Engineering Mechanical Strong Biomaterials Inspired by Structural Building Blocks in Nature

Jiahe Li , Chao Ma , Hongjie Zhang , Kai Liu

Chemical Research in Chinese Universities ›› 2023, Vol. 39 ›› Issue (1) : 92 -106.

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Chemical Research in Chinese Universities ›› 2023, Vol. 39 ›› Issue (1) : 92 -106. DOI: 10.1007/s40242-023-2357-1
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Engineering Mechanical Strong Biomaterials Inspired by Structural Building Blocks in Nature

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Abstract

The intricate multiscale architectures in natural structural building blocks provide many sources of inspiration for the designs of artificial biomaterials. In nature, the assembly of highly ordered molecular crystals and amorphous aggregates often derives from inter- and intra-molecular interactions of biomacromolecules, e.g., proteinaceous materials. The structural biomaterials derived from the protein self-assembly behave with remarkable mechanical performance. However, there is still a grand challenge to mimic the mechanical properties of natural protein-based biomaterials in a rational design fashion to yield comparable man-made synthetic ensembles. In this review, a brief perspective on current challenges and advances in terms of bioinspired structural materials is presented. We outline a framework for mimicking protein self-assembly of natural building blocks across multiscale and highlight the critical role of synthetic biology and chemical modifications in material biosynthesis. Particularly, we focus on the design and promising applications of protein-based fibers, adhesives, dynamic hydrogels and engineered living materials, in which natural mechanical functions are effectively reproduced.

Keywords

Bioinspired material / Protein self-assembly / Mechanical property / Synthetic biology / Molecular engineering

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Jiahe Li, Chao Ma, Hongjie Zhang, Kai Liu. Engineering Mechanical Strong Biomaterials Inspired by Structural Building Blocks in Nature. Chemical Research in Chinese Universities, 2023, 39(1): 92-106 DOI:10.1007/s40242-023-2357-1

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References

[1]

Egan P, Sinko R, LeDuc P R, Keten S. Nat. Commun., 2015, 6(1): 1.

[2]

Kono N, Nakamura H, Mori M, Yoshida Y, Ohtoshi R, Malay A D, Moran D A, Tomita M, Numata K, Arakawa K. Proc. Natl. Acad. Sci. USA, 2021, 118(31): e2107065118.

[3]

Almine J F, Bax D V, Mithieux S M, Smith L N, Rnjak J, Waterhouse A, Wise S G, Weiss A S. Chem. Soc. Rev., 2010, 39(9): 3371.

[4]

Yaari A, Schilt Y, Tamburu C, Raviv U, Shoseyov O. ACS Biomater. Sci. Eng., 201, 2(3): 349.

[5]

Lee H, Lee B P, Messersmith P B. Nature, 2007, 448(7151): 338.

[6]

Lee B P, Messersmith P B, Israelachvili J N, Waite J H. Annu. Rev. Mater. Res., 2011, 41: 99.

[7]

Yang B, Jin S, Park Y, Jung Y M, Cha H J. Small, 2018, 14(52): 1803377.

[8]

Wang C S, Stewart R J. Biomacromolecules, 2013, 14(5): 1607.

[9]

Bhagat V, Becker M L. Biomacromolecules, 2017, 18(10): 3009.

[10]

Brennan M J, Kilbride B F, Wilker J J, Liu J C. Biomaterials, 2017, 124: 116.

[11]

Zhong C, Gurry T, Cheng A A, Downey J, Deng Z, Stultz C M, Lu T K. Nat. Nanotechnol., 2014, 9(10): 858.

[12]

Yang B, Ayyadurai N, Yun H, Choi Y S, Hwang B H, Huang J, Lu Q, Zeng H, Cha H J. Angew. Chem. Int. Ed., 2014, 126(49): 13578.

[13]

Muir V G, Burdick J A. Chem. Rev., 2020, 121(18): 10908.

[14]

Xu T, Xu L P, Zhang X, Wang S. Chem. Soc. Rev., 2019, 48(12): 3153.

[15]

Wegst U G, Bai H, Saiz E, Tomsia A P, Ritchie R O. Nat. Mater., 2015, 14(1): 23.

[16]

Sun J, Su J, Ma C, Göstl R, Herrmann A, Liu K, Zhang H. Adv. Mater., 2020, 32(6): 1906360.

[17]

Keten S, Xu Z, Ihle B, Buehler M J. Nat. Mater., 2010, 9(4): 359.

[18]

Zhang S, Chen J, Liu J, Pyles H, Baker D, Chen C L, De Yoreo J J. Adv. Mater., 2021, 33(23): 1905784.

[19]

Tang T C, An B, Huang Y, Vasikaran S, Wang Y, Jiang X, Lu T K, Zhong C. Nat. Rev. Mater., 2021, 6(4): 332.

[20]

McBee R M, Lucht M, Mukhitov N, Richardson M, Srinivasan T, Meng D, Chen H, Kaufman A, Reitman M, Munck C, Schaak D, Voigt C, Wang H H. Nat. Mater., 2022, 21(4): 471.

[21]

Seliktar D. Science, 2012, 336(6085): 1124.

[22]

Becker M L, Burdick J A. Chem. Rev., 2021, 121(18): 10789.

[23]

Kirillova A, Yeazel T R, Asheghali D, Petersen S R, Dort S, Gall K, Becker M L. Chem. Rev., 2021, 121(18): 11238.

[24]

Du X, Zhou J, Shi J, Xu B. Chem. Rev., 2015, 115(24): 13165.

[25]

Liu A P, Appel E A, Ashby P D, Baker B M, Franco E, Gu L, Haynes K, Joshi N S, Kloxin A M, Kouwer P H, Mittal J, Morsut L, Noireaux V, Parekh S, Schulman R, Tang S K, Valentine M T, Vega S L, Weber W, Stephanopoulos N, Chaudhuri O. Nat. Mater., 2022, 21(4): 390.

[26]

Liu K, Cao M, Fujishima A, Jiang L. Chem. Rev., 2014, 114(19): 10044.

[27]

Hofman A H, van Hees I A, Yang J, Kamperman M. Adv. Mater., 2018, 30(19): 1704640.

[28]

Yang K, Guan J, Numata K, Wu C, Wu S, Shao Z, Ritchie R O. Nat. Commun., 2019, 10(1): 1.

[29]

Yarger J L, Cherry B R, Van Der Vaart A. Nat. Rev. Mater., 2018, 3(3): 1.

[30]

Omenetto F G, Kaplan D L. Science, 2010, 329(5991): 528.

[31]

Lv S, Dudek D M, Cao Y, Balamurali M M, Gosline J, Li H. Nature, 2010, 465(7294): 69.

[32]

Shang L, Yu Y, Liu Y, Chen Z, Kong T, Zhao Y. ACS Nano, 2019, 13(3): 2749.

[33]

Park J H, Rutledge G C. Macromolecules, 2017, 50(15): 5627.

[34]

Guo Q, Chen J, Wang J, Zeng H, Yu J. Nanoscale, 2020, 12(3): 1307.

[35]

Wei Z, Yang J H, Zhou J, Xu F, Zrínyi M, Dussault P H, Osada Y, Chen Y M. Chem. Soc. Rev., 2014, 43(23): 8114.

[36]

Lei Z, Wang Q, Sun S, Zhu W, Wu P. Adv. Mater., 2017, 29(22): 1700321.

[37]

Shang L, Zhang W, Xu K, Zhao Y. Mater. Horizons, 2019, 6(5): 945.

[38]

Hoffman A S. Adv. Drug Deliv. Rev., 2012, 64: 18.

[39]

Appel E A, del Barrio J, Loh X J, Scherman O A. Chem. Soc. Rev., 2012, 41(18): 6195.

[40]

Liu M, Wang S, Jiang L. Nat. Rev. Mater., 2017, 2(7): 1.

[41]

Reznikov N, Steele J A M, Fratzl P, Stevens M M. Nat. Rev. Mater., 201, 1(8): 1.

[42]

Rodrigo-Navarro A, Sankaran S, Dalby M J, del Campo A, Salmeron-Sanchez M. Nat. Rev. Mater., 2021, 6(12): 1175.

[43]

Rising A, Johansson J. Nat. Chem. Biol., 2015, 11(5): 309.

[44]

Pena-Francesch A, Jung H, Demirel M C, Sitti M. Nat. Mater., 2020, 19(11): 1230.

[45]

Ritchie R O. Nat. mater., 2011, 10(11): 817.

[46]

Liu X, Shi L, Wan X, Dai B, Chen Y, Wang S. ACS Mater. Lett., 2011, 3(10): 1453.

[47]

Lin S, Ryu S, Tokareva O, Gronau G, Jacobsen M M, Huang W, Rizzo D J, Li D, Staii C, Pugno N M, Wong J Y, Kaplan D L, Buehler M J. Nat. Commun., 2015, 6(1): 1.

[48]

Koeppel A, Holland C. ACS Biomater. Sci. Eng., 2017, 3(3): 226.

[49]

Terpe K. Appl. Microbio. Biotechnol., 200, 72(2): 211.

[50]

Zhu J. Biotechnol. Adv., 2012, 30(5): 1158.

[51]

Jarvis D L. Meth. Enzymol., 2009, 463: 191.

[52]

Sun J, Chen J, Liu K, Zeng H. Engineering, 2021, 7(5): 615.

[53]

Hayashi C Y, Shipley N H, Lewis R V. Int. J. Biol. Macromol., 1999, 24(2/3): 271.

[54]

Hagn F, Eisoldt L, Hardy J G, Vendrely C, Coles M, Scheibel T, Kessler H. Nature, 2010, 465(7295): 239.

[55]

Jung H, Pena-Francesch A, Saadat A, Sebastian A, Kim D H, Hamilton R F, Albert I, Allen B D, Demirel M C. Proc. Natl. Acad. Sci. USA, 201, 113(23): 6478.

[56]

Xia X X, Qian Z G, Ki C S, Park Y H, Kaplan D L, Lee S Y. Proc. Natl. Acad. Sci. USA, 2010, 107(32): 14059.

[57]

Elices M, Plaza G R, Arnedo M A, Pérez-Rigueiro J, Torres F G, Guinea G V. Biomacromolecules, 2009, 10(7): 1904.

[58]

Rosano G L, Ceccarelli E A. Front. Microbiol., 2014, 5: 172.

[59]

Bowen C H, Dai B, Sargent C J, Bai W, Ladiwala P, Feng H, Huang W, Kaplan D L, Galazka J M, Zhang F. Biomacromolecules, 2018, 19(9): 3853.

[60]

Stevens A J, Brown Z Z, Shah N H, Seka G, Cowburn D, Muir T W. J. Am. Chem. Soc., 201, 138(7): 2162.

[61]

Heidebrecht A, Eisoldt L, Diehl J, Schmidt A, Geffers M, Lang G, Scheibel T. Adv. Mater., 2015, 27(13): 2189.

[62]

Saric M, Eisoldt L, Döring V, Scheibel T. Adv. Mater., 2021, 33(9): 2006499.

[63]

Hu C F, Qian Z G, Peng Q, Zhang Y, Xia X X. ACS Biomater. Sci. Eng., 2021, 7(8): 3608.

[64]

Peng Q, Zhang Y, Lu L, Shao H, Qin K, Hu X, Xia X. Sci. Rep., 201, 6(1): 1.

[65]

Zhu H, Sun Y, Yi T, Wang S, Mi J, Meng Q. Biochimie, 2020, 175: 77.

[66]

Li X, Mi J, Wen R, Zhang J, Cai Y, Meng Q, Lin Y. ACS Appl. Bio Mater., 2020, 3(9): 5957.

[67]

Lang G, Grill C, Scheibel T. Angew. Chem. Int. Ed., 2022, 61(11): e202115232.

[68]

Yuan Y, Yu Q, Wen J, Li C, Guo Z, Wang X, Wang N. Angew. Chem. Int. Ed., 2019, 131(34): 11911.

[69]

Yaari A, Schilt Y, Tamburu C, Raviv U, Shoseyov O. ACS Biomater. Sci. Eng., 201, 2(3): 349.

[70]

Zhang J, Sun J, Li B, Yang C, Shen J, Wang N, Gu R, Wang D, Chen D, Hu H, Fan C, Zhang H, Liu K. Small, 2020, 16(8): 1907598.

[71]

Zhang J, Liu Y, Sun J, Gu R, Ma C, Liu K. Mater. Today Adv., 2020, 8: 100095.

[72]

Xu Z, Wu M, Ye Q, Chen D, Liu K, Bai H. Engineering, 2022, 14: 100.

[73]

He H, Yang C, Wang F, Wei Z, Shen J, Chen D, Fan C, Zhang H, Liu K. Angew. Chem. Int. Ed., 2020, 59(11): 4344.

[74]

Su J, Zhao K, Ren Y, Zhao L, Wei B, Liu B, Zhang Y, Wang F, Li J, Liu Y, Liu K, Zhang H. Angew. Chem. Int. Ed., 2022, 134(12): e202117538.

[75]

Ma C, Malessa A, Boersma A J, Liu K, Herrmann A. Adv. Mater., 2020, 32(20): 1905309.

[76]

Li Y, Li J, Sun J, He H, Li B, Ma C, Liu K, Zhang H. Angew. Chem. Int. Ed., 2020, 59(21): 8148.

[77]

Qin G, Hu X, Cebe P, Kaplan D L. Nat. Commun., 2012, 3(1): 1.

[78]

Su J, Liu B, He H, Ma C, Wei B, Li M, Li J, Wang F, Sun J, Liu K, Zhang H. Adv. Mater., 2022, 34(19): 2200842.

[79]

Wan S, Cheng W, Li J, Wang F, Xing X, Sun J, Liu K. Nano Res., 2022, 15(10): 9192.

[80]

Ma C, Su J, Li B, Herrmann A, Zhang H, Liu K. Adv. Mater., 2020, 32(10): 1907697.

[81]

Sun J, Li B, Wang F, Feng J, Ma C, Liu K, Zhang H. CCS Chem., 2021, 3(6): 1669.

[82]

Zhang P., Li J., Sun J., Li Y., Liu K., Wang F., Zhang H., Su J., Adv. Funct. Mater., 2022, 2209006

[83]

Sun J, Ma C, Maity S, Wang F, Zhou Y, Portale G, Göstl R, Roos W H, Zhang H, Liu K, Herrmann A. Angew. Chem. Int. Ed., 2021, 133(6): 3259.

[84]

Du N, Ye F, Sun J, Liu K. ChemBioChem, 2022, 23(6): e202100416.

[85]

Sun J., Zhang J., Zhao L., Wan S., Wu B., Ma C., Li J., Wang F., Xing X., Chen D., Zhang H., Liu K., CCS Chem., 2022, DOI: https://doi.org/10.31635/ccschem.022.202201946

[86]

Ma C, Li B, Shao B, Wu B, Chen D, Su J, Zhang H, Liu K. Angew. Chem. Int. Ed., 2020, 59(48): 21481.

[87]

Waite J H. J. Exp. Biol., 2017, 220(4): 517.

[88]

Shao H, Stewart R J. Adv. Mater., 2010, 22(6): 729.

[89]

Kamino K. Biofouling, 2013, 29(6): 735.

[90]

Sun J, Han J, Wang F, Liu K, Zhang H. Chem. Eur. J., 2022, 28(1): e202102902.

[91]

Zhang C, Wu B, Zhou Y, Zhou F, Liu W, Wang Z. Chem. Soc. Rev., 2020, 49(11): 3605.

[92]

Wijerathne B, Liao T, Ostrikov K, Sun Z. Small Struct., 2022, 3(9): 2100228.

[93]

Deepankumar K, Guo Q, Mohanram H, Lim J, Mu Y, Pervushin K, Yu J, Miserez A. Adv. Mater., 2021, 34(25): 2103828.

[94]

Cui M, Wang X, An B, Zhang C, Gui X, Li K, Li Y, Ge P, Zhang J, Liu C, Zhong C. Sci. Adv., 2019, 5(8): eaax3155.

[95]

Kim E, Jeon J, Zhu Y, Hoppe E D, Jun Y S, Genin G M, Zhang F. ACS Appl. Mater. Inter., 2021, 13(41): 48457.

[96]

Deepankumar K, Lim C, Polte I, Zappone B, Labate C, De Santo M P, Mohanram H, Palaniappan A, Hwang D S, Miserez A. Adv. Funct. Mater., 2020, 30(16): 1907534.

[97]

Sing C E, Perry S L. Soft Matter, 2020, 16(12): 2885.

[98]

Ma C, Sun J, Li B, Feng Y, Sun Y, Xiang L, Xiang L, Wu B, Xiao L, Liu B, Petrovskii V S, Liu B, Zhang J, Wang Z, Li H, Zhang L, Li J, Wang F, Göstl R, Potemkin I I, Chen D, Zeng H, Zhang H, Liu K, Herrmann A. Nat. Commun., 2021, 12(1): 1.

[99]

Sun J, Xiao L, Li B, Zhao K, Wang Z, Zhou Y, Ma C, Li J, Zhang H, Herrmann A, Liu K. Angew. Chem. Int. Ed., 2021, 60(44): 23687.

[100]

Xiao L, Wang Z, Sun Y, Li B, Wu B, Ma C, Petrovskii V S, Gu X, Chen D, Potemkin I I, Herrmann A, Zhang H, Liu K. Angew. Chem. Int. Ed., 2021, 133(21): 12189.

[101]

Wang Z, Gu X, Li B, Li J, Wang F, Sun J, Zhang H, Liu K, Guo W. Adv. Mater., 2022, 34(41): 2204590.

[102]

Zhang J, Li B, Zuo J, Gu R, Liu B, Ma C, Li J, Liu K. Adv. Healthc. Mater., 2021, 10(12): 2100109.

[103]

Zhao K, Liu Y, Ren Y, Li B, Li J, Wang F, Ma C, Ye F, Sun J, Zhang H, Liu K. Angew. Chem. Int. Ed., 2022, 134(33): e202207425.

[104]

Mohammed J S, Murphy W L. Adv. Mater., 2009, 21(23): 2361.

[105]

Wei Z, Yang J H, Zhou J, Xu F, Zrínyi M, Dussault P H, Osada Y, Chen Y M. Chem. Soc. Rev., 2014, 43(23): 8114.

[106]

Zhu M, Liu J, Gan L, Long M. Eur. Polym. J., 2020, 129: 109651.

[107]

Li Z, Zhou Y, Li T, Zhang J, Tian H. View, 2022, 3(2): 20200112.

[108]

Ganewatta M S, Wang Z, Tang C. Nat. Rev. Chem., 2021, 5(11): 753.

[109]

Kim S M, Jeon H, Shin S H, Park S A, Jegal J, Hwang S Y, Oh D X, Park J. Adv. Mater., 2018, 30(1): 1705145.

[110]

Lee S H, Shin S R, Lee D S. Mater. Design, 2019, 172: 107774.

[111]

Tanasi P, Santana M H, Carretero-González J, Verdejo R, López-Manchado M A. Polymer, 2019, 175: 15.

[112]

Deng Z, Yuan S, Xu R X, Liang H, Liu S. Angew. Chem. Int. Ed., 2018, 57(29): 8896.

[113]

Wan X, Liu T, Hu J, Liu S. Macromo. Rapid Comm., 2013, 34(4): 341.

[114]

Hu X, Zhao X, He B, Zhao Z, Zheng Z, Zhang P, Shi X, Kwok R T K, Lam J W Y, Qin A, Tang B. Research, 2018, 2018: 3152870.

[115]

Kord Forooshani P, Lee B P. J. Polym. Sci. Pol. Chem., 2017, 55(1): 9.

[116]

Li L, Yan B, Yang J, Chen L, Zeng H. Adv. Mater., 2015, 27(7): 1294.

[117]

Azevedo S, Costa A M, Andersen A, Choi I S, Birkedal H, Mano J F. Adv. Mater., 2017, 29(28): 1700759.

[118]

Holten-Andersen N, Harrington M J, Birkedal H, Lee B P, Messersmith P B, Lee K Y C, Waite J H. Proc. Natl. Acad. Sci. USA, 2011, 108(7): 2651.

[119]

Schmidt S, Reinecke A, Wojcik F, Pussak D, Hartmann L, Harrington M J. Biomacromolecules, 2014, 15(5): 1644.

[120]

Shi L, Wang F, Zhu W, Xu Z, Fuchs S, Hilborn J, Zhu L, Ma Q, Wang Y, Weng X, Ossipov D A. Adv. Funct. Mater., 2017, 27(37): 1700591.

[121]

Fu F, Chen Z, Zhao Z, Wang H, Shang L, Gu Z, Zhao Y. Proc. Natl. Acad. Sci. USA, 2017, 114(23): 5900.

[122]

Elvin C M, Carr A G, Huson M G, Maxwell J M, Pearson R D, Vuocolo T, Liyou N E, Wang D C C, Merritt D J, Dixon N E. Nature, 2005, 437(7061): 999.

[123]

McGann C L, Akins R E, Kiick K L. Biomacromolecules, 201, 17(1): 128.

[124]

Bing W, Wang H, Tian L, Zhao J, Jin H, Du W, Ren L. Small Struct., 2021, 2(9): 2100079.

[125]

Phillips J W, Prominski A, Tian B. View, 2022, 3(3): 20200157.

[126]

Wang Y, An B, Xue B, Pu J, Zhang X, Huang Y, Yu Y, Cao Y, Zhong C. Nat. Chem. Biol., 2021, 17(3): 351.

[127]

Kang S Y, Pokhrel A, Bratsch S, Benson J J, Seo S O, Quin M B, Aksan A, Schmidt-Dannert C. Nat. Commun., 2021, 12(1): 1.

[128]

Molinari S, Tesoriero R F, Li D, Sridhar S, Cai R, Soman J, Ryan K R, Ashby P D, Ajo-Franklin C M. Nat. Commun., 2022, 13(1): 1.

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