010; 141:656-667.
7. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 2009; 11:1433-1437.
8. Reggiori F. Membrane origin for autophagy. Curr Top Dev Biol 2006; 74:1-30.
9. Yla-Anttila P, Vihinen H, Jokita E, Eskelinen EL. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009; 5:1180-1185.
10. Liang CY, Lee JS, Inn KS, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008; 10:776-787.
11. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-580.
12. Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 2011; 80:125-156.
13. Fimia GM, Stoykova A, Romagnoli A, et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447:1121-1125.
14. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19:5360-5372.
15. Matsunaga K, Saitoh T, Tabata K, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11:385-396.
16. Zhong Y, Wang QJ, Li XT, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3- kinase complex. Nat Cell Biol 2009; 11:468-476.
17. Aita VM, Liang XH, Murty VVVS, et al. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999; 59:59-65.
18. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 2006; 119:605-614.
19. Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 2009; 186:773-782.
20. Yan Y, Flinn RJ, Wu HY, Schnur RS, Backer JM. hVps15, but not Ca2+/CaM, is required for the activity and regulation of hVps34 in mammalian cells. Biochem J 2009; 417:747-755.
21. Ku B, Woo JS, Liang C, Lee KH, Jung JU, Oh BH. An insight into the mechanistic role of Beclin 1 and its inhibition by prosurvival Bcl-2 family proteins. Autophagy 2008; 4:519-520.
22. Pattingre S, Tassa A, Qu XP, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-939.
23. Wei YJ, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of BcI-2 regulates starvation-induced autophagy. Mol Cell 2008; 30:678-688.
24. Di Bartolomeo S, Corazzari M, Nazio F, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010; 191:155-168.
25. Nazio F, Strappazzon F, Antonioli M, et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol 2013; 15:406-416.
26. Strappazzon F, Vietri-Rudan M, Campello S, et al. Mitochondrial BCL-2 inhibits AMBRA1-induced autophagy. EMBO J 2011; 30:1195-1208.
27. Xia P, Wang S, Du Y, et al. WASH inhibits autophagy through suppression of Beclin 1 ubiquitination. EMBO J 2013; 32:2685-2696.
28. Levine SS, Weiss A, Erdjument-Bromage H, Shao ZH, Tempst P, Kingston RE. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol Cell Biol 2002; 22:6070-6078.
29. Pirrotta V, Poux S, Melfi R, Pilyugin M. Assembly of polycomb complexes and silencing mechanisms. Genetica 2003; 117:191-197.
30. Buchwald G, van der Stoop P, Weichenrieder O, Perrakis A, van Lohuizen M, Sixma TK. Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J 2006; 25:2465-2474.
31. Wang HB, Wang LJ, Erdjument-Bromage H, et al. Role of histone H2A ubiquitination in polycomb silencing. Nature 2004; 431:873-878.
32. Voncken JW, Roelen BAJ, Roefs M, et al. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc Nat Acad Sci USA 2003; 100:2468-2473.
33. Ohtsubo M, Yasunaga S, Ohno Y, et al. Polycomb-group complex 1 acts as an E3 ubiquitin ligase for Geminin to sustain hematopoietic stem cell activity. Proc Nat Acad Sci USA 2008; 105:10396-10401.
34. Su WJ, Fang JS, Cheng F, Liu C, Zhou F, Zhang J. RNF2/ Ring1b negatively regulates p53 expression in selective cancer cell types to promote tumor development. Proc Nat Acad Sci USA 2013; 110:1720-1725.
35. Lee SJ, Choi D, Rhim H, Kang S. E3 ubiquitin ligase RNF2 interacts with the S6' proteasomal ATPase subunit and increases the ATP hydrolysis activity of S6'. Biochem J 2005; 389:457-463.
36. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005; 6:79-86.
37. Proikas-Cezanne T, Ruckerbauer S, Stierhof YD, Berg C, Nordheim A. Human WIPI-1 puncta-formation: A novel assay to assess mammalian autophagy. FEBS Lett 2007; 581:3396-3404.
38. Monfregola J, Napolitano G, D'Urso M, Lappalainen P, Ursini MV. Functional characterization of Wiskott-Aldrich syndrome protein and scar homolog (WASH), a bi-modular nucleation-promoting factor able to interact with biogenesis of lysosome-related organelle subunit 2 (BLOS2) and gamma-tubulin. J Biol Chem 2010; 285:16951-16957.
39. de Napoles M, Mermoud JE, Wakao R, et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 2004; 7:663-676.
40. Fischer ES, Scrima A, Bohm K, et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 2011; 147:1024-1039.
41. Jin J, Arias EE, Chen J, Harper JW, Walter JC. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 2006; 23:709-721.
42. Bennett EJ, Rush J, Gygi SP, Harper JW. Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010; 143:951-965.
43. Wertz IE, O'Rourke KM, Zhang Z, et al. Human De-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 2004; 303:1371-1374.
44. Kim W, Bennett EJ, Huttlin EL, et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 2011; 44:325-340.
45. Wagner SA, Beli P, Weinert BT, et al. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol Cell Proteomics 2012; 11:1578-1585.
46. Juhasz G, Neufeld TP. Autophagy: A forty-year search for a missing membrane source. PLoS Biol 2006; 4:161-164.
47. Liang C, Feng P, Ku B, et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006; 8:688-699.
48. Liu JL, Xia HG, Kim M, et al. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 2011; 147:223-234.
49. Takahashi Y, Coppola D, Matsushita N, et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007; 9:1142-1151.
50. Noble CG, Dong JM, Manser E, Song HW. Bcl-x(L) and UVRAG cause a monomer-dimer switch in Beclin1. J Biol Chem 2008; 283:26274-26282.
51. Cales C, Roman-Trufero M, Pavon L, et al. Inactivation of the polycomb group protein Ring1B unveils an antiproliferative role in hematopoietic cell expansion and cooperation with tumorigenesis associated with Ink4a deletion. Mol Cell Biol 2008; 28:1018-1028.
52. Fan ZS, Beresford PJ, Oh DY, Zhang D, Lieberman J. Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 2003; 112:659-672.
53. Wang S, Xia P, Ye B, Huang G, Liu J, Fan Z. Transient activation of autophagy via Sox2-mediated suppression of mTOR is an important early step in reprogramming to pluripotency. Cell Stem Cell 2013; 13:617-625.