Engineering of Reversible NIR-II Redox-Responsive Fluorescent Probes for Imaging of Inflammation In Vivo
Long He
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorLin-Hui He
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorShuai Xu
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorCorresponding Author
Dr. Tian-Bing Ren
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorXing-Xing Zhang
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorZuo-Jia Qin
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorProf. Xiao-Bing Zhang
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorCorresponding Author
Prof. Lin Yuan
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorLong He
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorLin-Hui He
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorShuai Xu
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorCorresponding Author
Dr. Tian-Bing Ren
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorXing-Xing Zhang
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorZuo-Jia Qin
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorProf. Xiao-Bing Zhang
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorCorresponding Author
Prof. Lin Yuan
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, 410082 PR China
Search for more papers by this authorAbstract
The second near-infrared (NIR-II) fluorescent imaging shows great potential for deep tissue analysis at high resolution in living body owing to low background autofluorescence and photon scattering. However, reversible monitoring of redox homeostasis using NIR-II fluorescent imaging remains a challenge due to the lack of appropriate probes. In this study, a series of stable and multifunctional NIR-II dyes (NIR-II Cy3s) were constructed based on trimethine skeleton. Significantly, introducing the 1,4-diethyl-decahydroquinoxaline group to the NIR-II Cy3s not only effectively increased the wavelength, but also served as an effective response site for HClO, which can be restored by reactive sulfur species (RSS). Based on this, NIR-II Cy3s were used for reversible monitoring of HClO/RSS-mediated redox processes in the pathophysiology environment. Finally, NIR-II Cy3-988 was successfully utilized for assessment of the redox environments and drug treatment effects in acute inflammation model.
Conflict of interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available in the Supporting Information 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 |
|---|---|
| ange202211409-sup-0001-misc_information.pdf9.8 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
- 1aA. L. Antaris, H. Chen, S. Diao, Z. R. Ma, Z. Zhang, S. J. Zhu, J. Wang, A. X. Lozano, Q. L. Fan, L. Chew, M. Zhu, K. Cheng, X. C. Hong, H. J. Dai, Z. Cheng, Nat. Commun. 2017, 8, 15269;
- 1bE. D. Cosco, J. R. Caram, O. T. Bruns, D. Franke, R. A. Day, E. P. Farr, M. G. Bawendi, E. M. Sletten, Angew. Chem. Int. Ed. 2017, 56, 13126–13129; Angew. Chem. 2017, 129, 13306–13309;
- 1cJ. G. Huang, C. Xie, X. D. Zhang, Y. Y. Jiang, J. C. Li, Q. L. Fan, K. Y. Pu, Angew. Chem. Int. Ed. 2019, 58, 15120–15127; Angew. Chem. 2019, 131, 15264–15271.
- 2
- 2aB. Li, L. Lu, M. Zhao, Z. Lei, F. Zhang, Angew. Chem. Int. Ed. 2018, 57, 7483–7487; Angew. Chem. 2018, 130, 7605–7609;
- 2bR. Tian, H. Ma, S. Zhu, J. Lau, R. Ma, Y. Liu, L. Lin, S. Chandra, S. Wang, X. Zhu, H. Deng, G. Niu, M. Zhang, A. L. Antaris, K. S. Hettie, B. Yang, Y. Liang, X. Chen, Adv. Mater. 2020, 32, 1907365;
- 2cH. J. Zhou, T. B. Ren, Chem. Asian J. 2022, 17, e202200147.
- 3K. Welsher, Z. Liu, S. P. Sherlock, J. T. Robinson, Z. Chen, D. Daranciang, H. J. Dai, Nat. Nanotechnol. 2009, 4, 773–780.
- 4
- 4aB. Li, M. Zhao, L. Feng, C. Dou, S. Ding, G. Zhou, L. Lu, H. Zhang, F. Chen, X. Li, G. Li, S. Zhao, C. Jiang, Y. Wang, D. Zhao, Y. Cheng, F. Zhang, Nat. Commun. 2020, 11, 3102;
- 4bQ. L. Yang, Z. B. Hu, S. J. Zhu, R. Ma, H. L. Ma, Z. R. Ma, H. Wan, T. Zhu, Z. Y. Jiang, W. Q. Liu, L. Y. Jiao, H. T. Sun, Y. Y. Liang, H. J. Dai, J. Am. Chem. Soc. 2018, 140, 1715–1724;
- 4cD. Liu, Z. He, Y. Zhao, Y. Yang, W. Shi, X. Li, H. M. Ma, J. Am. Chem. Soc. 2021, 143, 17136–17143;
- 4dY. Li, Z. Cai, S. Liu, H. Zhang, S. T. H. Wong, J. W. Y. Lam, R. T. K. Kwok, J. Qian, B. Z. Tang, Nat. Commun. 2020, 11, 1255.
- 5
- 5aM. Yang, R. Gui, H. Jin, Z. Wang, F. Zhang, J. Xia, S. Bi, Y. Xia, Colloids Surf. B 2015, 126, 115–120;
- 5bZ. Y. Liu, A. A. Liu, H. Fu, Q. Y. Cheng, M. Y. Zhang, M. M. Pan, L. P. Liu, M. Y. Luo, B. Tang, W. Zhao, J. Kong, X. Shao, D. W. Pang, J. Am. Chem. Soc. 2021, 143, 12867–12877;
- 5cY. Du, B. Xu, T. Fu, M. Cai, F. Li, Y. Zhang, Q. Wang, J. Am. Chem. Soc. 2010, 132, 1470–1471;
- 5dO. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, M. G. Bawendi, Nat. Biomed. Eng. 2017, 1, 0056.
- 6
- 6aS. Wang, J. Liu, G. Feng, L. G. Ng, B. Liu, Adv. Funct. Mater. 2019, 29, 1808365;
- 6bG. Hong, Y. Zou, A. L. Antaris, S. Diao, D. Wu, K. Cheng, X. Zhang, C. Chen, B. Liu, Y. He, J. Z. Wu, J. Yuan, B. Zhang, Z. Tao, C. Fukunaga, H. Dai, Nat. Commun. 2014, 5, 4206;
- 6cM. H. Liu, Z. Zhang, Y. C. Yang, Y. H. Chan, Angew. Chem. Int. Ed. 2021, 60, 983–989; Angew. Chem. 2021, 133, 996–1002.
- 7
- 7aR. Wang, X. Li, L. Zhou, F. Zhang, Angew. Chem. Int. Ed. 2014, 53, 12086–12090; Angew. Chem. 2014, 126, 12282–12286;
- 7bD. J. Naczynski, M. C. Tan, M. Zevon, B. Wall, J. Kohl, A. Kulesa, S. Chen, C. M. Roth, R. E. Riman, P. V. Moghe, Nat. Commun. 2013, 4, 2199.
- 8X. R. Song, W. Zhu, X. G. Ge, R. F. Li, S. H. Li, X. Chen, J. B. Song, J. P. Xie, X. Y. Chen, H. H. Yang, Angew. Chem. Int. Ed. 2021, 60, 1306–1312; Angew. Chem. 2021, 133, 1326–1332.
- 9
- 9aD. Li, S. Wang, Z. Lei, C. Sun, A. M. El-Toni, M. S. Alhoshan, Y. Fan, F. Zhang, Anal. Chem. 2019, 91, 4771–4779;
- 9bR. Wang, J. Chen, J. Gao, J. A. Chen, G. Xu, T. Zhu, X. Gu, Z. Guo, W. H. Zhu, C. C. Zhao, Chem. Sci. 2019, 10, 7222–7227;
- 9cT. B. Ren, Z. Y. Wang, Z. Xiang, P. Lu, H. H. Lai, L. Yuan, X. B. Zhang, W. Tan, Angew. Chem. Int. Ed. 2021, 60, 800–805; Angew. Chem. 2021, 133, 813–818;
- 9dX. Zhang, X. Li, W. Shi, H. Ma, Chem. Commun. 2021, 57, 8174–8177;
- 9eY. Tang, Y. Li, X. Hu, H. Zhao, Y. Ji, L. Chen, W. Hu, W. Zhang, X. Li, X. Lu, W. Huang, Q. Fan, Adv. Mater. 2018, 30, 1801140;
- 9fJ. Ouyang, L. Sun, Z. Zeng, C. Zeng, F. Zeng, S. Wu, Angew. Chem. Int. Ed. 2020, 59, 10111–10121; Angew. Chem. 2020, 132, 10197–10207.
- 10
- 10aX. Ge, Y. Lou, L. Su, B. Chen, Z. Guo, S. Gao, W. Zhang, T. Chen, J. B. Song, H. Yang, Anal. Chem. 2020, 92, 6111–6120;
- 10bM. Zhao, J. Wang, Z. Lei, L. Lu, S. Wang, H. Zhang, B. Li, F. Zhang, Angew. Chem. Int. Ed. 2021, 60, 5091–5095; Angew. Chem. 2021, 133, 5151–5155.
- 11H. Zhang, Y. Fan, P. Pei, C. Sun, L. Lu, F. Zhang, Angew. Chem. Int. Ed. 2019, 58, 10153–10157; Angew. Chem. 2019, 131, 10259–10263.
- 12C. Chen, R. Tian, Y. Zeng, C. Chu, G. Liu, Bioconjugate Chem. 2020, 31, 276–292.
- 13
- 13aR. Gambino, G. Musso, M. Cassader, Antioxid. Redox Signaling 2011, 15, 1325–1365;
- 13bC. Liu, X. Jiao, S. Cai, S. He, X. Zeng, Sens. Actuators B 2021, 329, 129213.
- 14
- 14aR. J. Mailloux, D. Craig Ayre, S. L. Christian, Redox. Biol. 2016, 8, 285–297;
- 14bA. Stein, S. M. Bailey, Redox. Biol. 2013, 1, 32–39;
- 14cG. Fujino, T. Noguchi, K. Takeda, H. Ichijo, Semin. Cancer Biol. 2006, 16, 427–435;
- 14dY. X. Lu, Q. N. Wu, D. L. Chen, L. Z. Chen, Z. X. Wang, C. Ren, H. Y. Mo, Y. Chen, H. Sheng, Y. N. Wang, Theranostics 2018, 8, 1312–1326;
- 14eX. Liu, L. He, X. Gong, Y. Yang, D. Cheng, J. Peng, L. Wang, X.-B. Zhang, L. Yuan, CCS Chem. 2022, 4, 356–368.
- 15
- 15aZ. Lei, C. Sun, P. Pei, S. Wang, D. Li, X. Zhang, F. Zhang, Angew. Chem. Int. Ed. 2019, 58, 8166–8171; Angew. Chem. 2019, 131, 8250–8255;
- 15bM. Zhao, B. Li, Y. Wu, H. He, X. Zhu, H. Zhang, C. Dou, L. Feng, Y. Fan, F. Zhang, Adv. Mater. 2020, 32, 2001172;
- 15cC. Li, W. Li, H. Liu, Y. Zhang, G. Chen, Z. Li, Q. Wang, Angew. Chem. Int. Ed. 2020, 59, 247–252; Angew. Chem. 2020, 132, 253–258
- 16
- 16aX. Zhang, Y. Chen, H. He, S. Wang, Z. Lei, F. Zhang, Angew. Chem. Int. Ed. 2021, 60, 26337–26341; Angew. Chem. 2021, 133, 26541–26545;
- 16bK. Dou, C. Fan, W. Feng, Y. kong, Y. Xiang, Z. Wang, Z. Liu, CCS Chem. 2021, 3, 3567–3584.
- 17G. Xu, Q. Yan, X. Lv, Y. Zhu, K. Xin, B. Shi, R. Wang, J. Chen, W. Gao, P. Shi, C. Fan, C. Zhao, H. Tian, Angew. Chem. Int. Ed. 2018, 57, 3626–3630; Angew. Chem. 2018, 130, 3688–3692.
- 18S. Wang, W. X. Ren, J. T. Hou, M. Won, J. An, X. Chen, J. Shu, J. S. Kim, Chem. Soc. Rev. 2021, 50, 8887–8902.
- 19W. Sun, S. Guo, C. Hu, J. Fan, X. Peng, Chem. Rev. 2016, 116, 7768–7817.
- 20J. L. Bricks, A. D. Kachkovskii, Y. L. Slominskii, A. O. Gerasov, S. V. Popov, Dyes Pigm. 2015, 121, 238–255.
- 21
- 21aE. D. Cosco, A. L. Spearman, S. Ramakrishnan , J. G. P. Lingg, M. Saccomano, M. Pengshung, B. A. Arús , K. C. Y. Wong , S. Glasl, V. Ntziachristos , M. Warmer, R. R. McLaughlin, O. T. Bruns , E. M. Sletten, Nat. Chem. 2020, 12, 1123–1130;
- 21bE. D. Cosco, B. A. Arus, A. L. Spearman, T. L. Atallah, I. Lim, O. S. Leland, J. R. Caram, T. S. Bischof, O. T. Bruns, E. M. Sletten, J. Am. Chem. Soc. 2021, 143, 6836–6846.
- 22S. Wang, Y. Fan, D. Li, C. Sun, Z. Lei, L. Lu, T. Wang, F. Zhang, Nat. Commun. 2019, 10, 1058.
- 23
- 23aB. B. Ding, Y. L. Xiao, H. Zhou, X. Zhang, C. R. Qu, F. C. Xu, Z. X. Deng, Z. Cheng, X. C. Hong, J. Med. Chem. 2019, 62, 2049–2059;
- 23bX. Ma, Y. Huang, S. A. A. Abedi, H. Kim, T. T. B. Davin, X. Liu, W.-C. Yang, Y. Sun, S. Liu, J. Yin, J. Yoon, G.-F. Yang, CCS Chem. 2022, 4, 1961–1976.
- 24
- 24aX. Jia, Q. Chen, Y. Yang, Y. Tang, R. Wang, Y. Xu, W. Zhu, X. Qian, J. Am. Chem. Soc. 2016, 138, 10778–10781;
- 24bD. Oushiki, H. Kojima, T. Terai, M. Arita, K. Hanaoka, Y. Urano, T. Nagano, J. Am. Chem. Soc. 2010, 132, 2795–2801;
- 24cZ. Wang, T. D. Cong, W. Zhong, J. W. Lau, G. Kwek, M. B. Chan-Park, B. Xing, Angew. Chem. Int. Ed. 2021, 60, 16900–16905; Angew. Chem. 2021, 133, 17037–17042.
- 25L. Yuan, W. Y. Lin, Y. T. Yang, H. Chen, J. Am. Chem. Soc. 2012, 134, 1200–1211.
- 26L. Yuan, W. Lin, S. Zhao, W. Gao, B. Chen, L. He, S. Zhu, J. Am. Chem. Soc. 2012, 134, 13510–13523.
- 27O. E. Semonin, J. C. Johnson, J. M. Luther, A. G. Midgett, A. J. Nozik, M. C. Beard, J. Phys. Chem. Lett. 2010, 1, 2445–2450.
- 28
- 28aT. B. Ren, W. Xu, W. Zhang, X. X. Zhang, Z. Y. Wang, Z. Xiang, L. Yuan, X. B. Zhang, J. Am. Chem. Soc. 2018, 140, 7716–7722;
- 28bE. Y. Zhou, H. J. Knox, C. Liu, W. Zhao, J. Chan, J. Am. Chem. Soc. 2019, 141, 17601–17609.
- 29K. Ponnuvel, J. Ramamoorthy, G. Sivaraman, V. Padmini, ChemistrySelect 2018, 3, 91–95.
- 30J. J. Chen, Y. C. Fang, L. H. Sun, F. Zeng, S. Z. Wu, Chem. Commun. 2020, 56, 11102–11105.
- 31
- 31aP. K. Moore, M. Whiteman, Handb. Exp. Pharmacol. 2015, 230, 3–25;
- 31bJ. Rost, S. Rapoport, Nature 1964, 201, 185;
- 31cD. A. Keire, E. Strauss, W. Guo, B. Noszal, D. L. Rabenstein, J. Org. Chem. 1992, 57, 123–127;
- 31dS. Sundaram, M. A. Kadir, A. S. Kumar, P. Nagamony, V. Chinnuswamy, Anal. Methods 2017, 9, 6791–6800.
- 32
- 32aH. R. Griffiths, D. Gao, C. Pararasa, Redox. Biol. 2017, 12, 50–57;
- 32bB. Wang, P. Li, F. Yu, P. Song, X. Sun, S. Yang, Z. Lou, K. Han, Chem. Commun. 2013, 49, 1014–1016;
- 32cT. Annaka, N. Nakata, A. Ishii, New J. Chem. 2019, 43, 11643–11652.
- 33
- 33aB. van der Veen, M. de Winther, P. Heeringa, Antioxid. Redox Signaling 2009, 11, 2899–2937;
- 33bE. Kolaczkowska, P. Kubes, Nat. Rev. Immunol. 2013, 13, 159–175;
- 33cY. Oishi, I. Manabe, Int. Immunol. 2018, 30, 511–528.
- 34
- 34aC. M. Whitfield-Cargile, N. D. Cohen, R. S. Chapkin, B. R. Weeks, L. A. Davidson, J. S. Goldsby, C. L. Hunt, S. H. Steinmeyer, R. Menon, J. S. Suchodolski, A. Jayaraman, R. C. Alaniz, Gut Microbes 2016, 7, 246–261;
- 34bG. C. Machado, C. Abdel-Shaheed, M. Underwood, R. O. Day, BMJ 2021, 372, n104.
- 35A. R. Bourgonje, A. K. Offringa, L. E. van Eijk, A. E. Abdulle, J. L. Hillebrands, P. H. J. van der Voort, H. van Goor, E. J. van Hezik, Antioxid. Redox Signaling 2021, 35, 1207–1225.
- 36A. Strzepa, K. A. Pritchard, B. N. Dittel, Cell. Immunol. 2017, 317, 1–8.
- 37
- 37aP. M. Brooks, W. Hill, R. Geddes, Med. J. Aust. 1980, 1, 29–30;
- 37bR. C. Zanardo, V. Brancaleone, E. Distrutti, S. Fiorucci, G. Cirino, J. L. Wallace, FASEB J. 2006, 20, 2118–2120.
- 38S. Abramson, H. Korchak, R. Ludewig, H. Edelson, K. Haines, R. I. Levin, R. Herman, L. Rider, K. G. Weissmann, Proc. Natl. Acad. Sci. USA 1985, 82, 7227–7231.
- 39X. Zhang, T. Ren, Q. Zhang, T. Zeng, Z. Li, F. Yang, X. Zhang, L. Yuan, Cell Rep. Phys. Sci. 2021, 2, 100471.
- 40Z. Qin, T. B. Ren, H. Zhou, X. Zhang, L. He, Z. Li, X. B. Zhang, L. Yuan, Angew. Chem. Int. Ed. 2022, 61, e202201541; Angew. Chem. 2022, 134, e202201541.
- 41R. M. Pope, S. Shahrara, Nat. Rev. Rheumatol. 2013, 9, 252–256.
- 42B. D. Paul, S. H. Snyder, Nat. Rev. Mol. Cell Biol. 2012, 13, 499–507.
- 43H. R. Ding, J. L. Wang, H. Z. Ren, X. L. Shi, BioMed Res. Int. 2018, 2018, 1287127.
- 44L. H. Ottesen, A. Flyvbjerg, S. MØller, F. Bendtsen, Aliment. Pharmacol. Ther. 1998, 12, 657–665.
- 45B. Pedre, U. Barayeu, D. Ezeriņa, T. P. Dick, Pharmacol. Ther. 2021, 228, 107916.
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.
