Overexpression of the Transcriptional Repressor Complex BCL-6/BCoR Leads to Nuclear Aggregates Distinct from Classical Aggresomes

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Buchberger, Elisabeth ^a   El Harchi, Miriam ^a   Payrhuber, Dietmar ^a   Zommer, Anna ^a   Schauer, Dominic ^a   Simonitsch Klupp, Ingrid ^a   Bilban, Martin ^a   Brostjan, Christine ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BCL 6 INTERACTING COREPRESSOR PROTEIN; COREPRESSOR PROTEIN; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE; PROTEIN BCL 6; UNCLASSIFIED DRUG;

AGGRESOME; AMINO ACID SEQUENCE; ARTICLE; CELL CYCLE PROGRESSION; CELL NUCLEUS; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; MALE; MOLECULAR SIZE; PROTEIN AGGREGATION; PROTEIN EXPRESSION; WILD TYPE;

CELL DEATH; CELL NUCLEUS; CYTOSOL; ENDOTHELIAL CELLS; GREEN FLUORESCENT PROTEINS; HISTONE DEACETYLASES; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INCLUSION BODIES; MITOSIS; NUCLEAR ENVELOPE; NUCLEAR PORE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-6; REPRESSOR PROTEINS; RNA, MESSENGER; SPHEROIDS, CELLULAR; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UBIQUITIN;

EID: 84885402228     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076845     Document Type: Article

References (60)

1. Morimoto RI, (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22: 1427-1438. doi:10.1101/gad.1657108. PubMed: 18519635.
2. Roth DM, Balch WE, (2011) Modeling general proteostasis: proteome balance in health and disease. Curr Opin Cell Biol 23: 126-134. doi:10.1016/j.ceb.2010.11.001. PubMed: 21131189.
3. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl, Ulrich FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82: 323-355. doi:10.1146/annurev-biochem-060208-092442. PubMed: 23746257.
4. Kirstein-Miles J, Scior A, Deuerling E, Morimoto RI, (2013) The nascent polypeptide-associated complex is a key regulator of proteostasis. EMBO J 32: 1451-1468. doi:10.1038/emboj.2013.87. PubMed: 23604074.
5. Preissler S, Deuerling E, (2012) Ribosome-associated chaperones as key players in proteostasis. Trends Biochem Sci 37: 274-283. doi:10.1016/j.tibs.2012.03.002. PubMed: 22503700.
6. Daugaard M, Rohde M, Jäättelä M, (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581: 3702-3710. doi:10.1016/j.febslet.2007.05.039. PubMed: 17544402.
7. Bukau B, Horwich AL, (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366. doi:10.1016/S0092-8674(00)80928-9. PubMed: 9476895.
8. Horwich AL, Fenton WA, Chapman E, Farr GW, (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23: 115-145. doi:10.1146/annurev.cellbio.23.090506.123555. PubMed: 17489689.
9. Taipale M, Jarosz DF, Lindquist S, (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528. doi:10.1038/nrm2918. PubMed: 20531426.
10. Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, et al. (2012) DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1: 251-264. doi:10.1016/j.celrep.2011.12.007. PubMed: 22832197.
11. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366. doi:10.1146/annurev.biochem.75.101304.123901. PubMed: 16756495.
12. Kettern N, Dreiseidler M, Tawo R, Höhfeld J, (2010) Chaperone-assisted degradation: multiple paths to destruction. Biol Chem 391: 481-489. PubMed: 20302520.
13. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, et al. (2005) Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 20: 525-538. doi:10.1016/j.molcel.2005.09.023. PubMed: 16307917.
14. Kon M, Cuervo AM, (2010) Chaperone-mediated autophagy in health and disease. FEBS Lett 584: 1399-1404. doi:10.1016/j.febslet.2009.12.025. PubMed: 20026330.
15. Hutt DM, Balch WE, (2013) Expanding proteostasis by membrane trafficking networks. Cold Spring Harb Perspect Biol 5. PubMed: 2342652423986914.
16. Stewart M, (2007) Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8: 195-208. doi:10.1038/nrm2114. PubMed: 17287812.
17. Zhang X, Clark AF, Yorio T, (2006) Heat shock protein 90 is an essential molecular chaperone for nuclear transport of glucocorticoid receptor beta. Invest Ophthalmol Vis Sci 47: 700-708. doi:10.1167/iovs.05-0697. PubMed: 16431970.
18. Bader N, Jung T, Grune T, (2007) The proteasome and its role in nuclear protein maintenance. Exp Gerontol 42: 864-870. doi:10.1016/j.exger.2007.03.010. PubMed: 17532163.
19. Garcia-Mata R, Gao YS, Sztul E, (2002) Hassles with taking out the garbage: aggravating aggresomes. Traffic 3: 388-396. doi:10.1034/j.1600-0854.2002.30602.x. PubMed: 12010457.
20. García-Mata R, Bebök Z, Sorscher EJ, Sztul ES, (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 146: 1239-1254. doi:10.1083/jcb.146.6.1239. PubMed: 10491388.
21. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, et al. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115: 727-738. doi:10.1016/S0092-8674(03)00939-5. PubMed: 14675537.
22. Fusco C, Micale L, Egorov M, Monti M, D'Addetta EV, et al. (2012) The E3-ubiquitin ligase TRIM50 interacts with HDAC6 and p62, and promotes the sequestration and clearance of ubiquitinated proteins into the aggresome. PLOS ONE 7: e40440. doi:10.1371/journal.pone.0040440. PubMed: 22792322.
23. Kopito RR, (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10: 524-530. doi:10.1016/S0962-8924(00)01852-3. PubMed: 11121744.
24. Harper JD, Lansbury PT Jr., (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66: 385-407. doi:10.1146/annurev.biochem.66.1.385. PubMed: 9242912.
25. Zaarur N, Meriin AB, Gabai VL, Sherman MY, (2008) Triggering aggresome formation. Dissecting aggresome-targeting and aggregation signals in synphilin 1. J Biol Chem 283: 27575-27584. doi:10.1074/jbc.M802216200. PubMed: 18635553.
26. Zoghbi HY, Orr HT, (2000) Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23: 217-247. doi:10.1146/annurev.neuro.23.1.217. PubMed: 10845064.
27. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, et al. (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat Genet 19: 148-154. doi:10.1038/502. PubMed: 9620770.
28. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993. doi:10.1126/science.277.5334.1990. PubMed: 9302293.
29. Chai Y, Koppenhafer SL, Bonini NM, Paulson HL, (1999) Analysis of the role of heat shock protein (Hsp) molecular chaperones in polyglutamine disease. J Neurosci 19: 10338-10347. PubMed: 10575031.
30. Chai Y, Koppenhafer SL, Shoesmith SJ, Perez MK, Paulson HL, (1999) Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum Mol Genet 8: 673-682. doi:10.1093/hmg/8.4.673. PubMed: 10072437.
31. Fu L, Gao YS, Tousson A, Shah A, Chen TL, et al. (2005) Nuclear aggresomes form by fusion of PML-associated aggregates. Mol Biol Cell 16: 4905-4917. doi:10.1091/mbc.E05-01-0019. PubMed: 16055507.
32. Park R, Wang'ondu R, Heston L, Shedd D, Miller G, (2011) Efficient induction of nuclear aggresomes by specific single missense mutations in the DNA-binding domain of a viral AP-1 homolog. J Biol Chem 286: 9748-9762. doi:10.1074/jbc.M110.198325. PubMed: 21233201.
33. Prichard MN, Sztul E, Daily SL, Perry AL, Frederick SL, et al. (2008) Human cytomegalovirus UL97 kinase activity is required for the hyperphosphorylation of retinoblastoma protein and inhibits the formation of nuclear aggresomes. J Virol 82: 5054-5067. doi:10.1128/JVI.02174-07. PubMed: 18321963.
34. Jardin F, Ruminy P, Bastard C, Tilly H, (2007) The BCL6 proto-oncogene: a leading role during germinal center development and lymphomagenesis. Pathol Biol (Paris)55: 73-83.
35. Fan Y, Wang Y, Tang Z, Zhang H, Qin X, et al. (2008) Suppression of pro-inflammatory adhesion molecules by PPAR-delta in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 28: 315-321. PubMed: 18048767.
36. Albagli O, Dhordain P, Bernardin F, Quief S, Kerkaert JP, et al. (1996) Multiple domains participate in distance-independent LAZ3/BCL6-mediated transcriptional repression. Biochem Biophys Res Commun 220: 911-915. doi:10.1006/bbrc.1996.0505. PubMed: 8607866.
37. Lemercier C, Brocard MP, Puvion-Dutilleul F, Kao HY, Albagli O, et al. (2002) Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor. J Biol Chem 277: 22045-22052. doi:10.1074/jbc.M201736200. PubMed: 11929873.
38. Huynh KD, Fischle W, Verdin E, Bardwell VJ, (2000) BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev 14: 1810-1823. PubMed: 10898795.
39. Gearhart MD, Corcoran CM, Wamstad JA, Bardwell VJ, (2006) Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol Cell Biol 26: 6880-6889. doi:10.1128/MCB.00630-06. PubMed: 16943429.
40. Lee JA, Suh DC, Kang JE, Kim MH, Park H, et al. (2005) Transcriptional activity of Sp1 is regulated by molecular interactions between the zinc finger DNA binding domain and the inhibitory domain with corepressors, and this interaction is modulated by MEK. J Biol Chem 280: 28061-28071. doi:10.1074/jbc.M414134200. PubMed: 15878880.
41. Srinivasan RS, de Erkenez AC, Hemenway CS, (2003) The mixed lineage leukemia fusion partner AF9 binds specific isoforms of the BCL-6 corepressor. Oncogene 22: 3395-3406. doi:10.1038/sj.onc.1206361. PubMed: 12776190.
42. Emiliani S, Fischle W, Van Lint C, Al-Abed Y, Verdin E, (1998) Characterization of a human RPD3 ortholog, HDAC3. Proc Natl Acad Sci U S A 95: 2795-2800. doi:10.1073/pnas.95.6.2795. PubMed: 9501169.
43. Fischle W, Emiliani S, Hendzel MJ, Nagase T, Nomura N, et al. (1999) A new family of human histone deacetylases related to Saccharomyces cerevisiae HDA1p. J Biol Chem 274: 11713-11720. doi:10.1074/jbc.274.17.11713. PubMed: 10206986.
44. Barros P, Jordan P, Matos P, (2009) Rac1 signaling modulates BCL-6-mediated repression of gene transcription. Mol Cell Biol 29: 4156-4166. doi:10.1128/MCB.01813-08. PubMed: 19487462.
45. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
46. Hetzer MW, (2010) The nuclear envelope. Cold Spring Harb Perspect Biol 2: a000539. doi:10.1101/cshperspect.a000539. PubMed: 20300205.
47. Heessen S, Fornerod M, (2007) The inner nuclear envelope as a transcription factor resting place. EMBO Rep 8: 914-919. doi:10.1038/sj.embor.7401075. PubMed: 17906672.
48. Fu L, Gao YS, Sztul E, (2005) Transcriptional repression and cell death induced by nuclear aggregates of non-polyglutamine protein. Neurobiol Dis 20: 656-665. doi:10.1016/j.nbd.2005.05.015. PubMed: 15964198.
49. Nucifora FC Jr., Sasaki M, Peters MF, Huang H, Cooper JK, et al. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291: 2423-2428. doi:10.1126/science.1056784. PubMed: 11264541.
50. Marquard L, Poulsen CB, Gjerdrum LM, de Nully Brown P, Christensen IJ, et al. (2009) Histone deacetylase 1, 2, 6 and acetylated histone H4 in B- and T-cell lymphomas. Histopathology 54: 688-698. doi:10.1111/j.1365-2559.2009.03290.x. PubMed: 19438744.
51. Pasqualucci L, Bereshchenko O, Niu H, Klein U, Basso K, et al. (2003) Molecular pathogenesis of non-Hodgkin's lymphoma: the role of Bcl-6. Leuk Lymphoma 44 (Suppl 3):: S5-12. doi:10.1080/10428190310001621588. PubMed: 15202519.
52. Chen TL, Wang PY, Luo W, Gwon SS, Flay NW, et al. (2001) Aggrecan domains expected to traffic through the exocytic pathway are misdirected to the nucleus. Exp Cell Res 263: 224-235. doi:10.1006/excr.2000.5093. PubMed: 11161721.
53. Moran DM, Shen H, Maki CG, (2009) Puromycin-based vectors promote a ROS-dependent recruitment of PML to nuclear inclusions enriched with HSP70 and Proteasomes. BMC Cell Biol 10: 32. doi:10.1186/1471-2121-10-32. PubMed: 19409099.
54. Miranker AD, (2005) Structural biology: fibres hinge on swapped domains. Nature 437: 197-198. doi:10.1038/437197a. PubMed: 16148916.
55. Rousseau F, Schymkowitz JW, Itzhaki LS, (2003) The unfolding story of three-dimensional domain swapping. Structure 11: 243-251. doi:10.1016/S0969-2126(03)00029-7. PubMed: 12623012.
56. Stead MA, Rosbrook GO, Hadden JM, Trinh CH, Carr SB, et al. (2008) Structure of the wild-type human BCL6 POZ domain. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 1101-1104. doi:10.1107/S1744309108036063. PubMed: 19052359.
57. Albagli O, Lindon C, Lantoine D, Quief S, Puvion E, et al. (2000) DNA replication progresses on the periphery of nuclear aggregates formed by the BCL6 transcription factor. Mol Cell Biol 20: 8560-8570. doi:10.1128/MCB.20.22.8560-8570.2000. PubMed: 11046151.
58. Puvion-Dutilleul F, Souquere-Besse S, Albagli-Curiel O, (2003) The relationship between BCL6 bodies and nuclear sites of normal and halogenated DNA and RNA synthesis. Microsc Res Tech 61: 389-407. doi:10.1002/jemt.10363. PubMed: 12811744.
59. Dellaire G, Eskiw CH, Dehghani H, Ching RW, Bazett-Jones DP, (2006) Mitotic accumulations of PML protein contribute to the re-establishment of PML nuclear bodies in G1. J Cell Sci 119: 1034-1042. doi:10.1242/jcs.02817. PubMed: 16492707.
60. Jana NR, Tanaka M, Wang Gh, Nukina N, (2000) Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity. Hum Mol Genet 9: 2009-2018. doi:10.1093/hmg/9.13.2009. PubMed: 10942430.