ACS Publications. Most Trusted. Most Cited. Most Read
Environment-Sensitive Probes for Illuminating Amyloid Aggregation In Vitro and in Zebrafish

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:ACS Sens. 2020, 5, 9, 2792-2799
    Article

    Environment-Sensitive Probes for Illuminating Amyloid Aggregation In Vitro and in Zebrafish
    Click to copy article linkArticle link copied!

    • Francisco Fueyo-González
      Francisco Fueyo-González
      Instituto de Química Médica (CSIC), Juan de la Cierva 3, 28006 Madrid, Spain
      More by Francisco Fueyo-González
    • Juan A. González-Vera*
      Juan A. González-Vera
      Instituto de Química Médica (CSIC), Juan de la Cierva 3, 28006 Madrid, Spain
      Departamento de Fisicoquímica, Unidad de Excelencia de Química Aplicada a Biomedicina y Medioambiente, Facultad de Farmacia, Universidad de Granada, Campus Cartuja, 18071 Granada, Spain
      *Email: [email protected]
      More by Juan A. González-Vera
      Orcidhttp://orcid.org/0000-0002-8199-1330
    • Ibon Alkorta
      Ibon Alkorta
      Instituto de Química Médica (CSIC), Juan de la Cierva 3, 28006 Madrid, Spain
      More by Ibon Alkorta
      Orcidhttp://orcid.org/0000-0001-6876-6211
    • Lourdes Infantes
      Lourdes Infantes
      Instituto de Química Física Rocasolano, IQFR-CSIC, Serrano 119, 28006 Madrid, Spain
      More by Lourdes Infantes
    • Maria Luisa Jimeno
      Maria Luisa Jimeno
      Centro de Química Orgánica Lora Tamayo (CSIC), Juan de la Cierva 3, 28006 Madrid, Spain
      More by Maria Luisa Jimeno
    • Paula Aranda
      Paula Aranda
      Departamento de Fisiología, Facultad de Medicina, Universidad de Granada, 18016 Granada, Spain
      More by Paula Aranda
    • Dario Acuña-Castroviejo
      Dario Acuña-Castroviejo
      Departamento de Fisiología, Facultad de Medicina, Universidad de Granada, 18016 Granada, Spain
      CIBER de Fragilidad y Envejecimiento, Ibs. Granada, Unidad de Gestión Clínica de Laboratorios Clínicos, Hospital Universitario San Cecilio, 18016 Granada, Spain
      More by Dario Acuña-Castroviejo
    • Alvaro Ruiz-Arias
      Alvaro Ruiz-Arias
      Departamento de Fisicoquímica, Unidad de Excelencia de Química Aplicada a Biomedicina y Medioambiente, Facultad de Farmacia, Universidad de Granada, Campus Cartuja, 18071 Granada, Spain
      More by Alvaro Ruiz-Arias
    • Angel Orte
      Angel Orte
      Departamento de Fisicoquímica, Unidad de Excelencia de Química Aplicada a Biomedicina y Medioambiente, Facultad de Farmacia, Universidad de Granada, Campus Cartuja, 18071 Granada, Spain
      More by Angel Orte
      Orcidhttp://orcid.org/0000-0003-1905-4183
    • Rosario Herranz*
      Rosario Herranz
      Instituto de Química Médica (CSIC), Juan de la Cierva 3, 28006 Madrid, Spain
      *Email: [email protected]
      More by Rosario Herranz
      Orcidhttp://orcid.org/0000-0002-0273-2761
    Other Access OptionsSupporting Information (1)

    ACS Sensors

    Cite this: ACS Sens. 2020, 5, 9, 2792–2799
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acssensors.0c00587
    Published June 18, 2020
    Copyright © 2020 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    The aberrant aggregation of certain peptides and proteins, forming extracellular plaques of fibrillar material, is one of the hallmarks of amyloid diseases, such as Alzheimer’s and Parkinson’s. Herein, we have designed a new family of solvatochromic dyes based on the 9-amino-quinolimide moiety capable of reporting during the early stages of amyloid fibrillization. We have rationally improved the photophysical properties of quinolimides by placing diverse amino groups at the 9-position of the quinolimide core, leading to higher solvatochromic and fluorogenic character and higher lifetime dependence on the hydrophobicity of the environment, which represent excellent properties for the sensitive detection of prefibrillar aggregates. Among the different probes prepared, the 9-azetidinyl-quinolimide derivative showed striking performance in the following β-amyloid peptide (Aβ) aggregation in solution in real time and identifying the formation of different types of early oligomers of Aβ, the most important species linked to cytotoxicity, using novel, multidimensional fluorescence microscopy, with one- or two-photon excitation. Interestingly, the new dye allowed the visualization of proteinaceous inclusion bodies in a zebrafish model with neuronal damage induced by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Our results support the potential of the novel fluorophores as powerful tools to follow amyloid aggregation using fluorescence microscopy in vivo, revealing heterogeneous populations of different types of aggregates and, more broadly, to study protein interactions.

    Copyright © 2020 American Chemical Society

    Subjects

    what are subjects

    Keywords

    what are keywords

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acssensors.0c00587.

    • Detailed information on the synthesis and photophysical, NMR, X-ray and TD-DFT characterization of quinolimides 1–6, along with additional data, figures, and tables (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!

    This article is cited by 24 publications.

    1. Natalie Trinh, Kaustubh R. Bhuskute, Nikhil R. Varghese, Jessica A. Buchanan, Yijia Xu, Fiona M. McCutcheon, Robert L. Medcalf, Katrina A. Jolliffe, Margaret Sunde, Elizabeth J. New, Amandeep Kaur. A Coumarin-Based Array for the Discrimination of Amyloids. ACS Sensors 2024, 9 (2) , 615-621. https://doi.org/10.1021/acssensors.3c01334
    2. Yulong Bai, Shengnan Zhang, Hui Dong, Yu Liu, Cong Liu, Xin Zhang. Advanced Techniques for Detecting Protein Misfolding and Aggregation in Cellular Environments. Chemical Reviews 2023, 123 (21) , 12254-12311. https://doi.org/10.1021/acs.chemrev.3c00494
    3. Ambra Dreos, Junyue Ge, Francisco Najera, Behabitu Ergette Tebikachew, Ezequiel Perez-Inestrosa, Kasper Moth-Poulsen, Kaj Blennow, Henrik Zetterberg, Jörg Hanrieder. Investigating New Applications of a Photoswitchable Fluorescent Norbornadiene as a Multifunctional Probe for Delineation of Amyloid Plaque Polymorphism. ACS Sensors 2023, 8 (4) , 1500-1509. https://doi.org/10.1021/acssensors.2c02496
    4. Dengbin Yu, Rongbing Li, Xiaoxuan Sun, He Zhang, Hongwen Yu, Shaojun Dong. Colorimetric and Electrochemical Dual-Signal Method for Water Toxicity Detection Based on Escherichia coli and p-Benzoquinone. ACS Sensors 2021, 6 (7) , 2674-2681. https://doi.org/10.1021/acssensors.1c00651
    5. Pankaj Gaur, Maksym Galkin, Andrii Kurochka, Subrata Ghosh, Dmytro A. Yushchenko, Volodymyr V. Shvadchak. Fluorescent Probe for Selective Imaging of α-Synuclein Fibrils in Living Cells. ACS Chemical Neuroscience 2021, 12 (8) , 1293-1298. https://doi.org/10.1021/acschemneuro.1c00090
    6. Ruiyu Wang, Yu Zhang, Zixuan Yuan, Jiaqi Dong, Jinping Wang, Lihua Jia. A novel colorimetric and fluorescent sensor for the highly specific detection of Cu2+ and glyphosate based on a quinolimide-Schiff base. Journal of Molecular Structure 2025, 1322 , 140333. https://doi.org/10.1016/j.molstruc.2024.140333
    7. Guillem Vázquez, Alba Espargaró, Ana B. Caballero, Ania Di Pede-Mattatelli, M. Antònia Busquets, Daria Nawrot, Raimon Sabaté, Ernesto Nicolás, Jordi Juárez-Jiménez, Patrick Gamez. A versatile luminescent probe for sensing and monitoring amyloid proteins. Dyes and Pigments 2024, 231 , 112348. https://doi.org/10.1016/j.dyepig.2024.112348
    8. Zhiyang An, Xiaoling Zhang, Jing Jing. Recent Advances in Fluorescent Probes Development for Interrogating Protein Misfolding and Aggregation. TrAC Trends in Analytical Chemistry 2024, 53 , 118066. https://doi.org/10.1016/j.trac.2024.118066
    9. Hongjie Cao, Yu Zhang, Wenjing Qu, Ruiyu Wang, Lihua Jia. A highly sensitive quinolimide-functionalized fluorescent sensor for Zn2+ with multifaceted applications. Journal of Photochemistry and Photobiology A: Chemistry 2024, 451 , 115497. https://doi.org/10.1016/j.jphotochem.2024.115497
    10. Wenjing Qu, Yu Zhang, Hongjie Cao, Lihua Jia. A highly selective fluorescence turn-on sensor for Hg2+ based on quinolimide in aqueous media and its applications. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 2024, 304 , 123376. https://doi.org/10.1016/j.saa.2023.123376
    11. Hongjie Cao, Jianhua Yang, Yu Zhang, Wenjing Qu, Lihua Jia. A simple quinolimide-based fluorescent sensor for formaldehyde and its applications in test strips and living cells. Journal of Photochemistry and Photobiology A: Chemistry 2023, 444 , 115023. https://doi.org/10.1016/j.jphotochem.2023.115023
    12. Jianhua Yang, Yu Zhang, Lan Li, Hongjie Cao, Wenjing Qu, Lihua Jia. A quinolimide-based reversible fluorescent sensor for Cu2+ and S2− and its applications. Journal of Molecular Structure 2023, 1275 , 134638. https://doi.org/10.1016/j.molstruc.2022.134638
    13. Lihua Liu, Yubo Huang, Yufeng Zhou, Yu Zhao, Jinzhi Qi, Xin Zhang, Baoxing Shen. Fluorogenic toolbox for visualizing protein aggregation: From designing principles to biological application. TrAC Trends in Analytical Chemistry 2022, 157 , 116764. https://doi.org/10.1016/j.trac.2022.116764
    14. Yu Zhang, Wenjing Qu, Jianhua Yang, Lihua Jia, Lan Li, Hongjie Cao, Xiangfeng Guo. Cd2+ and Zn2+ fluorescence turn-on sensing and the subsequent detection of S2− by a quinolimide-based sensor in water and living cells with application in the combinational logic gate. Tetrahedron 2022, 121 , 132916. https://doi.org/10.1016/j.tet.2022.132916
    15. Lan Li, Yu Zhang, Jianhua Yang, Wenjing Qu, Hongjie Cao. A turn-on fluorescent sensor for Cd2+ and sequential detection of S2− using the quinolimide scaffold. Tetrahedron 2022, 121 , 132917. https://doi.org/10.1016/j.tet.2022.132917
    16. Laura Espinar-Barranco, Jose Manuel Paredes, Angel Orte, Luis Crovetto, Emilio Garcia-Fernandez. A solvatofluorochromic dye as a fluorescent lifetime-based probe of β-amyloid aggregation. Dyes and Pigments 2022, 202 , 110274. https://doi.org/10.1016/j.dyepig.2022.110274
    17. Álvaro Ruiz-Arias, Rocío Jurado, Francisco Fueyo-González, Rosario Herranz, Natividad Gálvez, Juan A. González-Vera, Angel Orte. A FRET pair for quantitative and superresolution imaging of amyloid fibril formation. Sensors and Actuators B: Chemical 2022, 350 , 130882. https://doi.org/10.1016/j.snb.2021.130882
    18. Álvaro Ruiz-Arias, Rocío Jurado, Francisco Fueyo-González, Rosario Herranz, Natividad Gálvez, Juan A. González-Vera, Angel Orte. Selecting FRET pairs for visualizing amyloid aggregation. Results in Chemistry 2022, 4 , 100275. https://doi.org/10.1016/j.rechem.2021.100275
    19. Cristina Gila-Vilchez, Mari C. Mañas-Torres, Juan A. González-Vera, Francisco Franco-Montalban, Juan A. Tamayo, Francisco Conejero-Lara, Juan Manuel Cuerva, Modesto T. Lopez-Lopez, Angel Orte, Luis Álvarez de Cienfuegos. Insights into the co-assemblies formed by different aromatic short-peptide amphiphiles. Polymer Chemistry 2021, 12 (47) , 6832-6845. https://doi.org/10.1039/D1PY01366A
    20. Mari C. Mañas-Torres, Cristina Gila-Vilchez, Juan A. González-Vera, Francisco Conejero-Lara, Victor Blanco, Juan Manuel Cuerva, Modesto T. Lopez-Lopez, Angel Orte, Luis Álvarez de Cienfuegos. In situ real-time monitoring of the mechanism of self-assembly of short peptide supramolecular polymers. Materials Chemistry Frontiers 2021, 5 (14) , 5452-5462. https://doi.org/10.1039/D1QM00477H
    21. Francisco Fueyo-González, Rosario Herranz, Simona Plesselova, Maria D. Giron, Rafael Salto, Jose Manuel Paredes, Angel Orte, May C. Morris, Juan A. González-Vera. Quinolimide-based peptide biosensor for probing p25 in vitro and in living cells. Sensors and Actuators B: Chemical 2021, 339 , 129929. https://doi.org/10.1016/j.snb.2021.129929
    22. Xingxing Zhang, Tianbing Ren, Qianling Zhang, Ting Zeng, Zhe Li, Feiyu Yang, Xiaobing Zhang, Lin Yuan. Molecular design strategy to alleviate environmental interference on two-photon fluorescence probes. Cell Reports Physical Science 2021, 2 (6) , 100471. https://doi.org/10.1016/j.xcrp.2021.100471
    23. M. Carmen Gonzalez-Garcia, Pilar Herrero-Foncubierta, Emilio Garcia-Fernandez, Angel Orte. Building Accurate Intracellular Polarity Maps through Multiparametric Microscopy. Methods and Protocols 2020, 3 (4) , 78. https://doi.org/10.3390/mps3040078
    24. Álvaro Ruiz-Arias, Jose M. Paredes, Chiara Di Biase, Juan M. Cuerva, María D. Giron, Rafael Salto, Juan A. González-Vera, Angel Orte. Seeding and Growth of β-Amyloid Aggregates upon Interaction with Neuronal Cell Membranes. International Journal of Molecular Sciences 2020, 21 (14) , 5035. https://doi.org/10.3390/ijms21145035
    Download PDF
    Go to ACS Sensors
    Get e-Alerts
    Get e-Alerts

    ACS Sensors

    Cite this: ACS Sens. 2020, 5, 9, 2792–2799
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acssensors.0c00587
    Published June 18, 2020
    Copyright © 2020 American Chemical Society
    Request reuse permissions

    Article Views

    2162

    Altmetric

    -

    Citations

    24
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.