Pathways of Amyloid-β Aggregation Depend on Oligomer Shape

Journal of the American Chemical Society

Volumn 140, Issue 1, 2018, Pages 319-327

  Barz, Bogdan ^a,b   Liao, Qinghua ^a,c   Strodel, Birgit ^a,b  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; GLYCOPROTEINS; MOLECULAR DYNAMICS; NEURODEGENERATIVE DISEASES; PEPTIDES;

AGGREGATION PROCESS; ALZHEIMER'S DISEASE; AMYLOID-BETA PEPTIDES; HYDROPHOBIC RESIDUES; MOLECULAR DYNAMICS SIMULATIONS; OLIGOMER DISTRIBUTION; RESEARCH TOPICS; SOLVENT EXPOSURE;

OLIGOMERS;

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; OLIGOMER; AMYLOID BETA PROTEIN; PROTEIN AGGREGATE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CONFORMATION; CYTOTOXICITY; HYDROPHOBICITY; ION MOBILITY SPECTROMETRY; MOLECULAR DYNAMICS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; STATIC ELECTRICITY; CHEMICAL PHENOMENA; CHEMISTRY; HUMAN; PROTEINOSIS;

AMYLOID BETA-PEPTIDES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL;

EID: 85040323745     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.7b10343     Document Type: Article

References (61)

1. Bucciantini, M.; Giannoni, E.; Chiti, F.; Baroni, F.; Formigli, L.; Zurdo, J.; Taddei, N.; Ramponi, G.; Dobson, C. M.; Stefani, M. Nature 2002, 416, 507-511 10.1038/416507a
2. Chiti, F.; Dobson, C. M. Annu. Rev. Biochem. 2006, 75, 333-366 10.1146/annurev.biochem.75.101304.123901
3. Knowles, T. P. J.; Vendruscolo, M.; Dobson, C. M. Nat. Rev. Mol. Cell Biol. 2014, 15, 384-396 10.1038/nrm3810
4. Lambert, M. P.; Barlow, A. K.; Chromy, B. A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T. E.; Rozovsky, I.; Trommer, B.; Viola, K. L.; Wals, P.; Zhang, C.; Finch, C. E.; Krafft, G. A.; Klein, W. L. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 6448-6453 10.1073/pnas.95.11.6448
5. Huang, T.; Yang, D.-S.; Plaskos, N. P.; Go, S.; Yip, C. M.; Fraser, P. E.; Chakrabartty, A. J. Mol. Biol. 2000, 297, 73-87 10.1006/jmbi.2000.3559
6. Kirkitadze, M.; Bitan, G.; Teplow, D. J. Neurosci. Res. 2002, 69, 567-577 10.1002/jnr.10328
7. Fändrich, M. J. Mol. Biol. 2012, 421, 427-440 10.1016/j.jmb.2012.01.006
8. Nagel-Steger, L.; Owen, M. C.; Strodel, B. ChemBioChem 2016, 17, 657-676 10.1002/cbic.201500623
9. Lee, S. J. C.; Nam, E.; Lee, H. J.; Savelieff, M. G.; Lim, M. H. Chem. Soc. Rev. 2017, 46, 310-323 10.1039/C6CS00731G
10. Campioni, S.; Mannini, B.; Zampagni, M.; Pensalfini, A.; Parrini, C.; Evangelisti, E.; Relini, A.; Stefani, M.; Dobson, C. M.; Cecchi, C.; Chiti, F. Nat. Chem. Biol. 2010, 6, 140-147 10.1038/nchembio.283
11. Mannini, B.; Mulvihill, E.; Sgromo, C.; Cascella, R.; Khodarahmi, R.; Ramazzotti, M.; Dobson, C. M.; Cecchi, C.; Chiti, F. ACS Chem. Biol. 2014, 9, 2309-2317 10.1021/cb500505m
12. Ladiwala, A. R. A.; Litt, J.; Kane, R. S.; Aucoin, D. S.; Smith, S. O.; Ranjan, S.; Davis, J.; Van Nostrand, W. E.; Tessier, P. M. J. Biol. Chem. 2012, 287, 24765-24773 10.1074/jbc.M111.329763
13. Ono, K.; Condron, M. M.; Teplow, D. B. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 14745-14750 10.1073/pnas.0905127106
14. Teplow, D. B. Alzheimer's Res. Ther. 2013, 5, 39 10.1186/alzrt203
15. Hayden, E. Y.; Teplow, D. B. Alzheimer's Res. Ther. 2013, 5, 60 10.1186/alzrt226
16. Jakob-Roetne, R.; Jacobsen, H. Angew. Chem. Int. Ed. 2009, 48, 3030-3059 10.1002/anie.200802808
17. Meisl, G.; Yang, X.; Hellstrand, E.; Frohm, B.; Kirkegaard, J. B.; Cohen, S. I.; Dobson, C. M.; Linse, S.; Knowles, T. P. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 9384-9389 10.1073/pnas.1401564111
18. Pujol-Pina, R.; Vilaprinyó-Pascual, S.; Mazzucato, R.; Arcella, A.; Vilaseca, M.; Orozco, M.; Carulla, N. Sci. Rep. 2015, 5, 10489 10.1038/srep14809
19. Bitan, G.; Kirkitadze, M. D.; Lomakin, A.; Vollers, S. S.; Benedek, G. B.; Teplow, D. B. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 330-335 10.1073/pnas.222681699
20. Bernstein, S. L.; Dupuis, N. F.; Lazo, N. D.; Wyttenbach, T.; Condron, M. M.; Bitan, G.; Teplow, D. B.; Shea, J.-E.; Ruotolo, B. T.; Robinson, C. V.; Bowers, M. T. Nat. Chem. 2009, 1, 326-331 10.1038/nchem.247
21. Tarus, B.; Tran, T. T.; Nasica-Labouze, J.; Sterpone, F.; Nguyen, P. H.; Derreumaux, P. J. Phys. Chem. B 2015, 119, 10478-10487 10.1021/acs.jpcb.5b05593
22. Zhang, T.; Zhang, J.; Derreumaux, P.; Mu, Y. J. Phys. Chem. B 2013, 117, 3993-4002 10.1021/jp312573y
23. Man, V. H.; Nguyen, P. H.; Derreumaux, P. J. Phys. Chem. B 2017, 121, 5977-5987 10.1021/acs.jpcb.7b04689
24. Das, P.; Chacko, A. R.; Belfort, G. ACS Chem. Neurosci. 2017, 8, 606-618 10.1021/acschemneuro.6b00357
25. Urbanc, B.; Cruz, L.; Yun, S.; Buldyrev, S. V.; Bitan, G.; Teplow, D. B.; Stanley, H. E. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 17345-17350 10.1073/pnas.0408153101
26. Urbanc, B.; Betnel, M.; Cruz, L.; Bitan, G.; Teplow, D. B. J. Am. Chem. Soc. 2010, 132, 4266-4280 10.1021/ja9096303
27. Riccardi, L.; Nguyen, P. H.; Stock, G. J. Chem. Theory Comput. 2012, 8, 1471-1479 10.1021/ct200911w
28. Barz, B.; Wales, D. J.; Strodel, B. J. Phys. Chem. B 2014, 118, 1003-1011 10.1021/jp412648u
29. Barz, B.; Olubiyi, O. O.; Strodel, B. Chem. Commun. 2014, 50, 5373-5375 10.1039/C3CC48704K
30. Liao, Q.; Owen, M. C.; Olubiyi, O. O.; Barz, B.; Strodel, B. Isr. J. Chem. 2017, 57, 771-784 10.1002/ijch.201600108
31. Chiricotto, M.; Melchionna, S.; Derreumaux, P.; Sterpone, F. J. Chem. Phys. 2016, 145, 035102 10.1063/1.4958323
32. Kotler, S. A.; Brender, J. R.; Vivekanandan, S.; Suzuki, Y.; Yamamoto, K.; Monette, M.; Krishnamoorthy, J.; Walsh, P.; Cauble, M.; Holl, M. M. B.; Marsh, E. N. G.; Ramamoorthy, A. Sci. Rep. 2015, 5, 11811 10.1038/srep11811
33. Ahmed, M.; Davis, J.; Aucoin, D.; Sato, T.; Ahuja, S.; Aimoto, S.; Elliott, J. I.; Van Nostrand, W. E.; Smith, S. O. Nat. Struct. Mol. Biol. 2010, 17, 561-567 10.1038/nsmb.1799
34. Kłoniecki, M.; Jabłonowska, A.; Poznański, J.; Langridge, J.; Hughes, C.; Campuzano, I.; Giles, K.; Dadlez, M. J. Mol. Biol. 2011, 407, 110-124 10.1016/j.jmb.2011.01.012
35. Sitkiewicz, E.; Kłoniecki, M.; Poznański, J.; Bal, W.; Dadlez, M. J. Mol. Biol. 2014, 426, 2871-2885 10.1016/j.jmb.2014.05.015
36. Granata, D.; Baftizadeh, F.; Habchi, J.; Galvagnion, C.; De Simone, A.; Camilloni, C.; Laio, A.; Vendruscolo, M. Sci. Rep. 2015, 5, 15449 10.1038/srep15449
37. Banerjee, S.; Sun, Z.; Hayden, E. Y.; Teplow, D. B.; Lyubchenko, Y. L. ACS Nano 2017, 11, 12202-12209 10.1021/acsnano.7b05434
38. Nguyen, P. H.; Tarus, B.; Derreumaux, P. J. Phys. Chem. B 2014, 118, 501-510 10.1021/jp4115404
39. Dupuis, N. F.; Wu, C.; Shea, J.-E.; Bowers, M. T. J. Am. Chem. Soc. 2011, 133, 7240-7243 10.1021/ja1081537
40. Phillips, A. S.; Gomes, A. F.; Kalapothakis, J. M. D.; Gillam, J. E.; Gasparavicius, J.; Gozzo, F. C.; Kunath, T.; MacPhee, C.; Barran, P. E. Analyst 2015, 140, 3070-3081 10.1039/C4AN02306D
41. Wolff, M.; Zhang-Haagen, B.; Decker, C.; Barz, B.; Schneider, M.; Biehl, R.; Radulescu, A.; Strodel, B.; Willbold, D.; Nagel-Steger, L. Sci. Rep. 2017, 7, 2493 10.1038/s41598-017-02370-3
42. Emperador, A.; Sfriso, P.; Villarreal, M. A.; Gelpí, J. L.; Orozco, M. J. Chem. Theory Comput. 2015, 11, 5929-5938 10.1021/acs.jctc.5b00660
43. Barz, B.; Urbanc, B. PLoS One 2012, 7, e34345 10.1371/journal.pone.0034345
44. Brown, A.; Bevan, D. Biophys. J. 2016, 111, 937-949 10.1016/j.bpj.2016.08.001
45. Tarus, B.; Straub, J. E.; Thirumalai, D. J. Am. Chem. Soc. 2006, 128, 16159-16168 10.1021/ja064872y
46. Woods, L.; Radford, S.; Ashcroft, A. Biochim. Biophys. Acta, Proteins Proteomics 2013, 1834, 1257-1268 10.1016/j.bbapap.2012.10.002
47. Shvartsburg, A. A.; Jarrold, M. F. Chem. Phys. Lett. 1996, 261, 86-91 10.1016/0009-2614(96)00941-4
48. Mesleh, M. F.; Hunter, J. M.; Shvartsburg, A. A.; Schatz, G. C.; Jarrold, M. F. J. Phys. Chem. 1996, 100, 16082-16086 10.1021/jp961623v
49. Zheng, X.; Liu, D.; Roychaudhuri, R.; Teplow, D. B.; Bowers, M. T. ACS Chem. Neurosci. 2015, 6, 1732-1740 10.1021/acschemneuro.5b00171
50. Chandra, B.; Bhowmik, D.; Maity, B. K.; Mote, K. R.; Dhara, D.; Venkatramani, R.; Maiti, S.; Madhu, P. K. Biophys. J. 2017, 113, 805-816 10.1016/j.bpj.2017.06.068
51. Watanabe-Nakayama, T.; Ono, K.; Itami, M.; Takahashi, R.; Teplow, D. B.; Yamada, M. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 5835-5840 10.1073/pnas.1524807113
52. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
53. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. J. Am. Chem. Soc. 1996, 118, 11225-11236 10.1021/ja9621760
54. Kaminski, G. A.; Friesner, R. A.; Tirado-Rives, J.; Jorgensen, W. L. J. Phys. Chem. B 2001, 105, 6474-6487 10.1021/jp003919d
55. Qiu, D.; Shenkin, P. S.; Hollinger, F. P.; Still, W. C. J. Phys. Chem. A 1997, 101, 3005-3014 10.1021/jp961992r
56. Olubiyi, O. O.; Strodel, B. J. Phys. Chem. B 2012, 116, 3280-3291 10.1021/jp2076337
57. Bussi, G.; Donadio, D.; Parrinello, M. J. Chem. Phys. 2007, 126, 014101 10.1063/1.2408420
58. Feenstra, K. A.; Hess, B.; Berendsen, H. J. C. J. Comput. Chem. 1999, 20, 786-798 10.1002/(SICI)1096-987X(199906)20:8<786::AID-JCC5>3.0.CO;2-B
59. Bastian, M.; Heymann, S.; Jacomy, M. Gephi: An Open Source Software for Exploring and Manipulating Networks. Proceedings of the Third International AAAI Conference on Weblogs and Social Media; Hamilton, M., Ed.; San Jose, CA, May 17-20, 2009; AAAI Press: Menlo Park, CA, 2009.
60. Brandes, U.; Wagner, D. Visone-Analysis and Visualization of Social Networks. Graph Drawing Software; Springer, Berlin, 2003; pp 321-340.
61. Humphrey, W.; Dalke, A.; Schulten, K. J. Mol. Graph. 1996, 14, 33-38 10.1016/0263-7855(96)00018-5