Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism

Shukun Li; Rui Chang; Luyang Zhao; Ruirui Xing; Jan C. M. van Hest; Xuehai Yan

doi:10.1038/s41467-023-40897-4

journal article Open Access Aug 26, 2023

Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism

Shukun Li

Nature Communications Vol. 14 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/s41467-023-40897-4

Abstract

Abstract
Two-photon absorption (TPA) fluorescence imaging holds great promise in diagnostics and biomedicine owing to its unparalleled spatiotemporal resolution. However, the adaptability and applicability of currently available TPA probes, which act as a critical element for determining the imaging contrast effect, is severely challenged by limited photo-luminescence in vivo. This is particularly a result of uncontrollable aggregation that causes fluorescence quenching, and inevitable photo-oxidation in harsh physiological milieu, which normally leads to bleaching of the dye. Herein, we describe the remarkably enhanced TPA fluorescence imaging capacity of self-assembling near-infrared (NIR) cyanine dye-based nanoprobes (NPs), which can be explained by a photo-oxidation enhanced emission mechanism. Singlet oxygen generated during photo-oxidation enables chromophore dimerization to form TPA intermediates responsible for enhanced TPA fluorescence emission. The resulting NPs possess uniform size distribution, excellent stability, more favorable TPA cross-section and anti-bleaching ability than a popular TPA probe rhodamine B (RhB). These properties of cyanine dye-based TPA NPs promote their applications in visualizing blood circulation and tumoral accumulation in real-time, even to cellular imaging in vivo. The photo-oxidation enhanced emission mechanism observed in these near-infrared cyanine dye-based nanoaggregates opens an avenue for design and development of more advanced TPA fluorescence probes.

Topics

No keywords indexed for this article. Browse by subject →

References

59

[1]

Zhu, X., Su, Q., Feng, W. & Li, F. Anti-Stokes shift luminescent materials for bio-applications. Chem. Soc. Rev 46, 1025–1039 (2017). 10.1039/c6cs00415f

[2]

Deep tissue two-photon microscopy

Fritjof Helmchen, Winfried Denk

Nature Methods 2005 10.1038/nmeth818

[3]

Bort, G., Gallavardin, T., Ogden, D. & Dalko, P. I. From one-photon to two-photon probes: “caged” compounds, actuators, and photoswitches. Angew. Chem. Int. Ed. 52, 4526–4537 (2013). 10.1002/anie.201204203

[4]

Olesiak-Banska, J., Waszkielewicz, M., Obstarczyk, P. & Samoc, M. Two-photon absorption and photoluminescence of colloidal gold nanoparticles and nanoclusters. Chem. Soc. Rev. 48, 4087–4117 (2019). 10.1039/c8cs00849c

[5]

Cahalan, M. D., Parker, I., Wei, S. H. & Miller, M. J. Two-photon tissue imaging: seeing the immune system in a fresh light. Nat. Rev. Immunol. 2, 872–880 (2002). 10.1038/nri935

[6]

Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice

Weijian Zong, Mingli Li, Yanhui Hu et al.

Nature Methods 2017 10.1038/nmeth.4305

[7]

Fan, J. L. et al. High-speed volumetric two-photon fluorescence imaging of neurovascular dynamics. Nat. Commun. 11, 6020 (2020).

[8]

Pawlicki, M., Collins, H. A., Denning, R. G. & Anderson, H. L. Two-photon absorption and the design of two-photon dyes. Angew. Chem. Int. Ed. 48, 3244–3266 (2009). 10.1002/anie.200805257

[9]

Wang, X. et al. Observation of acetylcholinesterase in stress-induced depression phenotypes by two-photon fluorescence imaging in the mouse brain. J. Am. Chem. Soc. 141, 2061–2068 (2019). 10.1021/jacs.8b11414

[10]

Kim, H. M. & Cho, B. R. Small-molecule two-photon probes for bioimaging applications. Chem. Rev. 115, 5014–5055 (2015). 10.1021/cr5004425

[11]

Ceroni, P. Energy up-conversion by low-power excitation: new applications of an old concept. Chem. Eur. J. 17, 9560–9564 (2011). 10.1002/chem.201101102

[12]

Albota, M. et al. Design of organic molecules with large two-photon absorption cross sections. Science 281, 1653–1656 (1998). 10.1126/science.281.5383.1653

[13]

Li, Y. Y. et al. ACQ-to-AIE Transformation: Tuning molecular packing by regioisomerization for two-photon NIR bioimaging. Angew. Chem. Int. Ed. 59, 12822–12826 (2020). 10.1002/anie.202005785

[14]

Zhou, L. Y. et al. Molecular engineering of a TBET-based two-photon fluorescent probe for ratiometric imaging of living cells and tissues. J. Am. Chem. Soc. 136, 9838–9841 (2014). 10.1021/ja504015t

[15]

Furey, B. J. et al. Measurement of two-photon absorption of silicon nanocrystals in colloidal suspension for bio-imaging applications. Phys. Satus Solidi B 255, 1700501 (2018). 10.1002/pssb.201700501

[16]

Two-photon absorption properties of fluorescent proteins

Mikhail Drobizhev, Nikolay S Makarov, Shane E Tillo et al.

Nature Methods 2011 10.1038/nmeth.1596

[17]

Lv, Y. L. et al. Cancer cell membrane-biomimetic nanoprobes with two-photon excitation and near-infrared emission for intravital tumor fluorescence imaging. ACS Nano 12, 1350–1358 (2018). 10.1021/acsnano.7b07716

[18]

Shen, W. et al. A self-quenching system based on bis-naphthalimide: a dual two-photon-channel GSH fluorescent probe. Chem. Asian J. 12, 1532–1537 (2017). 10.1002/asia.201700340

[19]

Two-Photon Induced Photoluminescence and Singlet Oxygen Generation from Aggregated Gold Nanoparticles

Cuifeng Jiang, Tingting Zhao, Peiyan Yuan et al.

ACS Applied Materials & Interfaces 2013 10.1021/am4007403

[20]

Kim, S., Pudavar, H. E., Bonoiu, A. & Prasad, P. N. Aggregation-enhanced fluorescence in organically modified silica nanoparticles: A novel approach toward high-signal-output nanoprobes for two-photon fluorescence bioimaging. Adv. Mater. 19, 3791–3795 (2007). 10.1002/adma.200700098

[21]

Zhang, C. et al. Two-photon supramolecular nanoplatform for ratiometric bioimaging. Anal. Chem. 91, 6371–6377 (2019). 10.1021/acs.analchem.9b01455

[22]

Lu, Q., Wu, C. J., Liu, Z., Niu, G. & Yu, X. Fluorescent AIE-active materials for two-photon bioimaging applications. Front. Chem. 8, 617463 (2020). 10.3389/fchem.2020.617463

[23]

Wang, S., Liu, J., Goh, C. C., Ng, L. G. & Liu, B. NIR-II-excited intravital two-photon microscopy distinguishes deep cerebral and tumor vasculatures with an ultrabright NIR-I AIE luminogen. Adv. Mater. 31, 1904447 (2019). 10.1002/adma.201904447

[24]

Niu, G. L. et al. Functionalized acrylonitriles with aggregation-induced emission: structure tuning by simple reaction-condition variation, efficient red emission, and two-photon bioimaging. J. Am. Chem. Soc. 141, 15111–15120 (2019). 10.1021/jacs.9b06196

[25]

Huang, X. H., Neretina, S. & El-Sayed, M. A. Gold nanorods: from synthesis and properties to biological and biomedical applications. Adv. Mater. 21, 4880–4910 (2009). 10.1002/adma.200802789

[26]

Cao, L. et al. Carbon dots for multiphoton bioimaging. J. Am. Chem. Soc. 129, 11318–11319 (2007). 10.1021/ja073527l

[27]

Kwon, J. et al. FeSe quantum dots for in vivo multiphoton biomedical imaging. Sci. Adv. 5, eaay0044 (2019). 10.1126/sciadv.aay0044

[28]

Giant nonreciprocal second-harmonic generation from antiferromagnetic bilayer CrI3

Zeyuan Sun, Yangfan Yi, Tiancheng Song et al.

Nature 2019 10.1038/s41586-019-1445-3

[29]

Kim, D. et al. Two-photon in vivo imaging with porous silicon nanoparticles. Adv. Mater. 29, 1703309 (2017). 10.1002/adma.201703309

[30]

Mishra, A., Behera, R. K., Behera, P. K., Mishra, B. K. & Behera, G. B. Cyanines during the 1990s: A review. Chem. Rev. 100, 1973–2011 (2000). 10.1021/cr990402t

[31]

Shindy, H. A. Fundamentals in the chemistry of cyanine dyes: A review. Dyes Pigm. 145, 505–513 (2017). 10.1016/j.dyepig.2017.06.029

[32]

Albert, I. D. L., Marks, T. J. & Ratner, M. A. Rational design of molecules with large hyperpolarizabilities. Electric field, solvent polarity, and bond length alternation effects on merocyanine dye linear and nonlinear optical properties. J. Phys. Chem. 100, 9714–9725 (1996). 10.1021/jp960860v

[33]

Beverina, L. et al. Second harmonic generation in nonsymmetrical squaraines: tuning of the directional charge transfer character in highly delocalized dyes. J. Mater. Chem. B 19, 8190–8197 (2009). 10.1039/b914716k

[34]

Srinivas, N., Rao, S. V. & Rao, D. N. Saturable and reverse saturable absorption of rhodamine B in methanol and water. J. Opt. Soc. Am. B-Opt. Phys. 20, 2470–2479 (2003). 10.1364/josab.20.002470

[35]

Fan, Z., Sun, L. M., Huang, Y. J., Wang, Y. Z. & Zhang, M. J. Bioinspired fluorescent dipeptide nanoparticles for targeted cancer cell imaging and real-time monitoring of drug release. Nat. Nanotechnol. 11, 388–394 (2016). 10.1038/nnano.2015.312

[36]

Zou, Q. L. et al. Biological photothermal nanodots based on self-assembly of peptide-porphyrin conjugates for antitumor therapy. J. Am. Chem. Soc. 139, 1921–1927 (2017). 10.1021/jacs.6b11382

[37]

Hamley, I. W. Small bioactive peptides for biomaterials design and therapeutics. Chem. Rev. 117, 14015–14041 (2017). 10.1021/acs.chemrev.7b00522

[38]

Yuan, C. et al. Nucleation and growth of amino acid and peptide supramolecular polymers through liquid-liquid phase separation. Angew. Chem. Int. Ed. 58, 18116–18123 (2019). 10.1002/anie.201911782

[39]

Li, S. et al. Smart Peptide-Based Supramolecular Photodynamic Metallo-nanodrugs designed by multicomponent coordination self-assembly. J. Am. Chem. Soc. 140, 10794–10802 (2018). 10.1021/jacs.8b04912

[40]

Tao, K. et al. Quantum confined peptide assemblies with tunable visible to near-infrared spectral range. Nat. Commun. 9, 3217 (2018).

[41]

Sun, L. J. et al. Intermolecular charge-transfer interactions facilitate two-photon absorption in styrylpyridine–tetracyanobenzene cocrystals. Angew. Chem. Int. Ed. 56, 7831–7835 (2017). 10.1002/anie.201703439

[42]

Li, L. et al. Recent advances in the development of near-infrared organic photothermal agents. Chem. Eng. J. 417, 128844 (2021). 10.1016/j.cej.2021.128844

[43]

Abbas, M., Zou, Q., Li, S. & Yan, X. Self-assembled peptide- and protein-based nanomaterials for antitumor photodynamic and photothermal therapy. Adv. Mater. 29, 1605021 (2017). 10.1002/adma.201605021

[44]

Durr, N. J. et al. Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods. Nano Lett. 7, 941–945 (2007). 10.1021/nl062962v

[45]

Sun, C. L. et al. Rational design of small indolic squaraine dyes with large two-photon absorption cross section. Chem. Sci. 6, 761–769 (2015). 10.1039/c4sc02165g

[46]

Lion, Y., Delmelle, M. & Vandevorst, A. New method of detecting singlet oxygen production. Nature 263, 442–443 (1976). 10.1038/263442a0

[47]

Jung, B. S. & Anvari, B. Synthesis and characterization of bovine serum albumin-coated nanocapsules loaded with indocyanine green as potential multifunctional nanoconstructs. Biotechnol. Prog. 28, 533–539 (2012). 10.1002/btpr.732

[48]

Engel, E. et al. Light-induced decomposition of indocyanine green. Invest. Ophthalmol. Vis. Sci. 49, 1777–1783 (2008). 10.1167/iovs.07-0911

[49]

Rüttger, F., Mindt, S., Golz, C., Alcarazo, M. & John, M. Isomerization and dimerization of indocyanine green and a related heptamethine dye. Eur. J. Org. Chem. 2019, 4791–4796 (2019). 10.1002/ejoc.201900715

[50]

Zhao, L. Y., Liu, Y., Xing, R. & Yan, X. Supramolecular photothermal effects: a promising mechanism for efficient thermal conversion. Angew. Chem. Int. Ed. 59, 3793–3801 (2020). 10.1002/anie.201909825

Showing 50 of 59 references

Metrics

56

Citations

59

References

Details

Published: Aug 26, 2023
Vol/Issue: 14(1)
License: View

Authors

Peking University

State Key Laboratory of Biochemical Engineering; Institute of Process Engineering; Chinese Academy of Sciences; 100190 Beijing; China

Cite This Article

Shukun Li, Rui Chang, Luyang Zhao, et al. (2023). Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism. Nature Communications, 14(1). https://doi.org/10.1038/s41467-023-40897-4

Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism

You May Also Like