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Progress in Chemistry 2022, Vol. 34 Issue (11): 2462-2475 DOI: 10.7536/PC220308 Previous Articles   Next Articles

• Review •

Chemical Construction of Artificial Cells and Their Biomedical Applications

Xueer Cai, Meiling Jian, Shaohong Zhou, Zefeng Wang, Kemin Wang, Jianbo Liu()   

  1. State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Key Laboratory for Bio-Nanotechnology and Molecule Engineering of Hunan Province, Hunan University,Changsha 410082, China
  • Received: Revised: Online: Published:
  • Contact: Jianbo Liu
  • Supported by:
    the National Natural Science Foundation of China(22177032); the Hunan Province Outstanding Youth Fund Project(2021JJ10013)
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Artificial cells are micro-vesicles that are artificially engineered to possess some structures and functions, similar to biological cells. There are two approaches for fabricating artificial cells. The top-down approach mainly makes a kit in biological methods to redesign and modify biological gene sequences to create artificial cells, and the bottom-up approach mainly adopts chemical methods to prepare protocell models from non-living matter. Here we review in detail towards the different chemically constructed artificial cells, including lipid vesicles, proteosomes, polymersomes, coacervate droplets and colloidosomes. Taken together, this minireview unravels an update on recent efforts in biomedical applications of artificial cells over a broad range of analytical sensing, cell structure and function simulation, biological cargo delivery, micro-nano reactors, and disease diagnosis and treatment.

Contents

1 Introduction

2 Construction of artificial cells

2.1 Top-down approach

2.2 Bottom-up approach

3 Classification of chemically constructed artificial cells

3.1 Lipid vesicles

3.2 Proteosomes

3.3 Polymersomes

3.4 Coacervate droplets

3.5 Colloidosomes

4 Biomedical applications of artificial cells

4.1 Simulation of cell structure and function

4.2 Analytical sensing

4.3 Transport of biological carriers

4.4 Micro-reactors

4.5 Diagnosis and treatment of diseases

5 Conclusion and outlook

Key words: artificial cells, bottom-up, chemical construction, biomedical applications
Fig. 1 Types of artificial cells. (a) Lipid vesicles[42]; copyright 2018, Springer Nature. (b) Proteosomes[43]; copyright 2014, American Chemical Society. (c) Polymersomes[44]; copyright 2014, WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim. (d) Coacervate droplets[45]; copyright 2016, The Royal Society of Chemistry. (e) Colloidosomes[46]. Copyright 2002, The American Association for the Advancement of Science
Fig. 2 Existing forms of phospholipid assemblies and their applications. (a) Tubes; (b) cones; (c) bicelles; (d) vesicles; (e) cisternae stacks; (f) artificial cells with functional membranes, phase-separated cytosol, and metabolism process of protein synthesis; (g) the division of artificial cells; (h) Artificial tissues[55]. Copyright 2020, Wiley-VCH GmbH
Fig. 3 Methods for the preparation of multi-chambered vesicles and unilamellar vesicles. (a) Extrusion method; (b) electric field method; (c) droplet transfer formation method between different phases; (d) microfluidic technology[58]. Copyright 2017, American Chemical Society
Fig. 4 Schematic representation of polymerization-induced proteosome formation
Fig. 5 (a) Schematic diagram of polymersomes formed by diblock copolymers and diblock copolymers, triblock copolymers and graft copolymers[67]; Copyright 2018, The Royal Society of Chemistry. (b) Schematic diagram of the chemical structure of maltotriose-b-poly(N-n-propylglycine)block copolymer and self-assembly into solute-permeable vesicles[70]. Copyright 2021, American Chemical Society
Fig. 6 Construction of coacervate droplets. (a) Schematic illustration of the formation of coacervate droplets by mixing polycations and polyanions; (b) example of coacervate droplets formed by pLys and RNA, the right image is a freshly formed coacervate droplet labeled with fluorescein isothiocyanate; (c) schematic illustration of the dynamic compartmentalization of coacervate droplets in response to environmental stimuli[72]. Copyright 2020, AIP Publishing
Fig. 7 Schematic diagram of colloidosomes obtained from emulsion templates by microfluidic technology[77]. Copyright 2008, WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Fig. 8 Self-assemble of DPPC on the surface of coacervate droplets, which resulted in a new model of artificial cells with internal macromolecular crowding with phospholipid bilayer membrane structure, coacervate giant vesicles[83]. Copyright 2021, American Chemical Society
Fig. 9 Gold nanoparticles-mediated fusion of phospholipid vesicles, mimicking the process of cell fusion. (a) Schematic of the AuNP-labelled vesicle; (b) chemical structure of the biotinylated lipid; (c) schematic and fluorescence microscopy image of vesicle interface membrane(VIM) fusion[93]. Copyright 2018, Springer Nature
Fig. 10 Simulation of cell-to-cell interactions. (a) Schematic representation showing peroxidase activity in RBCs. (b) Schematic showing chemical signal transduction between a melittin-functionalized GOx-containing GUV and peroxidase active RBC. (c) Schematic illustration of custom-made acoustic trapping device. (d) Schematic illustrations and representative fluorescence microscopy images of 1D and 2D GUV assemblies[96]. Copyright 2020, WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Fig. 11 Design of a communication path enabling signal amplification between two artificial cell populations. (a) A signaling molecule (AMP) is produced by the sender artificial cell and diffuses to the receiver artificial cell, where it is sensed, processed, and an internal response is generated; (b) signal amplification in the receiver allows long-distance communication despite strong dilution of chemical signals in the external environment[102]. Copyright 2020, Springer Nature
Fig. 12 Cross-linked polymersomes with “boarding gate” and “debarkation gate” can be loaded with biomacromolecules by opening the “boarding gate” at room temperature. They are immobilized in pure water at body temperature and released through the “debarkation gate” under acidic conditions, such as in endosomes at physiological temperatures. Slightly lowering the temperature inside the cell can make the initial “boarding gate” become the second “debarkation gate”, further accelerating the release of biomacromolecules. The color of the bars in the upper right corner represents the different states of the polymersome membrane, depending on the on temperature and pH[110]. Copyright 2018, American Chemical Society
Fig. 13 Design of the micro-nanoreactor. (a) The glucose oxidase (GOx)/horseradish peroxidase (HRP) cascade enzyme reactions were immobilized in the inner and outer chambers of the artificial cell hydrogel particles, respectively, enabling the incompatible cascade reactions to proceed smoothly. (b) Brightfield image of an artificial cellular multi-chambered hydrogel particle[111]. Copyright 2017, Springer Nature
Fig. 14 Construction of biologically derived artificial cells. (a) An artificial cell covered by the membrane of red blood cells. Hemoglobin-containing membrane fragments were extracted from fresh sheep blood by hypotonic hemolysis, followed by addition of positively charged coacervate droplets. The spontaneous assembly of debris on the surface of coacervate droplets leads to the formation of biofilm coatings. (b) The constructed artificial cells exhibited enhanced blood compatibility and glucose oxidase/hemoglobin cascade activity[113]. Copyright 2020, Springer Nature
[1]
Chang T M S. Science, 1964, 146(3643): 524.

doi: 10.1126/science.146.3643.524
[2]
Arriaga L R, Datta S S, Kim S H, Amstad E, Kodger T E, Monroy F, Weitz D A. Small, 2014, 10(5): 950.

doi: 10.1002/smll.201301904 pmid: 24150883
[3]
Booth R, Qiao Y, Li M, Mann S. Angew. Chem. Int. Ed., 2019, 58(27): 9120.

doi: 10.1002/anie.201903756
[4]
Chang H Y, Sheng Y J, Tsao H K. Soft Matter, 2014, 10(34): 6373.

doi: 10.1039/C4SM01092B
[5]
Chen Y A, Scheller R H. Nat. Rev. Mol. Cell Biol., 2001, 2(2): 98.

doi: 10.1038/35052017
[6]
Altamura E, Milano F, Tangorra R R, Trotta M, Omar O H, Stano P, Mavelli F. PNAS, 2017, 114(15): 3837.

doi: 10.1073/pnas.1617593114
[7]
Cape J L, Monnard P A, Boncella J M. Chem. Sci., 2011, 2(4): 661.

doi: 10.1039/c0sc00575d
[8]
Chang T M S. Blood Purif., 2000, 18(2): 91.

doi: 10.1159/000014430
[9]
Chang T M S. Nat. Rev. Drug Discov., 2005, 4(3): 221.

doi: 10.1038/nrd1659
[10]
Chen I A, Salehi-Ashtiani K, Szostak J W. J. Am. Chem. Soc., 2005, 127(38): 13213.

doi: 10.1021/ja051784p
[11]
Gibson D G, Glass J I, Merryman C, Vashee S, Krishnakumar R, Assad-garcia N, Andrews-pfannkoch C, Denisova E A, Young L, Qi Z, Segall-shapiro T H, Calvey C H, Lartigue C, Parmar P P, Hutchison C A, Smith H O, Venter J C, Noskov V N, Chuang R, Algire M A, Benders G A, Montague M G, Ma L I, Moodie M M. Science, 2010, 329(5987): 52.

doi: 10.1126/science.1190719
[12]
Hutchison C A III, Chuang R Y, Noskov V N, Assad-Garcia N, Deerinck T J, Ellisman M H, Gill J, Kannan K, Karas B J, Ma L, Pelletier J F, Qi Z Q, Richter R A, Strychalski E A, Sun L J, Suzuki Y, Tsvetanova B, Wise K S, Smith H O, Glass J I, Merryman C, Gibson D G, Venter J C. Science, 2016, 351(6280): 1414.
[13]
Pelletier J F, Sun L J, Wise K S, Assad-Garcia N, Karas B J, Deerinck T J, Ellisman M H, Mershin A, Gershenfeld N, Chuang R Y, Glass J I, Strychalski E A. Cell, 2021, 184(9): 2430.

doi: 10.1016/j.cell.2021.03.008
[14]
Dora Tang T Y, Rohaida Che Hak C, Thompson A J, Kuimova M K, Williams D S, Perriman A W, Mann S. Nat. Chem., 2014, 6(6): 527.

doi: 10.1038/nchem.1921 pmid: 24848239
[15]
Lu T M, Spruijt E. J. Am. Chem. Soc., 2020, 142(6): 2905.

doi: 10.1021/jacs.9b11468
[16]
Saha B, Chatterjee A, Reja A, Das D. Chem. Commun., 2019, 55(94): 14194.

doi: 10.1039/C9CC07358B
[17]
Donau C, Späth F, Sosson M, Kriebisch B A K, Schnitter F, Tena-solsona M, Kang H, Salibi E, Sattler M, Mutschler H, Boekhoven J. Nat. Chem., 2020, 11(1):5167.
[18]
Olivi L, Berger M, Creyghton R N P, de Franceschi N, Dekker C, Mulder B M, Claassens N J, ten Wolde P R, van der Oost J. Nat. Commun., 2021, 12: 4531.

doi: 10.1038/s41467-021-24772-8
[19]
Salehi-Reyhani A, Ces O, Elani Y. Exp. Biol. Med., 2017, 242(13): 1309.

doi: 10.1177/1535370217711441
[20]
Klammt C, Schwarz D, Eifler N, Engel A, Piehler J, Haase W, Hahn S, Dötsch V, Bernhard F. J. Struct. Biol., 2007, 159(2): 194.

doi: 10.1016/S1047-8477(07)00164-5
[21]
Ishihara G, Goto M, Saeki M, Ito K, Hori T, Kigawa T, Shirouzu M, Yokoyama S. Protein Expr. Purif., 2005, 41(1): 27.

doi: 10.1016/j.pep.2005.01.013
[22]
Elani Y, Trantidou T, Wylie D, Dekker L, Polizzi K, Law R V, Ces O. Sci. Rep., 2018, 8: 4564.

doi: 10.1038/s41598-018-22263-3
[23]
Jayaraman P, Yeoh J W, Jayaraman S, Teh A Y, Zhang J Y, Poh C L. ACS Synth. Biol., 2018, 7(4): 986.

doi: 10.1021/acssynbio.7b00422
[24]
Dupin A, Simmel F C. Nat. Chem., 2019, 11(1): 32.

doi: 10.1038/s41557-018-0174-9
[25]
Casini A, Chang F Y, Eluere R, King A M, Young E M, Dudley Q M, Karim A, Pratt K, Bristol C, Forget A, Ghodasara A, Warden-Rothman R, Gan R, Cristofaro A, Borujeni A E, Ryu M H, Li J, Kwon Y C, Wang H, Tatsis E, Rodriguez-Lopez C, O’Connor S, Medema M H, Fischbach M A, Jewett M C, Voigt C, Gordon D B. J. Am. Chem. Soc., 2018, 140(12): 4302.

doi: 10.1021/jacs.7b13292
[26]
Ishikawa K, Sato K, Shima Y, Urabe I, Yomo T. FEBS Lett., 2004, 576(3): 387.

pmid: 15498568
[27]
Rustad M, Eastlund A, Jardine P, Noireaux V. Synth. Biol., 2018, 3(1): ysy002.

doi: 10.1093/synbio/ysy002
[28]
Elani Y. Biochem. Soc. Trans., 2016, 44(3): 723.

doi: 10.1042/BST20160052
[29]
Martino C, de Mello A J. Interface Focus., 2016, 6(4): 20160011.

doi: 10.1098/rsfs.2016.0011
[30]
Matosevic S, Paegel B M. J. Am. Chem. Soc., 2011, 133(9): 2798.

doi: 10.1021/ja109137s pmid: 21309555
[31]
Matosevic S, Paegel B M. Nat. Chem., 2013, 5(11): 958.

doi: 10.1038/nchem.1765 pmid: 24153375
[32]
Elani Y, Solvas X C I, Edel J B, Law R V, Ces O. Chem. Commun., 2016, 52(35): 5961.

doi: 10.1039/C6CC01434H
[33]
Chen Z W, De Queiros Silveira G, Ma X D, Xie Y S, Wu Y A, Barry E, Rajh T, Fry H C, Laible P D, Rozhkova E A. Angew. Chem. Int. Ed., 2019, 58(15): 4896.

doi: 10.1002/anie.201813963
[34]
Chemin M, Brun P M, Lecommandoux S, Sandre O, Le Meins J F. Soft Matter, 2012, 8(10): 2867.

doi: 10.1039/c2sm07188f
[35]
Cello J, Paul A V, Wimmer E. Science, 2002, 297(5583): 1016.

doi: 10.1126/science.1072266
[36]
Bonnaud C, Monnier C A, Demurtas D, Jud C, Vanhecke D, Montet X, Hovius R, Lattuada M, Rothen-Rutishauser B, Petri-Fink A. ACS Nano, 2014, 8(4): 3451.

doi: 10.1021/nn406349z pmid: 24611878
[37]
Ali S, Bleuel M, Prabhu V M. ACS Macro Lett., 2019, 8(3): 289.

doi: 10.1021/acsmacrolett.8b00952
[38]
Chen Y F, Yuan M, Zhang Y W, Liu S Y, Yang X H, Wang K M, Liu J B. Chem. Sci., 2020, 11(32): 8617.

doi: 10.1039/D0SC03849K
[39]
Huang J, Morin F J, Laaser J E. Macromolecules, 2019, 52(13): 4957.

doi: 10.1021/acs.macromol.9b00036
[40]
Jing H R, Lin Y N, Chang H J, Bai Q W, Liang D H. Langmuir, 2019, 35(16): 5587.

doi: 10.1021/acs.langmuir.9b00470
[41]
Dawson W M, Rhys G G, Woolfson D N. Curr. Opin. Chem. Biol., 2019, 52: 102.

doi: 10.1016/j.cbpa.2019.06.011
[42]
van Nies P, Westerlaken I, Blanken D, Salas M, Mencía M, Danelon C. Nat. Commun., 2018, 9: 1583.

doi: 10.1038/s41467-018-03926-1
[43]
Huang X, Patil A J, Li M, Mann S. J. Am. Chem. Soc., 2014, 136(25): 9225.

doi: 10.1021/ja504213m pmid: 24905973
[44]
Peters R J R W, Marguet M, Marais S, Fraaije M W, Van Hest J C M, Lecommandoux S. Angew. Chem. Int. Ed., 2014, 53(1): 146.

doi: 10.1002/anie.201308141 pmid: 24254810
[45]
Krishna Kumar R, Harniman R L, Patil A J, Mann S. Chem. Sci., 2016, 7(9): 5879.

doi: 10.1039/C6SC00205F
[46]
Dinsmore A D, Hsu M F, Nikolaides M G, Marquez M, Bausch A R, Weitz D A. Science, 2002, 298(5595): 1006.

pmid: 12411700
[47]
Chechetka S A, Yuba eiji, Kono K, Yudasaka M, Bianco A, Miyako E. Angew. Chem. Int. Ed., 2016, 55(22): 6476.

doi: 10.1002/anie.201602453 pmid: 27079747
[48]
Chang T M S. Artif. Organs, 2004, 28(3): 265.

doi: 10.1111/j.1525-1594.2004.47343.x
[49]
Carreras P, Elani Y, Law R V, Brooks N J, Seddon J M, Ces O. Biomicrofluidics, 2015, 9(6): 064121.

doi: 10.1063/1.4938731
[50]
Gao W W, Hu C M J, Fang R H, Zhang L F. J. Mater. Chem. B, 2013, 1(48): 6569.

doi: 10.1039/c3tb21238f
[51]
Dzieciol A J, Mann S. Chem. Soc. Rev., 2012, 41(1): 79.

doi: 10.1039/c1cs15211d pmid: 21952478
[52]
Li Q C, Han X J. iScience, 2018, 8: 138.

doi: 10.1016/j.isci.2018.09.020
[53]
Zong W, Ma S H, Zhang X N, Wang X J, Li Q C, Han X J. J. Am. Chem. Soc., 2017, 139(29): 9955.

doi: 10.1021/jacs.7b04009 pmid: 28677973
[54]
Vance J A, Devaraj N K. J. Am. Chem. Soc., 2021, 143(22): 8223.

doi: 10.1021/jacs.1c03436
[55]
Wang X J, Du H, Wang Z, Mu W, Han X J. Adv. Mater., 2021, 33(6): 2002635.

doi: 10.1002/adma.202002635
[56]
Li C, Li Q C, Wang Z, Han X J. Anal. Chem., 2020, 92(8): 6060.

doi: 10.1021/acs.analchem.0c00430
[57]
Deng N N, Yelleswarapu M, Huck W T S. J. Am. Chem. Soc., 2016, 138(24): 7584.

doi: 10.1021/jacs.6b02107
[58]
Trantidou T, Friddin M, Elani Y, Brooks N J, Law R V, Seddon J M, Ces O. ACS Nano, 2017, 11(7): 6549.

doi: 10.1021/acsnano.7b03245 pmid: 28658575
[59]
Wang X J, Tian L F, Du H, Li M, Mu W, Drinkwater B W, Han X J, Mann S. Chem. Sci., 2019, 10(41): 9446.

doi: 10.1039/C9SC04522H
[60]
Pattni B S, Chupin V V, Torchilin V P. Chem. Rev., 2015, 115(19): 10938.

doi: 10.1021/acs.chemrev.5b00046
[61]
Szostak J W, Mansy S S, Schrum J P, Krishnamurthy M, TobÉ S, Treco D A. Nature, 2008, 454(7200):122.

doi: 10.1038/nature07018
[62]
Zhou J, Wang Q X, Zhang C Y. J. Am. Chem. Soc., 2013, 135(6): 2056.

doi: 10.1021/ja3110329
[63]
Kuan S L, Bergamini F R G, Weil T. Chem. Soc. Rev., 2018, 47(24): 9069.

doi: 10.1039/C8CS00590G
[64]
Liu F, Cai Y Q, Wang H, Yang X L, Zhao H Y. J. Mater. Chem. B, 2021, 9(5): 1406.

doi: 10.1039/D0TB02635B
[65]
Rawlings A E, Bramble J P, Walker R, Bain J, Galloway J M, Staniland S S. PNAS, 2014, 111(45): 16094.

doi: 10.1073/pnas.1409256111 pmid: 25349410
[66]
Huang X, Li M, Green D C, Williams D S, Patil A J, Mann S. Nat. Commun., 2013, 4: 2239.

doi: 10.1038/ncomms3239 pmid: 23896993
[67]
Rideau E, Dimova R, Schwille P, Wurm F R, Landfester K. Chem. Soc. Rev., 2018, 47(23): 8572.

doi: 10.1039/C8CS00162F
[68]
So S, Lodge T P. Langmuir, 2015, 31(1): 594.

doi: 10.1021/la504605e
[69]
Deplazes A, Huppenbauer M. Syst. Synth. Biol., 2009, 3(1/4): 55.

doi: 10.1007/s11693-009-9029-4
[70]
Okuno Y, Nishimura T, Sasaki Y, Akiyoshi K. Biomacromolecules, 2021, 22(7): 3099.

doi: 10.1021/acs.biomac.1c00530
[71]
Valley B, Jing B X, Ferreira M, Zhu Y X. ACS Appl. Mater. Interfaces, 2019, 11(7): 7472.

doi: 10.1021/acsami.8b21674
[72]
Deng N N. Biomicrofluidics, 2020, 14(5): 051301.

doi: 10.1063/5.0023678
[73]
Liu Z, Chen J, Bai Q, Lin Y, Liang D. Langmuir, 2022, 38(20):6425.

doi: 10.1021/acs.langmuir.2c00580
[74]
Love C, Steinkühler J, Gonzales D T, Yandrapalli N, Robinson T, Dimova R, Tang T Y D. Angew. Chem. Int. Ed., 2020, 59(15): 5950.

doi: 10.1002/anie.201914893
[75]
Deng N N, Huck W T S. Angew. Chem. Int. Ed., 2017, 56(33): 9736.

doi: 10.1002/anie.201703145
[76]
Martin N, Tian L F, Spencer D, Coutable-Pennarun A, Anderson J L R, Mann S. Angew. Chem., 2019, 131(41): 14736.

doi: 10.1002/ange.201909228
[77]
Lee D, Weitz D A. Adv. Mater., 2008, 20(18): 3498.

doi: 10.1002/adma.200800918
[78]
Guan B Y, Yu L, Lou X W D. Adv. Mater., 2016, 28(43): 9596.

doi: 10.1002/adma.201603622
[79]
Gao J L, Ma S H, Major D T, Nam K, Pu J Z, Truhlar D G. Chem. Rev., 2006, 106(8): 3188.

doi: 10.1021/cr050293k
[80]
Gardner P M, Winzer K, Davis B G. Nat. Chem., 2009, 1(5): 377.

doi: 10.1038/nchem.296 pmid: 21378891
[81]
Grommet A B, Feller M, Klajn R. Nat. Nanotechnol., 2020, 15(4): 256.

doi: 10.1038/s41565-020-0652-2 pmid: 32303705
[82]
Elani Y. Angew. Chem. Int. Ed., 2021, 60(11): 5602.

doi: 10.1002/anie.202006941
[83]
Zhang Y W, Chen Y F, Yang X H, He X X, Li M, Liu S Y, Wang K M, Liu J B, Mann S. J. Am. Chem. Soc., 2021, 143(7): 2866.

doi: 10.1021/jacs.0c12494
[84]
Granieri L, Baret J C, Griffiths A D, Merten C A. Chem. Biol., 2010, 17(3): 229.
[85]
Diguet A, Yanagisawa M, Liu Y J, Brun E, Abadie S, Rudiuk S, Baigl D. J. Am. Chem. Soc., 2012, 134(10): 4898.

doi: 10.1021/ja211664f
[86]
Kunding A H, Mortensen M W, Christensen S M, Stamou D. Biophys. J., 2008, 95(3): 1176.

doi: 10.1529/biophysj.108.128819
[87]
Patil Y P, Ahluwalia A K, Jadhav S. Chem. Phys. Lipids, 2013, 167/168: 1.

doi: 10.1016/j.chemphyslip.2013.01.003
[88]
Woo Y, Heo Y, Shin K, Yi G R. J. Biomed. Nanotechnol., 2013, 9(4): 610.

doi: 10.1166/jbn.2013.1543
[89]
Buboltz J T, Bwalya C, Williams K, Schutzer M. Langmuir, 2007, 23(24): 11968.

doi: 10.1021/la702490r
[90]
Biner O, Schick T, Müller Y, von Ballmoos C. FEBS Lett., 2016, 590(14): 2051.

doi: 10.1002/1873-3468.12233
[91]
Xu Z, Hueckel T, Irvine W T M, Sacanna S. Nature, 2021, 597(7875): 220.

doi: 10.1038/s41586-021-03774-y
[92]
Damiati S. Macromol. Res., 2020, 28(11): 1046.

doi: 10.1007/s13233-020-8142-9
[93]
Bolognesi G, Friddin M S, Salehi-Reyhani A, Barlow N E, Brooks N J, Ces O, Elani Y. Nat. Commun., 2018, 9: 1882.

doi: 10.1038/s41467-018-04282-w pmid: 29760422
[94]
Ishmukhametov R R, Russell A N, Berry R M. Nat. Commun., 2016, 7: 13025.

doi: 10.1038/ncomms13025 pmid: 27708275
[95]
Qiao Y, Li M, Booth R, Mann S. Nat. Chem., 2017, 9(2): 110.

doi: 10.1038/nchem.2617 pmid: 28282044
[96]
Wang X J, Tian L F, Ren Y S, Zhao Z Y, Du H, Zhang Z Z, Drinkwater B W, Mann S, Han X J. Small, 2020, 16(27): 1906394.

doi: 10.1002/smll.201906394
[97]
Lin C, Zhang Q X, Yeh Y C. Anal. Methods, 2019, 11(10): 1400.

doi: 10.1039/C9AY00070D
[98]
Adamala K P, Martin-Alarcon D A, Guthrie-Honea K R, Boyden E S. Nat. Chem., 2017, 9(5): 431.

doi: 10.1038/nchem.2644
[99]
Lentini R, Santero S P, Chizzolini F, Cecchi D, Fontana J, Marchioretto M, del Bianco C, Terrell J L, Spencer A C, Martini L, Forlin M, Assfalg M, Serra M D, Bentley W E, Mansy S S. Nat. Commun., 2014, 5: 4012.

doi: 10.1038/ncomms5012
[100]
Dwidar M, Seike Y, Kobori S, Whitaker C, Matsuura T, Yokobayashi Y. J. Am. Chem. Soc., 2019, 141(28): 11103.

doi: 10.1021/jacs.9b03300
[101]
Boyd M A, Kamat N P. Trends Biotechnol., 2021, 39(9): 927.

doi: 10.1016/j.tibtech.2020.12.002
[102]
Buddingh B C, Elzinga J, van Hest J C M. Nat. Commun., 2020, 11: 1652.

doi: 10.1038/s41467-020-15482-8
[103]
Hindley J W, Zheleva D G, Elani Y, Charalambous K, Barter L M C, Booth P J, Bevan C L, Law R V, Ces O. PNAS, 2019, 116(34): 16711.

doi: 10.1073/pnas.1903500116 pmid: 31371493
[104]
Zhang Y, Kojima T, Kim G, Mcnerney M P, Takayama S, Styczynski M P. Nat. Chem., 2021, 12(1):5724.
[105]
Kamiya K, Kawano R, Osaki T, Akiyoshi K, Takeuchi S. Nat. Chem., 2016, 8(9): 881.

doi: 10.1038/nchem.2537 pmid: 27554415
[106]
Zou Y, Zheng M, Yang W J, Meng F H, Miyata K, Kim H J, Kataoka K, Zhong Z Y. Adv. Mater., 2017, 29(42): 1703285.

doi: 10.1002/adma.201703285
[107]
Ianeselli A, Tetiker D, Stein J, Kühnlein A, Mast C B, Braun D, Dora Tang T Y. Nat. Chem., 2022, 14(1): 32.

doi: 10.1038/s41557-021-00830-y
[108]
Samanta A, Sabatino V, Ward T R, Walther A. Nat. Nanotechnol., 2020, 15(11): 914.

doi: 10.1038/s41565-020-0761-y
[109]
Gao N, Xu C, Yin Z P, Li M, Mann S. J. Am. Chem. Soc., 2022, 144(9): 3855.

doi: 10.1021/jacs.1c11414
[110]
Wang F, Gao J Y, Xiao J G, Du J Z. Nano Lett., 2018, 18(9): 5562.

doi: 10.1021/acs.nanolett.8b01985
[111]
Tan H L, Guo S, Dinh N D, Luo R C, Jin L, Chen C H. Nat. Commun., 2017, 8: 663.

doi: 10.1038/s41467-017-00757-4
[112]
Bakh N A, Cortinas A B, Weiss M A, Langer R S, Anderson D G, Gu Z, Dutta S, Strano M S. Nat. Chem., 2017, 9(10): 937.

doi: 10.1038/nchem.2857
[113]
Liu S Y, Zhang Y W, Li M, Xiong L, Zhang Z J, Yang X H, He X X, Wang K M, Liu J B, Mann S. Nat. Chem., 2020, 12(12): 1165.

doi: 10.1038/s41557-020-00585-y
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[3] Xiao Xiao, Changsheng Chen, Weiqiang Liu, Yeshun Zhang. Structure, Features and Biomedical Applications of Silk Sericin [J]. Progress in Chemistry, 2017, 29(5): 513-523.
[4] Fu Xianbiao, Yu Guipeng. Covalent Organic Frameworks Catalysts [J]. Progress in Chemistry, 2016, 28(7): 1006-1015.
[5] Wang Jiaojiao, Feng Miao, Zhan Hongbing*. Advances in Preparation of Graphene Quantum Dots [J]. Progress in Chemistry, 2013, 25(01): 86-94.
[6] Du Kai, Zhu Yanhong, Xu Huibi, Yang Xiangliang. Multifunctional Magnetic Nanoparticles: Synthesis, Modification and Biomedical Applications [J]. Progress in Chemistry, 2011, 23(11): 2287-2298.
[7] Huang Yi|Huang Jinhua|Xie Qingji**|Yao Shouzhuo**. Carbohydrate-Protein Interactions [J]. Progress in Chemistry, 2008, 20(06): 942-950.