Elongation kinetics of polyglutamine peptide fibrils: A quartz crystal microbalance with dissipation study

Journal of Molecular Biology

Volumn 421, Issue 2-3, 2012, Pages 329-347

  Walters, Robert H ^a   Jacobson, Kurt H ^a   Pedersen, Joel A ^a,b   Murphy, Regina M ^a  

^a University of Wisconsin Madison   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

aggregation; fibril elongation; optical waveguide lightmode spectroscopy (OWLS); polyglutamine; quartz crystal microbalance with dissipation monitoring (QCM D)

Indexed keywords

DEXTRO PROLYLGLYCINE; GLUTAMINE; GLYCINE DERIVATIVE; POLYGLUTAMINE; UNCLASSIFIED DRUG; WATER;

ARTICLE; BETA TURN; CELL ELONGATION; CONTROLLED STUDY; FIBER; IMMOBILIZED CELL; IONIC STRENGTH; MOLECULAR MECHANICS; MOLECULAR WEIGHT; OPTICAL WAVEGUIDE LIGHTMODE SPECTROSCOPY; PEPTIDE ANALYSIS; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SYNTHESIS; QUALITATIVE ANALYSIS; QUARTZ CRYSTAL MICROBALANCE; SPECTROSCOPY;

EID: 84863983330     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.03.017     Document Type: Article

References (61)

1. Bates G. Huntingtin aggregation and toxicity in Huntington's disease Lancet 361 2003 1642 1644
2. Orr H.T. Beyond the Qs in the polyglutamine diseases Genes Dev. 15 2001 925 932
3. Wanker E.E. Protein aggregation and pathogenesis of Huntington's disease: mechanisms and correlations Biol. Chem. 381 2000 937 942
4. Albrecht M., Golatta M., Wullner U., and Lengauer T. Structural and functional analysis of ataxin-2 and ataxin-3 Eur. J. Biochem. 271 2004 3155 3170
5. Gusella J.F., and MacDonald M.E. Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease Nat. Rev. Neurosci. 1 2000 109 115
6. Williams A.J., and Paulson H.L. Polyglutamine neurodegeneration: protein misfolding revisited Trends Neurosci. 31 2008 521 528
7. Ordway J.M., Tallaksen-Greene S., Gutekunst C.A., Bernstein E.M., Cearley J.A., and Wiener H.W. Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse Cell 91 1997 753 763
8. Schiffer N.W., Broadley S.A., Hirschberger T., Tavan P., Kretzschmar H.A., and Giese A. Identification of anti-prion compounds as efficient inhibitors of polyglutamine protein aggregation in a zebrafish model J. Biol. Chem. 282 2007 9195 9203
9. Jana N.R., Tanaka M., Wang G.H., and Nukina N. 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 2000 2009 2018
10. Carmichael J., Chatellier J., Woolfson A., Milstein C., Fersht A.R., and Rubinsztein D.C. Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease Proc. Natl Acad. Sci. USA 97 2000 9701 9705
11. Gatchel J.R., and Zoghbi H.Y. Diseases of unstable repeat expansion: mechanisms and common principles Nat. Rev. Genet. 6 2005 743 755
12. Nagai Y., Inui T., Popiel H.A., Fujikake N., Hasegawa K., and Urade Y. A toxic monomeric conformer of the polyglutamine protein Nat. Struct. Mol. Biol. 14 2007 332 340
13. Takahashi T., Kikuchi S., Katada S., Nagai Y., Nishizawa M., and Onodera O. Soluble polyglutamine oligomers formed prior to inclusion body formation are cytotoxic Hum. Mol. Genet. 17 2008 345 356
14. Chen S.M., Ferrone F.A., and Wetzel R. Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation Proc. Natl Acad. Sci. USA 99 2002 11884 11889
15. Yang W., Dunlap J.R., Andrews R.B., and Wetzel R. Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells Hum. Mol. Genet. 11 2002 2905 2917
16. Chen S., Berthelier V., Yang W., and Wetzel R. Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity J. Mol. Biol. 311 2001 173 182
17. Chen S.M., Berthelier V., Hamilton J.B., O'Nuallain B., and Wetzel R. Amyloid-like features of polyglutamine aggregates and their assembly kinetics Biochemistry 41 2002 7391 7399
18. Slepko N., Bhattacharyya A.M., Jackson G.R., Steffan J.S., Marsh J.L., Thompson L.M., and Wetzel R. Normal-repeat-length polyglutamine peptides accelerate aggregation nucleation and cytotoxicity of expanded polyglutamine proteins Proc. Natl Acad. Sci. USA 103 2006 14367 14372
19. Lee C.C., Walters R.H., and Murphy R.M. Reconsidering the mechanism of polyglutamine peptide aggregation Biochemistry 46 2007 12810 12820
20. Walters R.H., and Murphy R.M. Examining polyglutamine peptide length: a connection between collapsed conformations and increased aggregation J. Mol. Biol. 393 2009 978 992
21. Perutz M.F., Johnson T., Suzuki M., and Finch J.T. Glutamine repeats as polar zippers - their possible role in inherited neurodegenerative diseases Proc. Natl Acad. Sci. USA 91 1994 5355 5358
22. Perutz M.F., Finch J.T., Berriman J., and Lesk A. Amyloid fibers are water-filled nanotubes Proc. Natl Acad. Sci. USA 99 2002 5591 5595
23. Raspe M., Gillis J., Krol H., Krom S., Bosch K., van Veen H., and Reits E. Mimicking proteasomal release of polyglutamine peptides initiates aggregation and toxicity J. Cell Sci. 122 2009 3262 3271
24. Kar K., Jayaraman M., Sahoo B., Kodali R., and Wetzel R. Critical nucleus size for disease-related polyglutamine aggregation is repeat-length dependent Nat. Struct. Mol. Biol. 18 2011 328
25. Bhattacharyya A.M., Thakur A.K., and Wetzel R. Polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction Proc. Natl Acad. Sci. USA 102 2005 15400 15405
26. Bernacki J.P., and Murphy R.M. Model discrimination and mechanistic interpretation of kinetic data in protein aggregation studies Biophys. J. 96 2009 2871 2887
27. Vitalis A., and Pappu R.V. Assessing the contribution of heterogeneous distributions of oligomers to aggregation mechanisms of polyglutamine peptides Biophys. Chem. 159 2011 14 23
28. Vitalis A., Wang X., and Pappu R.V. Atomistic simulations of the effects of polyglutamine chain length and solvent quality on conformational equilibria and spontaneous homodimerization J. Mol. Biol. 384 2008 279 297
29. Vitalis A., Lyle N., and Pappu R.V. Thermodynamics of β-sheet formation in polyglutamine Biophys. J. 97 2009 303 311
30. Scheibel T., Bloom J., and Lindquist S. The elongation of yeast prion fibers involves separable steps of association and conversion Proc. Natl Acad. Sci. USA 101 2004 2287 2292
31. Williamson T.E., Vitalis A., Crick S.L., and Pappu R.V. Modulation of polyglutamine conformations and dimer formation by the N-terminus of huntingtin J. Mol. Biol. 396 2010 1295 1309
32. Walters R.H., and Murphy R.M. Aggregation kinetics of interrupted polyglutamine peptides J. Mol. Biol. 412 2011 505 519
33. Rodahl M., Höök F., Krozer A., Brezezinski P., and Kasemo B. Quartz-crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments Rev. Sci. Instrum. 66 1995 3924 3930
34. Sauerbrey G. Verwendung von Schwingquarzen zur Wägung dünner Schichten und der Mikrowägung Z. Phys. 155 1959 206 222
35. Reviakine I., Johannsmann D., and Richter R.P. Hearing what you can't see and visualizing what you hear: interpreting quartz crystal microbalance data from solvated interfaces Anal. Chem. 83 2011 8838 8848
36. Rodahl M., Höök F., Fredriksson C., Keller C., Krozer A., and Brzezinski P. Simultaneous frequency and dissipation factor QCM measurements of biomolecular adsorption and cell adhesion Faraday Discuss. 107 1997 229 246
37. Rodahl M., Höök F., and Kasemo B. QCM operation in liquids: an explanation of measured variations in frequency and Q factor with liquid conductivity Anal. Chem. 68 1996 2219 2227
38. Kotarek J.A., Johnson K.C., and Moss M.A. Quartz crystal microbalance analysis of growth kinetics for aggregation intermediates of the amyloid-beta protein Anal. Biochem. 378 2008 15 24
39. Kotarek J.A., and Moss M.A. Impact of phospholipid bilayer saturation on amyloid-beta protein aggregation intermediate growth: a quartz crystal microbalance analysis Anal. Biochem. 399 2010 30 38
40. Saraiva A.M., Pereira M.C., and Brezesinski G. Is the viscoelasticity of Alzheimer's A beta 42 peptide oligomers a general property of protein oligomers related to their toxicity? Langmuir 26 2010 12060 12067
41. Hovgaard M.B., Dong M., Otzen D.E., and Besenbacher F. Quartz crystal microbalance studies of multilayer glucagon fibrillation at the solid-liquid interface Biophys. J. 93 2007 2162 2169
42. White D.A., Buell A.K., Knowles T.P.J., Welland M.E., and Dobson C.M. Protein aggregation in crowded environments J. Am. Chem. Soc. 132 2010 5170 5175
43. Tellechea E., Johannsmann D., Steinmetz N.F., Richter R.P., and Reviakine I. Model-independent analysis of QCM data on colloidal particle adsorption Langmuir 25 2009 5177 5184
44. Tsortos A., Papadakis G., and Gizeli E. Shear acoustic wave biosensor for detecting DNA intrinsic viscosity and conformation: a study with QCM-D Biosens. Bioelectron. 24 2008 836 841
45. Zhang G., and Wu C. Quartz crystal microbalance studies on conformational change of polymer chains at interface Macromol. Rapid Commun. 30 2009 328 335
46. Vörös J. The density and refractive index of adsorbing protein layers Biophys. J. 87 2004 553 561
47. Vörös J., Ramsden J.J., Csucs G., Szendro I., De Paul S.M., Textor M., and Spencer N.D. Optical grating coupler biosensors Biomaterials 23 2002 3699 3710
48. Lofas S., and Johnsson B. A novel hydrogel matrix on gold surfaces in surface-plasmon resonance sensors for fast and efficient covalent immobilization of ligands J. Chem. Soc.: Chem. Commun. 1990 1526 1528
49. Mao A.H., Crick S.L., Vitalis A., Chicoine C.L., and Pappu R.V. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Proc. Natl Acad. Sci. USA 107 2010 8183 8188
50. Höök F., Vörös J., Rodahl M., Kurrat R., Boni P., and Ramsden J. A comparative study of protein adsorption on titanium oxide surfaces using in situ ellipsometry, optical waveguide lightmode spectroscopy, and quartz crystal microbalance/dissipation RID A-5843-2008 Colloids Surf., B 24 2002 155 170
51. Legleiter J., Mitchell E., Lotz G.P., Sapp E., Ng C., and DiFiglia M. Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo J. Biol. Chem. 285 2010 14777 14790
52. Diaz-Hernandez M., Moreno-Herrero F., Gomez-Ramos P., Moran M.A., Ferrer I., and Baro A.M. Biochemical, ultrastructural, and reversibility studies on huntingtin filaments isolated from mouse and human brain J. Neurosci. 24 2004 9361 9371
53. Thirumalai D., Govardhan R., and Straub J.E. Role of water in protein aggregation and amyloid polymorphism Acc. Chem. Res. 45 2012 83 92
54. Wacker J.L., Zareie M.H., Fong H., Sarikaya M., and Muchowski P.J. Hsp70 and Hsp40 attenuate formation of spherical and annular polyglutamine oligomers by partitioning monomer Nat. Struct. Mol. Biol. 11 2004 1215 1222
55. Diguet E., Petit F., Escartin C., Cambon K., Bizat N., and Dufour N. Normal aging modulates the neurotoxicity of mutant huntingtin PLoS One 4 2009 e4637
56. Arrasate M., Mitra S., Schweitzer E.S., Segal M.R., and Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431 2004 805 810
57. Chen S.M., and Wetzel R. Solubilization and disaggregation of polyglutamine peptides Protein Sci. 10 2001 887 891
58. Kurrat R., Ramsden J.J., and Prenosil J.E. Kinetic-model for serum-albumin adsorption - experimental verification J. Chem. Soc., Faraday Trans. 90 1994 587 590
59. Kurrat R., Textor M., Ramsden J.J., Boni P., and Spencer N.D. Instrumental improvements in optical waveguide light mode spectroscopy for the study of biomolecule adsorption Rev. Sci. Instrum. 68 1997 2172 2176
60. Ramsden J.J. Review of new experimental-techniques for investigating random sequential adsorption J. Stat. Phys. 73 1993 853 877
61. Defeijter J.A., Benjamins J., and Veer F.A. Ellipsometry as a tool to study adsorption behavior of synthetic and biopolymers at air-water-interface Biopolymers 17 1978 1759 1772