Role of the coiled-coil structural motif in polyglutamine aggregation

Biochemistry

Volumn 53, Issue 43, 2014, Pages 6738-6746

  Kokona, Bashkim ^a   Rosenthal, Zachary P ^a   Fairman, Robert ^a  

^a HAVERFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURODEGENERATIVE DISEASES; PROTEINS;

EFFECTIVE CONCENTRATION; FLANKING SEQUENCE; HELICAL STRUCTURES; INTER-DOMAIN INTERACTIONS; PAIRING INTERACTIONS; PROTEIN AGGREGATION; STRUCTURAL MOTIFS; TRANSFORMATION MODEL;

CROSSTALK;

OLIGOMER; POLYGLUTAMINE; HTT PROTEIN, HUMAN; NERVE PROTEIN; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; FLUORESCENCE SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LIGHT SCATTERING; PEPTIDE SYNTHESIS; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SEDIMENTATION RATE; THERMOSTABILITY; ULTRACENTRIFUGATION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; PROTEIN MOTIF; PROTEINOSIS;

AMINO ACID MOTIFS; HUMANS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; PEPTIDES; PROTEIN AGGREGATION, PATHOLOGICAL;

EID: 84908509758     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500449a     Document Type: Article

References (46)

1. Wetzel, R. (2012) Physical chemistry of polyglutamine: Intriguing tales of a monotonous sequence J. Mol. Biol. 421, 466-490
2. Dobson, C. M. (2001) The structural basis of protein folding and its links with human disease Philos. Trans. R. Soc., B 356, 133-145
3. Sikorski, P. and Atkins, E. (2005) New model for crystalline polyglutamine assemblies and their connection with amyloid fibrils Biomacromolecules 6, 425-432
4. Perutz, M. F., Johnson, T., Suzuki, M., and Finch, J. T. (1994) Glutamine repeats as polar zippers: Their possible role in inherited neurodegenerative diseases Proc. Natl. Acad. Sci. U.S.A. 91, 5355-5358
5. Kirkitadze, M. D., Condron, M. M., and Teplow, D. B. (2001) Identification and characterization of key kinetic intermediates in amyloid BETA;-protein fibrillogenesis J. Mol. Biol. 312, 1103-1119
6. Williamson, J. A., Loria, J. P., and Miranker, A. D. (2009) Helix stabilization precedes aqueous and bilayer-catalyzed fiber formation in islet amyloid polypeptide J. Mol. Biol. 393, 383-396
7. Wiltzius, J. J., Sievers, S. A., Sawaya, M. R., and Eisenberg, D. (2009) Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process Protein Sci. 18, 1521-1530
8. Abedini, A. and Raleigh, D. P. (2009) A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides Protein Eng., Des. Sel. 22, 453-459
9. Abedini, A. and Raleigh, D. P. (2009) A role for helical intermediates in amyloid formation by natively unfolded polypeptides? Phys. Biol. 6, 015005
10. Goldsbury, C., Goldie, K., Pellaud, J., Seelig, J., Frey, P., Muller, S. A., Kistler, J., Cooper, G. J., and Aebi, U. (2000) Amyloid fibril formation from full-length and fragments of amylin J. Struct. Biol. 130, 352-362
11. Mishra, R., Jayaraman, M., Roland, B. P., Landrum, E., Fullam, T., Kodali, R., Thakur, A. K., Arduini, I., and Wetzel, R. (2012) Inhibiting the nucleation of amyloid structure in a huntingtin fragment by targeting α-helix-rich oligomeric intermediates J. Mol. Biol. 415, 900-917
12. Jayaraman, M., Kodali, R., Sahoo, B., Thakur, A. K., Mayasundari, A., Mishra, R., Peterson, C. B., and Wetzel, R. (2012) Slow amyloid nucleation via α-helix-rich oligomeric intermediates in short polyglutamine-containing huntingtin fragments J. Mol. Biol. 415, 881-899
13. Kelley, N. W., Huang, X., Tam, S., Spiess, C., Frydman, J., and Pande, V. S. (2009) The predicted structure of the headpiece of the Huntingtin protein and its implications on Huntingtin aggregation J. Mol. Biol. 388, 919-927
14. Kim, M. W., Chelliah, Y., Kim, S. W., Otwinowski, Z., and Bezprozvanny, I. (2009) Secondary structure of Huntingtin amino-terminal region Structure 17, 1205-1212
15. Jayaraman, M., Mishra, R., Kodali, R., Thakur, A. K., Koharudin, L. M., Gronenborn, A. M., and Wetzel, R. (2012) Kinetically competing huntingtin aggregation pathways control amyloid polymorphism and properties Biochemistry 51, 2706-2716
16. Thakur, A. K., Jayaraman, M., Mishra, R., Thakur, M., Chellgren, V. M., Byeon, I. J., Anjum, D. H., Kodali, R., Creamer, T. P., Conway, J. F., Gronenborn, A. M., and Wetzel, R. (2009) Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism Nat. Struct. Mol. Biol. 16, 380-389
17. Fiumara, F., Fioriti, L., Kandel, E. R., and Hendrickson, W. A. (2010) Essential role of coiled coils for aggregation and activity of Q/N-rich prions and PolyQ proteins Cell 143, 1121-1135
18. Sivanandam, V. N., Jayaraman, M., Hoop, C. L., Kodali, R., Wetzel, R., and van der Wel, P. C. A. (2011) The Aggregation-Enhancing Huntingtin N-Terminus Is Helical in Amyloid Fibrils J. Am. Chem. Soc. 133, 4558-4566
19. Crick, S. L., Ruff, K. M., Garai, K., Frieden, C., and Pappu, R. V. (2013) Unmasking the roles of N- and C-terminal flanking sequences from exon 1 of huntingtin as modulators of polyglutamine aggregation Proc. Natl. Acad. Sci. U.S.A. 110, 20075-20080
20. Mao, A. H., Crick, S. L., Vitalis, A., Chicoine, C. L., and Pappu, R. V. (2010) Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Proc. Natl. Acad. Sci. U.S.A. 107, 8183-8188
21. Vitalis, A. and Pappu, R. V. (2011) Assessing the contribution of heterogeneous distributions of oligomers to aggregation mechanisms of polyglutamine peptides Biophys. Chem. 159, 14-23
22. Uversky, V. N. and Fink, A. L. (2004) Conformational constraints for amyloid fibrillation: The importance of being unfolded Biochim. Biophys. Acta 1698, 131-153
23. Williamson, T. E., Vitalis, A., Crick, S. L., and Pappu, R. V. (2010) Modulation of polyglutamine conformations and dimer formation by the N-terminus of huntingtin J. Mol. Biol. 396, 1295-1309
24. Root, B. C., Pellegrino, L. D., Crawford, E. D., Kokona, B., and Fairman, R. (2009) Design of a heterotetrameric coiled coil Protein Sci. 18, 329-336
25. Crestfield, A. M., Moore, S., and Stein, W. H. (1963) The preparation and enzymatic hydrolysis of reduced and S-carboxymethylated proteins J. Biol. Chem. 238, 622-627
26. Rosen, H. (1957) A modified ninhydrin colorimetric analysis for amino acids Arch. Biochem. Biophys. 67, 10-15
27. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4, 2411-2423
28. Wall, J., Schell, M., Murphy, C., Hrncic, R., Stevens, F. J., and Solomon, A. (1999) Thermodynamic instability of human lambda 6 light chains: Correlation with fibrillogenicity Biochemistry 38, 14101-14108
29. Mok, Y. F., Ryan, T. M., Yang, S., Hatters, D. M., Howlett, G. J., and Griffin, M. D. (2011) Sedimentation velocity analysis of amyloid oligomers and fibrils using fluorescence detection Methods 54, 67-75
30. Roy, S., Ratnaswamy, G., Boice, J. A., Fairman, R., McLendon, G., and Hecht, M. H. (1997) A protein designed by binary patterning of polar and nonpolar amino acids displays native-like properties J. Am. Chem. Soc. 119, 5302-5306
31. Schuck, P. and Zhao, H. (2011) Editorial for the special issue of methods "Modern Analytical Ultracentrifugation" Methods 1-3
32. Kar, K., Jayaraman, M., Sahoo, B., Kodali, R., and Wetzel, R. (2011) Critical nucleus size for disease-related polyglutamine aggregation is repeat-length dependent Nat. Struct. Mol. Biol. 18, 328-336
33. Rohl, C. A. and Baldwin, R. L. (1998) Deciphering rules of helix stability in peptides Methods Enzymol. 295, 1-26
34. Baldwin, R. L. (1996) How Hofmeister ion interactions affect protein stability Biophys. J. 71, 2056-2063
35. Semisotnov, G. V., Rodionova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas, A. F., and Gilmanshin, R. I. (1991) Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe Biopolymers 31, 119-128
36. Mulqueen, P. M. and Kronman, M. J. (1982) Binding of naphthalene dyes to the N and A conformers of bovine α-lactalbumin Arch. Biochem. Biophys. 215, 28-39
37. Goto, Y. and Fink, A. L. (1989) Conformational states of BETA;-lactamase: Molten-globule states at acidic and alkaline pH with high salt Biochemistry 28, 945-952
38. Chen, S. and Wetzel, R. (2001) Solubilization and disaggregation of polyglutamine peptides Protein Sci. 10, 887-891
39. ONuallain, B., Thakur, A. K., Williams, A. D., Bhattacharyya, A. M., Chen, S., Thiagarajan, G., and Wetzel, R. (2006) Kinetics and thermodynamics of amyloid assembly using a high-performance liquid chromatography-based sedimentation assay Methods Enzymol. 413, 34-74
40. Bertoncini, C. W. and Celej, M. S. (2011) Small molecule fluorescent probes for the detection of amyloid self-assembly in vitro and in vivo Curr. Protein Pept. Sci. 12, 205-220
41. Chen, S., Berthelier, V., Hamilton, J. B., ONuallain, B., and Wetzel, R. (2002) Amyloid-like features of polyglutamine aggregates and their assembly kinetics Biochemistry 41, 7391-7399
42. Chen, S., Berthelier, V., Yang, W., and Wetzel, R. (2001) Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity J. Mol. Biol. 311, 173-182
43. Jayaraman, M., Thakur, A. K., Kar, K., Kodali, R., and Wetzel, R. (2011) Assays for studying nucleated aggregation of polyglutamine proteins Methods 53, 246-254
44. 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
45. Huston, J. S., Levinson, D., Mudgett-Hunter, M., Tai, M. S., Novotny, J., Margolies, M. N., Ridge, R. J., Bruccoleri, R. E., Haber, E., and Crea, R. 1988, Protein engineering of antibody binding sites: Recovery of specific activity in an anti-digoxin single-chain Fv analogue produced in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 85, 5879-5883
46. Mishra, R., Hoop, C. L., Kodali, R., Sahoo, B., van der Wel, P. C., and Wetzel, R. (2012) Serine phosphorylation suppresses huntingtin amyloid accumulation by altering protein aggregation properties J. Mol. Biol. 424, 1-14