Biochemical characterization of mutants in chaperonin proteins CCT4 and CCT5 associated with hereditary sensory neuropathy

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27470-27480

  Sergeeva, Oksana A ^a   Tran, Meme T ^a   Haase Pettingell, Cameron ^a   King, Jonathan A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; ESCHERICHIA COLI; PHYSIOLOGICAL MODELS; SUBSTRATES;

BIOCHEMICAL CHARACTERIZATION; BIOCHEMICAL PROPERTIES; DISEASE PHENOTYPES; EXPRESSION SYSTEM; MUTANT HUNTINGTIN; PHYSIOLOGICAL SUBSTRATE; SPRAGUE-DAWLEY RATS; SUCROSE GRADIENTS;

PROTEINS;

CHAPERONIN; CHAPERONIN CCT4; CHAPERONIN CCT5; HUNTINGTIN; UNCLASSIFIED DRUG; CCT4 PROTEIN, RAT; CCT5 PROTEIN, HUMAN; CHAPERONIN CONTAINING TCP1;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ESCHERICHIA COLI; EXPRESSION VECTOR; HUMAN; IN VITRO STUDY; MUTATIONAL ANALYSIS; NEUROPATHY; NONHUMAN; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; PROTEIN FOLDING; PROTEIN TRANSPORT; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CHAPERONIN CONTAINING TCP-1; HEREDITARY SENSORY AND AUTONOMIC NEUROPATHIES; HUMANS; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84907482425     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.576033     Document Type: Article

References (40)

1. Auer-Grumbach, M. (2008) Hereditary sensory neuropathy type I. Orphanet j.Rare Dis. 3, 7
2. Thomas, P. IC, Misra, V. P., King, R. H. M., Muddle, J. R., Wroe, S., Bhatia,K. P., Anderson, M., Cabello, A., Vilchez, J., and Wadia, N. H. (1994) Autosomal recessive hereditary sensory neuropathy with spastic paraplegia. Brain 117, 651- 659
3. Cavanagh, N. P. C, Eames, R. A., Galvin, R. J., Brett, E. M., and Kelly, R. E. (1979) Hereditary sensory neuropathy with spastic paraplegia. Brain 102,79-94
4. Rotthier, A., Baets, J., De Vriendt, E., Jacobs, A., Auer-Grumbach, M., Lévy, N., Bonello-Palot, N., Kilic, S. S., Weis, J., Nascimento, A., Swinkels, M., Kruyt, M. C., Jordanova, A., De Jonghe, P., and Timmerman, V. (2009) Genes for hereditary sensory and autonomic neuropathies: a genotypephenotype correlation. Brain 132, 2699 -2711
5. Bouhouche, A., Benomar, A., Bouslam, N., Chkili, T., and Yahyaoui, M. (2006) Mutation in the epsilon subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia. J. Med. Genet. 43, 441-443
6. Hansen, J. J., Dürr, A., Cournu-Rebeix, L, Georgopoulos, C., Ang, D., Nielsen, M. N., Davoine, C.-S., Brice, A., Fontaine, B., Gregersen, N., and Bross, P. (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am.J. Hum. Genet. 70,1328-1332
7. Lee, M.-J., Stephenson, D. A., Groves, M. J., Sweeney, M. G., Davis, M. B., An, S.-F., Houlden, H., Salih, M. A. M., Timmerman, V., de Jonghe, P., Auer-Grumbach, M., Di Maria, E., Scaravilli, F., Wood, N. W., and Reilly, M. M. (2003) Hereditary sensory neuropathy is caused by a mutation in the delta subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct4) gene. Hum. Mol. Genet. 12, 1917-1925
8. Timmerman, V., Clowes, V. E., and Reid, E. (2013) Overlapping molecular pathological themes link Charcot-Marie-Tooth neuropathies and hereditary spastic paraplegias. Exp. Neurol. 246,14-25
9. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332
10. Frydman, J. (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 70, 603-647
11. Lundin, V. F., Leroux, M. R., and Stirling, P. C. (2010) Quality control of cytoskeletal proteins and human disease. Trends Biochem. Sci. 35, 288-297
12. Bross, P., Naundrup, S., Hansen, J., Nielsen, M. N., Christensen, J. H., Kruhoffer, M., Palmfeldt, J., Corydon, T. J., Gregersen, N., Ang, D., Georgopoulos, C, and Nielsen, K. L. (2008) The Hsp60-(p.V98I) mutation associated with hereditary spastic paraplegia SPG13 compromises chaperonin function both in vitro and in vivo.J. Biol. Chem. 283,15694-15700
13. Knee, K. M., Sergeeva, O. A., and King, J. A. (2013) Human TRiC complex purified from HeLa cells contains all eight CCT subunits and is active in vitro. Cell Stress Chaperones 18,137-144
14. 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
15. Reissmann, S., Parnot, C, Booth, C. R., Chiu, W., and Frydman, J. (2007) Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins. Nat. Struct. Mol. Biol. 14, 432-440
16. Acosta-Sampson, L., and King, J. (2010) Partially folded aggregation intermediates of human γD-, γC-, and γS-crystallin are recognized and bound by human αB-crystallin chaperone.J. Mol. Biol. 401,134-152
17. Knee, K. M., Goulet, D. R., Zhang, J., Chen, B., Chiu, W., and King, J. A. (2011) The group II chaperonin Mm-Cpn binds and refolds human γD crystallin. Protein Sci. 20, 30-41
18. Sergeeva, O. A., Yang, J., King, J. A., and Knee, K. M. (2014) Group II archaeal chaperonin recognition of partially folded human γD-crystallin mutants. Protein Sci. 23, 693-702
19. Tam, S., Geller, R., Spiess, C., and Frydman, J. (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunitspecificinteractions. Nat. Cell Biol. 8,1155-1162
20. Machida, K., Masutani, M., Kobayashi, T., Mikami, S., Nishino, Y., Miyazawa, A., and Imataka, H. (2012) Reconstitution of the human chaperonin CCT by co-expression of the eight distinct subunits in mammalian cells. Protein Expr. Purif. 82, 61-69
21. Chen, J., Flaugh, S. L., Callis, P. R., and King, J. (2006) Mechanism of the highly efficient quenching of tryptophan fluorescence in human γD-crystallin. Biochemistry 45,11552-11563
22. Flaugh, S. L., Kosinski-Collins, M. S., and King, J. (2005) Contributions of hydrophobic domain interface interactions to the folding and stability of human γD-crystallin. Protein Sci. 14, 569-581
23. Flaugh, S. L., Kosinski-Collins, M. S., and King, J. (2005) Interdomain side-chain interactions in human γD crystallin influencing folding and stability. Protein Sci. 14, 2030-2043
24. Flaugh, S. L., Mills, I. A., and King, J. (2006) Glutamine deamidation destabilizes human γD-crystallin and lowers the kinetic barrier to unfolding.J. Biol. Chem. 281, 30782-30793
25. Kong, F., and King, J. (2011) Contributions of aromatic pairs to the folding and stability of long-lived human γD-crystallin. Protein Sci. 20, 513-528
26. Kosinski-Collins, M. S., Flaugh, S. L., and King, J. (2004) Probing folding and fluorescence quenching in human γD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Sci. 13, 2223-2235
27. Kosinski-Collins, M. S., and King, J. (2003) In vitro unfolding, refolding, and polymerization of human γD crystallin, a protein involved in cataract formation. Protein Sci. 12, 480-490
28. Moreau, K. L., and King, J. (2009) Hydrophobic core mutations associated with cataract development in mice destabilize human γD-crystallin.J. Biol. Chem. 284, 33285-33295
29. Wetzel, R. (2012) Physical chemistry of polyglutamine: intriguing tales of a monotonous sequence.J. Mol. Biol. 421, 466-490
30. Bates, G. P. (2005) History of genetic disease: the molecular genetics of Huntington disease-a history. Nat. Rev. Genet. 6, 766 -773
31. Walker, F. O. (2007) Huntington's disease. Lancet 369, 218-228
32. Arrasate, M., and Finkbeiner, S. (2012) Protein aggregates in Huntington's disease. Exp. Neurol. 238,1-11
33. Clabough, E. B. D. (2013) Huntington's disease: the past, present, and future search for disease modifiers. Yale J. Biol. Med. 86, 217-233
34. Tam, S., Spiess, C., Auyeung, W., Joachimiak, L., Chen, B., Poirier, M. A., and Frydman, J. (2009) The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation. Nat. Struct. Mol. Biol. 16,1279-1285
35. 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
36. 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
37. Pappenberger, G., McCormack, E. A., and Willison, K. R. (2006) Quantitative actin folding reactions using yeast CCT purified via an internal tag in the CCT3/y subunit.J. Mol. Biol. 360, 484-496
38. Llorca, O., McCormack, E. A., Hynes, G., Grantham, J., Cordell, J., Carrascosa, J. L., Willison, K. R., Fernandez, J. J., and Valpuesta, J. M. (1999) Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 402, 693- 696
39. Abe, Y., Yoon, S.-O., Kubota, K., Mendoza, M. C, Gygi, S. P., and Blenis, J. (2009) p90 ribosomal S6 kinase and p70 ribosomal S6 kinase link phosphorylation of the eukaryotic chaperonin containing TCP-1 to growth factor, insulin, and nutrient signaling.J. Biol. Chem. 284,14939-14948
40. Hagiwara, H., and Sunada, Y. (2004) Mechanism of taxane neurotoxicity. Breast Cancer 11, 82- 85