Tetrazine Carbon Nanotubes for Pretargeted In Vivo "Click-to-Release" Bioorthogonal Tumour Imaging

Overview

Journal Angew Chem Int Ed Engl

Specialty Chemistry

Date 2020 Jun 20

PMID 32558207

Citations 19

Authors

He Li

Joao Conde

Ana Guerreiro

Goncalo J L Bernardes

Affiliations

Soon will be listed here.

Abstract

The bioorthogonal inverse-electron-demand Diels-Alder (IEDDA) cleavage reaction between tetrazine and trans-cyclooctene (TCO) is a powerful way to control the release of bioactive agents and imaging probes. In this study, a pretargeted activation strategy using single-walled carbon nanotubes (SWCNTs) that bear tetrazines (TZ@SWCNTs) and a TCO-caged molecule was used to deliver active effector molecules. To optimize a turn-on signal by using in vivo fluorescence imaging, we developed a new fluorogenic near-infrared probe that can be activated by bioorthogonal chemistry and image tumours in mice by caging hemicyanine with TCO (tHCA). With our pretargeting strategy, we have shown selective doxorubicin prodrug activation and instantaneous fluorescence imaging in living cells. By combining a tHCA probe and a pretargeted bioorthogonal approach, real-time, non-invasive tumour visualization with a high target-to-background ratio was achieved in a xenograft mice tumour model. The combined advantages of enhanced stability, kinetics and biocompatibility, and the superior pharmacokinetics of tetrazine-functionalised SWCNTs could allow application of targeted bioorthogonal decaging approaches with minimal off-site activation of fluorophore/drug.

Citing Articles

Polymeric PEG-based bioorthogonal triggers for prodrug activation in breast cancer.

Mitry M, Osborn H, Greco F RSC Adv. 2025; 15(9):7127-7138.

PMID: 40045955 PMC: 11881796. DOI: 10.1039/d4ra08758e.

Exploring New Bioorthogonal Catalysts: Scaffold Diversity in Catalysis for Chemical Biology.

Zhang Y, Huang Q, Lei F, Qian W, Zhang C, Wang Q Adv Sci (Weinh). 2025; 12(9):e2404431.

PMID: 39921286 PMC: 11884534. DOI: 10.1002/advs.202404431.

Benzyl Ammonium Carbamates Undergo Two-Step Linker Cleavage and Improve the Properties of Antibody Conjugates.

Li X, Patel N, Kalen J, Schnermann M Angew Chem Int Ed Engl. 2024; 64(6):e202417651.

PMID: 39696914 PMC: 11795738. DOI: 10.1002/anie.202417651.

Fluorogenic Reactions in Chemical Biology: Seeing Chemistry in Cells.

Chen Y, Jiang H, Hao T, Zhang N, Li M, Wang X Chem Biomed Imaging. 2024; 1(7):590-619.

PMID: 39474135 PMC: 11504613. DOI: 10.1021/cbmi.3c00029.

Chemistry-driven translocation of glycosylated proteins in mice.

Yamada K, Mukaimine A, Nakamura A, Kusakari Y, Pradipta A, Chang T Nat Commun. 2024; 15(1):7409.

PMID: 39358337 PMC: 11446924. DOI: 10.1038/s41467-024-51342-5.

References

Maeda H, Wu J, Sawa T, Matsumura Y, Hori K . Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release. 2000; 65(1-2):271-84. DOI: 10.1016/s0168-3659(99)00248-5. View

te Velde E, Veerman T, Subramaniam V, Ruers T . The use of fluorescent dyes and probes in surgical oncology. Eur J Surg Oncol. 2009; 36(1):6-15. DOI: 10.1016/j.ejso.2009.10.014. View

Rossin R, van Duijnhoven S, Ten Hoeve W, Janssen H, Kleijn L, Hoeben F . Triggered Drug Release from an Antibody-Drug Conjugate Using Fast "Click-to-Release" Chemistry in Mice. Bioconjug Chem. 2016; 27(7):1697-706. DOI: 10.1021/acs.bioconjchem.6b00231. View

Czuban M, Srinivasan S, Yee N, Agustin E, Koliszak A, Miller E . Bio-Orthogonal Chemistry and Reloadable Biomaterial Enable Local Activation of Antibiotic Prodrugs and Enhance Treatments against Infections. ACS Cent Sci. 2019; 4(12):1624-1632. PMC: 6311693. DOI: 10.1021/acscentsci.8b00344. View

Kong F, Liu F, Li W, Guo X, Wang Z, Zhang H . Smart Carbon Nanotubes with Laser-Controlled Behavior in Gene Delivery and Therapy through a Non-Digestive Trafficking Pathway. Small. 2016; 12(48):6753-6766. DOI: 10.1002/smll.201601092. View

Haun J, Devaraj N, Hilderbrand S, Lee H, Weissleder R . Bioorthogonal chemistry amplifies nanoparticle binding and enhances the sensitivity of cell detection. Nat Nanotechnol. 2010; 5(9):660-5. PMC: 2934903. DOI: 10.1038/nnano.2010.148. View

Knorr G, Kozma E, Herner A, Lemke E, Kele P . New Red-Emitting Tetrazine-Phenoxazine Fluorogenic Labels for Live-Cell Intracellular Bioorthogonal Labeling Schemes. Chemistry. 2016; 22(26):8972-9. DOI: 10.1002/chem.201600590. View

Zhang G, Li J, Xie R, Fan X, Liu Y, Zheng S . Bioorthogonal Chemical Activation of Kinases in Living Systems. ACS Cent Sci. 2016; 2(5):325-31. PMC: 4882735. DOI: 10.1021/acscentsci.6b00024. View

Wieczorek A, Werther P, Euchner J, Wombacher R . Green- to far-red-emitting fluorogenic tetrazine probes - synthetic access and no-wash protein imaging inside living cells. Chem Sci. 2017; 8(2):1506-1510. PMC: 5452268. DOI: 10.1039/c6sc03879d. View

10.

Kong F, Liang Z, Luan D, Liu X, Xu K, Tang B . A Glutathione (GSH)-Responsive Near-Infrared (NIR) Theranostic Prodrug for Cancer Therapy and Imaging. Anal Chem. 2016; 88(12):6450-6. DOI: 10.1021/acs.analchem.6b01135. View

11.

Wu H, Yang J, Seckute J, Devaraj N . In situ synthesis of alkenyl tetrazines for highly fluorogenic bioorthogonal live-cell imaging probes. Angew Chem Int Ed Engl. 2014; 53(23):5805-9. PMC: 4104127. DOI: 10.1002/anie.201400135. View

12.

He X, Hu Y, Shi W, Li X, Ma H . Design, synthesis and application of a near-infrared fluorescent probe for in vivo imaging of aminopeptidase N. Chem Commun (Camb). 2017; 53(68):9438-9441. DOI: 10.1039/c7cc05142e. View

13.

Ghosh D, Bagley A, Na Y, Birrer M, Bhatia S, Belcher A . Deep, noninvasive imaging and surgical guidance of submillimeter tumors using targeted M13-stabilized single-walled carbon nanotubes. Proc Natl Acad Sci U S A. 2014; 111(38):13948-53. PMC: 4183329. DOI: 10.1073/pnas.1400821111. View

14.

Siegl S, Galeta J, Dzijak R, Vazquez A, Del Rio-Villanueva M, Dracinsky M . An Extended Approach for the Development of Fluorogenic trans-Cyclooctene-Tetrazine Cycloadditions. Chembiochem. 2018; 20(7):886-890. PMC: 6471176. DOI: 10.1002/cbic.201800711. View

15.

Li H, Conde J, Guerreiro A, Bernardes G . Tetrazine Carbon Nanotubes for Pretargeted In Vivo "Click-to-Release" Bioorthogonal Tumour Imaging. Angew Chem Int Ed Engl. 2020; 59(37):16023-16032. PMC: 7540421. DOI: 10.1002/anie.202008012. View

16.

Ji X, Pan Z, Yu B, De La Cruz L, Zheng Y, Ke B . Click and release: bioorthogonal approaches to "on-demand" activation of prodrugs. Chem Soc Rev. 2019; 48(4):1077-1094. DOI: 10.1039/c8cs00395e. View

17.

Siegl S, Galeta J, Dzijak R, Dracinsky M, Vrabel M . Bioorthogonal Fluorescence Turn-On Labeling Based on Bicyclononyne-Tetrazine Cycloaddition Reactions that Form Pyridazine Products. Chempluschem. 2019; 84(5):493-497. PMC: 6582594. DOI: 10.1002/cplu.201900176. View

18.

Mejia Oneto J, Khan I, Seebald L, Royzen M . In Vivo Bioorthogonal Chemistry Enables Local Hydrogel and Systemic Pro-Drug To Treat Soft Tissue Sarcoma. ACS Cent Sci. 2016; 2(7):476-82. PMC: 4965853. DOI: 10.1021/acscentsci.6b00150. View

19.

Adumeau P, Carnazza K, Brand C, Carlin S, Reiner T, Agnew B . A Pretargeted Approach for the Multimodal PET/NIRF Imaging of Colorectal Cancer. Theranostics. 2016; 6(12):2267-2277. PMC: 5135447. DOI: 10.7150/thno.16744. View

20.

He X, Li L, Fang Y, Shi W, Li X, Ma H . imaging of leucine aminopeptidase activity in drug-induced liver injury and liver cancer a near-infrared fluorescent probe. Chem Sci. 2017; 8(5):3479-3483. PMC: 5418645. DOI: 10.1039/c6sc05712h. View