Citation: Qiang Yin, Jing-jing Liu, Meng-ting Tian, Hao Xie, Lei Shen, Tao-lei Sun. Protein Fibrillation in Neurodegenerative Diseases and Its Chiral Interaction with Interfaces[J]. Acta Polymerica Sinica, ;2019, 50(6): 575-587. doi: 10.11777/j.issn1000-3304.2019.18276 shu

Protein Fibrillation in Neurodegenerative Diseases and Its Chiral Interaction with Interfaces

Qiang Yin ¹ ,
Jing-jing Liu ¹ ,
Meng-ting Tian ¹ ,
Hao Xie ¹ ,
Lei Shen ^1,, ,
Tao-lei Sun ^1,2,,

Corresponding author: Lei Shen, leishen@whut.edu.cn Tao-lei Sun, suntl@whut.edu.cn
Received Date: 27 December 2018
Revised Date: 22 January 2019
Available Online: 1 March 2019

A hallmark event of neurodegenerative diseases (NDs) is the misfolding, aggregation and fibrillation of related proteins, namely amyloidosis. For example, amyloid-β (Aβ) and Tau, α-synuclein (α-syn), superoxide dismutase 1 (SOD1) and huntingtin exon 1 (HTTexon1) are tightly linked to Alzheimer’s Disease (AD), Parkinson Disease (PD), Amyotrophic Lateral Sclerosis (ALS) and Huntington ’s Disease (HD), respectively. Plasma membrane plays a crucial role in the pathological processes of NDs, including the production, intracellular diffusion, intercellular transmission, endocytosis and clearance of NDs proteins and the resulting aggregates. Therefore, the interactions between NDs proteins and membrane interfaces significantly influence the protein fibrillation and NDs pathogenesis. Properties of membrane interfaces including amphiphilicity and charge density can influence the adsorption of proteins onto membranes and thus the protein folding and aggregation. As the basic chemical property of plasma membranes, chirality can determine key biophysical interactions. The alternation of molecule chirality can cause entirely different biophysical interactions and thus the biofunctions. From this biomimetic perspective, extensive works have demonstrated that the chirality of interfaces can significantly affect protein-surface interactions and thus the fibrillation processes. This brings us to reconsider the stereoselective interactions between NDs proteins and the chiral moieties on membrane interfaces and their impact during NDs pathogenesis. This review article is aimed to reveal the key role of membrane interfaces in protein fibrillation and discuss the impact of interfaces during NDs pathogenesis. The stereoselective protein-membrane interactions and their effects on protein fibrillation are elucidated from a molecular level. The designs of NDs drugs based on chiral interactions are also discussed. These specific aims will deepen our mechanistic insights into how interfaces affect NDs pathogenesis and facilitate the discovery of effective drugs for preventing protein fibrillation and eventually the cure of NDs.
- Neurodegenerative diseases,
- Protein fibrillation,
- Interface,
- Chirality
1. [1]
  Riek R, Eisenberg D S. Nature, 2016, 539: 227 − 235 doi: 10.1038/nature20416
2. [2]
  Pannee J, Portelius E, Oppermann M, Atkins A, Hornshaw M, Zegers I, Hojrup P, Minthon L, Hansson O, Zetterberg H. Alzeimer’s Dis, 2013, 33: 1021 − 1032 doi: 10.3233/JAD-2012-121471
3. [3]
  Li C Z, Gotz J. Nat Rev Drug Discov, 2017, 16: 863 − 883 doi: 10.1038/nrd.2017.155
4. [4]
  Goedert M. Nat Rev Neurosci, 2001, 2: 492 − 501 doi: 10.1038/35081564
5. [5]
  Ruegsegger C, Maharjan N, Goswami A, Filezac L, Weis J, Troost D, Heller M, Gut H, Saxena S. Acta Neuropathol, 2016, 131: 427 − 451 doi: 10.1007/s00401-015-1510-4
6. [6]
  Ruiz-Arlandis G, Pieri L, Bousset L, Melki R. Neuropathol Appl Neurobiol, 2016, 42: 137 − 152 doi: 10.1111/nan.2016.42.issue-2
7. [7]
  Chiti F, Dobson C M. Annu Rev Biochem, 2006, 75: 333 − 366 doi: 10.1146/annurev.biochem.75.101304.123901
8. [8]
  Goedert M. Science, 2015, 349: 1255555 doi: 10.1126/science.1255555
9. [9]
  Lorenzo A, Yankner B A. Proc Nat Acad Sci USA, 1994, 91: 12243 − 12247 doi: 10.1073/pnas.91.25.12243
10. [10]
  Kayed R, Head E, Thompson J L, McIntire T M, Milton S C, Cotman C W, Glabe C G. Science, 2003, 300: 486 − 489 doi: 10.1126/science.1079469
11. [11]
  Makin S. Nature, 2018, 559: S4 − S7 doi: 10.1038/d41586-018-05719-4
12. [12]
  Butterfield S M, Lashuel H. A, Angew Chem Int Ed, 2010, 49: 5628 − 5654 doi: 10.1002/anie.v49:33
13. [13]
  Shrivastava A N, Aperia A, Melki R, Triller A. Neuron, 2017, 95: 33 − 50 doi: 10.1016/j.neuron.2017.05.026
14. [14]
  Baig A M. ACS Chem Neurosci, 2019, 10: 21 − 24 doi: 10.1021/acschemneuro.8b00409
15. [15]
  Stopschinski B E, Diamond M I. Lancet Neurol, 2017, 16: 323 − 332 doi: 10.1016/S1474-4422(17)30037-6
16. [16]
  Collinge J. Nature, 2016, 539: 217 − 226 doi: 10.1038/nature20415
17. [17]
  LaFerla F M, Green K N, Oddo S. Nat Rev Neurosci, 2007, 8: 499 − 509 doi: 10.1038/nrn2168
18. [18]
  Strooper B D, Karran E. Cell, 2016, 164: 603 − 615 doi: 10.1016/j.cell.2015.12.056
19. [19]
  Matsuzaki K. Biochim Biophys Acta, 2007, 1768: 1935 − 1942 doi: 10.1016/j.bbamem.2007.02.009
20. [20]
  Seubert P, Vigo-Pelfrey C, Esch F, Lee M, Dovey H, Davis D, Schiossmacher M, Whaley J, Swindlehurst C, McCormack R, Wolfert R, Selkoe D, Lieberburg I, Schenk D. Nature, 1992, 359: 325 − 327 doi: 10.1038/359325a0
21. [21]
  Shen L, Adachi T, Vanden Bout D, Zhu X Y. J Am Chem Soc, 2012, 134: 14172 − 14178 doi: 10.1021/ja305398f
22. [22]
  Burke K A, Yates E A, Legleiter J. Front Neurol, 2013, 4: 1 − 17
23. [23]
  Mason S F. Nature, 1984, 311: 19 − 23 doi: 10.1038/311019a0
24. [24]
  Blackmond D G. Cold Spring Harb Perspect Biol, 2010, 2: a002147
25. [25]
  Bada J L. Method Enzymology, 1984, 106: 98 − 115 doi: 10.1016/0076-6879(84)06011-0
26. [26]
  Cintas P. Angew Chem Int Ed, 2002, 41: 1139 − 1145 doi: 10.1002/(ISSN)1521-3773
27. [27]
  Koo E H, Squazzo S L. J Biol Chem, 1994, 269: 17386 − 17389
28. [28]
  Kojro E, Gimpl G, Lammich S, Marz W, Fahrenholz F. Proc Natl Acad Sci USA, 2001, 98: 5815 − 5820 doi: 10.1073/pnas.081612998
29. [29]
  Marquer C, Devauges V, Cossec J C, Liot G, Lecart S, Saudou F, Duyckaerts C, Leveque-Fort S, Potier M C. FASEB J, 2011, 25: 1295 − 1305 doi: 10.1096/fj.10-168633
30. [30]
  Buffone M G, Verstraeten S V, Calamera J C, Doncel G F. J Androl, 2009, 30: 552 − 558 doi: 10.2164/jandrol.108.006551
31. [31]
  Bodovitz S, Klein W L. J Biol Chem, 1996, 271: 4436 − 4440 doi: 10.1074/jbc.271.8.4436
32. [32]
  Thompson A G, Gray E, Heman-Ackah S M, Mager I, Talbot K, Andaloussi, S E, Wood M J, Turner M R. Nat Rev Neurol, 2016, 8: 1 − 12
33. [33]
  Arbor S C, LaFontaine M, Cumbay M. Yale J Biol Med, 2016, 89: 5 − 21
34. [34]
  Bharadwaj P, Solomon T, Malajczuk C J, Mancera R L, Howard M, Arrigan D W M, Newsholme P, Martins R N. Biochim Biophys Acta Biomembr, 2018, 1860: 1639 − 1651 doi: 10.1016/j.bbamem.2018.03.015
35. [35]
  Kayed R, Sokolov Y, Edmonds B, Mclntire T M, Milton S C, Hall J E, Glabe C G. J Biol Chem, 2004, 279: 46363 − 46366 doi: 10.1074/jbc.C400260200
36. [36]
  Aisenbrey C, Borowik T, Bystrom R, Bokvist M, Lindstrom F, Misiak H, Sani M A, Grobner G. Eur Biophys J, 2008, 37: 247 − 255 doi: 10.1007/s00249-007-0237-0
37. [37]
  Ehehalt R, Keller P, Haass C, Thiele C, Simons K. J Cell Biol, 2003, 160: 113 − 123 doi: 10.1083/jcb.200207113
38. [38]
  Riddell D R, Christie G, Hussain I, Dingwall C. Curr Biol, 2001, 11: 1288 − 1293 doi: 10.1016/S0960-9822(01)00394-3
39. [39]
  Rausch J M, Marks J R, Rathinakumar R, Wimley W C. Biochemistry, 2007, 46: 12124 − 12130 doi: 10.1021/bi700978h
40. [40]
  Gonzalez M R, Bischofberger M, Pernot L, van der Goot F G, Freche B. Cell Mol Life Sci, 2008, 65: 493 − 507 doi: 10.1007/s00018-007-7434-y
41. [41]
  Bechinger B, Lohner K. Biochim Biophys Acta Biomembr, 2006, 1758: 1529 − 1539 doi: 10.1016/j.bbamem.2006.07.001
42. [42]
  Danzer K M, Haasen D, Karow A R, Moussaud S, Habeck M, Giese A, Kretzschmar H, Hengerer B, Kostka M. J Neurosci, 2007, 27: 9220 − 9232 doi: 10.1523/JNEUROSCI.2617-07.2007
43. [43]
  Lashuel H A. Sci Aging Konwl Environ, 2005, 38: 28 − 39
44. [44]
  Pearce M M P, Spartz E J, Hong W, Luo L, Kopito R R. Nat Commun, 2015, 6: 6768 doi: 10.1038/ncomms7768
45. [45]
  Wong Y C, Krainc D. Nat Med, 2017, 23: 1 − 13
46. [46]
  Rajendran L, Honsho M, Zahn T R, Keller P, Geiger K D, Verkade P, Simons K. Proc Natl Acad Sci USA, 2006, 103: 11172 − 11177 doi: 10.1073/pnas.0603838103
47. [47]
  Lee H J, Suk J E, Bae E J, Lee S J. Biochem Biophys Res Commun, 2008, 372: 423 − 428 doi: 10.1016/j.bbrc.2008.05.045
48. [48]
  Yuyama K, Sun H, Mitsutake S, Igarashi Y. J Biol Chem, 2012, 287: 10977 − 10989 doi: 10.1074/jbc.M111.324616
49. [49]
  Alvarez-Erviti L, Seow Y, Schapira A H, Gardiner C, Sargent I L, Wood M J A, Cooper J M. Neurobiol Dis, 2011, 42: 360 − 367 doi: 10.1016/j.nbd.2011.01.029
50. [50]
  Saman S, Kim W H, Raya M, Visnick Y, Miro S, Saman S, Jackson B, McKee A C, Alvarez V E, Lee N C Y, Hall G F. J Biol Chem, 2012, 287: 3842 − 3849 doi: 10.1074/jbc.M111.277061
51. [51]
  Asai H, Ikezu S, Tsunoda S, Medalla M, Luebke J, Haydar T, Wolozin B, Kugler S, Ikezu T. Nat Neurosci, 2015, 18: 1584 − 1593 doi: 10.1038/nn.4132
52. [52]
  Munch C, O’Brien J, Bertolotti A. Proc Natl Acad Sci USA, 2011, 108: 3548 − 3553 doi: 10.1073/pnas.1017275108
53. [53]
  Kfoury N, Holmes B B, Jiang H, Holtzman D M, Diamond M I. J Biol Chem, 2012, 287: 19440 − 19451 doi: 10.1074/jbc.M112.346072
54. [54]
  Wegmann S, Nicholls S, Takeda S, Fan Z, Hyman B T. J Neurochem, 2016, 139: 1163 − 1174 doi: 10.1111/jnc.2016.139.issue-6
55. [55]
  Perrais D, Merrifield C J. Develop Cell, 2005, 9: 581 − 592 doi: 10.1016/j.devcel.2005.10.002
56. [56]
  Fiandaca M S, Kapogiannis D, Mapstone M, Boxer A, Eitan E, Schwartz J B, Abner E L, Petersen R C, Federoff H J, Miller B L, Goetzl E J. Alzheimers Dement, 2015, 11: 600 − 607 doi: 10.1016/j.jalz.2014.06.008
57. [57]
  Lobb R J, Becker M, Wen S W, Wong C S F, Wiegmans A P, Leimgruber A, Moller A. J Extracell Vesicles, 2015, 4: 27031 doi: 10.3402/jev.v4.27031
58. [58]
  Marcus M E, Leonard J N. Pharmaceuticals (Basel), 2013, 6: 659 − 680 doi: 10.3390/ph6050659
59. [59]
  Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood M J. Nat Biotechnol, 2011, 29: 341 − 345 doi: 10.1038/nbt.1807
60. [60]
  Wang H Y, Lee D H, D’Andrea M R, Peterson P A, Shank R P, Reitz A B. J Biol Chem, 2000, 275: 5626 − 5632 doi: 10.1074/jbc.275.8.5626
61. [61]
  Nagele R G, D’Andrea M R, Anderson W J, Wang H Y. Neuroscience, 2002, 110: 199 − 211 doi: 10.1016/S0306-4522(01)00460-2
62. [62]
  Kim T, Vidal G S, Djurisic M, William C M, Birnbaum M E, Garcia K C, Hyman B T, Sharz C J. Science, 2013, 341: 1399 − 1404 doi: 10.1126/science.1242077
63. [63]
  Ohnishi T, Yanazawa M, Sasahara T, Kitamura Y, Hiroaki H, Fukazawa Y, Kii I, Nishiyama T, Kakita A, Takeda H. Proc Natl Acad Sci USA, 2015, 112: E4465 − E4474 doi: 10.1073/pnas.1421182112
64. [64]
  Cisse M, Halabisky B, Harris J, Devidze N, Dubal D B, Sun B, Orr A, Lotz G, Kim D H, Hamto P. Nature, 2011, 469: 47 − 52 doi: 10.1038/nature09635
65. [65]
  Snyder E M, Nong Y, Almeida C G, Paul S, Moran T, Choi E Y, Nairn A C, Salter M W, Lombroso P J, Gouras G K, Greengard P. Nat Neurosci, 2005, 8: 1051 − 1058 doi: 10.1038/nn1503
66. [66]
  Lauren J, Gimbel D A, Nygaard H B, Gilbert J W, Strittmatter S M. Nature, 2009, 457: 1128 − 1132 doi: 10.1038/nature07761
67. [67]
  Renner M, Lacor P N, Velasco P T, Xu J, Contractor A, Klein W L, Triller A. Neuron, 2010, 66: 739 − 754 doi: 10.1016/j.neuron.2010.04.029
68. [68]
  Haas L T, Salazar S V, Kostylev M A, Um J W, Kaufman A C, Strittmatter S M. Brain, 2016, 139: 526 − 546 doi: 10.1093/brain/awv356
69. [69]
  Hu N W, Nicoll A J, Zhang D, Mably A J, O’Malley, T, Pirro S A, Terry C, Collinge J, Walsh D M, Rowan M J. Nat Commun, 2014, 5: 3374 doi: 10.1038/ncomms4374
70. [70]
  Gomez-Ramos A, Diaz-Hernandez M, Rubio A, Miras-Portugal M T, Avila J. Mol Cell Neurosci, 2008, 37: 673 − 681 doi: 10.1016/j.mcn.2007.12.010
71. [71]
  Shrivastava A N, Redeker V, Fritz N, Pieri L, Almeida L G, Spolidoro M, Liebmann T, Bousset L, Renner M, Lena C. EMBO J, 2015, 34: 2408 − 2423 doi: 10.15252/embj.201591397
72. [72]
  Mao X, Ou M T, Karuppagounder S S, Kam T I, Yin X, Xiong Y, Ge P, Umanah G E, Brahmachari S, Shin J H. Science, 2016, 353: 3374 doi: 10.1126/science.aah3374
73. [73]
  Bellani S, Mescola A, Ronzitti G, Tsushima H, Tilve S, Canale C, Valtorta F, Chieregatti E. Cell Death Differ, 2014, 21: 1971 − 1983 doi: 10.1038/cdd.2014.111
74. [74]
  Jackson K, Barisone G A, Diaz E, Jin L W, DeCarli C, Despa F. Ann Neurol, 2013, 74: 517 − 526 doi: 10.1002/ana.v74.4
75. [75]
  Bharadwaj P, Wijesekara N, Liyanapathirana M, Newsholme P, Ittner L, Fraser P, Verdile G. J Alzheimers Dis, 2017, 59: 421 − 432 doi: 10.3233/JAD-161192
76. [76]
  Tarasoff-Conway J M, Carare R O, Osorio R S, Glodzik L, Butler T, Fieremans E, Axel L, Rusinek H, Nicholson C, Zlokovic B V, Frangione B, Blennow K, Menard J, Zetterberg H, Wisniewski T, de Leon M J. Nat Rev Neurol, 2015, 11: 457 − 470 doi: 10.1038/nrneurol.2015.119
77. [77]
  Shibata M, Yamada S, Kumar S R, Calero M, Bading J, Frangione B, Holtzman D M, Miller C A, Strickland D K, Ghiso J, Zlokovic B V. J Clin Invest, 2000, 106: 1489 − 1499 doi: 10.1172/JCI10498
78. [78]
  Liu C C, Liu C C, Kanekiyo T, Xu H, Bu G. Nat Rev Neurol, 2013, 9: 106 − 118 doi: 10.1038/nrneurol.2012.263
79. [79]
  Deane R, Du Yan S, Submamaryan R K, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt A M, Armstrong D L, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D, Zlokovic B. Nat Med, 2003, 9: 907 − 913 doi: 10.1038/nm890
80. [80]
  Boland B, Wai H Y, Olga C, Bertrand M, Alexandre H, Erwan B, Olivier R M, Mark J M. Nat Rev Drug Dis, 2018, 17: 660 − 689 doi: 10.1038/nrd.2018.109
81. [81]
  Schilling M A. J Alzheimers Dis, 2016, 51: 961 − 977 doi: 10.3233/JAD-150980
82. [82]
  Duckworth W C, Bennett R G, Hamel F G. Endocr Rev, 1998, 19: 608 − 624
83. [83]
  Del Campo M, Stargardt A, Veerhuis R, Reits E, Teunissen C E. Neurosci Lett, 2015, 589: 47 − 51 doi: 10.1016/j.neulet.2015.01.036
84. [84]
  Xie L, Helmerhorst E, Taddei K, Plewright B, van Bronswijk W, Martins R. J Neurosci, 2002, 22: RC221 − RC226 doi: 10.1523/JNEUROSCI.22-10-j0001.2002
85. [85]
  Perez A, Morelli L, Cresto J C, Castano E M. Neurochem Res, 2000, 25: 247 − 255 doi: 10.1023/A:1007527721160
86. [86]
  Wilkinson K, El Khoury J. Int J Alzheimers Dis, 2012, 2012: 489456
87. [87]
  Sevigny J, Chiao P, Bussiere T, Weinreb P H, Williams L, Maier M, Dunstan R, Salloway S, Chen T, Ling Y, O'Gorman J, Qian F, Arastu M, Li M, Chollate S, Brennan M S, Quintero-Monzon O, Scannevin R H, Moore Arnold H, Engber T, Rhodes K, Ferrero J, Hang Y, Mikulskis A, Grimm J, Hock C, Nitsch R M, Sandrock A. Nature, 2016, 537: 50 − 70 doi: 10.1038/nature19323
88. [88]
  Brandenbury L O, Konrad M, Wruck C J, Koch T, Lucius R, Pufe T. J Neurochem, 2010, 113: 749 − 760 doi: 10.1111/jnc.2010.113.issue-3
89. [89]
  Fujii N, Kaji Y, Fujii N. J Chromatogr B, 2011, 879: 3141 − 3147 doi: 10.1016/j.jchromb.2011.05.051
90. [90]
  Nishikawa, T. J Chromatogr B, 2011, 879: 3169 − 3183 doi: 10.1016/j.jchromb.2011.08.030
91. [91]
  Man E H, Sandhouse M E, Burg J, Fisher G H. Science, 1983, 220: 1407 − 1408 doi: 10.1126/science.6857259
92. [92]
  Wiklund L, Toggenburger G, Cuenod M. Science, 1982, 216: 78 − 80 doi: 10.1126/science.6121375
93. [93]
  Jonhson J W, Ascher P. Nature, 1987, 325: 529 − 530 doi: 10.1038/325529a0
94. [94]
  Suzuki M, Imanishi N, Mita M, Hamase K, Aiso S, Sasabe J. ASN Neuro, 2017, 5: 1 − 10
95. [95]
  Fisher G H, Payan I L, Chou S J, Man E H, Cerwinski S, Martin T, Emory C, Frey W H. Brain Res Bull, 1991, 28: 127 − 131
96. [96]
  Payan I L, Chou S J, Fisher G H, Man E H, Emory C, Frey W H. Neurochem Res, 1992, 17: 187 − 191 doi: 10.1007/BF00966798
97. [97]
  Chouinard M, Gaitan D, Wood P. J Neurochem, 1993, 61: 1561 − 1564 doi: 10.1111/jnc.1993.61.issue-4
98. [98]
  Lowe S L, Bowen D M, Francis P T, Toru M. Neurosci, 1990, 38: 571 − 577 doi: 10.1016/0306-4522(90)90051-5
99. [99]
  Sakai-Kato K, Naito M, Utsunomiya-Tate N. Biochem Biophys Res Commun, 2007, 364: 464 − 469 doi: 10.1016/j.bbrc.2007.10.014
100. [100]
  Oda A, Kobayashi K, Takahashi O. Chem Biodiversity, 2010, 7: 1357 − 1363 doi: 10.1002/cbdv.200900299
101. [101]
  Roher A E, Lowenson J D, Clarke S, Wolkow C, Wang R, Cotter R J, Reardon I M, Zurcher-Neely H A, Heinrikson R L, Ball M J, Greenberg B D. J Biol Chem, 1993, 268: 3072 − 3083
102. [102]
  Wilson C C, Myles D, Ghosh M, Johnson L N, Wang W Q. New J Chem, 2005, 29: 1318 − 1322 doi: 10.1039/b419295h
103. [103]
  Ollivaux C, Soyez D, Toullec J Y. J Peptide Sci, 2014, 20: 595 − 612 doi: 10.1002/psc.v20.8
104. [104]
  Demarchi B, Collins M, Bergstrom E, Dowle A, Penkman K, Thomas-Oates J, Wilson J. Anal Chem, 2013, 85: 5835 − 5842 doi: 10.1021/ac4005869
105. [105]
  Song X, Bao M, Li D, Li Y M. Mech Ageing Dev, 1999, 108: 239 − 251 doi: 10.1016/S0047-6374(99)00022-6
106. [106]
  Wei H F, Li L, Song Q J, Ai H X, Chu J, Li W. Behav Brain Res, 2005, 157: 245 − 251 doi: 10.1016/j.bbr.2004.07.003
107. [107]
  Rehman S U, Shah S A, Ali T, Chung J I, Kim M O. Mol Neurobiol, 2017, 54: 255 − 271 doi: 10.1007/s12035-015-9604-5
108. [108]
  Lu J, Wu D W, Zheng Y L, Hu B, Zhang Z F, Ye Q, Liu C M, Shan Q, Wang Y J. Cereb Cortex, 2010, 20: 2540 − 2548 doi: 10.1093/cercor/bhq002
109. [109]
  Yu Y, Bai F, Liu Y, Yang Y, Yuan Q, Zou D, Qu S, Tian G, Song L, Zhang T, Li S, Liu Y, Wang W, Ren G, Li D. Mol Cell Biochem, 2015, 403: 287 − 299 doi: 10.1007/s11010-015-2358-6
110. [110]
  Qing G Y, Zhao S L, Xiong Y T, Lv Z Y, Jiang F L, Liu Y, Chen H, Zhang M X, Sun T L. J Am Chem Soc, 2014, 136: 10736 − 10742 doi: 10.1021/ja5049626
111. [111]
  Gao G B, Zhang M X, Lu P, Guo G, Wang D, Sun T L. Angew Chem Int Ed, 2015, 54: 2245 − 2250 doi: 10.1002/anie.201410768
112. [112]
  Malishev R, Arad E, Bhunia S K, Shaham-Niv S, Kolusheva S, Gazit E, Jelinek R. Chem Commun, 2018, 54: 7762 − 7767 doi: 10.1039/C8CC03235A
113. [113]
  Wei W, Xu C, Gao N, Ren J S, Qu X G. Chem Sci, 2014, 5: 4367 − 4374 doi: 10.1039/C4SC01386G
114. [114]
  Sen S, DasGupta S, DasGupta S. J Phys Chem C, 2017, 121: 18935 − 18946 doi: 10.1021/acs.jpcc.7b05354
115. [115]
  Wadai H, Yamaguchi K, Takahashi S, Kanno T, Kawai T, Naiki H, Goto Y. Biochemistry, 2005, 44: 157 − 164 doi: 10.1021/bi0485880
116. [116]
  Dutta S, Foley A R, Warner C J A, Zhang X, Rolandi M, Abrams B, Raskatov J A. Angew Chem Int Ed, 2017, 56: 11506 − 11510 doi: 10.1002/anie.201706279
117. [117]
  Chalifour R J, McLaughlin R W, Lavoie L, Morissette C, Tremblay N, Boule M, Sarazin P, Stea D, Lacombe D, Tremblay P, Gervais F. J Biol Chem, 2003, 278: 34874 − 34881 doi: 10.1074/jbc.M212694200
118. [118]
  Wiesehan K, Stohr J, Nagel-Steger L, van Groen T, Riesner D, Willbold D. Protein Eng Des Sel, 2008, 21: 241 − 246 doi: 10.1093/protein/gzm054
119. [119]
  Leithold L H E, Jiang N, Post J, Ziehm T, Schartmann E, Kutzsche J, Jon Shah N, Breitkreutz J, Langen K J, Willuweit A, Willbold D. Pharm Res, 2016, 33: 328 − 336 doi: 10.1007/s11095-015-1791-2
120. [120]
  Guan Y J, Du Z, Gao N, Cao Y, Wang X H, Scott P, Song H L, Ren J S, Qu X G. Sci Adv, 2018, 4: eaao6718 doi: 10.1126/sciadv.aao6718
121. [121]
  Sood A, Abid M, Hailemichael S, Foster M, Török B, Török M. Bioorg Med Chem Lett, 2009, 19: 6931 − 6934 doi: 10.1016/j.bmcl.2009.10.066
122. [122]
  Wang Y X, Zhou L, Wang J, Lin B, Wang X B, Huang X X, Song S J. Bioorg Chem, 2018, 77: 579 − 585 doi: 10.1016/j.bioorg.2018.02.001
123. [123]
  Root-Bernstein R S, Holsworth D D. J Theor Biol, 1998, 190: 107 − 119 doi: 10.1006/jtbi.1997.0544
124. [124]
  Heal J R, Roberts G W, Christie G, Miller A D. ChemBioChem, 2002, 3: 86 − 92 doi: 10.1002/(ISSN)1439-7633
125. [125]
  Evers M M, Toonen L J A, van Roon-Mom W M C. Adv Drug Del Rev, 2015, 87: 90 − 103 doi: 10.1016/j.addr.2015.03.008
126. [126]
  Baker S K, Chen Z L, Norris E H, Revenko A S, MacLeod A R, Strickland S. Proc Natl Acad Sci USA, 2018, 115: E9687 − E9696 doi: 10.1073/pnas.1811172115
127. [127]
  Engel M F M, van den Akker C C, Schleeger M, Velikov K P, Koenderink G H, Bonn M. J Am Chem Soc, 2012, 134: 14781 − 14788 doi: 10.1021/ja3031664
128. [128]
  Galvagnion C. J Parkinson’s Dis, 2017, 7: 433 − 450 doi: 10.3233/JPD-171103
129. [129]
  Yang M, Wang K, Lin J, Wang L, Wei F, Zhu J, Zheng W, Shen L. Langmuir, 2018, 34: 8408 − 8414 doi: 10.1021/acs.langmuir.8b01315
130. [130]
  Ikeda K, Matsuzaki K. Biochem Biophys Res Commun, 2008, 370: 525 − 529 doi: 10.1016/j.bbrc.2008.03.130
131. [131]
  Rangachari V, Dean D N, Rana P, Vaidya A, Ghosh P. Biochim Biophy Acta Biomembr, 2018, 1860: 1652 − 1662 doi: 10.1016/j.bbamem.2018.03.004
132. [132]
  Hong S, Beja-Glasser V F, Nfonoyim B M, Frouin A, Li S, Ramakrishnan S, Merry K M, Shi Q, Rosenthal A, Barres B A. Science, 2016, 352: 712 − 716 doi: 10.1126/science.aad8373
133. [133]
  Liebmann T, Renier N, Bettayeb K, Greengard P, Tessier-Lavigne M, Flajolet M. Cell Rep, 2016, 16: 1138 − 1152 doi: 10.1016/j.celrep.2016.06.060
134. [134]
  Ulmschneider J P, Ulmschneider M B. Acc Chem Res, 2018, 51: 1106 − 1116 doi: 10.1021/acs.accounts.7b00613
135. [135]
  Press-Sandler O, Miller Y. Biochim Biophys Acta Biomembr, 2018, 1860: 1889 − 1905 doi: 10.1016/j.bbamem.2018.03.014
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沈阳化工大学材料科学与工程学院沈阳 110142