NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets

Cell Cycle

Volumn 8, Issue 13, 2009, Pages 1986-1990

  Lamark, Trond ^a   Kirkin, Vladimir ^b,d   Dikic, Ivan ^b,c   Johansen, Terje ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b GOETHE UNIVERSITY   (Germany)

^c Mediterranean Institute for Life Sciences   (Croatia)

^d MERCK KGAA   (Germany)

Author keywords

LIR; NBR1; P62; Protein aggregates; Selective autophagy; Ubiquitin

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; ACTIVATING TRANSCRIPTION FACTOR 8; BINDING PROTEIN; NBR1 PROTEIN; PROTEIN P62; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AUTOPHAGY; ENZYME SUBSTRATE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; REVIEW; UBIQUITINATION;

MAMMALIA;

EID: 67650517556     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.13.8892     Document Type: Review

References (54)

1. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42.
2. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-1109 (Pubitemid 47500484)
3. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-1075 (Pubitemid 351317450)
4. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001; 2:211-216 (Pubitemid 33675746)
5. He H, Dang Y, Dai F, Guo Z, Wu J, She X, et al. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 2003; 278:29278-29287 (Pubitemid 36935844)
6. Xin Y, Yu L, Chen Z, Zheng L, Fu Q, Jiang J, et al. Cloning, expression patterns and chromosome localization of three human and two mouse homologues of GABA(A) receptor-associated protein. Genomics 2001; 74:408-413 (Pubitemid 32675366)
7. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117:2805-2812 (Pubitemid 38997262)
8. Tanida I, Ueno T, Kominami E. Human light chain 3/MAP1LC3B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 2004; 279:47704-47710 (Pubitemid 39540917)
9. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-175 (Pubitemid 351231180)
10. Sou YS, Tanida I, Komatsu M, Ueno T, Kominami E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP and GATE-16. J Biol Chem 2006; 281:3017-3024 (Pubitemid 43845910)
11. Nakatogawa H, Ichimura Y, Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007; 130:165-178 (Pubitemid 47031316)
12. Dice JF. Chaperone-mediated autophagy. Autophagy 2007; 3:295-299
13. Rubinsztein DC. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006; 443:780-786 (Pubitemid 44622682)
14. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, Yoshimori T, et al. ALIS are Stress-Induced Protein Storage Compartments for Substrates of the Proteasome and Autophagy. Autophagy 2006; 2:189-199 (Pubitemid 44030883)
15. Bjoørkoøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn A, et al. 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 (Pubitemid 41668720)
16. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C. Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 2009; 28:889-901.
17. Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA, et al. A Role for NBR1 in Autophagosomal Degradation of Ubiquitinated Substrates. Mol Cell 2009; 33:505-516
18. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149-1163 (Pubitemid 350235021)
19. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-24145 (Pubitemid 47328003)
20. van der Vaart A, Mari M, Reggiori F. A picky eater: exploring the mechanisms of selective autophagy in human pathologies. Traffic 2008; 9:281-289 (Pubitemid 351188990)
21. Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, et al. Excess peroxisomes are degraded by autophagic machinery in mammals. J Biol Chem 2006; 281:4035-4041 (Pubitemid 43847828)
22. Tolkovsky AM. Mitophagy. Biochim Biophys Acta 2009; In press.
23. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 2005; 120:159-162 (Pubitemid 40174758)
24. Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006; 4:423. (Pubitemid 44917620)
25. Kraft C, Deplazes A, Sohrmann M, Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 2008; 10:602-610 (Pubitemid 351627380)
26. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885-889 (Pubitemid 43910423)
27. Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 2008; 105:20567-20574
28. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441:880-884 (Pubitemid 43910422)
29. Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH. Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr Biol 2004; 14:806-811 (Pubitemid 38583717)
30. Pohl C, Jentsch S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat Cell Biol 2009; 11:65-70.
31. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, et al. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 2008; 283:22847-22857
32. Bjorkoy G, Lamark T, Pankiv S, Overvatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452:181-197
33. Noda NN, Kumeta H, Nakatogawa H, Satoo K, Adachi W, Ishii J, et al. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 2008; 13:1211-1218
34. Moscat J, Diaz-Meco MT, Wooten MW. Signal integration and diversification through the p62 scaffold protein. Trends Biochem Sci 2007; 32:95-100. (Pubitemid 46199192)
35. Cavey JR, Ralston SH, Hocking LJ, Sheppard PW, Ciani B, Searle MS, et al. Loss of ubiquitin-binding associated with Paget's disease of bone p62 (SQSTM1) mutations. J Bone Miner Res 2005; 20:619-624 (Pubitemid 40393070)
36. Pursiheimo JP, Rantanen K, Heikkinen PT, Johansen T, Jaakkola PM. Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62. Oncogene 2009; 28:334-344
37. Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E, et al. The kinase domain of titin controls muscle gene expression and protein turnover. Science 2005; 308: 1599-1603 (Pubitemid 40807503)
38. Shvets E, Fass E, Scherz-Shouval R, Elazar Z. The N-terminus and Phe52 residue of LC3 recruit p62/SQSTM1 into autophagosomes. J Cell Sci 2008; 121:2685-2695
39. Zhang Y, Yan L, Zhou Z, Yang P, Tian E, Zhang K, et al. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell 2009; 136:308-321
40. Mohrluder J, Hoffmann Y, Stangler T, Hanel K, Willbold D. Identification of clathrin heavy chain as a direct interaction partner for the gamma-aminobutyric acid type A receptor associated protein. Biochemistry 2007; 46:14537-14543 (Pubitemid 350276359)
41. Mohrluder J, Stangler T, Hoffmann Y, Wiesehan K, Mataruga A, Willbold D. Identification of calreticulin as a ligand of GABARAP by phage display screening of a peptide library. FEBS J 2007; 274:5543-5555 (Pubitemid 47622066)
42. Schwarten M, Mohrluder J, Ma P, Stoldt M, Thielmann Y, Stangler T, et al. Nix directly binds to GABARAP: A possible crosstalk between apoptosis and autophagy. Autophagy 2009; In press.
43. Strnad P, Zatloukal K, Stumptner C, Kulaksiz H, Denk H. Mallory-Denk-bodies: lessons from keratin-containing hepatic inclusion bodies. Biochim Biophys Acta 2008; 1782:764-774
44. 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 (Pubitemid 32646250)
45. Nagaoka U, Kim K, Jana NR, Doi H, Maruyama M, Mitsui K, et al. Increased expression of p62 in expanded polyglutamine-expressing cells and its association with polyglutamine inclusions. J Neurochem 2004; 91:57-68. (Pubitemid 39314937)
46. Zatloukal K, Stumptner C, Fuchsbichler A, Heid H, Schnoelzer M, Kenner L, et al. p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol 2002; 160:255-263 (Pubitemid 34052286)
47. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, et al. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 2007; 179:485-500. (Pubitemid 350074792)
48. Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell 2009; 33:517-527
49. Lindmo K, Brech A, Finley KD, Gaumer S, Contamine D, Rusten TE, et al. The PI 3-kinase regulator Vps15 is required for autophagic clearance of protein aggregates. Autophagy 2008; 4:500-506 (Pubitemid 351705146)
50. Nezis IP, Simonsen A, Sagona AP, Finley K, Gaumer S, Contamine D, et al. Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J Cell Biol 2008; 180:1065-1071
51. Lamark T, Perander M, Outzen H, Kristiansen K, Øvervatn A, Michaelsen E, et al. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 2003; 278:34568-34581
52. Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, David A, et al. Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 2004; 164:667-675 (Pubitemid 38282951)
53. Wang Z, Figueiredo-Pereira ME. Inhibition of sequestosome 1/p62 upregulation prevents aggregation of ubiquitinated proteins induced by prostaglandin J2 without reducing its neurotoxicity. Mol Cell Neurosci 2005; 29:222-231 (Pubitemid 40725612)
54. Lelouard H, Gatti E, Cappello F, Gresser O, Camosseto V, Pierre P. Transient aggregation of ubiquitinated proteins during dendritic cell maturation. Nature 2002; 417:177-182 (Pubitemid 34506798)