NIR-II Hydrogen-Bonded Organic Frameworks (HOFs) Used for Target-Specific Amyloid-β Photooxygenation in an Alzheimer's Disease Model
Haochen Zhang
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorDongqin Yu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorShuting Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorChun Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorZhenqi Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorProf. Jinsong Ren
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Xiaogang Qu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorHaochen Zhang
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorDongqin Yu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
These authors contributed equally to this work.
Search for more papers by this authorShuting Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorChun Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorZhenqi Liu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorProf. Jinsong Ren
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorCorresponding Author
Prof. Xiaogang Qu
Laboratory of Chemical Biology and State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Science, Changchun, Jilin, 130022 P. R. China
University of Science and Technology of China, Hefei, Anhui, 230026 P. R. China
Search for more papers by this authorGraphical Abstract
NIR-II hydrogen-bonded organic frameworks (HOFs) were devised to oxidize β-amyloid spatiotemporally and noninvasively. The well-designed photocatalyst shows an inhibitory effect of Aβ aggregation and recovery of memory deficits in triple-transgenic AD model mice upon the NIR-II irradiation.
Abstract
Phototherapy has emerged as a powerful approach for interrupting β-amyloid (Aβ) self-assembly. However, deeper tissue penetration and safer photosensitizers are urgent to be exploited for avoiding damaging nearby normal tissues and improving therapeutic effectiveness. A hydrogen-bonded organic framework (HOF)-based NIR-II photooxygenation catalyst is presented here to settle the abovementioned challenges. By encapsulating the pyridinium hemicyanine dye DSM with a large two-photon absorption (TPA) cross-section in NIR-II window into the porphyrin-based HOF, the resultant DSM@n-HOF-6 exhibits significant two-photon NIR-II-excited Fluorescence Resonance Energy Transfer (FRET) to generate singlet oxygen (1O2) for Aβ oxidation. Further, the target peptides of KLVFFAED (KD8) are covalently grafted on DSM@n-HOF-6 to enhance the blood–brain barrier (BBB) permeability and Aβ selectivity. The HOF-based photooxygenation catalyst shows an outstanding inhibitory effect of Aβ aggregation upon the NIR-II irradiation. Further in vivo studies demonstrate the obvious decrease of craniocerebral Aβ plaques and recovery of memory deficits in triple-transgenic AD (3×Tg-AD) model mice.
Conflict of interest
The authors declare no conflict of interest.
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 |
|---|---|
| anie202109068-sup-0001-misc_information.pdf3.8 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
- 1J. Hardy, D. J. Selkoe, Science 2002, 297, 353–356.
- 2H. W. Querfurth, F. M. LaFerla, N. Engl. J. Med. 2010, 362, 329–344.
- 3R. Riek, D. S. Eisenberg, Nature 2016, 539, 227–235.
- 4P. C. Ke, M. A. Sani, F. Ding, A. Kakinen, I. Javed, F. Separovic, T. P. Davis, R. Mezzenga, Chem. Soc. Rev. 2017, 46, 6492–6531.
- 5J. Wang, B. J. Gu, C. L. Masters, Y. J. Wang, Nat. Rev. Neurol. 2017, 13, 612–623.
- 6Z. Du, M. Li, J. Ren, X. Qu, Acc. Chem. Res. 2021, 54, 2172–2184.
- 7H. Wang, X. Xu, Y. C. Pan, Y. Yan, X. Y. Hu, R. Chen, B. J. Ravoo, D. S. Guo, T. Zhang, Adv. Mater. 2021, 33, 2006483.
- 8D. Yu, C. Liu, H. Zhang, J. Ren, X. Qu, Chem. Sci. 2021, 12, 4963–4969.
- 9Y. Guan, Z. Du, N. Gao, Y. Cao, X. Wang, P. Scott, H. Song, J. Ren, X. Qu, Sci. Adv. 2018, 4, eaao6718.
- 10P. C. Ke, E. H. Pilkington, Y. Sun, I. Javed, A. Kakinen, G. Peng, F. Ding, T. P. Davis, Adv. Mater. 2020, 32, 1901690.
- 11K. Hou, J. Zhao, H. Wang, B. Li, K. Li, X. Shi, K. Wan, J. Ai, J. Lv, D. Wang, Q. Huang, H. Wang, Q. Cao, S. Liu, Z. Tang, Nat. Commun. 2020, 11, 4790.
- 12H. Sun, J. Liu, S. Li, L. Zhou, J. Wang, L. Liu, F. Lv, Q. Gu, B. Hu, Y. Ma, S. Wang, Angew. Chem. Int. Ed. 2019, 58, 5988–5993; Angew. Chem. 2019, 131, 6049–6054.
- 13Y. S. Eisele, C. Monteiro, C. Fearns, S. E. Encalada, R. L. Wiseman, E. T. Powers, J. W. Kelly, Nat. Rev. Drug Discovery 2015, 14, 759–780.
- 14H. Jung, Y. J. Chung, R. Wilton, C. H. Lee, B. I. Lee, J. Lim, H. Lee, J. H. Choi, H. Kang, B. Lee, E. A. Rozhkova, C. B. Park, J. Lee, Adv. Funct. Mater. 2020, 30, 1910475.
- 15H. Sun, Y. Zhong, X. Zhu, H. Liao, J. Lee, Y. Chen, L. Ma, J. Ren, M. Zhao, M. Tu, F. Li, H. Zhang, M. Tian, D. Ling, ACS Nano 2021, 15, 5263–5275.
- 16Y. Sohma, M. Kanai in Handbook of In Vivo Chemistry in Mice (Eds.: K. Tanaka, K. Vong), Wiley-VCH, Weinheim, 2020, pp. 355–371.
- 17B. I. Lee, Y. J. Chung, C. B. Park, Biomaterials 2019, 190–191, 121–132.
- 18Z. Liu, M. Ma, D. Yu, J. Ren, X. Qu, Chem. Sci. 2020, 11, 11003–11008.
- 19N. Nagashima, S. Ozawa, M. Furuta, M. Oi, Y. Hori, T. Tomita, Y. Sohma, M. Kanai, Sci. Adv. 2021, 7, eabc9750.
- 20P. Bondia, J. Torra, C. M. Tone, T. Sawazaki, A. Del Valle, B. Sot, S. Nonell, M. Kanai, Y. Sohma, C. Flors, J. Am. Chem. Soc. 2020, 142, 922–930.
- 21D. Yu, Y. Guan, F. Bai, Z. Du, N. Gao, J. Ren, X. Qu, Chem. Eur. J. 2019, 25, 3489–3495.
- 22K. Kim, S. H. Lee, D. S. Choi, C. B. Park, Adv. Funct. Mater. 2018, 28, 1802813.
- 23A. Taniguchi, Y. Shimizu, K. Oisaki, Y. Sohma, M. Kanai, Nat. Chem. 2016, 8, 974–982.
- 24B. I. Lee, S. Lee, Y. S. Suh, J. S. Lee, A. K. Kim, O. Y. Kwon, K. Yu, C. B. Park, Angew. Chem. Int. Ed. 2015, 54, 11472–11476; Angew. Chem. 2015, 127, 11634–11638.
- 25A. Taniguchi, D. Sasaki, A. Shiohara, T. Iwatsubo, T. Tomita, Y. Sohma, M. Kanai, Angew. Chem. Int. Ed. 2014, 53, 1382–1385; Angew. Chem. 2014, 126, 1406–1409.
- 26Y. Ishida, S. Tanimoto, D. Takahashi, K. Toshima, MedChemComm 2010, 1, 212.
- 27Y. Li, Z. Du, X. Liu, M. Ma, D. Yu, Y. Lu, J. Ren, X. Qu, Small 2019, 15, 1901116.
- 28Z. Du, N. Gao, X. Wang, J. Ren, X. Qu, Small 2018, 14, 1801852.
- 29H. Zhang, C. Hao, A. Qu, M. Sun, L. Xu, C. Xu, H. Kuang, Angew. Chem. Int. Ed. 2020, 59, 7131–7138; Angew. Chem. 2020, 132, 7197–7204.
- 30Y. Heo, K. Kim, J. Kim, J. Jang, C. B. Park, ACS Appl. Mater. Interfaces 2020, 12, 23667–23676.
- 31J. Wang, Y. Fan, Y. Tan, X. Zhao, Y. Zhang, C. Cheng, M. Yang, ACS Appl. Mater. Interfaces 2018, 10, 36615–36621.
- 32J. Ni, A. Taniguchi, S. Ozawa, Y. Hori, Y. Kuninobu, T. Saito, T. C. Saido, T. Tomita, Y. Sohma, M. Kanai, Chem 2018, 4, 807–820.
- 33S. Kuk, B. I. Lee, J. S. Lee, C. B. Park, Small 2017, 13, 1603139.
- 34G. Hong, A. L. Antaris, H. Dai, Nat. Biomed. Eng. 2017, 1, 0010.
- 35Y. Jiang, J. Huang, C. Xu, K. Pu, Nat. Commun. 2021, 12, 742.
- 36M. Ma, N. Gao, X. Li, Z. Liu, Z. Pi, X. Du, J. Ren, X. Qu, ACS Nano 2020, 14, 9894–9903.
- 37B. Guo, Z. Sheng, D. Hu, C. Liu, H. Zheng, B. Liu, Adv. Mater. 2018, 30, 1802591.
- 38H. Lin, S. Gao, C. Dai, Y. Chen, J. Shi, J. Am. Chem. Soc. 2017, 139, 16235–16247.
- 39Y. Jiang, J. Li, X. Zhen, C. Xie, K. Pu, Adv. Mater. 2018, 30, 1705980.
- 40H. Xiang, H. Lin, L. Yu, Y. Chen, ACS Nano 2019, 13, 2223–2235.
- 41W. Guo, C. Guo, N. Zheng, T. Sun, S. Liu, Adv. Mater. 2017, 29, 1604157.
- 42Q. Chen, J. Chen, Z. Yang, L. Zhang, Z. Dong, Z. Liu, Nano Res. 2018, 11, 5657–5669.
- 43H. Zhang, T. Wang, H. Liu, F. Ren, W. Qiu, Q. Sun, F. Yan, H. Zheng, Z. Li, M. Gao, Nanoscale 2019, 11, 7600–7608.
- 44L. Jin, S. Shen, Y. Huang, D. Li, X. Yang, Biomaterials 2021, 268, 120582.
- 45D. Wang, H. Wang, L. Ji, M. Xu, B. Bai, X. Wan, D. Hou, Z.-Y. Qiao, H. Wang, J. Zhang, ACS Nano 2021, 15, 8694–8705.
- 46Z. Cheng, A. Al Zaki, J. Z. Hui, V. R. Muzykantov, A. Tsourkas, Science 2012, 338, 903–910.
- 47L. Cheng, C. Wang, L. Feng, K. Yang, Z. Liu, Chem. Rev. 2014, 114, 10869–10939.
- 48A. C. Anselmo, S. Mitragotri, Bioeng. Transl. Med. 2016, 1, 10–29.
- 49G. Yu, X. Zhao, J. Zhou, Z. Mao, X. Huang, Z. Wang, B. Hua, Y. Liu, F. Zhang, Z. He, O. Jacobson, C. Gao, W. Wang, C. Yu, X. Zhu, F. Huang, X. Chen, J. Am. Chem. Soc. 2018, 140, 8005–8019.
- 50S. Wang, H. Chen, J. Liu, C. Chen, B. Liu, Adv. Funct. Mater. 2020, 30, 2002546.
- 51H. Bian, D. Ma, X. Zhang, K. Xin, Y. Yang, X. Peng, Y. Xiao, Small 2021, 17, 2100398.
- 52M. A. Rajora, J. W. H. Lou, G. Zheng, Chem. Soc. Rev. 2017, 46, 6433–6469.
- 53B. Wang, R. B. Lin, Z. Zhang, S. Xiang, B. Chen, J. Am. Chem. Soc. 2020, 142, 14399–14416.
- 54R. B. Lin, Y. He, P. Li, H. Wang, W. Zhou, B. Chen, Chem. Soc. Rev. 2019, 48, 1362–1389.
- 55I. Hisaki, C. Xin, K. Takahashi, T. Nakamura, Angew. Chem. Int. Ed. 2019, 58, 11160–11170; Angew. Chem. 2019, 131, 11278–11288; Corrigendum: I. Hisaki, C. Xin, K. Takahashi, T. Nakamura, Angew. Chem. Int. Ed. 2019, 58, 14794–14794; Angew. Chem. 2019, 131, 14938–14938.
- 56H. Yamagishi, H. Sato, A. Hori, Y. Sato, R. Matsuda, K. Kato, T. Aida, Science 2018, 361, 1242–1246.
- 57Y. He, S. Xiang, B. Chen, J. Am. Chem. Soc. 2011, 133, 14570–14573.
- 58W. Yang, A. Greenaway, X. Lin, R. Matsuda, A. J. Blake, C. Wilson, W. Lewis, P. Hubberstey, S. Kitagawa, N. R. Champness, M. Schröder, J. Am. Chem. Soc. 2010, 132, 14457–14469.
- 59L. Yu-Lin, Y. Qi, L. Tian-Fu, C. Rong, Y. Wen-Bing, Chin. J. Struct. Chem. 2019, 38, 2083–2088.
- 60G. A. Jeffrey, An Introduction to Hydrogen Bonding, Oxford University Press, New York, 1997.
- 61T. Steiner, Angew. Chem. Int. Ed. 2002, 41, 48–76; Angew. Chem. 2002, 114, 50–80.
- 62P. Li, P. Li, M. R. Ryder, Z. Liu, C. L. Stern, O. K. Farha, J. F. Stoddart, Angew. Chem. Int. Ed. 2019, 58, 1664–1669; Angew. Chem. 2019, 131, 1678–1683.
- 63B. Han, H. Wang, C. Wang, H. Wu, W. Zhou, B. Chen, J. Jiang, J. Am. Chem. Soc. 2019, 141, 8737–8740.
- 64T.-U. Yoon, S. B. Baek, D. Kim, E.-J. Kim, W.-G. Lee, B. K. Singh, M. S. Lah, Y.-S. Bae, K. S. Kim, Chem. Commun. 2018, 54, 9360–9363.
- 65Z. Bao, D. Xie, G. Chang, H. Wu, L. Li, W. Zhou, H. Wang, Z. Zhang, H. Xing, Q. Yang, M. J. Zaworotko, Q. Ren, B. Chen, J. Am. Chem. Soc. 2018, 140, 4596–4603.
- 66A. Pulido, L. Chen, T. Kaczorowski, D. Holden, M. A. Little, S. Y. Chong, B. J. Slater, D. P. McMahon, B. Bonillo, C. J. Stackhouse, A. Stephenson, C. M. Kane, R. Clowes, T. Hasell, A. I. Cooper, G. M. Day, Nature 2017, 543, 657–664.
- 67F. Hu, C. Liu, M. Wu, J. Pang, F. Jiang, D. Yuan, M. Hong, Angew. Chem. Int. Ed. 2017, 56, 2101–2104; Angew. Chem. 2017, 129, 2133–2136.
- 68Q. Yin, P. Zhao, R. J. Sa, G. C. Chen, J. Lu, T. F. Liu, R. Cao, Angew. Chem. Int. Ed. 2018, 57, 7691–7696; Angew. Chem. 2018, 130, 7817–7822.
- 69Y. Yang, L. Li, R.-B. Lin, Y. Ye, Z. Yao, L. Yang, F. Xiang, S. Chen, Z. Zhang, S. Xiang, B. Chen, Nat. Chem. 2021, 13, 933–939.
- 70H. Wang, B. Li, H. Wu, T.-L. Hu, Z. Yao, W. Zhou, S. Xiang, B. Chen, J. Am. Chem. Soc. 2015, 137, 9963–9970.
- 71I. Hisaki, S. Nakagawa, Y. Suzuki, N. Tohnai, Chem. Lett. 2018, 47, 1143–1146.
- 72B. T. Liu, X. H. Pan, D. Y. Nie, X. J. Hu, E. P. Liu, T. F. Liu, Adv. Mater. 2020, 32, 2005912.
- 73V. Almeida-Marrero, E. van de Winckel, E. Anaya-Plaza, T. Torres, A. de la Escosura, Chem. Soc. Rev. 2018, 47, 7369–7400.
- 74J. M. Park, K.-I. Hong, H. Lee, W.-D. Jang, Acc. Chem. Res. 2021, 54, 2249–2260.
- 75S. Lin, C. S. Diercks, Y.-B. Zhang, N. Kornienko, E. M. Nichols, Y. Zhao, A. R. Paris, D. Kim, P. Yang, O. M. Yaghi, C. J. Chang, Science 2015, 349, 1208–1213.
- 76J. Chen, Y. Zhu, S. Kaskel, Angew. Chem. Int. Ed. 2021, 60, 5010–5035; Angew. Chem. 2021, 133, 5064–5091.
- 77L. Zhang, S. Wang, Y. Zhou, C. Wang, X. Z. Zhang, H. Deng, Angew. Chem. Int. Ed. 2019, 58, 14213–14218; Angew. Chem. 2019, 131, 14351–14356.
- 78M. Lismont, L. Dreesen, S. Wuttke, Adv. Funct. Mater. 2017, 27, 1606314.
- 79K. Lu, C. He, W. Lin, J. Am. Chem. Soc. 2014, 136, 16712–16715.
- 80M. Ma, Z. Liu, N. Gao, Z. Pi, X. Du, J. Ren, X. Qu, J. Am. Chem. Soc. 2020, 142, 21702–21711.
- 81Y. Lu, Z. Guo, Y. Zhang, C. Li, Y. Zhang, Q. Guo, Q. Chen, X. Chen, X. He, L. Liu, C. Ruan, T. Sun, B. Ji, W. Lu, C. Jiang, Adv. Sci. 2019, 6, 1801586.
- 82E. Cuevas, H. Rosas-Hernandez, S. M. Burks, M. A. Ramirez-Lee, A. Guzman, S. Z. Imam, S. F. Ali, S. Sarkar, Metab. Brain Dis. 2019, 34, 1365–1374.
- 83G. R. Desiraju, T. Steiner, The weak hydrogen bond: in structural chemistry and biology, Vol. 9, International Union of Crystal, Oxford, 2001.
10.1093/acprof:oso/9780198509707.001.0001 Google Scholar
- 84A. L. Spek, J. Appl. Crystallogr. 2003, 36, 7–13.
- 85W. Liang, F. Carraro, M. B. Solomon, S. G. Bell, H. Amenitsch, C. J. Sumby, N. G. White, P. Falcaro, C. J. Doonan, J. Am. Chem. Soc. 2019, 141, 14298–14305.
- 86J.-L. Lin, Z.-K. Wang, Z.-Y. Xu, L. Wei, Y.-C. Zhang, H. Wang, D.-W. Zhang, W. Zhou, Y.-B. Zhang, Y. Liu, Z.-T. Li, J. Am. Chem. Soc. 2020, 142, 3577–3582.
- 87M. Wang, J. Tang, J. Liu, Q. Zheng, W. Li, J. Sheng, L. Mao, Angew. Chem. Int. Ed. 2021, 60, 22315; Angew. Chem. 2021, 133, 22489.
- 88Z. Wang, Y. Zhang, E. Ju, Z. Liu, F. Cao, Z. Chen, J. Ren, X. Qu, Nat. Commun. 2018, 9, 3334.
- 89I. U. Ali, X. Chen, ACS Nano 2015, 9, 9470–9474.
- 90D. Gopalan, A. Pandey, N. Udupa, S. Mutalik, J. Controlled Release 2020, 319, 183–200.
- 91W. Chen, J. Ouyang, X. Yi, Y. Xu, C. Niu, W. Zhang, L. Wang, J. Sheng, L. Deng, Y.-N. Liu, S. Guo, Adv. Mater. 2018, 30, 1703458.
- 92B. Guo, Z. Sheng, Kenry, D. Hu, X. Lin, S. Xu, C. Liu, H. Zheng, B. Liu, Mater. Horiz. 2017, 4, 1151–1156.
