Structural mechanisms of mutant huntingtin aggregation suppression by the synthetic chaperonin-like CCT5 complex explained by cryoelectron tomography

Journal of Biological Chemistry

Volumn 290, Issue 28, 2015, Pages 17451-17461

  Darrow, Michele C ^a   Sergeeva, Oksana A ^b   Isas, Jose M ^c   Galaz Montoya, Jesús G ^a   King, Jonathan A ^b   Langen, Ralf ^c   Schmid, Michael F ^a   Chiu, Wah ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; OLIGOMERS; PROTEINS; TOMOGRAPHY;

AGGREGATION SUPPRESSION; CLASSIFICATION METHODS; CRYO-ELECTRON TOMOGRAPHY; NEURODEGENERATIVE DISORDERS; PROTEIN AGGREGATION; STRUCTURAL DESCRIPTIONS; STRUCTURAL MECHANISMS; SUBSTRATE-REFOLDING ACTIVITY;

NEURODEGENERATIVE DISEASES;

CHAPERONIN; CHAPERONIN CONTAINING TCP1; GLUTAMINE DERIVATIVE; HUNTINGTIN; OLIGOMER; PROTEIN CCT5; UNCLASSIFIED DRUG; CCT5 PROTEIN, HUMAN; HTT PROTEIN, HUMAN; MUTANT PROTEIN; NERVE PROTEIN; PROTEIN AGGREGATE; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; EXON; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; HUMAN; HUNTINGTON CHOREA; METABOLISM; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE; PROTEINOSIS; ULTRASTRUCTURE;

CHAPERONIN CONTAINING TCP-1; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; HUNTINGTON DISEASE; MODELS, MOLECULAR; MUTANT PROTEINS; NERVE TISSUE PROTEINS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS;

EID: 84940100058     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.655373     Document Type: Article

References (47)

1. Bates, G. P. (2005) History of genetic disease: the molecular genetics of Huntington disease: a history. Nat. Rev. Genet. 6, 766-773
2. Walker, F. O. (2007) Huntington's disease. Lancet 369, 218-228
3. Wetzel, R. (2012) Physical chemistry of polyglutamine: intriguing tales of a monotonous sequence. J. Mol. Biol. 421, 466-490
4. Davies, S. W., Turmaine, M., Cozens, B. A., DiFiglia, M., Sharp, A. H., Ross, C. A., Scherzinger, E., Wanker, E. E., Mangiarini, L., and Bates, G. P. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548
5. DiFiglia, M., Sapp, E., Chase, K. O., Davies, S. W., Bates, G. P., Vonsattel, J. P., and Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993
6. Hatters, D. M. (2012) Putting huntingtin "aggregation" in view with windows into the cellular milieu. Curr. Top. Med. Chem. 12, 2611-2622
7. Gipson, T. A., Neueder, A., Wexler, N. S., Bates, G. P., and Housman, D. (2013) Aberrantly spliced HTT, a new player in Huntington's disease pathogenesis. RNA Biol. 10, 1647-1652
8. Sathasivam, K., Neueder, A., Gipson, T. A., Landles, C., Benjamin, A. C., Bondulich, M. K., Smith, D. L., Faull, R. L., Roos, R. A., Howland, D., Detloff, P. J., Housman, D. E., and Bates, G. P. (2013) Aberrant splicing of HTT generates the pathogenic exon 1 protein in Huntington disease. Proc. Natl. Acad. Sci. U.S.A. 110, 2366-2370
9. Clabough, E. B. (2013) Huntington's disease: the past, present, and future search for disease modifiers. Yale J. Biol. Med. 86, 217-233
10. Margulis, B. A., Vigont, V., Lazarev, V. F., Kaznacheyeva, E. V., and Guzhova, I. V. (2013) Pharmacological protein targets in polyglutamine diseases: Mutant polypeptides and their interactors. FEBS Lett. 587, 1997-2007
11. Van der Putten, H., and Lotz, G. P. (2013) Opportunities and challenges for molecular chaperone modulation to treat protein-conformational brain diseases. Neurother. 10, 416-428
12. Behrends, C., Langer, C. A., Boteva, R., Böttcher, U. M., Stemp, M. J., Schaffar, G., Rao, B. V., Giese, A., Kretzschmar, H., Siegers, K., and Hartl, F. U. (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol. Cell 23, 887-897
13. Frydman, J. (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 70, 603-647
14. Horwich, A. L., Fenton, W. A., Chapman, E., and Farr, G. W. (2007) Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 23, 115-145
15. Kitamura, A., Kubota, H., Pack, C.-G., Matsumoto, G., Hirayama, S., Takahashi, Y., Kimura, H., Kinjo, M., Morimoto, R. I., and Nagata, K. (2006) Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state. Nat. Cell Biol. 8, 1163-1170
16. Shahmoradian, S. H., Galaz-Montoya, J. G., Schmid, M. F., Cong, Y., Ma, B., Spiess, C., Frydman, J., Ludtke, S. J., and Chiu, W. (2013) TRiC's tricks inhibit huntingtin aggregation. eLife 2, e00710
17. Tam, S., Geller, R., Spiess, C., and Frydman, J. (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat. Cell Biol. 8, 1155-1162
18. Frydman, J., Nimmesgern, E., Erdjument-Bromage, H., Wall, J. S., Tempst, P., and Hartl, F. U. (1992) Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J. 11, 4767-4778
19. Thulasiraman, V., Yang, C. F., and Frydman, J. (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 18, 85-95
20. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L., and Sigler, P. B. (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371, 578-586
21. Yang, W., Dunlap, J. R., Andrews, R. B., and Wetzel, R. (2002) Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet. 11, 2905-2917
22. Sontag, E. M., Joachimiak, L. A., Tan, Z., Tomlinson, A., Housman, D. E., Glabe, C. G., Potkin, S. G., Frydman, J., and Thompson, L. M. (2013) Exogenous delivery of chaperonin subunit fragment ApiCCT1 modulates mutant Huntingtin cellular phenotypes. Proc. Natl. Acad. Sci. U.S.A. 110, 3077-3082
23. Sergeeva, O. A., Chen, B., Haase-Pettingell, C., Ludtke, S. J., Chiu, W., and King, J. A. (2013) Human CCT4 and CCT5 chaperonin subunits expressed in Escherichia coli form biologically active homo-oligomers. J. Biol. Chem. 288, 17734-17744
24. Sergeeva, O. A., Tran, M. T., Haase-Pettingell, C., and King, J. A. (2014) Biochemical characterization of mutants in chaperonin proteins CCT4 and CCT5 Associated with hereditary sensory neuropathy. J. Biol. Chem. 289, 27470-27480
25. Bennett, M. J., Huey-Tubman, K. E., Herr, A. B., West, A. P., Jr., Ross, S. A., and Bjorkman, P. J. (2002) A linear lattice model for polyglutamine in CAG-expansion diseases. Proc. Natl. Acad. Sci. U.S.A. 99, 11634-11639
26. Fodale, V., Kegulian, N. C., Verani, M., Cariulo, C., Azzollini, L., Petricca, L., Daldin, M., Boggio, R., Padova, A., Kuhn, R., Pacifici, R., Macdonald, D., Schoenfeld, R. C., Park, H., Isas, J. M., Langen, R., Weiss, A., and Caricasole, A. (2014) Polyglutamine- and temperature-dependent conformational rigidity in mutant huntingtin revealed by immunoassays and circular dichroism spectroscopy. PloS ONE 9, e112262
27. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
28. Lepault, J., Booy, F. P., and Dubochet, J. (1983) Electron microscopy of frozen biological suspensions. J. Microsc. 129, 89-102
29. Mastronarde, D. N. (2005) Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51
30. Kremer, J. R., Mastronarde, D. N., and McIntosh, J. R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76
31. Pruggnaller, S., Mayr, M., and Frangakis, A. S. (2008) A visualization and segmentation toolbox for electron microscopy. J. Struct. Biol. 164, 161-165
32. Tang, G., Peng, L., Baldwin, P. R., Mann, D. S., Jiang, W., Rees, I., and Ludtke, S. J. (2007) EMAN2: An extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46
33. Galaz-Montoya, J. G., Flanagan, J., Schmid, M. F., and Ludtke, S. J. (2015) Single particle tomography in EMAN2. J. Struct. Biol. 190, 279-290
34. Schmid, M. F., and Booth, C. R. (2008) Methods for aligning and for averaging 3D volumes with missing data. J. Struct. Biol. 161, 243-248
35. Goddard, T. D., Huang, C. C., and Ferrin, T. E. (2007) Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157, 281-287
36. Bhardwaj, V., Panicker, M. M., and Udgaonkar, J. B. (2014) Fluorescence anisotropy uncovers changes in protein packing with inclusion growth in a cellular model of polyglutamine aggregation. Biochemistry 53, 3621-3636
37. Caron, N. S., Hung, C. L., Atwal, R. S., and Truant, R. (2014) Live cell imaging and biophotonic methods reveal two types of mutant huntingtin inclusions. Hum. Mol. Genet. 23, 2324-2338
38. Legleiter, J., Mitchell, E., Lotz, G. P., Sapp, E., Ng, C., DiFiglia, M., Thompson, L. M., and Muchowski, P. J. (2010) Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo. J. Biol. Chem. 285, 14777-14790
39. Gronenborn, A. M., Clore, G. M., Louis, J. M., and Wingfield, P. T. (1999) Is human thioredoxin monomeric or dimeric? Protein Sci. 8, 426-429
40. Harpaz, Y., Gerstein, M., and Chothia, C. (1994) Volume changes on protein folding. Struct. 2, 641-649
41. Myers, R. H. (2004) Huntington's disease genetics. NeuroRX 1, 255-262
42. Barbaro, B. A., Lukacsovich, T., Agrawal, N., Burke, J., Bornemann, D. J., Purcell, J. M., Worthge, S. A., Caricasole, A., Weiss, A., Song, W., Morozova, O. A., Colby, D. W., and Marsh, J. L. (2015) Comparative study of naturally occurring huntingtin fragments in Drosophila points to exon 1 as the most pathogenic species in Huntington's disease. Hum. Mol. Genet. 24, 913-925
43. Hendrick, J. P., and Hartl, F. U. (1995) The role of molecular chaperones in protein folding. FASEB J. 9, 1559-1569
44. Young, J. C., Agashe, V. R., Siegers, K., and Hartl, F. U. (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 5, 781-791
45. Rüßmann, F., Stemp, M. J., Mönkemeyer, L., Etchells, S. A., Bracher, A., and Hartl, F. U. (2012) Folding of large multidomain proteins by partial encapsulation in the chaperonin TRiC/CCT. Proc. Natl. Acad. Sci. 109, 21208-21215
46. Arrasate, M., and Finkbeiner, S. (2012) Protein aggregates in Huntington's disease. Exp. Neurol. 238, 1-11
47. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R., and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810