中文
Earlier issues
Announcement
More
Progress in Chemistry 2021, Vol. 33 Issue (10): 1797-1811 DOI: 10.7536/PC200912 Previous Articles   Next Articles

• Review •

Molecular Simulation of the Antifreeze Mechanism of Antifreeze Proteins

Weijia Zhang1, Xueguang Shao1,2(), Wensheng Cai1()   

  1. 1 Research Center for Analytical Sciences, College of Chemistry, Tianjin Key Laboratory of Biosensing and Molecular Recognition, Nankai University,Tianjin 300071, China
    2 State Key Laboratory of Medicinal Chemical Biology, Nankai University,Tianjin 300071, China
  • Received: Revised: Online: Published:
  • Contact: Xueguang Shao, Wensheng Cai
  • Supported by:
    National Natural Science Foundation of China(21773125); National Natural Science Foundation of China(21775076); National Natural Science Foundation of China(22073050); Fundamental Research Funds for the Central Universities, Nankai University(63201043)
Richhtml ( 36 ) PDF ( 541 ) Cited
Export

EndNote

Ris

BibTeX

Antifreeze proteins enable organisms to survive in subzero environments. Owing to this unique property, antifreeze proteins have great potential application in a variety of fields. Antifreeze proteins have been extensively studied, but the antifreeze mechanism is still fragmentary, due to the limitation of experimental means. Molecular dynamics, as a method to simulate the interaction between molecules at the atomic level, has been widely used in the study of the mechanism of antifreeze proteins in recent years. In this paper, the functional and structural characteristics of antifreeze proteins, and the research progress of antifreeze mechanisms are described and reviewed from the perspective of structure. Furthermore, the structural characteristics of 29 wild-type antifreeze proteins with known crystal structure, and the hydrophobicity of the residues distributed on the protein surface and at the ice-binding site are analyzed. Both the affinity of the interaction between hydrophilic residues and water and the specificity of the interaction between hydrophobic residues and ice-like water are found either on the surface or at the ice-binding site of antifreeze proteins. The relationship between the secondary structure, the hydrophobicity of the residues at ice-binding site and the antifreeze activity is discussed. Finally, the mechanisms of antifreeze proteins and the factors affecting the antifreeze activity are discussed from the perspective of structure, and the progress in the design and application of bioinspired antifreeze materials with low toxicity and cost is briefly summarized.

Contents

1 Introduction

2 Functional characteristics of antifreeze proteins

3 Structure and mechanisms of antifreeze proteins

3.1 Fish AFPs

3.2 Insect AFPs

3.3 Plant AFPs

3.4 Microorganism AFPs

3.5 Similarities and differences of antifreeze mechanisms of different antifreeze proteins

3.6 Structural factors affecting antifreeze activity

4 Bioinspired antifreeze materials

5 Conclusion and outlook

Key words: antifreeze proteins, bioinspired antifreeze materials, thermal hysteresis activity, adsorption-inhibition mechanism, ACW mechanism, molecular dynamics simulations
Fig. 1 Schematic representation of ice crystal.(a) Different ice planes of ice crystal, the green area represents the basal plane, the blue area represents the primary prism plane and the purple area represents the pyramidal plane.(b) Ice crystal forms a hexagonal bipyramid shape, when the growth of it in the a-axis direction is inhibited.(c) Ice crystal forms a hexagonal plate shape, when the growth of it in both a-axis and c-axis directions is inhibited
Fig. 2 Schematic representation of functional characteristics.(a) Microorganisms secreted AFPs to maintain a local liquid environment;(b) MpAFP serves to adhere bacteria to ice surfaces
Fig. 3 Schematic representation of adsorption-inhibition mechanism, the green hemispheres represent antifreeze proteins, the cyan pillars represent ice crystals. Free water molecules are not shown
Fig. 4 Schematic representation of antifreeze mechanism.(a) hydrogen bonding hypothesis,(b) hydrophobic effect,(c) ACW mechanism. An example of ice binding site is threonine, the green hemispheres represent antifreeze proteins, the cyan pillars represent ice crystals, the blue spheres represent anchored clathrate water, the black dotted lines represent hydrogen bonds. Free water molecules are not shown
Fig. 5 Schematic representation of “local melting” mechanism, the green hemispheres represent antifreeze proteins, the cyan pillars represent ice crystals, the deep blue area represents supercooled water. Free water molecules are not shown
Fig. 6 Comparison of surface structural characteristics of AFPⅠ(PDB ID: 1WFA) and ubiquitin(PDB ID: 1UBQ)
Fig. 7 Comparison of putative IBSs of(a) Ca2+-independent BrAFP(PDB ID: 2ZIB) and(b) Ca2+-dependent hAFP(PDB ID: 2PY2), the green sphere represents Ca2+ and the yellow dotted line area represents Ca2+-binding loop
Fig. 8 Surface structural characteristics of three AFPⅡ
Fig. 9 Surface structural characteristics of eight AFPⅢ
Fig. 10 Ice-binding sites of two insect AFPs with TxT motifs(PDB ID: 1L0S,1EZG)
Table 1 Summary of structural characteristics, properties and mechanisms of antifreeze proteinsa
Origin and type Structural characteristics PDB ID R1
(%)b		 R2
(%)C		 R3
(%)d		 R4 (%)e Antifreeze Mechnism ref.
Fish AFPⅠ α-helix, 65% alanine 1WFA 68 33 14 0 a hydration mediated AFP
adsorption mechanism/“local
melting” mechanism		 33, 79
AFPⅡ Globular, 2α-helix+2 β-sheet 2ZIB 52 12 24 38 ACW mechanism 84, 88
2PY2 35 41 28 24
6JK4 32 0 26 50
AFPⅢ Globular, no dominant nonpolar
amino acids		 1MSI 31 56 19 0 a hydration mediated AFP
adsorption mechanism		 67, 92, 93, 95
1OPS 32 50 14 0
1UCS 38 56 19 0
1GZI 39 56 19 0
3QF6 27 56 19 0
1HG7 38 56 16 0
4UR4 37 56 15 0
1AME 36 56 16 0
AFPⅣ 4 antiparallel helical bundles, Glu-rich The Adsorption-Inhibition
Hypothesis		 98
AFGP (Ala-Thr-Ala)n with a
disaccharide moiety(Galβ1-
3GalNAcα1-) attached to each Thr residue		 The Adsorption-Inhibition
Hypothesis/Perturbation of Long-
Range Water Dynamics		 17, 29, 31, 34, 35
Insect Polyproline type II 3BOI 34 47 18 7 “local melting” mechanism 104
2PNE 38 47 21 7
β-solenoid, seven coils of
TCTxSxxCxxAx repeats		 1EZG 16 44 14 0 ACW mechanism 28, 76
β-solenoid, flat β-sheet of
Thr-x-Thr motifs		 1EWW 19 27 19 0 16, 69
1L0S 21 20 19 0
1M8N 24 33 16 0

Flat β-solenoid		 4DT5 13 29 20 4
β-solenoid, Thr-rich, Cys- rich 1L1I 15 44 15 0
Plant
Micro-organism		 Bacteria β-solenoid 3ULT 15 50 14 0 ACW mechanism 50
β-solenoid 3P4G 20 5 29 18 ACW mechanism 32
β-solenoid with a triangular cross-section alongside an α-helix 3WP9 21 32 25 10 ACW mechanism 15, 118, 119
4NU2 28 38 16 5
6EIO 32 20 8 10
Fungus β-solenoid with a triangular cross-section alongside an α-helix 3UYU 24 41 22 13 ACW mechanism 14, 51, 120, 121
5B5H 24 48 6 8
6A8K 24 50 10 5
3VN3 25 35 13 12
Ubiquitin Globular 1UBQ 16 41 Non-antifreeze protein(as a reference)
Fig. 11 Ice-binding site of plant AFP(PDB ID: 3ULT). The front is “a” side, and the back is “b” side
Fig. 12 Bioinspired antifreeze materials.(a) different shapes of antifreeze gold colloids[135]. Copyright(2019) American Chemical Society.(b) oxidized quasi-carbon nitride quantum dots OQCNs[136]. Copyright John Wiley & Sons.(c) side and front views of TmAFP, an AFP from insects, and a supramolecular ice growth inhibitor[11], the blue spheres represent the amine groups, the gray part represents the carbon skeleton and the red spheres represent the hydroxyl groups. Copyright 2016, American Chemical Society.(d) schematic of the supramolecular ice growth inhibitors based on self-assembling peptides[137]. Copyright 2019, American Chemical Society
[1]
DeVries A L, Wohlschlag D E. Science, 1969, 163(3871): 1073.

pmid: 5764871
[2]
Marshall C B, Fletcher G L, Davies P L. Nature, 2004, 429(6988): 153.

doi: 10.1038/429153a
[3]
Duman J G. Biochim. Et Biophys. Acta BBA Protein Struct. Mol. Enzymol., 1994, 1206(1): 129.
[4]
Graether S P, Kuiper M J, GagnÉ S M, Walker V K, Jia Z C, Sykes B D, Davies P L. Nature, 2000, 406(6793): 325.

doi: 10.1038/35018610
[5]
Duman J G. J. Exp. Biol., 2015, 218(12): 1846.

doi: 10.1242/jeb.116905
[6]
Li C M, Guo X R, Jia Z C, Xia B, Jin C W. J. Biomol. NMR, 2005, 32(3): 251.

doi: 10.1007/s10858-005-8206-3
[7]
Hakim A, Nguyen J B, Basu K, Zhu D F, Thakral D, Davies P L, Isaacs F J, Modis Y, Meng W Y. J. Biol. Chem., 2013, 288(17): 12295.

doi: 10.1074/jbc.M113.450973
[8]
He Z Y, Liu K, Wang J J. Acc. Chem. Res., 2018, 51(5): 1082.

doi: 10.1021/acs.accounts.7b00528
[9]
Lv J, Song Y L, Jiang L, Wang J J. ACS Nano, 2014, 8(4): 3152.

doi: 10.1021/nn406522n
[10]
Deville S, Viazzi C, Leloup J, Lasalle A, Guizard C, Maire E, Adrien J, Gremillard L. PLoS One, 2011, 6(10): e26474.

doi: 10.1371/journal.pone.0026474
[11]
Drori R, Li C, Hu C H, Raiteri P, Rohl A L, Ward M D, Kahr B. J. Am. Chem. Soc., 2016, 138(40): 13396.

pmid: 27618560
[12]
Sicheri F, Yang D S C. Nature, 1995, 375(6530): 427.

doi: 10.1038/375427a0
[13]
Kwan A H Y, Fairley K, Anderberg P I, Liew C W, Harding M M, Mackay J P. Biochemistry, 2005, 44(6): 1980.

pmid: 15697223
[14]
Lee J H, Park A K, Do H, Park K S, Moh S H, Chi Y M, Kim H J. J. Biol. Chem., 2012, 287(14): 11460.

doi: 10.1074/jbc.M111.331835
[15]
Mangiagalli M, Sarusi G, Kaleda A, Bar Dolev M, Nardone V, Vena V F, Braslavsky I, Lotti M, Nardini M. FEBS J., 2018, 285(9): 1653.

doi: 10.1111/febs.14434 pmid: 29533528
[16]
Zanetti-Polzi L, Biswas A D, Del Galdo S, Barone V, Daidone I. J. Phys. Chem. B, 2019, 123(30): 6474.

doi: 10.1021/acs.jpcb.9b06375
[17]
Meister K, DeVries A L, Bakker H J, Drori R. J. Am. Chem. Soc., 2018, 140(30): 9365.

doi: 10.1021/jacs.8b04966 pmid: 30028137
[18]
Davies P L. Trends Biochem. Sci., 2014, 39(11): 548.

doi: 10.1016/j.tibs.2014.09.005 pmid: 25440715
[19]
Raymond J A, DeVries A L. PNAS, 1977, 74(6): 2589.

pmid: 267952
[20]
Cai W S, Chipot C. Acta Chimica Sin., 2013, 71(2): 159.
( 蔡文生, Chipot Christophe. 化学学报, 2013, 71(2): 159.)
[21]
Zong Z Y, Li Q Y, Hong Z Y, Fu H H, Cai W S, Chipot C, Jiang H F, Zhang D Y, Chen S L, Shao X G. J. Am. Chem. Soc., 2019, 141(36): 14451.

doi: 10.1021/jacs.9b08477
[22]
Liu P, Shao X G, Cai W S. Prog. Chem., 2013, 25(5): 692.
( 刘鹏, 邵学广, 蔡文生. 化学进展, 2013, 25(5): 692.)
[23]
Wang T, Cai W S, Shao X G. Prog. Chem., 2010, 22(5): 803.
( 王腾, 蔡文生, 邵学广. 化学进展, 2010, 22(5): 803.)
[24]
Fu H H, Zhang H, Chen H C, Shao X G, Chipot C, Cai W S. J. Phys. Chem. Lett., 2018, 9(16): 4738.

doi: 10.1021/acs.jpclett.8b01994
[25]
Fu H H, Shao X G, Cai W S, Chipot C. Acc. Chem. Res., 2019, 52(11): 3254.

doi: 10.1021/acs.accounts.9b00473
[26]
Chen H C, Fu H H, Shao X G, Cai W S. Prog. Chem., 2018, 30(7): 921.
( 陈淏川, 付浩浩, 邵学广, 蔡文生. 化学进展, 2018, 30(7): 921.)

doi: 10.7536/PC171026
[27]
Todde G, Hovmöller S, Laaksonen A. J. Phys. Chem. B, 2015, 119(8): 3407.

doi: 10.1021/jp5119713
[28]
Hudait A, Qiu Y Q, Odendahl N, Molinero V. J. Am. Chem. Soc., 2019, 141(19): 7887.

doi: 10.1021/jacs.9b02248 pmid: 31020830
[29]
Mochizuki K, Molinero V. J. Am. Chem. Soc., 2018, 140(14): 4803.

doi: 10.1021/jacs.7b13630 pmid: 29392937
[30]
Kuffel A, Czapiewski D, Zielkiewicz J. J. Chem. Phys., 2014, 141(5): 055103.

doi: 10.1063/1.4891810
[31]
Mallajosyula S S, Vanommeslaeghe K, MacKerell A D. J. Phys. Chem. B, 2014, 118(40): 11696.

doi: 10.1021/jp508128d
[32]
Garnham C P, Campbell R L, Davies P L. PNAS, 2011, 108(18): 7363.

doi: 10.1073/pnas.1100429108
[33]
Calvaresi M, Höfinger S, Zerbetto F. Biomacromolecules, 2012, 13(7): 2046.

doi: 10.1021/bm300366f pmid: 22657839
[34]
Ebbinghaus S, Meister K, Born B, DeVries A L, Gruebele M, Havenith M. J. Am. Chem. Soc., 2010, 132(35): 12210.

doi: 10.1021/ja1051632 pmid: 20712311
[35]
Meister K, Ebbinghaus S, Xu Y, Duman J G, DeVries A, Gruebele M, Leitner D M, Havenith M. PNAS, 2013, 110(5): 1617.

doi: 10.1073/pnas.1214911110 pmid: 23277543
[36]
DeVries A L. Science, 1971, 172(3988): 1152.

pmid: 5574522
[37]
Braslavsky I, Drori R. J. Visualized Exp., 2013, 72: e4189.
[38]
Amornwittawat N, Wang S, Duman J G, Wen X. Biochim. Et Biophys. Acta BBA Proteins Proteom., 2008, 1784(12): 1942.
[39]
Olijve L L C, Meister K, DeVries A L, Duman J G, Guo S Q, Bakker H J, Voets I K. PNAS, 2016, 113(14): 3740.

doi: 10.1073/pnas.1524109113 pmid: 26936953
[40]
Drori R, Celik Y, Davies P L, Braslavsky I. J. R. Soc. Interface, 2014, 11(98): 20140526.

doi: 10.1098/rsif.2014.0526 pmid: 25008081
[41]
Kozuch D J, Stillinger F H, Debenedetti P G. PNAS, 2018, 115(52): 13252.

doi: 10.1073/pnas.1814945115
[42]
Bar Dolev M, Braslavsky I, Davies P L. Annu. Rev. Biochem., 2016, 85(1): 515.

doi: 10.1146/biochem.2016.85.issue-1
[43]
Drori R, Davies P L, Braslavsky I. Langmuir, 2015, 31(21): 5805.

doi: 10.1021/acs.langmuir.5b00345 pmid: 25946514
[44]
Mahatabuddin S, Hanada Y, Nishimiya Y, Miura A, Kondo H, Davies P L, Tsuda S. Sci. Rep., 2017, 7: 42501.

doi: 10.1038/srep42501 pmid: 28211917
[45]
Marshall C B, Daley M E, Graham L A, Sykes B D, Davies P L. FEBS Lett., 2002, 529(2-3): 261.
[46]
Drori R, Davies P L, Braslavsky I. RSC Adv., 2015, 5(11): 7848.

doi: 10.1039/C4RA12638F
[47]
Celik Y, Drori R, Pertaya-Braun N, Altan A, Barton T, Bar-Dolev M, Groisman A, Davies P L, Braslavsky I. PNAS, 2013, 110(4): 1309.

doi: 10.1073/pnas.1213603110
[48]
Jia Z C, Davies P L. Trends Biochem. Sci., 2002, 27(2): 101.

doi: 10.1016/S0968-0004(01)02028-X
[49]
Bar-Dolev M, Celik Y, Wettlaufer J S, Davies P L, Braslavsky I. J. R. Soc. Interface, 2012, 9(77): 3249.

doi: 10.1098/rsif.2012.0388 pmid: 22787007
[50]
Middleton A J, Marshall C B, Faucher F, Bar-Dolev M, Braslavsky I, Campbell R L, Walker V K, Davies P L. J. Mol. Biol., 2012, 416(5): 713.

doi: 10.1016/j.jmb.2012.01.032 pmid: 22306740
[51]
Kondo H, Mochizuki K, Bayer-Giraldi M. Phys. Chem. Chem. Phys., 2018, 20(39): 25295.

doi: 10.1039/C8CP04727H
[52]
Mazur P. Am. J. Physiol., 1984, 247(3): 125.
[53]
Yu S O, Brown A, Middleton A J, Tomczak M M, Walker V K, Davies P L. Cryobiology, 2010, 61(3): 327.

doi: 10.1016/j.cryobiol.2010.10.158
[54]
Budke C, Dreyer A, Jaeger J, Gimpel K, Berkemeier T, Bonin A S, Nagel L, Plattner C, DeVries A L, Sewald N, Koop T. Cryst. Growth Des., 2014, 14(9): 4285.
[55]
Raymond J A, Janech M G, Fritsen C H. J. Phycol., 2009, 45(1): 130.

doi: 10.1111/j.1529-8817.2008.00623.x pmid: 27033652
[56]
Guo S Q, Garnham C P, Whitney J C, Graham L A, Davies P L. PLoS One, 2012, 7(11): e48805.

doi: 10.1371/journal.pone.0048805
[57]
DeVries A L. Annu. Rev. Physiol., 1983, 45(1): 245.

doi: 10.1146/physiol.1983.45.issue-1
[58]
Yang D S C, Sax M, Chakrabartty A, Hew C L. Nature, 1988, 333(6170): 232.

doi: 10.1038/333232a0
[59]
Knight C A, Driggers E, DeVries A L. Biophys. J., 1993, 64(1): 252.

pmid: 8431545
[60]
Zhang W, Laursen R A. J. Biol. Chem., 1998, 273(52): 34806.

pmid: 9857006
[61]
Sönnichsen F D, DeLuca C I, Davies P L, Sykes B D. Structure, 1996, 4(11): 1325.

pmid: 8939756
[62]
Haymet A D J, Ward L G, Harding M M. J. Am. Chem. Soc., 1999, 121(5): 941.

doi: 10.1021/ja9801341
[63]
Baardsnes J, Davies P L. Biochim. Et Biophys. Acta BBA Proteins Proteom., 2002, 1601(1): 49.
[64]
Zhou Y X, Zhang Y, Tan H W, Jia Z C, Chen J G. Chem. J. Chinese U., 2007, 28(03): 144.
( 周艳霞, 张勇, 谭宏伟, 贾宗超, 陈光巨. 高等学校化学学报. 2007, 28(03): 144.)
[65]
Jorov A, Zhorov B S, Yang D S C. Protein Sci., 2004, 13(6): 1524.
[66]
Baardsnes J, Kondejewski L H, Hodges R S, Chao H M, Kay C, Davies P L. FEBS Lett., 1999, 463(1-2): 87.

doi: 10.1016/S0014-5793(99)01499-4
[67]
Yang C, Sharp K A. Biophys. Chem., 2004, 109(1): 137.

doi: 10.1016/j.bpc.2003.10.024
[68]
Yang C, Sharp K A. Proteins, 2005, 59(2): 266.

doi: 10.1002/prot.20429
[69]
Nutt D R, Smith J C. J. Am. Chem. Soc., 2008, 130(39): 13066.

doi: 10.1021/ja8034027
[70]
Midya U S, Bandyopadhyay S. J. Phys. Chem. B, 2014, 118(18): 4743.

doi: 10.1021/jp412528b
[71]
Sharp K A. PNAS, 2011, 108(18): 7281.

doi: 10.1073/pnas.1104618108 pmid: 21518869
[72]
Naullage P M, Lupi L, Molinero V. J. Phys. Chem. C, 2017, 121(48): 26949.

doi: 10.1021/acs.jpcc.7b10265
[73]
Hudait A, Moberg D R, Qiu Y Q, Odendahl N, Paesani F, Molinero V. PNAS, 2018, 115(33): 8266.

doi: 10.1073/pnas.1806996115 pmid: 29987018
[74]
Modig K, Qvist J, Marshall C B, Davies P L, Halle B. Phys. Chem. Chem. Phys., 2010, 12(35): 10189.

doi: 10.1039/c002970j
[75]
Liu K, Wang C, Ma J, Shi G, Yao X, Fang H, Song Y, Wang J. PNAS, 2016, 113(51): 14739.

doi: 10.1073/pnas.1614379114
[76]
Grabowska J, Kuffel A, Zielkiewicz J. J. Phys. Chem. B, 2019, 123(38): 8010.

doi: 10.1021/acs.jpcb.9b05664
[77]
Tien M Z, Meyer A G, Sydykova D K, Spielman S J, Wilke C O. PLoS One, 2013, 8(11): e80635.

doi: 10.1371/journal.pone.0080635
[78]
Knight C A, Cheng C C, DeVries A L. Biophys. J., 1991, 59(2): 409.

pmid: 2009357
[79]
Chakraborty S, Jana B. Phys. Chem. Chem. Phys., 2017, 19(18): 11678.

doi: 10.1039/c7cp00221a pmid: 28435965
[80]
Pertaya N, Marshall C B, DiPrinzio C L, Wilen L, Thomson E S, Wettlaufer J S, Davies P L, Braslavsky I. Biophys. J., 2007, 92(10): 3663.
[81]
Ba Y, Wongskhaluang J, Li J B. J. Am. Chem. Soc., 2003, 125(2): 330.

doi: 10.1021/ja027557u
[82]
Wang C, Liu J J. JIMU, 2019, 50(1): 65.
( 王超, 刘俊杰. 内蒙古大学学报, 2019, 50(1): 65.)
[83]
Shi M H, Liu J J, Zhao X J, Liu J P. JIMU, 2017, 48(5): 515.
( 史明卉, 刘俊杰, 赵雪珺, 刘俊平. 内蒙古大学学报, 2017, 48(5): 515.)
[84]
Arai T, Nishimiya Y, Ohyama Y, Kondo H, Tsuda S. Biomolecules, 2019, 9(5): 162.

doi: 10.3390/biom9050162
[85]
Nishimiya Y, Kondo H, Takamichi M, Sugimoto H, Suzuki M, Miura A, Tsuda S. J. Mol. Biol., 2008, 382(3): 734.
[86]
Ewart K V, Li Z J, Yang D S C, Fletcher G L, Hew C L. Biochemistry, 1998, 37(12): 4080.

pmid: 9521729
[87]
Liu Y, Li Z J, Lin Q S, Kosinski J, Seetharaman J, Bujnicki J M, Sivaraman J, Hew C L. PLoS One, 2007, 2(6): e548.

doi: 10.1371/journal.pone.0000548
[88]
Chakraborty S, Jana B. Metallomics, 2019, 11(8): 1387.

doi: 10.1039/c9mt00100j pmid: 31267120
[89]
Siemer A B, McDermott A E. J. Am. Chem. Soc., 2008, 130(51): 17394.

doi: 10.1021/ja8047893
[90]
Garnham C P, Natarajan A, Middleton A J, Kuiper M J, Braslavsky I, Davies P L. Biochemistry, 2010, 49(42): 9063.

doi: 10.1021/bi100516e
[91]
Garnham C P, Nishimiya Y, Tsuda S, Davies P L. FEBS Lett., 2012, 586(21): 3876.

doi: 10.1016/j.febslet.2012.09.017
[92]
Siemer A B, Huang K Y, McDermott A E. PNAS, 2010, 107(41): 17580.

doi: 10.1073/pnas.1009369107
[93]
Grabowska J, Kuffel A, Zielkiewicz J. J. Chem. Phys., 2016, 145(7): 075101.

doi: 10.1063/1.4961094
[94]
Chakraborty S, Jana B. Phys. Chem. Chem. Phys., 2019, 21(35): 19298.

doi: 10.1039/c9cp03135a pmid: 31451813
[95]
Kumari S, Muthachikavil A V, Tiwari J K, Punnathanam S N. Langmuir, 2020, 36(9): 2439.

doi: 10.1021/acs.langmuir.0c00065
[96]
Deng G, Laursen R A. Biochim. Et Biophys. Acta BBA Protein Struct. Mol. Enzymol., 1998, 1388(2): 305.
[97]
Gauthier S Y, Scotter A J, Lin F H, Baardsnes J, Fletcher G L, Davies P L. Cryobiology, 2008, 57(3): 292.

doi: 10.1016/j.cryobiol.2008.10.122 pmid: 18938150
[98]
Lee J K, Kim H J. Fish. Aquat. Sci., 2016, 19(8): 33.

doi: 10.1186/s41240-016-0033-9
[99]
Tsvetkova N M, Phillips B L, Krishnan V V, Feeney R E, Fink W H, Crowe J H, Risbud S H, Tablin F, Yeh Y. Biophys. J., 2002, 82(1): 464.

doi: 10.1016/S0006-3495(02)75411-8
[100]
Ahmed A I, Yeh Y, Osuga Y Y, Feeney R E. J. Biol. Chem., 1976, 251(10): 3033.

pmid: 5450
[101]
Giubertoni G, Meister K, DeVries A L, Bakker H J. J. Phys. Chem. Lett., 2019, 10(3): 352.

doi: 10.1021/acs.jpclett.8b03468 pmid: 30615465
[102]
Pentelute B L, Gates Z P, Tereshko V, Dashnau J L, Vanderkooi J M, Kossiakoff A A, Kent S B H. J. Am. Chem. Soc., 2008, 130(30): 9695.

doi: 10.1021/ja8013538 pmid: 18598029
[103]
Lin F H, Graham L A, Campbell R L, Davies P L. Biophys. J., 2007, 92(5): 1717.

doi: 10.1529/biophysj.106.093435
[104]
Todde G, Whitman C, Hovmöller S, Laaksonen A. J. Phys. Chem. B, 2014, 118(47): 13527.

doi: 10.1021/jp508992e
[105]
Liou Y C, Tocilj A, Davies P L, Jia Z C. Nature, 2000, 406(6793): 322.

doi: 10.1038/35018604
[106]
Bar M, Celik Y, Fass D, Braslavsky I. Cryst. Growth Des., 2008, 8(8): 2954.

doi: 10.1021/cg800066g
[107]
Lee H. J. Mol. Graph. Model., 2019, 87: 48.
[108]
Midya U S, Bandyopadhyay S. J. Phys. Chem. B, 2018, 122(40): 9389.

doi: 10.1021/acs.jpcb.8b08506
[109]
Hudait A, Odendahl N, Qiu Y Q, Paesani F, Molinero V. J. Am. Chem. Soc., 2018, 140(14): 4905.

doi: 10.1021/jacs.8b01246 pmid: 29564892
[110]
Grabowska J, Kuffel A, Zielkiewicz J. J. Mol. Liq., 2020, 306: 112909.

doi: 10.1016/j.molliq.2020.112909
[111]
Sidebottom C, Buckley S, Pudney P, Twigg S, Jarman C, Holt C, Telford J, McArthur A, Worrall D, Hubbard R, Lillford P. Nature, 2000, 406(6793): 256.

doi: 10.1038/35018639
[112]
Worrall D, Elias L, Ashford D, Smallwood M, Sidebottom C, Lillford P, Telford J, Holt C, Bowles D. Science, 1998, 282(5386): 115.

pmid: 9756474
[113]
Gupta R, Deswal R. PLoS One, 2014, 9(3): e91723.

doi: 10.1371/journal.pone.0091723
[114]
Hon W C, Griffith M, Mlynarz A, Kwok Y C, Yang D S C. Plant Physiol., 1995, 109(3): 879.

pmid: 8552719
[115]
Gupta R, Deswal R. J. Proteome Res., 2012, 11(5): 2684.

doi: 10.1021/pr200944z pmid: 22486727
[116]
Kuiper M J, Davies P L, Walker V K. Biophys. J., 2001, 81(6): 3560.

pmid: 11721016
[117]
Middleton A J, Brown A M, Davies P L, Walker V K. FEBS Lett., 2009, 583(4): 815.

doi: 10.1016/j.febslet.2009.01.035 pmid: 19185572
[118]
Hanada Y, Nishimiya Y, Miura A, Tsuda S, Kondo H. FEBS J., 2014, 281(16): 3576.
[119]
Do H, Kim S-J, Kim H J, Lee J H. Acta Crystallogr., 2014, 70(4): 1061.
[120]
Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham C P, Davies P L, Tsuda S. PNAS, 2012, 109(24): 9360.

doi: 10.1073/pnas.1121607109
[121]
Cheng J, Hanada Y, Miura A, Tsuda S, Kondo H. Biochem. J., 2016, 473(21): 4011.

pmid: 27613857
[122]
Meister K, Strazdaite S, DeVries A L, Lotze S, Olijve L L C, Voets I K, Bakker H J. PNAS, 2014, 111(50): 17732.

doi: 10.1073/pnas.1414188111 pmid: 25468976
[123]
Marks S M, Patel A J. PNAS, 2018, 115(33): 8244.

doi: 10.1073/pnas.1810812115 pmid: 30082393
[124]
Amir G, Rubinsky B, Kassif Y, Horowitz L, Smolinsky A K, Lavee J. Eur. J. Cardio-Thorac. Surg., 2003, 24(2): 292.

doi: 10.1016/S1010-7940(03)00306-3
[125]
Amir G, Rubinsky B, Horowitz L, Miller L, Leor J, Kassif Y, Mishaly D, Smolinsky A K, Lavee J. Ann. Thorac. Surg., 2004, 77(5): 1648.

doi: 10.1016/j.athoracsur.2003.04.004
[126]
Khanna H K, Daggard G E. Plant Cell Rep., 2006, 25(12): 1336.
[127]
Holmberg N, FarrÉs J, Bailey J E, Kallio P T. Gene, 2001, 275(1): 115.

pmid: 11574159
[128]
Graham B, Bailey T L, Healey J R J, Marcellini M, Deville S, Gibson M I. Angew. Chem. Int. Ed., 2017, 56(50): 15941.
[129]
Voets I K. Soft Matter, 2017, 13(28): 4808.

doi: 10.1039/c6sm02867e pmid: 28657626
[130]
Xiang H, Yang X H, Ke L, Hu Y. Int. J. Biol. Macromol., 2020, 153: 661.

doi: S0141-8130(20)30373-1 pmid: 32156540
[131]
Kreder M J, Alvarenga J, Kim P, Aizenberg J. Nat. Rev. Mater., 2016, 1(1): 15503.
[132]
Deller R C, Vatish M, Mitchell D A, Gibson M I. Nat. Commun., 2014, 5: 3244.
[133]
Mizrahy O, Bar-Dolev M, Guy S, Braslavsky I. PLoS One, 2013, 8(3): e59540. DOI: 10.1371/journal.pone.0059540.

doi: 10.1371/journal.pone.0059540
[134]
Bonati L, Zhang Y Y, Parrinello M. PNAS, 2019, 116(36): 17641.

doi: 10.1073/pnas.1907975116 pmid: 31416918
[135]
Lee J, Lee S Y, Lim D K, Ahn D J, Lee S. J. Am. Chem. Soc., 2019, 141(47): 18682.
[136]
Bai G Y, Song Z P, Geng H Y, Gao D, Liu K, Wu S W, Rao W, Guo L Q, Wang J J. Adv. Mater., 2017, 29(28): 1606843.

doi: 10.1002/adma.v29.28
[137]
Xue B, Zhao L S, Qin X H, Qin M, Lai J C, Huang W M, Lei H, Wang J J, Wang W, Li Y, Cao Y. ACS Macro Lett., 2019, 8(10): 1383.

doi: 10.1021/acsmacrolett.9b00610
[138]
Jin S L, Yin L K, Kong B, Wu S W, He Z Y, Xue H, Liu Z, Cheng Q, Zhou X, Wang J J. Sci. China Chem., 2019, 62(7): 909.

doi: 10.1007/s11426-018-9428-4
[139]
Naullage P M, Molinero V. J. Am. Chem. Soc., 2020, 142(9): 4356.

doi: 10.1021/jacs.9b12943
[140]
Dou R M, Chen J, Zhang Y F, Wang X P, Cui D P, Song Y L, Jiang L, Wang J J. ACS Appl. Mater. Interfaces, 2014, 6(10): 6998.

doi: 10.1021/am501252u
[141]
Li S X, Lv R, Yan Z S, Huang F, Zhang X R, Chen G J, Yue T T. ACS Sustainable Chem. Eng., 2020, 8(10): 4256.

doi: 10.1021/acssuschemeng.9b07701
[142]
Qin Q Y, Zhao L S, Liu Z, Liu T, Qu J X, Zhang X W, Li R, Yan L Y, Yan J, Jin S L, Wang J J, Qiao J. ACS Appl. Mater. Interfaces, 2020, 12(16): 18352.
[1] . Theoretical Calculation of Cyclodextrins [J]. Progress in Chemistry, 2010, 22(05): 803-811.