Vaccinia-related kinase 2 mediates accumulation of polyglutamine aggregates via negative regulation of the chaperonin TRiC

Molecular and Cellular Biology

Volumn 34, Issue 4, 2014, Pages 643-652

  Kim, Sangjune ^a   Park, Do Young ^a   Lee, Dohyun ^a   Kim, Wanil ^a   Jeong, Young Hun ^a   Lee, Juhyun ^a   Chung, Sung Kee ^a   Ha, Hyunjung ^b   Choi, Bo Hwa ^c   Kim, Kyong Tai ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b Chungbuk National University   (South Korea)

^c Pohang Center of Evolution of Biomaterials   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; HUNTINGTIN; POLYGLUTAMINE; PROTEIN RING BOX 1; PROTEIN SERINE THREONINE KINASE; PROTEIN TRIC; UBIQUITIN PROTEIN LIGASE COP1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 2;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA INTERFERENCE; UBIQUITINATION; WILD TYPE;

ANIMALS; CELLS, CULTURED; CHAPERONIN CONTAINING TCP-1; GENE EXPRESSION REGULATION; HUMANS; HUNTINGTON DISEASE; MICE; MUTATION; NERVE TISSUE PROTEINS; PEPTIDES; PROTEIN FOLDING; PROTEIN-SERINE-THREONINE KINASES;

EID: 84893019973     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00756-13     Document Type: Article

References (48)

1. Ross CA. 2002. Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 35: 819-822. http://dx.doi.org/10.1016/S0896-6273(02)00872-3.
2. Young AB. 2003. Huntingtin in health and disease. J. Clin. Invest. 111: 299-302. http://dx.doi.org/10.1172/JCI200317742.
3. MacDonald ME, Gines S, Gusella JF, Wheeler VC. 2003. Huntington's disease. Neuromol. Med. 4:7-20. http://dx.doi.org/10.1385/NMM:4:1-2:7.
4. Nagai Y, Inui T, Popiel HA, Fujikake N, Hasegawa K, Urade Y, Goto Y, Naiki H, Toda T. 2007. A toxic monomeric conformer of the polyglutamine protein. Nat. Struct. Mol. Biol. 14:332-340. http://dx.doi.org/10 .1038/nsmb1215.
5. Kim YJ, Yi Y, Sapp E, Wang Y, Cuiffo B, Kegel KB, Qin ZH, Aronin N, DiFiglia M. 2001. Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. U. S. A. 98:12784-12789. http://dx.doi.org /10.1073/pnas.221451398.
6. McClellan AJ, Tam S, Kaganovich D, Frydman J. 2005. Protein quality control: chaperones culling corrupt conformations. Nat. Cell Biol. 7:736- 741. http://dx.doi.org/10.1038/ncb0805-736.
7. Zoghbi HY, Orr HT. 2000. Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23:217-247. http://dx.doi.org/10.1146/annurev.neuro.23.1.217.
8. Muchowski PJ, Wacker JL. 2005. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6:11-22. http://dx.doi.org/10 .1038/nrn1587.
9. Wacker JL, Zareie MH, Fong H, Sarikaya M, Muchowski PJ. 2004. Hsp70 and Hsp40 attenuate formation of spherical and annular polyglutamine oligomers by partitioning monomer. Nat. Struct. Mol. Biol. 11: 1215-1222. http://dx.doi.org/10.1038/nsmb860.
10. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. 1999. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23:425-428. http://dx.doi.org/10.1038/70532.
11. Schaffar G, Breuer P, Boteva R, Behrends C, Tzvetkov N, Strippel N, Sakahira H, Siegers K, Hayer-Hartl M, Hartl FU. 2004. Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 15:95-105. http://dx.doi.org/10.1016/j.molcel .2004.06.029.
12. Muchowski PJ, Schaffar G, Sittler A, Wanker EE, Hayer-Hartl MK, Hartl FU. 2000. Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. U. S. A. 97:7841-7846. http://dx.doi.org/10.1073/pnas.140202897.
13. Nollen EA, Garcia SM, van Haaften G, Kim S, Chavez A, Morimoto RI, Plasterk RH. 2004. Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc. Natl. Acad. Sci. U. S. A. 101:6403-6408. http://dx.doi.org/10.1073/pnas.0307697101.
14. Horwich AL, Fenton WA, Chapman E, Farr GW. 2007. Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 23: 115-145. http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123555.
15. Meyer AS, Gillespie JR, Walther D, Millet IS, Doniach S, Frydman J. 2003. Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113:369-381. http://dx.doi.org /10.1016/S0092-8674(03)00307-6.
16. Spiess C, Meyer AS, Reissmann S, Frydman J. 2004. Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol. 14:598-604. http://dx.doi.org/10.1016/j.tcb.2004.09.015.
17. Tam S, Geller R, Spiess C, Frydman J. 2006. The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat. Cell Biol. 8:1155-1162. http://dx.doi.org/10.1038/ncb1477.
18. Behrends C, Langer CA, Boteva R, Bottcher UM, Stemp MJ, Schaffar G, Rao BV, Giese A, Kretzschmar H, Siegers K, Hartl FU. 2006. Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol. Cell 23:887-897. http://dx.doi.org/10.1016/j.molcel .2006.08.017.
19. Kitamura A, Kubota H, Pack CG, Matsumoto G, Hirayama S, Takahashi Y, Kimura H, Kinjo M, Morimoto RI, Nagata K. 2006. Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state. Nat. Cell Biol. 8:1163-1170. http://dx.doi.org/10.1038/ncb1478.
20. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. 2002. The protein kinase complement of the human genome. Science 298:1912- 1934. http://dx.doi.org/10.1126/science.1075762.
21. Blanco S, Klimcakova L, Vega FM, Lazo PA. 2006. The subcellular localization of vaccinia-related kinase-2 (VRK2) isoforms determines their different effect on p53 stability in tumour cell lines. FEBS J. 273: 2487-2504. http://dx.doi.org/10.1111/j.1742-4658.2006.05256.x.
22. Blanco S, Santos C, Lazo PA. 2007. Vaccinia-related kinase 2 modulates the stress response to hypoxia mediated by TAK1. Mol. Cell. Biol. 27: 7273-7283. http://dx.doi.org/10.1128/MCB.00025-07.
23. Fernandez IF, Blanco S, Lozano J, Lazo PA. 2010. VRK2 inhibits mitogen- activated protein kinase signaling and inversely correlates with ErbB2 in human breast cancer. Mol. Cell. Biol. 30:4687-4697. http://dx.doi.org /10.1128/MCB.01581-09.
24. Li LY, Liu MY, Shih HM, Tsai CH, Chen JY. 2006. Human cellular protein VRK2 interacts specifically with Epstein-Barr virus BHRF1, a homologue of Bcl-2, and enhances cell survival. J. Gen. Virol. 87:2869-2878. http://dx.doi.org/10.1099/vir.0.81953-0.
25. Monsalve DM, Merced T, Fernandez IF, Blanco S, Vazquez-Cedeira M, Lazo PA. 2013. Human VRK2 modulates apoptosis by interaction with Bcl-xL and regulation of BAX gene expression. Cell Death Dis. 4:e513. http://dx.doi.org/10.1038/cddis.2013.40.
26. Sanz-Garcia M, Lopez-Sanchez I, Lazo PA. 2008. Proteomics identification of nuclear Ran GTPase as an inhibitor of human VRK1 and VRK2 (vaccinia-related kinase) activities. Mol. Cell. Proteomics 7:2199-2214. http://dx.doi.org/10.1074/mcp.M700586-MCP200.
27. Nichols RJ, Wiebe MS, Traktman P. 2006. The vaccinia-related kinases phosphorylate the N= terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol. Biol. Cell 17:2451-2464. http: //dx.doi.org/10.1091/mbc.E05-12-1179.
28. Vazquez-Cedeira M, Lazo PA. 2012. Human VRK2 (vaccinia-related kinase 2) modulates tumor cell invasion by hyperactivation of NFAT1 and expression of cyclooxygenase-2. J. Biol. Chem. 287:42739-42750. http: //dx.doi.org/10.1074/jbc.M112.404285.
29. Yokota S, Kayano T, Ohta T, Kurimoto M, Yanagi H, Yura T, Kubota H. 2000. Proteasome-dependent degradation of cytosolic chaperonin CCT. Biochem. Biophys. Res. Commun. 279:712-717. http://dx.doi.org /10.1006/bbrc.2000.4011.
30. Kang TH, Kim KT. 2006. Negative regulation of ERK activity by VRK3- mediated activation of VHR phosphatase. Nat. Cell Biol. 8:863-869. http: //dx.doi.org/10.1038/ncb1447.
31. Jung H, Kim T, Chae HZ, Kim KT, Ha H. 2001. Regulation of macrophage migration inhibitory factor and thiol-specific antioxidant protein PAG by direct interaction. J. Biol. Chem. 276:15504-15510. http://dx.doi .org/10.1074/jbc.M009620200.
32. Ditzel L, Lowe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S. 1998. Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93:125-138. http://dx.doi.org/10.1016/S0092 -8674(00)81152-6.
33. Kim S, Willison KR, Horwich AL. 1994. Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains. Trends Biochem. Sci. 19:543-548. http://dx.doi.org/10.1016/0968 -0004(94)90058-2.
34. Petroski MD, Deshaies RJ. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6:9-20. http://dx.doi.org/10 .1038/nrm1547.
35. Yi C, Li S, Wang J, Wei N, Deng XW. 2006. Affinity purification reveals the association of WD40 protein constitutive photomorphogenic 1 with the hetero-oligomeric TCP-1 chaperonin complex in mammalian cells. Int. J. Biochem. Cell Biol. 38:1076-1083. http://dx.doi.org/10.1016/j .biocel.2005.12.019.
36. Yi C, Deng XW. 2005. COP1-from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol. 15:618-625. http://dx.doi.org/10 .1016/j.tcb.2005.09.007.
37. Chan HY, Warrick JM, Gray-Board GL, Paulson HL, Bonini NM. 2000. Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum. Mol. Genet. 9:2811-2820. http://dx.doi.org/10.1093/hmg/9.19.2811.
38. Hay DG, Sathasivam K, Tobaben S, Stahl B, Marber M, Mestril R, Mahal A, Smith DL, Woodman B, Bates GP. 2004. Progressive decrease in chaperone protein levels in a mouse model of Huntington's disease and induction of stress proteins as a therapeutic approach. Hum. Mol. Genet. 13:1389-1405. http://dx.doi.org/10.1093/hmg/ddh144.
39. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. 2002. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865-868. http://dx.doi.org/10.1126 /science.1067389.
40. Bauer PO, Goswami A, Wong HK, Okuno M, Kurosawa M, Yamada M, Miyazaki H, Matsumoto G, Kino Y, Nagai Y, Nukina N. 2010. Harnessing chaperone-mediated autophagy for the selective degradation of mutant huntingtin protein. Nat. Biotechnol. 28:256-263. http://dx.doi .org/10.1038/nbt.1608.
41. Tanaka M, Machida Y, Niu S, Ikeda T, Jana NR, Doi H, Kurosawa M, Nekooki M, Nukina N. 2004. Trehalose alleviates polyglutaminemediated pathology in a mouse model of Huntington disease. Nat. Med. 10:148-154. http://dx.doi.org/10.1038/nm985.
42. Jeong H, Then F, Melia TJ, Jr, Mazzulli JR, Cui L, Savas JN, Voisine C, Paganetti P, Tanese N, Hart AC, Yamamoto A, Krainc D. 2009. Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell 137:60-72. http://dx.doi.org/10.1016/j.cell.2009.03.018.
43. Li M, Wang Y, Zheng XB, Ikeda M, Iwata N, Luo XJ, Chong SA, Lee J, Rietschel M, Zhang F, Muller-Myhsok B, Cichon S, Weinberger DR, Mattheisen M, Schulze TG, Martin NG, Mitchell PB, Schofield PR, Liu JJ, Su B, Moo DSC. 2012. Meta-analysis and brain imaging data support the involvement of VRK2 (rs2312147) in schizophrenia susceptibility. Schizophr. Res. 142:200-205. http://dx.doi.org/10.1016/j.schres.2012.10 .008.
44. Steinberg S, de Jong S, Irish Schizophrenia Genomics Consortium, Andreassen OA, Werge T, Borglum AD, Mors O, Mortensen PB, Gustafsson O, Costas J, Pietilainen OP, Demontis D, Papiol S, Huttenlocher J, Mattheisen M, Breuer R, Vassos E, Giegling I, Fraser G, Walker N, Tuulio-Henriksson A, Suvisaari J, Lonnqvist J, Paunio T, Agartz I, Melle I, Djurovic S, Strengman E, GROUP, Jurgens G, Glenthoj B, Terenius L, Hougaard DM, Orntoft T, Wiuf C, Didriksen M, Hollegaard MV, Nordentoft M, van Winkel R, Kenis G, Abramova L, Kaleda V, Arrojo M, Sanjuan J, Arango C, Sperling S, Rossner M, Ribolsi M, Magni V, Siracusano A, et al. 2011. Common variants at VRK2 and TCF4 conferring risk of schizophrenia. Hum. Mol. Genet. 20: 4076-4081. http://dx.doi.org/10.1093/hmg/ddr325.
45. Helbig I, Lowenstein DH. 2013. Genetics of the epilepsies: where are we and where are we going? Curr. Opin. Neurol. 26:179-185. http://dx.doi .org/10.1097/WCO.0b013e32835ee6ff.
46. EPICURE Consortium, EMINet Consortium, Steffens M, Leu C, Ruppert AK, Zara F, Striano P, Robbiano A, Capovilla G, Tinuper P, Gambardella A, Bianchi A, La Neve A, Crichiutti G, de Kovel CG, Kasteleijn-Nolst Trenite D, de Haan GJ, Lindhout D, Gaus V, Schmitz B, Janz D, Weber YG, Becker F, Lerche H, Steinhoff BJ, Kleefuss-Lie AA, Kunz WS, Surges R, Elger CE, Muhle H, von Spiczak S, Ostertag P, Helbig I, Stephani U, Moller RS, Hjalgrim H, Dibbens LM, Bellows S, Oliver K, Mullen S, Scheffer IE, Berkovic SF, Everett KV, Gardiner MR, Marini C, Guerrini R, Lehesjoki AE, Siren A, Guipponi M, Malafosse A, et al. 2012. Genome-wide association analysis of genetic generalized epilepsies implicates susceptibility loci at 1q43, 2p16.1, 2q22.3 and 17q21.32. Hum. Mol. Genet. 21:5359-5372. http://dx.doi.org/10.1093/hmg/dds373.
47. Nezu J, Oku A, Jones MH, Shimane M. 1997. Identification of two novel human putative serine/threonine kinases, VRK1 and VRK2, with structural similarity to vaccinia virus B1R kinase. Genomics 45:327-331. http: //dx.doi.org/10.1006/geno.1997.4938.
48. Tang B, Seredenina T, Coppola G, Kuhn A, Geschwind DH, Luthi-Carter R, Thomas EA. 2011. Gene expression profiling of R6/2 transgenic mice with different CAG repeat lengths reveals genes associated with disease onset and progression in Huntington's disease. Neurobiol. Dis. 42: 459-467. http://dx.doi.org/10.1016/j.nbd.2011.02.008.