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Research Article

Assembly of highly efficient aqueous light-harvesting system from sequence-defined peptoids for cytosolic microRNA detection

Yang Song1,2Xiaoli Cai1Mingming Wang2Dan Du1Yuehe Lin1( )Chun-Long Chen2,3( )
Department of Mechanical and Materials Engineering, Washington State University, Pullman, WA 99164, USA
Division of Physical Sciences, Pacific Northwest National Laboratory, Richland, WA 99352, USA
Department of Chemical Engineering, University of Washington, Seattle, WA 98195, USA
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Graphical Abstract

Self-assembly of sequence-defined peptoids into crystalline nanotubes enabled the creation of a highly efficient artificial light-harvesting system that can sensitively detect microRNA within cells.

Abstract

Precisely controlled spatial distributions of artificial light-harvesting systems in aqueous media are of significant importance for mimicking natural light-harvesting systems; however, they are often restrained by the solubility and the aggregation-caused quenching effect of the hydrophobic chromophores. Herein, we report one highly efficient artificial light-harvesting system based on peptoid nanotubes that mimic the hierarchical cylindrical structure of natural systems. The high crystallinity of these nanotubes enabled the organization of arrays of donor chromophores with precisely controlled spatial distributions, favoring an efficient Förster resonance energy transfer (FRET) process in aqueous media. This FRET system exhibits an extremely high efficiency of 98.6% with a fluorescence quantum yield of 40% and an antenna effect of 29.9. We further demonstrated the use of this artificial light-harvesting system for quantifying miR-210 within cancer cells. The fluorescence intensity ratio of donor to acceptor is linearly related to the concentration of intercellular miR-210 in the range of 3.3–156 copies/cell. Such high sensitivity in intracellular detection of miR-210 using this artificial light-harvesting system offers a great opportunity and pathways for biological imaging and detection, and for the further creation of microRNA (miRNA) toolbox for quantitative epigenetics and personalized medicine.

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References

[1]

McDermott, G.; Prince, S. M.; Freer, A. A.; Hawthornthwaite-Lawless, A. M.; Papiz, M. Z.; Cogdell, R. J.; Isaacs, N. W. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 1995, 374, 517–521.

[2]

Huh, J.; Saikin, S. K.; Brookes, J. C.; Valleau, S.; Fujita, T.; Aspuru-Guzik, A. Atomistic study of energy funneling in the light-harvesting complex of green sulfur bacteria. J. Am. Chem. Soc. 2014, 136, 2048–2057.

[3]

Hu, X. C.; Damjanović, A.; Ritz, T.; Schulten, K. Architecture and mechanism of the light-harvesting apparatus of purple bacteria. Proc. Natl. Acad. Sci. USA 1998, 95, 5935–5941.

[4]

Scholes, G. D.; Fleming, G. R.; Olaya-Castro, A.; van Grondelle, R. Lessons from nature about solar light harvesting. Nat. Chem. 2011, 3, 763–774.

[5]

Chmeliov, J.; Trinkunas, G.; van Amerongen, H.; Valkunas, L. Light harvesting in a fluctuating antenna. J. Am. Chem. Soc. 2014, 136, 8963–8972.

[6]

Tian, Y. X.; Camacho, R.; Thomsson, D.; Reus, M.; Holzwarth, A. R.; Scheblykin, I. G. Organization of bacteriochlorophylls in individual chlorosomes from Chlorobaculum tepidum studied by 2-dimensional polarization fluorescence microscopy. J. Am. Chem. Soc. 2011, 133, 17192–17199.

[7]

Dostál, J.; Mančal, T.; Augulis, R. N.; Vácha, F.; Pšenčík, J.; Zigmantas, D. Two-dimensional electronic spectroscopy reveals ultrafast energy diffusion in chlorosomes. J. Am. Chem. Soc. 2012, 134, 11611–11617.

[8]

Malý, P.; Gruber, J. M.; Cogdell, R. J.; Mančal, T.; van Grondelle, R. Ultrafast energy relaxation in single light-harvesting complexes. Proc. Natl. Acad. Sci. USA 2016, 113, 2934–2939.

[9]

Li, J. J.; Chen, Y.; Yu, J.; Cheng, N.; Liu, Y. A supramolecular artificial light-harvesting system with an ultrahigh antenna effect. Adv. Mater. 2017, 29, 1701905.

[10]

Winiger, C. B.; Li, S. G.; Kumar, G. R.; Langenegger, S. M.; Häner, R. Long-distance electronic energy transfer in light-harvesting supramolecular polymers. Angew. Chem., Int. Ed. 2014, 53, 13609–13613.

[11]

Choi, M. S.; Yamazaki, T.; Yamazaki, I.; Aida, T. Bioinspired molecular design of light-harvesting multiporphyrin arrays. Angew. Chem., Int. Ed. 2003, 43, 150–158.

[12]

Chen, P. Z.; Weng, Y. X.; Niu, L. Y.; Chen, Y. Z.; Wu, L. Z.; Tung, C. H.; Yang, Q. Z. Light-harvesting systems based on organic nanocrystals to mimic chlorosomes. Angew. Chem., Int. Ed. 2016, 55, 2759–2763.

[13]

Wang, J.; Liu, K.; Xing, R. R.; Yan, X. H. Peptide self-assembly: Thermodynamics and kinetics. Chem. Soc. Rev. 2016, 45, 5589–5604.

[14]

Levin, A.; Hakala, T. A.; Schnaider, L.; Bernardes, G. J. L.; Gazit, E.; Knowles, T. P. J. Biomimetic peptide self-assembly for functional materials. Nat. Rev. Chem. 2020, 4, 615–634.

[15]

De Santis, E.; Ryadnov, M. G. Peptide self-assembly for nanomaterials: The old new kid on the block. Chem. Soc. Rev. 2015, 44, 8288–8300.

[16]

Shao, L.; Ma, J. R.; Prelesnik, J. L.; Zhou, Y. C.; Nguyen, M.; Zhao, M. F.; Jenekhe, S. A.; Kalinin, S. V.; Ferguson, A. L.; Pfaendtner, J. et al. Hierarchical materials from high information content macromolecular building blocks: Construction, dynamic interventions, and prediction. Chem. Rev. 2022, 122, 17397–17478.

[17]

Song, Q.; Goia, S.; Yang, J.; Hall, S. C. L.; Staniforth, M.; Stavros, V. G.; Perrier, S. Efficient artificial light-harvesting system based on supramolecular peptide nanotubes in water. J. Am. Chem. Soc. 2021, 143, 382–389.

[18]

Zou, Q. L.; Liu, K.; Abbas, M.; Yan, X. H. Peptide-modulated self-assembly of chromophores toward biomimetic light-harvesting nanoarchitectonics. Adv. Mater. 2016, 28, 1031–1043.

[19]

Li, Z. L.; Cai, B.; Yang, W. C.; Chen, C. L. Hierarchical nanomaterials assembled from peptoids and other sequence-defined synthetic polymers. Chem. Rev. 2021, 121, 14031–14087.

[20]

Cai, B.; Li, Z. L.; Chen, C. L. Programming amphiphilic peptoid oligomers for hierarchical assembly and inorganic crystallization. Acc. Chem. Res. 2021, 54, 81–91.

[21]

Jiao, F.; Wu, X. P.; Jian, T. Y.; Zhang, S.; Jin, H. B.; He, P. G.; Chen, C. L.; De Yoreo, J. J. Hierarchical assembly of peptoid-based cylindrical micelles exhibiting efficient resonance energy transfer in aqueous solution. Angew. Chem., Int. Ed. 2019, 58, 12223–12230.

[22]

Wang, M. M.; Song, Y.; Zhang, S.; Zhang, X.; Cai, X. L.; Lin, Y. H.; De Yoreo, J. J.; Chen, C. L. Programmable two-dimensional nanocrystals assembled from POSS-containing peptoids as efficient artificial light-harvesting systems. Sci. Adv. 2021, 7, eabg1448.

[23]

Capretti, A.; Ringsmuth, A. K.; van Velzen, J. F.; Rosnik, A.; Croce, R.; Gregorkiewicz, T. Nanophotonics of higher-plant photosynthetic membranes. Light: Sci. Appl. 2019, 8, 5.

[24]

Ruban, A. V.; Johnson, M. P.; Duffy, C. D. P. Natural light harvesting: Principles and environmental trends. Energy Environ. Sci. 2011, 4, 1643–1650.

[25]

Mirkovic, T.; Ostroumov, E. E.; Anna, J. M.; van Grondelle, R.; Govindjee; Scholes, G. D. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem. Rev. 2017, 117, 249–293.

[26]

Leishman, C. W.; McHale, J. L. Light-harvesting properties and morphology of porphyrin nanostructures depend on ionic species inducing aggregation. J. Phys. Chem. C 2015, 119, 28167–28181.

[27]

Eisele, D. M.; Cone, C. W.; Bloemsma, E. A.; Vlaming, S. M.; van der Kwaak, C. G. F.; Silbey, R. J.; Bawendi, M. G.; Knoester, J.; Rabe, J. P.; Vanden Bout, D. A. Utilizing redox-chemistry to elucidate the nature of exciton transitions in supramolecular dye nanotubes. Nat. Chem. 2012, 4, 655–662.

[28]

Zhang, D. P.; Liu, Y. N.; Fan, Y. J.; Yu, C. Y.; Zheng, Y. L.; Jin, H. B.; Fu, L.; Zhou, Y. F.; Yan, D. Y. Hierarchical self-assembly of a dandelion-like supramolecular polymer into nanotubes for use as highly efficient aqueous light-harvesting systems. Adv. Funct. Mater. 2016, 26, 7652–7661.

[29]

Wang, K. Y.; Velmurugan, K.; Li, B.; Hu, X. Y. Artificial light-harvesting systems based on macrocycle-assisted supramolecular assembly in aqueous media. Chem. Commun. 2021, 57, 13641–13654.

[30]

Löhner, A.; Kunsel, T.; Röhr, M. I. S.; Jansen, T. L. C.; Sengupta, S.; Würthner, F.; Knoester, J.; Köhler, J. Spectral and structural variations of biomimetic light-harvesting nanotubes. J. Phys. Chem. Lett. 2019, 10, 2715–2724.

[31]

Li, Z. L.; Tran, D. K.; Nguyen, M.; Jian, T. Y.; Yan, F.; Jenekhe, S. A.; Chen, C. L. Amphiphilic peptoid-directed assembly of oligoanilines into highly crystalline conducting nanotubes. Macromol. Rapid Commun. 2022, 43, 2100639.

[32]

Cai, X. L.; Wang, M. M.; Mu, P.; Jian, T. Y.; Liu, D.; Ding, S. C.; Luo, Y. N.; Du, D.; Song, Y.; Chen, C. L. et al. Sequence-defined nanotubes assembled from IR780-conjugated peptoids for chemophototherapy of malignant glioma. Research 2021, 2021, 9861384.

[33]

Luo, Y. N.; Song, Y.; Wang, M. M.; Jian, T. Y.; Ding, S. C.; Mu, P.; Liao, Z. H.; Shi, Q. R.; Cai, X. L.; Jin, H. B. et al. Bioinspired peptoid nanotubes for targeted tumor cell imaging and chemo-photodynamic therapy. Small 2019, 15, 1902485.

[34]

Jin, H. B.; Jian, T. Y.; Ding, Y. H.; Chen, Y. L.; Mu, P.; Wang, L.; Chen, C. L. Solid-phase synthesis of three-armed star-shaped peptoids and their hierarchical self-assembly. Biopolymers 2019, 110, e23258.

[35]

Jin, H. B.; Ding, Y. H.; Wang, M. M.; Song, Y.; Liao, Z. H.; Newcomb, C. J.; Wu, X. P.; Tang, X. Q.; Li, Z.; Lin, Y. H. et al. Designable and dynamic single-walled stiff nanotubes assembled from sequence-defined peptoids. Nat. Commun. 2018, 9, 270.

[36]

Sun, J.; Jiang, X.; Lund, R.; Downing, K. H.; Balsara, N. P.; Zuckermann, R. N. Self-assembly of crystalline nanotubes from monodisperse amphiphilic diblock copolypeptoid tiles. Proc. Natl. Acad. Sci. USA 2016, 113, 3954–3959.

[37]

Sun, Y. S.; Rombola, C.; Jyothikumar, V.; Periasamy, A. Förster resonance energy transfer microscopy and spectroscopy for localizing protein–protein interactions in living cells. Cytom. Part A 2013, 83, 780–793.

[38]

Ge, J.; Hu, Y.; Deng, R. J.; Li, Z. H.; Zhang, K. X.; Shi, M. L.; Yang, D.; Cai, R.; Tan, W. H. Highly sensitive microRNA detection by coupling nicking-enhanced rolling circle amplification with MoS2 quantum dots. Anal. Chem. 2020, 92, 13588–13594.

[39]

Li, J. X.; Cai, R.; Tan, W. H. A novel ECL sensing system for ultrahigh sensitivity miRNA-21 detection based on catalytic hairpin assembly cascade nonmetallic SPR effect. Anal. Chem. 2022, 94, 12280–12285.

[40]

Wang, F. T.; Cai, R.; Tan, W. H. Self-powered biosensor for a highly efficient and ultrasensitive dual-biomarker assay. Anal. Chem. 2023, 95, 6046–6052.

[41]

Wang, F. T.; Hou, Y. Y.; Tan, X. C.; Huang, K. J.; Xu, J.; Cai, R. Real-time multiple signal amplification self-powered biosensing platform for ultrasensitive detection of microRNA. Biosens. Bioelectron. 2023, 222, 114933.

[42]

Wang, F. T.; Yang, H. F.; Wu, J. W.; Lyu, Y. F.; Huang, K. J.; Cai, R.; Tan, W. H. An “on–off” self-powered biosensor via GOD activated signal transduction for ultrasensitive detection of multiple biomarkers. Chem. Eng. J. 2023, 468, 143732.

[43]

Jian, T. Y.; Zhou, Y. C.; Wang, P. P.; Yang, W. C.; Mu, P.; Zhang, X.; Zhang, X.; Chen, C. L. Highly stable and tunable peptoid/hemin enzymatic mimetics with natural peroxidase-like activities. Nat. Commun. 2022, 13, 3025.

[44]
Cai, Y. P.; Zhang, H. X.; Xu, A. W.; Su, C. Y.; Chen, C. L.; Liu, H. Q.; Zhang, L.; Kang, B. S. Self-assembly of silver(I) polymers with single strand double-helical structures containing the ligand O,O′-bis(8-quinolyl)-1,8-dioxaoctane. J. Chem. Soc., Dalton Trans., in press, https://doi.org/10.1039/B102525M.
[45]

Chen, C. L.; Tan, H. Y.; Yao, J. H.; Wan, Y. Q.; Su, C. Y. Disilver(I) rectangular-shaped metallacycles: X-ray crystal structure and dynamic behavior in solution. Inorg. Chem. 2005, 44, 8510–8520.

[46]

Chen, C. L.; Beatty, A. M. Guest inclusion and structural dynamics in 2D hydrogen-bonded metal-organic frameworks. J. Am. Chem. Soc. 2008, 130, 17222–17223.

[47]

Guy, J.; Caron, K.; Dufresne, S.; Michnick, S. W.; Skene; Keillor, J. W. Convergent preparation and photophysical characterization of dimaleimide dansyl fluorogens:  Elucidation of the maleimide fluorescence quenching mechanism. J. Am. Chem. Soc. 2007, 129, 11969–11977.

[48]

Chen, Z. J.; Lohr, A.; Saha-Möller, C. R.; Würthner, F. Self-assembled π-stacks of functional dyes in solution: Structural and thermodynamic features. Chem. Soc. Rev. 2009, 38, 564–584.

[49]

Liu, Y. N.; Jin, J. Y.; Deng, H. P.; Li, K.; Zheng, Y. L.; Yu, C. Y.; Zhou, Y. F. Protein-framed multi-porphyrin micelles for a hybrid natural-artificial light-harvesting nanosystem. Angew. Chem., Int. Ed. 2016, 55, 7952–7957.

[50]

Guo, S. W.; Song, Y. S.; He, Y. L.; Hu, X. Y.; Wang, L. Y. Highly efficient artificial light-harvesting systems constructed in aqueous solution based on supramolecular self-assembly. Angew. Chem., Int. Ed. 2018, 57, 3163–3167.

[51]

Sun, G. P.; Qian, W. R.; Jiao, J. M.; Han, T. T.; Shi, Y. K.; Hu, X. Y.; Wang, L. Y. A highly efficient artificial light-harvesting system with two-step sequential energy transfer based on supramolecular self-assembly. J. Mater. Chem. A 2020, 8, 9590–9596.

[52]

Cheng, N.; Song, Y.; Fu, Q. Q.; Du, D.; Luo, Y. B.; Wang, Y.; Xu, W. T.; Lin, Y. H. Aptasensor based on fluorophore-quencher nano-pair and smartphone spectrum reader for on-site quantification of multi-pesticides. Biosens. Bioelectron. 2018, 117, 75–83.

[53]

Li, J.; Wang, J. L.; Liu, S. Y.; Xie, N. L.; Quan, K.; Yang, Y. J.; Yang, X. H.; Huang, J.; Wang, K. M. Amplified FRET nanoflares: An endogenous mRNA-powered nanomachine for intracellular microRNA imaging. Angew. Chem., Int. Ed. 2020, 59, 20104–20111.

[54]

Ye, S. J.; Li, X. X.; Wang, M. L.; Tang, B. Fluorescence and SERS imaging for the simultaneous absolute quantification of multiple miRNAs in living cells. Anal. Chem. 2017, 89, 5124–5130.

[55]

Degliangeli, F.; Kshirsagar, P.; Brunetti, V.; Pompa, P. P.; Fiammengo, R. Absolute and direct microRNA quantification using DNA-gold nanoparticle probes. J. Am. Chem. Soc. 2014, 136, 2264–2267.

[56]

Chan, H. M.; Chan, L. S.; Wong, R. N. S.; Li, H. W. Direct quantification of single-molecules of microRNA by total internal reflection fluorescence microscopy. Anal. Chem. 2010, 82, 6911–6918.

Nano Research
Pages 788-796
Cite this article:
Song Y, Cai X, Wang M, et al. Assembly of highly efficient aqueous light-harvesting system from sequence-defined peptoids for cytosolic microRNA detection. Nano Research, 2024, 17(2): 788-796. https://doi.org/10.1007/s12274-023-6008-0
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Received: 11 May 2023
Revised: 07 July 2023
Accepted: 15 July 2023
Published: 20 August 2023
© Tsinghua University Press 2023
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