The Selective Autophagy Receptor p62 Forms a Flexible Filamentous Helical Scaffold

Cell Reports

Volumn 11, Issue 5, 2015, Pages 748-758

  Ciuffa, Rodolfo ^a   Lamark, Trond ^b   Tarafder, Abul K ^a   Guesdon, Audrey ^a   Rybina, Sofia ^a   Hagen, Wim J H ^a   Johansen, Terje ^b   Sachse, Carsten ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; LC3 PROTEIN; MOLECULAR SCAFFOLD; PROTEIN P62; SCAFFOLD PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL BODY; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; EUKARYOTIC CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION; AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; ELECTRON MICROSCOPY; GENETICS; HELA CELL LINE; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY;

EUKARYOTA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; HELA CELLS; HUMANS; MICROSCOPY, ELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STATIC ELECTRICITY; UBIQUITIN;

EID: 84933679024     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.062     Document Type: Article

References (44)

1. Bjørkøy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., Stenmark H., Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J.Cell Biol. 2005, 171:603-614.
2. Chen S., McMullan G., Faruqi A.R., Murshudov G.N., Short J.M., Scheres S.H., Henderson R. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 2013, 135:24-35.
3. Christian F., Krause E., Houslay M.D., Baillie G.S. PKA phosphorylation of p62/SQSTM1 regulates PB1 domain interaction partner binding. Biochim. Biophys. Acta 2014, 1843:2765-2774.
4. Ciani B., Layfield R., Cavey J.R., Sheppard P.W., Searle M.S. Structure of the ubiquitin-associated domain of p62 (SQSTM1) and implications for mutations that cause Paget's disease of bone. J.Biol. Chem. 2003, 278:37409-37412.
5. Desfosses A., Ciuffa R., Gutsche I., Sachse C. SPRING - an image processing package for single-particle based helical reconstruction from electron cryomicrographs. J.Struct. Biol. 2014, 185:15-26.
6. Diaz-Avalos R., King C.Y., Wall J., Simon M., Caspar D.L. Strain-specific morphologies of yeast prion amyloid fibrils. Proc. Natl. Acad. Sci. USA 2005, 102:10165-10170.
7. Egelman E.H. Single-particle reconstruction from EM images of helical filaments. Curr. Opin. Struct. Biol. 2007, 17:556-561.
8. Hohn M., Tang G., Goodyear G., Baldwin P.R., Huang Z., Penczek P.A., Yang C., Glaeser R.M., Adams P.D., Ludtke S.J. SPARX, a new environment for Cryo-EM image processing. J.Struct. Biol. 2007, 157:47-55.
9. Ichimura Y., Kumanomidou T., Sou Y.S., Mizushima T., Ezaki J., Ueno T., Kominami E., Yamane T., Tanaka K., Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J.Biol. Chem. 2008, 283:22847-22857.
10. Isogai S., Morimoto D., Arita K., Unzai S., Tenno T., Hasegawa J., Sou Y.S., Komatsu M., Tanaka K., Shirakawa M., Tochio H. Crystal structure of the ubiquitin-associated (UBA) domain of p62 and its interaction with ubiquitin. J.Biol. Chem. 2011, 286:31864-31874.
11. Itakura E., Mizushima N. p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J.Cell Biol. 2011, 192:17-27.
12. Jain A., Lamark T., Sjøttem E., Larsen K.B., Awuh J.A., Øvervatn A., McMahon M., Hayes J.D., Johansen T. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J.Biol. Chem. 2010, 285:22576-22591.
13. Johansen T., Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7:279-296.
14. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
15. Kishi-Itakura C., Koyama-Honda I., Itakura E., Mizushima N. Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J.Cell Sci. 2014, 127:4089-4102.
16. Komatsu M., Waguri S., Koike M., Sou Y.S., Ueno T., Hara T., Mizushima N., Iwata J., Ezaki J., Murata S., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131:1149-1163.
17. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.S., Ueno I., Sakamoto A., Tong K.I., et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 2010, 12:213-223.
18. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J.Struct. Biol. 1996, 116:71-76.
19. Kuusisto E., Salminen A., Alafuzoff I. Ubiquitin-binding protein p62 is present in neuronal and glial inclusions in human tauopathies and synucleinopathies. Neuroreport 2001, 12:2085-2090.
20. Lamark T., Perander M., Outzen H., Kristiansen K., Øvervatn A., Michaelsen E., Bjørkøy G., Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J.Biol. Chem. 2003, 278:34568-34581.
21. Lau A., Wang X.J., Zhao F., Villeneuve N.F., Wu T., Jiang T., Sun Z., White E., Zhang D.D. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 2010, 30:3275-3285.
22. Leach R.J., Singer F.R., Ench Y., Wisdom J.H., Pina D.S., Johnson-Pais T.L. Clinical and cellular phenotypes associated with sequestosome 1 (SQSTM1) mutations. J.Bone Miner. Res. 2006, 21(2):45-50.
23. Long J., Garner T.P., Pandya M.J., Craven C.J., Chen P., Shaw B., Williamson M.P., Layfield R., Searle M.S. Dimerisation of the UBA domain of p62 inhibits ubiquitin binding and regulates NF-kappaB signalling. J.Mol. Biol. 2010, 396:178-194.
24. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J.Struct. Biol. 2005, 152:36-51.
25. Matsumoto G., Wada K., Okuno M., Kurosawa M., Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol. Cell 2011, 44:279-289.
26. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J.Struct. Biol. 2003, 142:334-347.
27. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
28. Morimoto D., Walinda E., Fukada H., Sou Y.S., Kageyama S., Hoshino M., Fujii T., Tsuchiya H., Saeki Y., Arita K., et al. The unexpected role of polyubiquitin chains in the formation of fibrillar aggregates. Nat. Commun. 2015, 6:6116.
29. Moscat J., Diaz-Meco M.T. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009, 137:1001-1004.
30. Moscat J., Diaz-Meco M.T. p62: a versatile multitasker takes on cancer. Trends Biochem. Sci. 2012, 37:230-236.
31. Paine M.G., Babu J.R., Seibenhener M.L., Wooten M.W. Evidence for p62 aggregate formation: role in cell survival. FEBS Lett. 2005, 579:5029-5034.
32. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Øvervatn A., Bjørkøy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J.Biol. Chem. 2007, 282:24131-24145.
33. Ramesh Babu J., Lamar Seibenhener M., Peng J., Strom A.L., Kemppainen R., Cox N., Zhu H., Wooten M.C., Diaz-Meco M.T., Moscat J., Wooten M.W. Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration. J.Neurochem. 2008, 106:107-120.
34. Sachse C., Chen J.Z., Coureux P.D., Stroupe M.E., Fändrich M., Grigorieff N. High-resolution electron microscopy of helical specimens: a fresh look at tobacco mosaic virus. J.Mol. Biol. 2007, 371:812-835.
35. Saio T., Yokochi M., Inagaki F. The NMR structure of the p62 PB1 domain, a key protein in autophagy and NF-kappaB signaling pathway. J.Biomol. NMR 2009, 45:335-341.
36. Saio T., Yokochi M., Kumeta H., Inagaki F. PCS-based structure determination of protein-protein complexes. J.Biomol. NMR 2010, 46:271-280.
37. Sawa-Makarska J., Abert C., Romanov J., Zens B., Ibiricu I., Martens S. Cargo binding to Atg19 unmasks additional Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy. Nat. Cell Biol. 2014, 16:425-433.
38. Scheres S.H.W., Chen S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 2012, 9:853-854.
39. Stumptner C., Fuchsbichler A., Zatloukal K., Denk H. Invitro production of Mallory bodies and intracellular hyaline bodies: the central role of sequestosome 1/p62. Hepatology 2007, 46:851-860.
40. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., Rees I., Ludtke S.J. EMAN2: an extensible image processing suite for electron microscopy. J.Struct. Biol. 2007, 157:38-46.
41. Wall J.S., Simon M.N. Scanning transmission electron microscopy of DNA-protein complexes. Methods Mol. Biol. 2001, 148:589-601.
42. Wilson M.I., Gill D.J., Perisic O., Quinn M.T., Williams R.L. PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol. Cell 2003, 12:39-50.
43. Zatloukal K., Stumptner C., Fuchsbichler A., Heid H., Schnoelzer M., Kenner L., Kleinert R., Prinz M., Aguzzi A., Denk H. p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am. J. Pathol. 2002, 160:255-263.
44. Zhang Y., Wang W., Chen J., Zhang K., Gao F., Gao B., Zhang S., Dong M., Besenbacher F., Gong W., et al. Structural insights into the intrinsic self-assembly of Par-3 N-terminal domain. Structure 2013, 21:997-1006.