Phosphorylation of NBR1 by GSK3 modulates protein aggregation

Autophagy

Volumn 10, Issue 6, 2014, Pages 1036-1053

  Nicot, Anne Sophie ^a   Verso, Francesca Lo ^b   Ratti, Francesca ^a   Pilot Storck, Fanny ^a,d   Streichenberger, Nathalie ^a,c   Sandri, Marco ^b   Schaeffer, Laurent ^a,c   Goillot, Evelyne ^a  

^a UNIVERSITÉ DE LYON   (France)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c HOSPICES CIVILS DE LYON   (France)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Autophagy; GSK3; NBR1; SIBM; Skeletal muscle; Sporadic inclusion body myositis; Ubiquitinated protein aggregates

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; NEIGHBOR OF BRCA1 GENE 1; PROTEIN; PUROMYCIN; THREONINE; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; ATG7 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; NBR1 PROTEIN, HUMAN; NBR1 PROTEIN, MOUSE; PROTEIN AGGREGATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEGRADATION; DNA LIBRARY; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INCLUSION BODY MYOSITIS; MUSCLE BIOPSY; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; SELECTIVE AUTOPHAGY; WESTERN BLOTTING; ANIMAL; AUTOPHAGY; BIOLOGICAL MODEL; CELL CULTURE; CELL LINE; CHEMISTRY; DEFICIENCY; GENETICS; HEK293 CELL LINE; HELA CELL LINE; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEOSTASIS DEFICIENCY; UBIQUITINATION;

ANIMALS; AUTOPHAGY; CELL LINE; CELLS, CULTURED; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; MYOSITIS, INCLUSION BODY; PHOSPHORYLATION; PROTEIN AGGREGATES; PROTEINS; PROTEOSTASIS DEFICIENCIES; UBIQUITINATION;

EID: 84903627153     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28479     Document Type: Article

References (51)

1. Taylor JP, Hardy J, Fischbeck KH. Toxic proteins in neurodegenerative disease. Science 2002; 296:1991-5; PMID:12065827; http://dx.doi.org/10.1126/ science.1067122 (Pubitemid 34627514)
2. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585-95; PMID:15146184; http://dx.doi.org/10.1038/ng1362 (Pubitemid 38715985)
3. Yamamoto A, Lucas JJ, Hen R. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 2000; 101:57-66; PMID:10778856; http://dx.doi.org/10.1016/S0092-8674(00)80623-6
4. Zu T, Duvick LA, Kaytor MD, Berlinger MS, Zoghbi HY, Clark HB, Orr HT. Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J Neurosci 2004; 24:8853-61; PMID:15470152; http://dx.doi.org/10.1523/JNEUROSCI.2978-04.2004 (Pubitemid 39362981)
5. Holmberg CI, Staniszewski KE, Mensah KN, Matouschek A, Morimoto RI. Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO J 2004; 23:4307-18; PMID:15470501; http://dx.doi.org/10.1038/sj.emboj. 7600426 (Pubitemid 39546168)
6. Venkatraman P, Wetzel R, Tanaka M, Nukina N, Goldberg AL. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol Cell 2004; 14:95-104; PMID:15068806; http://dx.doi.org/10.1016/S1097-2765(04)00151-0 (Pubitemid 38469912)
7. Filimonenko M, Isakson P, Finley KD, Anderson M, Jeong H, Melia TJ, Bartlett BJ, Myers KM, Birkeland HC, Lamark T, et al. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol Cell 2010; 38:265-79; PMID:20417604; http://dx.doi.org/10. 1016/j. molcel.2010.04.007
8. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
9. Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33:505-16; PMID:19250911; http://dx.doi.org/10.1016/j.molcel.2009.01.020
10. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, 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; 282:24131-45; PMID:17580304; http://dx.doi.org/10.1074/jbc. M702824200 (Pubitemid 47328003)
11. Waters S, Marchbank K, Solomon E, Whitehouse C, Gautel M. Interactions with LC3 and polyubiquitin chains link nbr1 to autophagic protein turnover. FEBS Lett 2009; 583:1846-52; PMID:19427866; http://dx.doi.org/10.1016/j.febslet. 2009.04.049
12. 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; 44:279-89; PMID:22017874; http://dx.doi.org/10.1016/j. molcel.2011.07.039
13. Gal J, Ström AL, Kilty R, Zhang F, Zhu H. p62 accumulates and enhances aggregate formation in model systems of familial amyotrophic lateral sclerosis. J Biol Chem 2007; 282:11068-77; PMID:17296612; http://dx.doi.org/10. 1074/jbc. M608787200 (Pubitemid 47100749)
14. Odagiri S, Tanji K, Mori F, Kakita A, Takahashi H, Wakabayashi K. Autophagic adapter protein NBR1 is localized in Lewy bodies and glial cytoplasmic inclusions and is involved in aggregate formation in α-synucleinopathy. Acta Neuropathol 2012; 124:173-86; PMID:22484440; http://dx.doi.org/10.1007/s00401-012-0975-7
15. D'Agostino C, Nogalska A, Cacciottolo M, Engel WK, Askanas V. Abnormalities of NBR1, a novel autophagy-associated protein, in muscle fibers of sporadic inclusion-body myositis. Acta Neuropathol 2011; 122:627-36; PMID:21935636; http://dx.doi.org/10.1007/s00401-011-0874-3
16. 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; 160:255-63; PMID:11786419; http://dx.doi.org/10.1016/S0002-9440(10)64369-6 (Pubitemid 34052286)
17. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011; 333:228-33; PMID:21617041; http://dx.doi.org/10.1126/science.1205405
18. Deosaran E, Larsen KB, Hua R, Sargent G, Wang Y, Kim S, Lamark T, Jauregui M, Law K, Lippincott-Schwartz J, et al. NBR1 acts as an autophagy receptor for peroxisomes. J Cell Sci 2013; 126:939-52; PMID:23239026; http://dx.doi.org/10.1242/jcs.114819
19. Kuo TC, Chen CT, Baron D, Onder TT, Loewer S, Almeida S, Weismann CM, Xu P, Houghton JM, Gao FB, et al. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat Cell Biol 2011; 13:1214-23; PMID:21909099; http://dx.doi.org/10.1038/ncb2332
20. Mardakheh FK, Yekezare M, Machesky LM, Heath JK. Spred2 interaction with the late endosomal protein NBR1 down-regulates fibroblast growth factor receptor signaling. J Cell Biol 2009; 187:265-77; PMID:19822672; http://dx.doi.org/10. 1083/jcb.200905118
21. Mardakheh FK, Auciello G, Dafforn TR, Rappoport JZ, Heath JK. Nbr1 is a novel inhibitor of ligandmediated receptor tyrosine kinase degradation. Mol Cell Biol 2010; 30:5672-85; PMID:20937771; http://dx.doi.org/10.1128/MCB.00878-10
22. Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E, Kristensen J, Brandmeier B, Franzen G, Hedberg B, et al. The kinase domain of titin controls muscle gene expression and protein turnover. Science 2005; 308:1599-603; PMID:15802564; http://dx.doi.org/10.1126/science.1110463 (Pubitemid 40807503)
23. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378:785-9; PMID:8524413; http://dx.doi.org/10.1038/378785a0 (Pubitemid 26004411)
24. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004; 29:95-102; PMID:15102436; http://dx.doi.org/10.1016/j. tibs.2003.12.004 (Pubitemid 38186580)
25. Wills J, Jones J, Haggerty T, Duka V, Joyce JN, Sidhu A. Elevated tauopathy and alpha-synuclein pathology in postmortem Parkinson's disease brains with and without dementia. Exp Neurol 2010; 225:210-8; PMID:20599975; http://dx.doi.org/10.1016/j. expneurol.2010.06.017
26. Carmichael J, Sugars KL, Bao YP, Rubinsztein DC. Glycogen synthase kinase-3beta inhibitors prevent cellular polyglutamine toxicity caused by the Huntington's disease mutation. J Biol Chem 2002; 277:33791-8; PMID:12097329; http://dx.doi.org/10.1074/jbc.M204861200
27. Grimes CA, Jope RS. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 2001; 65:391-426; PMID:11527574; http://dx.doi.org/10.1016/S0301-0082(01)00011-9 (Pubitemid 32781670)
28. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 2005; 170:1101-11; PMID:16186256; http://dx.doi.org/10.1083/jcb.200504035 (Pubitemid 41362642)
29. Pilot-Storck F, Chopin E, Rual JF, Baudot A, Dobrokhotov P, Robinson-Rechavi M, Brun C, Cusick ME, Hill DE, Schaeffer L, et al. Interactome mapping of the phosphatidylinositol 3-kinasemammalian target of rapamycin pathway identifies deformed epidermal autoregulatory factor-1 as a new glycogen synthase kinase-3 interactor. Mol Cell Proteomics 2010; 9:1578-93; PMID:20368287; http://dx.doi.org/10.1074/mcp.M900568-MCP200
30. Kunick C, Lauenroth K, Leost M, Meijer L, Lemcke T. 1-Azakenpaullone is a selective inhibitor of glycogen synthase kinase-3 beta. Bioorg Med Chem Lett 2004; 14:413-6; PMID:14698171; http://dx.doi.org/10.1016/j.bmcl.2003.10.062 (Pubitemid 38045135)
31. Cohen P, Frame S. The renaissance of GSK3. Nat Rev Mol Cell Biol 2001; 2:769-76; PMID:11584304; http://dx.doi.org/10.1038/35096075 (Pubitemid 33679839)
32. Frame S, Cohen P, Biondi RM. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 2001; 7:1321-7; PMID:11430833; http://dx.doi.org/10.1016/S1097-2765(01) 00253-2 (Pubitemid 32607364)
33. Jackson GR, Wiedau-Pazos M, Sang TK, Wagle N, Brown CA, Massachi S, Geschwind DH. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 2002; 34:509-19; PMID:12062036; http://dx.doi.org/10.1016/S0896-6273(02)00706-7 (Pubitemid 34628749)
34. Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, David A, Gatti E, Pierre P. Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 2004; 164:667-75; PMID:14981091; http://dx.doi.org/10.1083/jcb.200312073 (Pubitemid 38282951)
35. Selcen D. Myofibrillar myopathies. Neuromuscul Disord 2011; 21:161-71; PMID:21256014; http://dx.doi.org/10.1016/j.nmd.2010.12.007
36. Olivé M, van Leeuwen FW, Janué A, Moreno D, Torrejón-Escribano B, Ferrer I. Expression of mutant ubiquitin (UBB+1) and p62 in myotilinopathies and desminopathies. Neuropathol Appl Neurobiol 2008; 34:76-87; PMID:17931355
37. Dalakas MC, Dagvadorj A, Goudeau B, Park KY, Takeda K, Simon-Casteras M, Vasconcelos O, Sambuughin N, Shatunov A, Nagle JW, et al. Progressive skeletal myopathy, a phenotypic variant of desmin myopathy associated with desmin mutations. Neuromuscul Disord 2003; 13:252-8; PMID:12609507; http://dx.doi.org/10.1016/s0960-8966(02)00271-7 (Pubitemid 36279430)
38. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10:507-15; PMID:19945408; http://dx.doi.org/10.1016/j. cmet.2009.10.008
39. Askanas V, Engel WK. Sporadic inclusion-body myositis: conformational multifactorial ageingrelated degenerative muscle disease associated with proteasomal and lysosomal inhibition, endoplasmic reticulum stress, and accumulation of amyloid-β42 oligomers and phosphorylated tau. Presse Med 2011; 40:e219-35; PMID:21392932; http://dx.doi.org/10.1016/j.lpm.2010.11.024
40. Morosetti R, Broccolini A, Sancricca C, Gliubizzi C, Gidaro T, Tonali PA, Ricci E, Mirabella M. Increased aging in primary muscle cultures of sporadic inclusion-body myositis. Neurobiol Aging 2010; 31:1205-14; PMID:18823681; http://dx.doi.org/10.1016/j.neurobiolaging.2008.08.011
41. Terracciano C, Nogalska A, Engel WK, Askanas V. In AbetaPP-overexpressing cultured human muscle fibers proteasome inhibition enhances phosphorylation of AbetaPP751 and GSK3beta activation: effects mitigated by lithium and apparently relevant to sporadic inclusion-body myositis. J Neurochem 2010; 112:389-96; PMID:19878439; http://dx.doi.org/10.1111/j.1471-4159.2009.06461.x
42. Lei P, Ayton S, Bush AI, Adlard PA. GSK-3 in Neurodegenerative Diseases. Int J Alzheimers Dis 2011; 2011:189246; PMID:21629738; http://dx.doi.org/10. 4061/2011/189246
43. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91; PMID:19211835; http://dx.doi.org/10.1091/mbc.E08-12-1248
44. Lin SY, Li TY, Liu Q, Zhang C, Li X, Chen Y, Zhang SM, Lian G, Liu Q, Ruan K, et al. GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science 2012; 336:477-81; PMID:22539723; http://dx.doi.org/10. 1126/science.1217032
45. Ohlsson M, Hedberg C, Brådvik B, Lindberg C, Tajsharghi H, Danielsson O, Melberg A, Udd B, Martinsson T, Oldfors A. Hereditary myopathy with early respiratory failure associated with a mutation in A-band titin. Brain 2012; 135:1682-94; PMID:22577218; http://dx.doi.org/10.1093/brain/aws103
46. Pfeffer G, Barresi R, Wilson IJ, Hardy SA, Griffin H, Hudson J, Elliott HR, Ramesh AV, Radunovic A, Winer JB, et al. Titin founder mutation is a common cause of myofibrillar myopathy with early respiratory failure. J Neurol Neurosurg Psychiatry 2014; 85:331-8; PMID:23486992; http://dx.doi.org/10.1136/ jnnp-2012-304728
47. Kramer T, Schmidt B, Lo Monte F. Small-Molecule Inhibitors of GSK-3: Structural Insights and Their Application to Alzheimer's Disease Models. Int J Alzheimers Dis 2012; 2012:381029; PMID:22888461; http://dx.doi.org/10.1155/2012/ 381029
48. MacAulay K, Doble BW, Patel S, Hansotia T, Sinclair EM, Drucker DJ, Nagy A, Woodgett JR. Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell Metab 2007; 6:329-37; PMID:17908561; http://dx.doi.org/10.1016/j.cmet.2007.08.013 (Pubitemid 47450185)
49. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117:399-412; PMID:15109499; http://dx.doi.org/10.1016/S0092-8674(04) 00400-3 (Pubitemid 38534545)
50. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to Image J: 25 years of image analysis. Nat Methods 2012; 9:671-5; PMID:22930834; http://dx.doi.org/10. 1038/nmeth.2089
51. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885-9; PMID:16625204; http://dx.doi.org/10.1038/nature04724