Prediction of Early Atherosclerotic Plaques Using a Sequence-Activated Fluorescence Probe for the Simultaneous Detection of γ-Glutamyl Transpeptidase and Hypobromous Acid
Dr. Hui Wang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
These authors contributed equally to this work.
Search for more papers by this authorXiaoting Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
These authors contributed equally to this work.
Search for more papers by this authorCorresponding Author
Prof. Ping Li
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorFang Huang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorTiancong Xiu
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorHongTong Wang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorDr. Wei Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorDr. Wen Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorCorresponding Author
Prof. Bo Tang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
People's Republic of China; Laoshan Laboratory, 168 Wenhai Middle Rd, Aoshanwei Jimo, Qingdao, 266237 Shandong, P. R. China
Search for more papers by this authorDr. Hui Wang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
These authors contributed equally to this work.
Search for more papers by this authorXiaoting Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
These authors contributed equally to this work.
Search for more papers by this authorCorresponding Author
Prof. Ping Li
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorFang Huang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorTiancong Xiu
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorHongTong Wang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorDr. Wei Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorDr. Wen Zhang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
Search for more papers by this authorCorresponding Author
Prof. Bo Tang
College of Chemistry, Chemical Engineering and Materials Science, Key Laboratory of Molecular and Nano Probes, Ministry of Education, Collaborative Innovation Center of Functionalized Probes for Chemical Imaging in Universities of Shandong, Institutes of Biomedical Sciences, Shandong Normal University, Jinan, 250014 Shandong, P. R. China
People's Republic of China; Laoshan Laboratory, 168 Wenhai Middle Rd, Aoshanwei Jimo, Qingdao, 266237 Shandong, P. R. China
Search for more papers by this authorAbstract
Atherosclerosis is a lipoprotein-driven disease, and there is no effective therapy to reverse atherosclerosis or existing plaques. Therefore, it is urgently necessary to create a noninvasive and reliable approach for early atherosclerosis detection to prevent initial plaque formation. Atherosclerosis is intimately associated with inflammation, which is accompanied by an excess of reactive oxygen species (ROS), leading to cells requiring more glutathione (GSH) to resist severe oxidative stress. Therefore, the GSH-hydrolyzed protein γ-glutamyl transpeptidase (GGT) and the ROS-hypobromous acid (HBrO) are potential biomarkers for predicting atherogenesis. Hence, to avoid false-positive diagnoses caused by a single biomarker, we constructed an ingenious sequence-activated double-locked TP fluorescent probe, C-HBrO-GGT, in which two sequential triggers of GGT and HBrO are meticulously designed to ensure that the probe fluoresces in response to HBrO only after GGT hydrolyzes the probe. By utilization of C-HBrO-GGT, the voltage-gated chloride channel (CLC-1)-HBrO-catalase (CAT)-GGT signaling pathway was confirmed in cellular level. Notably, the forthcoming atherosclerotic plaques were successfully predicted before the plaques could be observed via the naked eye or classical immunofluorescent staining. Collectively, this research proposed a powerful tool to indicate the precise position of mature plaques and provide early warning of atherosclerotic plaques.
Open Research
Data Availability Statement
The data that support the findings of this study are available in the supplementary material of this article.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
| Filename | Description |
|---|---|
| ange202315861-sup-0001-misc_information.pdf2.5 MB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1
- 1aR. Saigusa, H. Winkels, K. Ley, Nat. Rev. Cardiol. 2020, 17, 387–401;
- 1bY. Su, P. Guan, D. Li, Y. Hang, X. Ye, L. Han, Y. Lu, X. Bai, P. Zhang, W. Hu, Biochem. Biophys. Res. Commun. 2021, 583, 35–42;
- 1cZ. Zhou, Y. Tang, X. Jin, C. Chen, Y. Lu, L. Liu, C. Shen, J. Diabetes Res. 2016, 2016, 4847812.
- 2J. F. Bentzon, F. Otsuka, R. Virmani, E. Falk, Circ. Res. 2014, 114, 1852–1866.
- 3
- 3aC. Weber, H. Noels, Nat. Med. 2011, 17, 1410–1422;
- 3bY. Xia, J. Li, L. Wang, Y. Xie, L. Zhang, X. Han, W. Tan, Y. Liu, Angew. Chem. Int. Ed. 2023, 62, e202214169.
- 4
- 4aY. Ma, L. Xu, B. Yin, J. Shang, F. Chen, J. Xu, Z. L. Song, B. Nan, G. Song, X. B. Zhang, Nano Lett. 2021, 21, 4484–4493;
- 4bV. Fuster, B. Stein, J. A. Ambrose, L. Badimon, J. J. Badimon, J. H. Chesebro, Circulation 1990, 82, 47–59;
- 4cA. V. Sterpetti, Curr. Atheroscler. Rep. 2020, 22, 75.
- 5
- 5aP. Balakumar, K. Maung-U, G. Jagadeesh, Pharmacol. Res. 2016, 113, 600–609;
- 5bT. A. Gaziano, A. Bitton, S. Anand, S. Abrahams-Gessel, A. Murphy, Curr. Problems Cardiol. 2010, 35, 72–115;
- 5cT. Nag, A. Ghosh, J. Cardiovasc. Dis. Res. 2013, 4, 222–228.
- 6
- 6aK. K. Teo, H. Dokainish, Can. J. Cardiol. 2017, 33, 358–365;
- 6bK. K. Teo, S. Ounpuu, S. Hawken, M. R. Pandey, V. Valentin, D. Hunt, R. Diaz, W. Rashed, R. Freeman, L. Jiang, X. Zhang, S. Yusuf, Lancet 2006, 368, 647–658;
- 6cO. S. Descamps, S. Tenoutasse, X. Stephenne, I. Gies, V. Beauloye, M. C. Lebrethon, C. De Beaufort, K. De Waele, A. Scheen, E. Rietzschel, A. Mangano, J. P. Panier, J. Ducobu, M. Langlois, J. L. Balligand, P. Legat, V. Blaton, E. Muls, L. Van Gaal, E. Sokal, R. Rooman, Y. Carpentier, G. De Backer, F. R. Heller, Atherosclerosis 2011, 218, 272–280.
- 7
- 7aA. C. Carr, E. A. Decker, Y. Park, B. Frei, Free Radical Biol. Med. 2001, 31, 62–72;
- 7bA. Daugherty, J. L. Dunn, D. L. Rateri, J. W. Heinecke, J. Clin. Invest. 1994, 94, 437–444;
- 7cO. J. de Boer, A. C. van der Wal, A. E. Becker, J. Pathol. 2000, 190, 237–243.
10.1002/(SICI)1096-9896(200002)190:3<237::AID-PATH541>3.0.CO;2-N CAS PubMed Web of Science® Google Scholar
- 8
- 8aM. Hulsmans, E. Van Dooren, P. Holvoet, Curr. Atheroscler. Rep. 2012, 14, 264–276;
- 8bH. E. Seifried, D. E. Anderson, E. I. Fisher, J. A. Milner, J. Nutritional Biochem. 2007, 18, 567–579;
- 8cE. A. Podrez, H. M. Abu-Soud, S. L. Hazen, Free Radical Biol. Med. 2000, 28, 1717–1725;
- 8dL. J. Hazell, J. J. M. van den Berg, R. Stocker, Biochem. J. 1994, 302, 297–304;
- 8eM. L. Senders, W. J. M. Mulder, Eur. Heart J. 2018, 39, 3311–3313.
- 9
- 9aA. Ulfig, L. I. Leichert, Cell. Mol. Life Sci. 2021, 78, 385–414;
- 9bY. Fang, W. Dehaen, Molecules 2021, 26, 363;
- 9cL. Mei, S. Zhu, Y. Liu, W. Yin, Z. Gu, Y. Zhao, Chem. Eng. J. 2021, 418, 129431;
- 9dA. Korotaeva, E. Samoilova, T. Pavlunina, O. M. Panasenko, Chem. Phys. Lipids 2013, 167–168, 51–56.
- 10
- 10aH. Huang, Y. Tian, Chem. Commun. 2018, 54, 12198–12201;
- 10bK. C. Yan, A. C. Sedgwick, Y. Zang, G. R. Chen, X.-P. He, J. Li, J. Yoon, T. D. James, Small Methods 2019, 3, 1900013;
- 10cY. Lei, K. Wang, L. Deng, Y. Chen, E. C. Nice, C. Huang, Med. Res. Rev. 2015, 35, 306–340.
- 11
- 11aY. Wen, Z. Long, F. Huo, C. Yin, Sci. China Chem. 2022, 65, 2517–2527;
- 11bH. Yan, F. Huo, Y. Yue, J. Chao, C. Yin, J. Am. Chem. Soc. 2021, 143, 318–325.
- 12
- 12aA. Corti, E. Belcastro, S. Dominici, E. Maellaro, A. Pompella, Free Radical Biol. Med. 2020, 160, 807–819;
- 12bH. J. Forman, H. Zhang, Nat. Rev. Drug Discovery 2021, 20, 689–709.
- 13
- 13aM. M. Capelletti, H. Manceau, H. Puy, K. Peoc'h, Int. J. Mol. Sci. 2020, 21, 4908;
- 13bG. Ndrepepa, R. Colleran, A. Kastrati, Clin. Chim. Acta 2018, 476, 130–138.
- 14
- 14aG. Schmitz, M. Grandl, Antioxid. Redox Signaling 2007, 9, 1499–1518;
- 14bT. Goyal, S. Mitra, M. Khaidakov, X. Wang, S. Singla, Z. Ding, S. Liu, J. L. Mehta, Curr. Atheroscler. Rep. 2012, 14, 150–159;
- 14cM. Hulsmans, P. Holvoet, J. Cell. Mol. Med. 2010, 14, 70–78.
- 15
- 15aZ. A. Fayad, V. Fuster, K. Nikolaou, C. Becker, Circulation 2002, 106, 2026–2034;
- 15bD. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, P. K. Woodard, Circulation 2008, 118, 586–606;
- 15cK. C. Briley-Saebo, W. J. M. Mulder, V. Mani, F. Hyafil, V. Amirbekian, J. G. S. Aguinaldo, E. A. Fisher, Z. A. Fayad, J. Magn. Reson. Imaging 2007, 26, 460–479;
- 15dE. Ovalle Magallanes, J. G. Avina Cervantes, I. Cruz Aceves, J. Ruiz Pinales, Mathematics 2020, 8, 1510;
- 15eK. Michaud, S. Grabherr, F. Doenz, P. Mangin, Int. J. Cardiovasc. Imaging 2012, 28, 1807–1822.
- 16
- 16aJ. Sanz, Z. A. Fayad, Nature 2008, 451, 953–957;
- 16bJ. M. Tarkin, M. R. Dweck, N. R. Evans, R. A. P. Takx, A. J. Brown, A. Tawakol, Z. A. Fayad, J. H. F. Rudd, Circ. Res. 2016, 118, 750–769.
- 17
- 17aZ. He, D. Liu, Y. Liu, X. Li, W. Shi, H. Ma, Anal. Chem. 2022, 94, 10256–10262;
- 17bH.-M. Meng, Z. Jin, Y. Lv, C. Yang, X.-B. Zhang, W. Tan, R.-Q. Yu, Anal. Chem. 2014, 86, 12321–12326;
- 17cY. Cui, S. J. Park, X. Wu, R. Wang, S. Qi, H. M. Kim, J. Yoon, Chem. Commun. 2021, 57, 6911–6914;
- 17dN. Kwon, M. K. Cho, S. J. Park, D. Kim, S. J. Nam, L. Cui, H. M. Kim, J. Yoon, Chem. Commun. 2017, 53, 525–528.
- 18
- 18aY. X. Wu, D. Zhang, X. Hu, R. Peng, J. Li, X. Zhang, W. Tan, Angew. Chem. Int. Ed. 2021, 60, 12569–12576;
- 18bL. Wu, J. Liu, P. Li, B. Tang, T. D. James, Chem. Soc. Rev. 2021, 50, 702–734;
- 18cW. Li, B. Fang, M. Jin, Y. Tian, Anal. Chem. 2017, 89, 2553–2560.
- 19
- 19aM. Weber, N. Yamada, X. Tian, S. D. Bull, M. Minoshima, K. Kikuchi, A. B. Mackenzie, T. D. James, Front. Chem. 2020, 8, 39;
- 19bY. Fan, Y. Wu, J. Hou, P. Wang, X. Peng, G. Ge, Coord. Chem. Rev. 2023, 480, 215020;
- 19cB. Roubinet, L. Bailly, E. Petit, P.-Y. Renard, A. Romieu, Tetrahedron Lett. 2015, 56, 1015–1019.
- 20
- 20aK. Xu, D. Luan, X. Wang, B. Hu, X. Liu, F. Kong, B. Tang, Angew. Chem. Int. Ed. 2016, 55, 12751–12754;
- 20bD. Zhang, X. Yang, T. Wang, X. Ji, X. Wu, Anal. Chim. Acta 2023, 1244, 340626.
- 21
- 21aK. Li, Y. Lyu, Y. Huang, S. Xu, H.-W. Liu, L. Chen, T. B. Ren, M. Xiong, S. Huan, L. Yuan, X.-B. Zhang, W. Tan, Proc. Natl. Acad. Sci. USA 2021, 118, e2018033118;
- 21bF. Liu, Z. Wang, W. Wang, J. G. Luo, L. Kong, Anal. Chem. 2018, 90, 7467–7473;
- 21cS. Park, D. J. Bae, Y. M. Ryu, S. Y. Kim, S. J. Myung, H. J. Kim, Chem. Commun. 2016, 52, 10400–10402.
- 22
- 22aM. C. Huang, S. K. Lin, C. H. Chen, C. H. Pan, C. H. Lee, H. C. Liu, Psychiatry Clin. Neurosci. 2013, 67, 92–100;
- 22bP. Singh, S. Kumar, Enzymes in Food Biotechnology, Academic Press, San Diego, 2019, pp. 19–28;
- 22cR. Senthilmohan, A. J. Kettle, Arch. Biochem. Biophys. 2006, 445, 235–244;
- 22dA. C. Carr, C. C. Winterbourn, J. J. van den Berg, Arch. Biochem. Biophys. 1996, 327, 227–233.
- 23
- 23aC. Ravuri, G. Svineng, S. Pankiv, N. E. Huseby, Free Radical Res. 2011, 45, 600–610;
- 23bP. Wang, J. Zhang, H. W. Liu, X. X. Hu, L. L. Feng, X. Yin, X. B. Zhang, Analyst 2017, 142, 1813–1820.
- 24
- 24aF. Yan, Y. Sun, Y. Mao, M. Wu, Z. Deng, S. Li, X. Liu, L. Xue, H. Zheng, Theranostics 2018, 8, 1879–1891.
Citing Literature
This is the
German version
of Angewandte Chemie.
Note for articles published since 1962:
Do not cite this version alone.
Take me to the International Edition version with citable page numbers, DOI, and citation export.
We apologize for the inconvenience.
