BAG3 induces the sequestration of proteasomal clients into cytoplasmic puncta Implications for a proteasome-to-autophagy switch

Autophagy

Volumn 10, Issue 9, 2014, Pages 1603-1621

  Minoia, Melania ^a   Boncoraglio, Alessandra ^a,b   Vinet, Jonathan ^c   Morelli, Federica F ^c   Brunsting, Jeanette F ^a   Poletti, Angelo ^b   Krom, Sabine ^d   Reits, Eric ^d   Kampinga, Harm H ^a   Carra, Serena ^a,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Autophagy linkers; BAG3; Proteasome inhibition; Ubiquitinated proteins

Indexed keywords

BAG 1 PROTEIN; BAG3 PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; HEAT SHOCK COGNATE PROTEIN 70; PROTEASOME; UBIQUITIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BAG3 PROTEIN, HUMAN; BCL2-ASSOCIATED ATHANOGENE 1 PROTEIN; DNA BINDING PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BINDING COMPETITION; CONTROLLED STUDY; CYTOPLASM; EMBRYO; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; UBIQUITINATION; UPREGULATION; HUMAN; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; CYTOPLASM; DNA-BINDING PROTEINS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; TRANSCRIPTION FACTORS; UBIQUITIN;

EID: 84907166419     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.29409     Document Type: Article

References (61)

1. Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003; 4:181-91; PMID:12612637; http://dx.doi.org/10.1038/nrm1052
2. Feldman DE, Frydman J. Protein folding in vivo: the importance of molecular chaperones. Curr Opin Struct Biol 2000; 10:26-33; PMID:10679467; http://dx.doi.org/10.1016/S0959-440X(99)00044-5
3. Hartl FU, Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 2009; 16:574-81; PMID:19491934; http://dx.doi.org/10.1038/nsmb.1591
4. Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: the long road to destruction. Nat Cell Biol 2005; 7:766-72; PMID:16056268; http://dx.doi.org/10.1038/ncb0805-766
5. Rubinsztein DC. The roles of intracellular proteindegradation pathways in neurodegeneration. Nature 2006; 443:780-6; PMID:17051204; http://dx.doi.org/10.1038/nature05291
6. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005; 6:79-87; PMID:15688069; http://dx.doi.org/10.1038/nrm1552
7. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010; 22:124-31; PMID:20034776; http://dx.doi.org/10.1016/j.ceb.2009.11.014
8. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, Yin XM. Linking of autophagy to ubiquitinproteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007; 171:513-24; PMID:17620365; http://dx.doi.org/10.2353/ajpath.2007.070188
9. Ding WX, Yin XM. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 2008; 4:141-50; PMID:17986870
10. Gamerdinger M, Carra S, Behl C. Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J Mol Med (Berl) 2011; 89:1175-82; PMID:21818581; http://dx.doi.org/10.1007/s00109-011-0795-6
11. 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; PMID:19229298; http://dx.doi.org/10.1038/emboj.2009.29
12. Martinez-Vicente M, Sovak G, Cuervo AM. Protein degradation and aging. Exp Gerontol 2005; 40:622-33; PMID:16125351; http://dx.doi.org/10.1016/j.exger.2005.07.005
13. Ward WF. Protein degradation in the aging organism. Prog Mol Subcell Biol 2002; 29:35-42; PMID:11908071; http://dx.doi.org/10.1007/978-3-642-56373-7-3
14. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009; 78:959-91; PMID:19298183; http://dx.doi.org/10.1146/annurev.biochem.052308.114844
15. Morimoto RI. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 2008; 22:1427-38; PMID:18519635; http://dx.doi.org/10.1101/gad.1657108
16. Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Fürst DO, Saftig P, Saint R, Fleischmann BK, et al. Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 2010; 20:143-8; PMID:20060297; http://dx.doi.org/10.1016/j.cub.2009.11.022
17. Carra S, Seguin SJ, Lambert H, Landry J. HspB8 chaperone activity toward poly(Q)-containing proteins depends on its association with Bag3, a stimulator of macroautophagy. J Biol Chem 2008; 283:1437-44; PMID:18006506; http://dx.doi.org/10.1074/jbc.M706304200
18. Kalia SK, Lee S, Smith PD, Liu L, Crocker SJ, Thorarinsdottir TE, Glover JR, Fon EA, Park DS, Lozano AM. BAG5 inhibits parkin and enhances dopaminergic neuron degeneration. Neuron 2004; 44:931-45; PMID:15603737; http://dx.doi.org/10.1016/j.neuron.2004.11.026
19. Lüders J, Demand J, Höhfeld J. The ubiquitinrelated BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 2000; 275:4613-7; PMID:10671488; http://dx.doi.org/10.1074/jbc.275.7.4613
20. Crippa V, Sau D, Rusmini P, Boncoraglio A, Onesto E, Bolzoni E, Galbiati M, Fontana E, Marino M, Carra S, et al. The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS). Hum Mol Genet 2010; 19:3440-56; PMID:20570967; http://dx.doi.org/10.1093/hmg/ddq257
21. Gamerdinger M, Kaya AM, Wolfrum U, Clement AM, Behl C. BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep 2011; 12:149-56; PMID:21252941; http://dx.doi.org/10.1038/embor.2010.203
22. Carra S, Seguin SJ, Landry J. HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 2008; 4:237-9; PMID:18094623
23. Anckar J, Sistonen L. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 2011; 80:1089-115; PMID:21417720; http://dx.doi.org/10.1146/annurev-biochem-060809-095203
24. Nivon M, Abou-Samra M, Richet E, Guyot B, Arrigo AP, Kretz-Remy C. NF-κB regulates protein quality control after heat stress through modulation of the BAG3-HspB8 complex. J Cell Sci 2012; 125:1141-51; PMID:22302993; http://dx.doi.org/10.1242/jcs.091041
25. Nivon M, Richet E, Codogno P, Arrigo AP, Kretz-Remy C. Autophagy activation by NFkappaB is essential for cell survival after heat shock. Autophagy 2009; 5:766-83; PMID:19502777
26. Ron D. Translational control in the endoplasmic reticulum stress response. J Clin Invest 2002; 110:1383-8; PMID:12438433; http://dx.doi.org/10.1172/JCI0216784
27. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519-29; PMID:17565364; http://dx.doi.org/10.1038/nrm2199
28. Carra S, Brunsting JF, Lambert H, Landry J, Kampinga HH. HspB8 participates in protein quality control by a non-chaperone-like mechanism that requires eIF2alpha phosphorylation. J Biol Chem 2009; 284:5523-32; PMID:19114712; http://dx.doi.org/10.1074/jbc.M807440200
29. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgó J, Díaz J, Lavandero S, Harper F, et al. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 2007; 14:1029-39; PMID:17256008
30. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007; 14:230-9; PMID:16794605; http://dx.doi.org/10.1038/sj.cdd.4401984
31. Tallóczy Z, Jiang W, Virgin HW 4th, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B. Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A 2002; 99:190-5; PMID:11756670; http://dx.doi.org/10.1073/pnas.012485299
32. Salomons FA, Menéndez-Benito V, Böttcher C, McCray BA, Taylor JP, Dantuma NP. Selective accumulation of aggregation-prone proteasome substrates in response to proteotoxic stress. Mol Cell Biol 2009; 29:1774-85; PMID:19158272; http://dx.doi.org/10.1128/MCB.01485-08
33. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007; 447:859-63; PMID:17568747; http://dx.doi.org/10.1038/nature05853
34. Iwata A, Riley BE, Johnston JA, Kopito RR. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 2005; 280:40282-92; PMID:16192271; http://dx.doi.org/10.1074/jbc.M508786200
35. Du ZX, Zhang HY, Meng X, Gao YY, Zou RL, Liu BQ, Guan Y, Wang HQ. Proteasome inhibitor MG132 induces BAG3 expression through activation of heat shock factor 1. J Cell Physiol 2009; 218:631-7; PMID:19006120; http://dx.doi.org/10.1002/jcp.21634
36. Gentilella A, Khalili K. BAG3 expression in glioblastoma cells promotes accumulation of ubiquitinated clients in an Hsp70-dependent manner. J Biol Chem 2011; 286:9205-15; PMID:21233200; http://dx.doi.org/10.1074/jbc.M110.175836
37. Wang HQ, Liu HM, Zhang HY, Guan Y, Du ZX. Transcriptional upregulation of BAG3 upon proteasome inhibition. Biochem Biophys Res Commun 2008; 365:381-5; PMID:17996194; http://dx.doi.org/10.1016/j.bbrc.2007.11.001
38. Carra S, Boncoraglio A, Kanon B, Brunsting JF, Minoia M, Rana A, Vos MJ, Seidel K, Sibon OC, Kampinga HH. Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases. J Biol Chem 2010; 285:37811-22; PMID:20858900; http://dx.doi.org/10.1074/jbc.M110.127498
39. 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 huntingtininduced cell death. J Cell Biol 2005; 171:603-14; PMID:16286508; http://dx.doi.org/10.1083/jcb.200507002
40. Doong H, Rizzo K, Fang S, Kulpa V, Weissman AM, Kohn EC. CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: accumulation of poly-ubiquitinated Hsp90 client proteins. J Biol Chem 2003; 278:28490-500; PMID:12750378; http://dx.doi.org/10.1074/jbc.M209682200
41. Takayama S, Reed JC. Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 2001; 3:E237-41; PMID:11584289; http://dx.doi.org/10.1038/ncb1001-e237
42. Höhfeld J, Cyr DM, Patterson C. From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBO Rep 2001; 2:885-90; PMID:11600451; http://dx.doi.org/10.1093/embo-reports/kve206
43. Moore DJ, West AB, Dikeman DA, Dawson VL, Dawson TM. Parkin mediates the degradationindependent ubiquitination of Hsp70. J Neurochem 2008; 105:1806-19; PMID:18248624; http://dx.doi.org/10.1111/j.1471-4159.2008.05261.x
44. Glickman MH, Ciechanover A. The ubiquitinproteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82:373-428; PMID:11917093
45. Johnston JA, Ward CL, Kopito RR. Aggresomes: a cellular response to misfolded proteins. J Cell Biol 1998; 143:1883-98; PMID:9864362; http://dx.doi.org/10.1083/jcb.143.7.1883
46. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
47. Rapino F, Jung M, Fulda S. BAG3 induction is required to mitigate proteotoxicity via selective autophagy following inhibition of constitutive protein degradation pathways. Oncogene 2014; 33:1713-24; PMID:23644654; http://dx.doi.org/10.1038/onc.2013.110
48. Dantuma NP, Lindsten K, Glas R, Jellne M, Masucci MG. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat Biotechnol 2000; 18:538-43; PMID:10802622; http://dx.doi.org/10.1038/75406
49. Yanagida M. Cell cycle mechanisms of sister chromatid separation; roles of Cut1/separin and Cut2/securin. Genes Cells 2000; 5:1-8; PMID:10651900; http://dx.doi.org/10.1046/j.1365-2443.2000.00306.x
50. Florea BI, Verdoes M, Li N, van der Linden WA, Geurink PP, van den Elst H, Hofmann T, de Ru A, van Veelen PA, Tanaka K, et al. Activity-based profiling reveals reactivity of the murine thymoproteasomespecific subunit beta5t. Chem Biol 2010; 17:795-801; PMID:20797608; http://dx.doi.org/10.1016/j.chembiol.2010.05.027
51. Rauch JN, Gestwicki JE. Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J Biol Chem 2014; 289:1402-14; PMID:24318877; http://dx.doi.org/10.1074/jbc.M113.521997
52. Pagliuca MG, Lerose R, Cigliano S, Leone A. Regulation by heavy metals and temperature of the human BAG-3 gene, a modulator of Hsp70 activity. FEBS Lett 2003; 541:11-5; PMID:12706811; http://dx.doi.org/10.1016/S0014-5793(03)00274-6
53. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, Dynlacht BD. XBP1 controls diverse cell type-and conditionspecific transcriptional regulatory networks. Mol Cell 2007; 27:53-66; PMID:17612490; http://dx.doi.org/10.1016/j.molcel.2007.06.011
54. de Bie P, van de Sluis B, Burstein E, Duran KJ, Berger R, Duckett CS, Wijmenga C, Klomp LW. Characterization of COMMD protein-protein interactions in NF-kappaB signalling. Biochem J 2006; 398:63-71; PMID:16573520; http://dx.doi.org/10.1042/BJ20051664
55. 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
56. Fuchs M, Poirier DJ, Seguin SJ, Lambert H, Carra S, Charette SJ, Landry J. Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochem J 2010; 425:245-55; PMID:19845507; http://dx.doi.org/10.1042/BJ20090907
57. Seidel K, Vinet J, Dunnen WF, Brunt ER, Meister M, Boncoraglio A, Zijlstra MP, Boddeke HW, Rüb U, Kampinga HH, et al. The HSPB8-BAG3 chaperone complex is upregulated in astrocytes in the human brain affected by protein aggregation diseases. Neuropathol Appl Neurobiol 2012; 38:39-53; PMID:21696420; http://dx.doi.org/10.1111/j.1365-2990.2011.01198.x
58. Carra S, Crippa V, Rusmini P, Boncoraglio A, Minoia M, Giorgetti E, Kampinga HH, Poletti A. Alteration of protein folding and degradation in motor neuron diseases: Implications and protective functions of small heat shock proteins. Prog Neurobiol 2012; 97:83-100; PMID:21971574; http://dx.doi.org/10.1016/j.pneurobio.2011.09.009
59. Carra S, Sivilotti M, Chávez Zobel AT, Lambert H, Landry J. HspB8, a small heat shock protein mutated in human neuromuscular disorders, has in vivo chaperone activity in cultured cells. Hum Mol Genet 2005; 14:1659-69; PMID:15879436; http://dx.doi.org/10.1093/hmg/ddi174
60. Hageman J, Rujano MA, van Waarde MA, Kakkar V, Dirks RP, Govorukhina N, Oosterveld-Hut HM, Lubsen NH, Kampinga HH. A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation. Mol Cell 2010; 37:355-69; PMID:20159555; http://dx.doi.org/10.1016/j.molcel.2010.01.001
61. Heldens L, Hensen SM, Onnekink C, van Genesen ST, Dirks RP, Lubsen NH. An atypical unfolded protein response in heat shocked cells. PLoS One 2011; 6:e23512; PMID:21853144; http://dx.doi.org/10.1371/journal.pone.0023512