Dimensionality of Carbon Nanomaterials Determines the Binding and Dynamics of Amyloidogenic Peptides: Multiscale Theoretical Simulations

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Todorova, Nevena ^a   Makarucha, Adam J ^a   Hine, Nicholas D M ^b   Mostofi, Arash A ^b   Yarovsky, Irene ^a  

^a Yarra Valley Water   (Australia)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; DENSITY FUNCTIONAL THEORY; GLYCOPROTEINS; MOLECULAR DYNAMICS; NANOPARTICLES; NANOSTRUCTURED MATERIALS; NANOTUBES; NEURODEGENERATIVE DISEASES; PEPTIDES; SELF ASSEMBLY; YARN;

ALZHEIMERS DISEASE; AMYLOIDOGENIC PEPTIDES; CARBON NANO-MATERIALS; FIBRIL FORMATION; PARKINSON'S DISEASE; PRION DISEASE; PROTEIN MISFOLDING; PROTEIN SELF-ASSEMBLIES; STACKINGS; THEORETICAL SIMULATION;

GRAPHENE;

AMYLOID; AMYLOID PROTEIN; APOLIPOPROTEIN C2; CARBON NANOTUBE; GRAPHENE; NANOPARTICLE;

ALZHEIMER DISEASE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; DENSITY FUNCTIONAL THEORY; FIBER; MATERIALS TESTING; MOLECULAR DYNAMICS; NANOTECHNOLOGY; NERVE FIBER GROWTH; PARKINSON DISEASE; PRION DISEASE; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SURFACE PROPERTY;

AMYLOID; CARBON; MODELS, MOLECULAR; MODELS, THEORETICAL; NANOSTRUCTURES; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; THERMODYNAMICS;

EID: 84892770558     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003360     Document Type: Article

References (84)

1. Mout R, Moyano DF, Rana S, Rotello VM, (2012) Surface functionalization of nanoparticles for nanomedicine. Chem Soc Rev 41: 2539-2544.
2. Lee J, Mahendra S, Alvarez PJ, (2010) Nanomaterials in the construction industry: a review of their applications and environmental health and safety considerations. Acs Nano 4: 3580-3590.
3. de la Rica R, Matsui H, (2010) Applications of peptide and protein-based materials in bionanotechnology. Chem Soc Rev 39: 3499-3509.
4. Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, et al. (2011) Protein-nanoparticle interactions: opportunities and challenges. Chem Rev 111: 5610-5637.
5. Love SA, Maurer-Jones MA, Thompson JW, Lin YS, Haynes CL, (2012) Assessing nanoparticle toxicity. Annu Rev Anal Chem (Palo Alto Calif) 5: 181-205.
6. van der Zande M, Junker R, Walboomers XF, Jansen JA, (2011) Carbon nanotubes in animal models: a systematic review on toxic potential. Tissue Eng Part B Rev 17: 57-69.
7. Cabaleiro-Lago C, Szczepankiewicz O, Linse S, (2012) The effect of nanoparticles on amyloid aggregation depends on the protein stability and intrinsic aggregation rate. Langmuir 28: 1852-1857.
8. Cukalevski R, Lundqvist M, Oslakovic C, Dahlback B, Linse S, et al. (2011) Structural changes in apolipoproteins bound to nanoparticles. Langmuir 27: 14360-14369.
9. Linse S, Cabaleiro-Lago C, Xue WF, Lynch I, Lindman S, et al. (2007) Nucleation of protein fibrillation by nanoparticles. Proc Natl Acad Sci U S A 104: 8691-8696.
10. Mahmoudi M, Kalhor HR, Laurent S, Lynch I, (2013) Protein fibrillation and nanoparticle interactions: opportunities and challenges. Nanoscale 5: 2570-2588.
11. Kayat J, Gajbhiye V, Tekade RK, Jain NK, (2011) Pulmonary toxicity of carbon nanotubes: a systematic report. Nanomedicine 7: 40-49.
12. Yang ST, Liu Y, Wang YW, Cao A, (2013) Biosafety and bioapplication of nanomaterials by designing protein-nanoparticle interactions. Small 9: 1635-1653.
13. Fischer HC, Chan WC, (2007) Nanotoxicity: the growing need for in vivo study. Curr Opin Biotechnol 18: 565-571.
14. Monopoli MP, Aberg C, Salvati A, Dawson KA, (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7: 779-786.
15. Gajewicz A, Rasulev B, Dinadayalane TC, Urbaszek P, Puzyn T, et al. (2012) Advancing risk assessment of engineered nanomaterials: application of computational approaches. Adv Drug Deliv Rev 64: 1663-1693.
16. Makarucha AJ, Todorova N, Yarovsky I, (2011) Nanomaterials in biological environment: a review of computer modelling studies. Eur Biophys J 40: 103-115.
17. Zuo G, Kang SG, Xiu P, Zhao Y, Zhou R, (2013) Interactions between proteins and carbon-based nanoparticles: exploring the origin of nanotoxicity at the molecular level. Small 9: 1546-1556.
18. Li C, Mezzenga R, (2013) The interplay between carbon nanomaterials and amyloid fibrils in bio-nanotechnology. Nanoscale 5: 6207-18 DOI: 10.1039/C3NR01644G.
19. Zhang M, Yu Y, Wang CX, Yang YL, Wang C, (2013) Nanomaterials for reducing amyloid cytotoxicity. Adv Mater 25: 3780-801 DOI: 10.1002/adma.201301210.
20. Albanese A, Tang PS, Chan WC, (2012) The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 14: 1-16.
21. D'Rozario RS, Wee CL, Wallace EJ, Sansom MS, (2009) The interaction of C60 and its derivatives with a lipid bilayer via molecular dynamics simulations. Nanotechnology 20: 115102.
22. Sanchez VC, Jachak A, Hurt RH, Kane AB, (2012) Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 25: 15-34.
23. Zuo G, Zhou X, Huang Q, Fang HP, Zhou RH, (2011) Adsorption of villin headpiece onto graphene, carbon nanotube, and C60: effect of contacting surface curvatures on binding affinity. J Phys Chem C 115: 23323-23328.
24. Shvedova AA, Pietroiusti A, Fadeel B, Kagan VE, (2012) Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol Appl Pharmacol 261: 121-133.
25. Colvin VL, Kulinowski KM, (2007) Nanoparticles as catalysts for protein fibrillation. Proc Natl Acad Sci U S A 104: 8679-8680.
26. Zhu M, Souillac PO, Ionescu-Zanetti C, Carter SA, Fink AL, (2002) Surface-catalyzed amyloid fibril formation. J Biol Chem 277: 50914-50922.
27. Ghule AV, Kathir KM, Kumar TKS, Tzing SH, Chang JY, et al. (2007) Carbon nanotubes prevent 2,2,2 trifluoroethanol induced aggregation of protein. Carbon 45: 1586-1589.
28. Fu Z, Luo Y, Derreumaux P, Wei G, (2009) Induced beta-barrel formation of the Alzheimer's Abeta25-35 oligomers on carbon nanotube surfaces: implication for amyloid fibril inhibition. Biophys J 97: 1795-1803.
29. Li H, Luo Y, Derreumaux P, Wei G, (2011) Carbon nanotube inhibits the formation of beta-sheet-rich oligomers of the Alzheimer's amyloid-beta(16-22) peptide. Biophys J 101: 2267-2276.
30. Chiu CC, Dieckmann GR, Nielsen SO, (2008) Molecular dynamics study of a nanotube-binding amphiphilic helical peptide at different water/hydrophobic interfaces. J Phys Chem B 112: 16326-16333.
31. Chiu CC, Dieckmann GR, Nielsen SO, (2009) Role of peptide-peptide interactions in stabilizing peptide-wrapped single-walled carbon nanotubes: a molecular dynamics study. Biopolymers 92: 156-163.
32. De Miranda Tomásio S, Walsh TR, (2007) Atomistic modelling of the interaction between peptides and carbon nanotubes. Mol Phys 105: 221-229.
33. Hung A, Griffin MD, Howlett GJ, Yarovsky I, (2009) Lipids enhance apolipoprotein C-II-derived amyloidogenic peptide oligomerization but inhibit fibril formation. J Phys Chem B 113: 9447-9453.
34. Hung A, Griffin MD, Howlett GJ, Yarovsky I, (2008) Effects of oxidation, pH and lipids on amyloidogenic peptide structure: implications for fibril formation? Eur Biophys J 38: 99-110.
35. Hung A, Mager M, Hembury M, Stellacci F, Stevens MM, et al. (2013) Amphiphilic amino acids: a key to adsorbing proteins to nanopatterned surfaces? Chem Sci 4: 928.
36. Hung A, Mwenifumbo S, Mager M, Kuna JJ, Stellacci F, et al. (2011) Ordering surfaces on the nanoscale: implications for protein adsorption. J Am Chem Soc 133: 1438-1450.
37. Todorova N, Hung A, Maaser SM, Griffin MD, Karas J, et al. (2010) Effects of mutation on the amyloidogenic propensity of apolipoprotein C-II(60-70) peptide. Phys Chem Chem Phys 12: 14762-14774.
38. Todorova N, Hung A, Yarovsky I, (2010) Lipid concentration effects on the amyloidogenic apoC-II(60-70) peptide: a computational study. J Phys Chem B 114: 7974-7982.
39. Todorova N, Yeung L, Hung A, Yarovsky I, (2013) "Janus" cyclic peptides: a new approach to amyloid fibril inhibition? PLoS One 8: e57437.
40. Walsh TR, (2008) Modelling the nanoscale patterning of nucleic acid base pairs deposited on graphite. Mol Phys 106: 1613-1619.
41. MacRaild CA, Hatters DM, Howlett GJ, Gooley PR, (2001) NMR structure of human apolipoprotein C-II in the presence of sodium dodecyl sulfate. Biochemistry 40: 5414-5421.
42. MacRaild CA, Howlett GJ, Gooley PR, (2004) The structure and interactions of human apolipoprotein C-II in dodecyl phosphocholine. Biochemistry 43: 8084-8093.
43. Hatters DM, MacPhee CE, Lawrence LJ, Sawyer WH, Howlett GJ, (2000) Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops. Biochemistry 39: 8276-8283.
44. Teoh CL, Pham CL, Todorova N, Hung A, Lincoln CN, et al. (2011) A structural model for apolipoprotein C-II amyloid fibrils: experimental characterization and molecular dynamics simulations. J Mol Biol 405: 1246-1266.
45. Li Z, Hulderman T, Salmen R, Chapman R, Leonard SS, et al. (2007) Cardiovascular effects of pulmonary exposure to single-wall carbon nanotubes. Environ Health Perspect 115: 377-382.
46. Sun Q, Wang A, Jin X, Natanzon A, Duquaine D, et al. (2005) Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. JAMA 294: 3003-3010.
47. Vesterdal LK, Folkmann JK, Jacobsen NR, Sheykhzade M, Wallin H, et al. (2009) Modest vasomotor dysfunction induced by low doses of C60 fullerenes in apolipoprotein E knockout mice with different degree of atherosclerosis. Part Fibre Toxicol 6: 5.
48. Wilson LM, Mok YF, Binger KJ, Griffin MD, Mertens HD, et al. (2007) A structural core within apolipoprotein C-II amyloid fibrils identified using hydrogen exchange and proteolysis. J Mol Biol 366: 1639-1651.
49. Griffin MDW, Yeung L, Hung A, Todorova N, Mok YF, et al. (2012) A Cyclic peptide inhibitor of apoC-II peptide fibril formation: Mechanistic insight from NMR and molecular dynamics analysis. J Mol Biol 416: 642-655.
50. Hung A, Yarovsky I, (2011) Inhibition of peptide aggregation by lipids: Insights from coarse-grained molecular simulations. J Mol Graph Model 29: 597-607.
51. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718.
52. Tomasio SM, Walsh TR, (2009) Modeling the binding affinity of peptides for graphitic surfaces. Influences of aromatic content and interfacial Shape. J Phys Chem C 113: 8778-8785.
53. Frishman D, Argos P, (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579.
54. Oren EE, Tamerler C, Sarikaya M, (2005) Metal recognition of septapeptides via polypod molecular architecture. Nano Lett 5: 415-419.
55. Cheatham TE, Miller JL, Fox T, Darden TA, Kollman PA, (1995) Molecular-dynamics simulations on solvated biomolecular systems- the particle mesh ewald method leads to stable trajectories of DNA, RNA, and proteins. J Am Chem Soc 117: 4193-4194.
56. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM, (1997) LINCS: A linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
57. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 33-38, 27-38.
58. Berendsen HJC, Postma JPM, VanGunsteren WF (1981) Interaction models for water in relation to protein hydration. In: Pullman B, editor. Intermolecular Forces. Dordrecht: D. Reidel Publishing Company. pp. 331-342.
59. Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR, (1984) Molecular-dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
60. Roux B, (1995) The calculation of the potential of mean force using computer-simulations. Comput Phys Commun 91: 275-282.
61. Lever G, Cole DJ, Hine ND, Haynes PD, Payne MC, (2013) Electrostatic considerations affecting the calculated HOMO-LUMO gap in protein molecules. J Phys Condens Matter 25: 152101.
62. Skylaris CK, Haynes PD, Mostofi AA, Payne MC, (2005) Introducing ONETEP: linear-scaling density functional simulations on parallel computers. J Chem Phys 122: 84119.
63. Cole DJ, Rajendra E, Roberts-Thomson M, Hardwick B, McKenzie GJ, et al. (2011) Interrogation of the protein-protein interactions between human BRCA2 BRC repeats and RAD51 reveals atomistic determinants of affinity. PLoS Comput Biol 7: e1002096.
64. Dziedzic J, Fox SJ, Fox T, Tautermann CS, Skylaris C-K, (2013) Large-scale DFT calculations in implicit solvent-A case study on the T4 lysozyme L99A/M102Q protein. Int J Quantum Chem 113: 771-785.
65. Lee LP, Cole DJ, Payne MC, Skylaris CK, (2013) Natural bond orbital analysis in the ONETEP code: applications to large protein systems. J Comput Chem 34: 429-444.
66. Hine NDM, Haynes PD, Mostofi AA, Skylaris CK, Payne MC, (2009) Linear-scaling density-functional theory with tens of thousands of atoms: Expanding the scope and scale of calculations with ONETEP. Comput Phys Commun 180: 1041-1053.
67. Skylaris C-K, Haynes PD, Mostofi AA, Payne MC, (2005) Using ONETEP for accurate and efficient density functional calculations. J Phys: Condens Matter 17: 5757-5769.
68. Skylaris CK, Mostofi AA, Haynes PD, Dieguez O, Payne MC, (2002) Nonorthogonal generalized Wannier function pseudopotential plane-wave method. Phys Rev B 66: 035119.
69. Mostofi AA, Haynes PD, Skylaris CK, Payne MC, (2003) Preconditioned iterative minimization for linear-scaling electronic structure calculations. J Chem Phys 119: 8842-8848.
70. Perdew JP, Burke K, Ernzerhof M, (1996) Generalized gradient approximation made simple. Phys Rev Lett 77: 3865-3868.
71. Hill Q, Skylaris CK, (2009) Including dispersion interactions in the ONETEP program for linear-scaling density functional theory calculations. P R Soc A 465: 669-683.
72. Ehrlich S, Moellmann J, Grimme S, (2013) Dispersion-corrected density functional theory for aromatic interactions in complex systems. Acc Chem Res 46: 916-926.
73. Antony J, Grimme S, (2012) Fully ab initio protein-ligand interaction energies with dispersion corrected density functional theory. J Comput Chem 33: 1730-1739.
74. McGaughey GB, Gagne M, Rappe AK, (1998) pi-Stacking interactions. Alive and well in proteins. J Biol Chem 273: 15458-15463.
75. Yang Z, Wang Z, Tian X, Xiu P, Zhou R, (2012) Amino acid analogues bind to carbon nanotube via pi-pi interactions: comparison of molecular mechanical and quantum mechanical calculations. J Chem Phys 136: 025103.
76. Andujar SA, Lugli F, Hofinger S, Enriz RD, Zerbetto F, (2012) Amyloid-beta fibril disruption by C(60)-molecular guidance for rational drug design. Phys Chem Chem Phys 14: 8599-8607.
77. Liang LJ, Wang Q, Wu T, Shen JW, Kang Y, (2009) Molecular dynamics simulation on stability of insulin on graphene. Chinese J Chem Phys 22: 627-634.
78. Noon WH, Kong Y, Ma J, (2002) Molecular dynamics analysis of a buckyball-antibody complex. Proc Natl Acad Sci U S A 99 Suppl 2: 6466-6470.
79. Zuo G, Huang Q, Wei G, Zhou R, Fang H, (2010) Plugging into proteins: poisoning protein function by a hydrophobic nanoparticle. Acs Nano 4: 7508-7514.
80. de Leon A, Jalbout AF, Basiuk VA, (2008) SWNT-amino acid interactions: A theoretical study. Chem Phys Lett 457: 185-190.
81. Leon Ad, Jalbout AF, Basiuk VA, (2008) Fullerene-amino acid interactions. A theoretical study. Chem Phys Lett 452: 306-314.
82. Chamberlain AK, Lee Y, Kim S, Bowie JU, (2004) Snorkeling preferences foster an amino acid composition bias in transmembrane helices. J Mol Biol 339: 471-479.
83. Segrest JP, De Loof H, Dohlman JG, Brouillette CG, Anantharamaiah GM, (1990) Amphipathic helix motif: classes and properties. Proteins 8: 103-117.
84. Poenitzsch VZ, Winters DC, Xie H, Dieckmann GR, Dalton AB, et al. (2007) Effect of electron-donating and electron-withdrawing groups on peptide/single-walled carbon nanotube interactions. J Am Chem Soc 129: 14724-14732.