NIR-Triggered Multifunctional NO Nanoplatform for Conquering Thermal Resistance in Biofilms
Bingshuai Zhou
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorCorresponding Author
Biao Dong
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorSongtao Hu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorWei Liu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLiheng Sun
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLin Xu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorXue Bai
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLin Wang
Department of Oral Implantology, Jilin Provincial Key Laboratory of Sciences and Technology for Stomatology Nanoengineering, School and Hospital of Stomatology, Jilin University, Changchun, 130021 China
Search for more papers by this authorCorresponding Author
Manlin Qi
Department of Oral Implantology, Jilin Provincial Key Laboratory of Sciences and Technology for Stomatology Nanoengineering, School and Hospital of Stomatology, Jilin University, Changchun, 130021 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Hongwei Song
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorBingshuai Zhou
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorCorresponding Author
Biao Dong
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorSongtao Hu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorWei Liu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLiheng Sun
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLin Xu
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorXue Bai
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
Search for more papers by this authorLin Wang
Department of Oral Implantology, Jilin Provincial Key Laboratory of Sciences and Technology for Stomatology Nanoengineering, School and Hospital of Stomatology, Jilin University, Changchun, 130021 China
Search for more papers by this authorCorresponding Author
Manlin Qi
Department of Oral Implantology, Jilin Provincial Key Laboratory of Sciences and Technology for Stomatology Nanoengineering, School and Hospital of Stomatology, Jilin University, Changchun, 130021 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Hongwei Song
State Key Laboratory on Integrated Optoelectronics, College of Electronic Science and Engineering, Jilin University, Changchun, 130012 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorAbstract
Photothermal treatment (PTT) has emerged as a promising avenue for biofilm elimination, yet its potential drawbacks, such as local hyperpyrexia and bacterial heat resistance, have posed challenges. To address these concerns, an innovative nanoplatform (Au@mSiO2-arg/ICG) is devised that integrates phototherapeutic and gas therapeutic functionalities. This multifaceted nanoplatform is composed of mesoporous silica-coated Au nanorods (Au@mSiO2), supplemented with l-arginine (l-arg) and indocyanine green (ICG), and is engineered for mild temperature PTT aimed at biofilm eradication. Au@mSiO2-arg/ICG nanoparticles (NPs) show excellent antibacterial effects through the generation of nitric oxide (NO) gas, heat, and reactive oxygen species (ROS) under 808 nm light irradiation. The ROS generated by ICG initiates a cascade reaction with l-arg, ultimately yielding NO gas molecules. This localized release of NO not only effectively curbs the expression of heat shock proteins 70 mitigating bacterial thermoresistance, but also reduces extracellular polymeric substance allowing better penetration of the therapeutic agents. Furthermore, this nanoplatform achieves an outstanding biofilm elimination rate of over 99% in an abscess model under 808 nm light irradiation (0.8 W·cm−2), thereby establishing its potential as a dependable strategy for NO-enhanced mild PTT and antibacterial photodynamic therapy (aPDT) in clinical settings.
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 from the corresponding author upon reasonable request.
Supporting Information
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smll202310706-sup-0001-SuppMat.docx9.7 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
- 1L.-X. Yan, L.-J. Chen, X. Zhao, X.-P. Yan, Adv. Funct. Mater. 2020, 30, 1909042.
- 2H.-C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, S. Kjelleberg, Nat. Rev. Microbiol. 2016, 14, 563.
- 3H. C. Flemming, J. Wingender, Nat. Rev. Microbiol. 2010, 8, 623.
- 4Q. Q. Deng, P. P. Sun, L. Zhang, Z. W. Liu, H. Wang, J. S. Ren, X. G. Qu, Adv. Funct. Mater. 2019, 29, 1903018.
- 5Z. Yuan, C. C. Lin, Y. He, B. L. Tao, M. W. Chen, J. X. Zhang, P. Liu, K. Y. Cai, ACS Nano 2020, 14, 3546.
- 6Y. Chen, Y. J. Gao, Y. Chen, L. Liu, A. C. Mo, Q. Peng, J. Controlled Release 2020, 328, 251.
- 7J. Fang, Y. Wan, Y. Sun, X. L. Sun, M. L. Qi, S. Cheng, C. Y. Li, Y. M. Zhou, L. Xu, B. Dong, L. Wang, Chem. Eng. J. 2022, 435, 134935.
- 8M. Qi, X. Ren, W. Li, Y. Sun, X. Sun, C. Li, S. Yu, L. Xu, Y. Zhou, S. Song, B. Dong, L. Wang, Nano Today 2022, 43, 101447.
- 9X. R. Wu, M. L. Qi, C. Y. Liu, Q. J. Yang, S. J. Li, F. Y. Shi, X. L. Sun, L. Wang, C. Y. Li, B. Dong, Theranostics 2023, 13, 2350.
- 10Z. K. Liu, S. K. Li, Z. W. Yin, Z. T. Zhu, L. Chen, W. H. Tan, Z. Chen, Adv. Sci. 2022, 9, 2104576.
- 11J. W. Mei, D. D. Xu, L. T. Wang, L. T. Kong, Q. Liu, Q. M. Li, X. Z. Zhang, Z. Su, X. L. Hu, W. B. Zhu, M. Ye, J. X. Wang, C. Zhu, Adv. Mater. 2023, 35, 36.
- 12T. Luo, D. Wang, L. Liu, Y. Zhang, C. Han, Y. Xie, Y. Liu, J. Liang, G. Qiu, H. Li, D. Su, J. Liu, K. Zhang, Adv. Sci. 2021, 8, 2101065.
- 13M. Z. Sun, L. G. Xu, W. Ma, X. L. Wu, H. Kuang, L. B. Wang, C. L. Xu, Adv. Mater. 2016, 28, 898.
- 14D. Peng, G. H. Liu, Y. He, P. F. Gao, S. Q. Gou, J. Wu, J. X. Yu, P. Liu, K. Y. Cai, Biomater. Sci. 2021, 9, 7483.
- 15Z. Jahangirizadeh, H. Ghafouri, R. H. Sajedi, S. Sarikhan, M. Taghdir, R. Sariri, Int. Bio. l. Macromol. 2018, 108, 798.
- 16M. Y. Chang, Z. Y. Hou, M. Wang, C. Z. Yang, R. F. Wang, F. Li, D. L. Liu, T. L. Peng, C. X. Li, J. Lin, Angew. Chem., Int. Ed. 2021, 60, 12971.
- 17B. Zhou, X. Sun, B. Dong, S. Yu, L. Cheng, S. Hu, W. Liu, L. Xu, X. Bai, L. Wang, H. Song, Theranostics 2022, 12, 2580.
- 18Z. X. Wang, A. L. Jin, Z. Yang, W. Huang, ACS Nano 2023, 17, 8935.
- 19N. Yang, H. Guo, C. Y. Cao, X. R. Wang, X. J. Song, W. J. Wang, D. L. Yang, L. Xi, X. Z. Mou, X. C. Dong, Biomaterials 2021, 275, 120918.
- 20J. X. Wang, L. T. Wang, J. Pan, J. H. Zhao, J. Tang, D. J. Jiang, P. Hu, W. T. Jia, J. L. Shi, Adv. Sci. 2021, 8, 2004010.
- 21S. S. Wan, J. Y. Zeng, H. Cheng, X. Z. Zhang, Biomaterials 2018, 185, 51.
- 22M. Y. Chang, M. Wang, Y. H. Liu, M. Liu, Al. A. A. Kheraif, P. A. Ma, Y. L. Zhao, J. Lin, Small 2023, 19, 10.
- 23C. C. Wu, D. Q. Wang, M. P. Cen, L. Y. Cao, Y. Ding, J. Wang, X. L. Yuan, Y. Wang, T. T. Chen, Y. Yao, Chem. Commun. 2020, 56, 14491.
- 24H. T. Hu, D. Li, W. B. Dai, Q. Jin, D. Wang, J. Ji, B. Z. Tang, Z. Tang, Adv. Funct. Mater. 2023, 2213134.
10.1002/adfm.202213134 Google Scholar
- 25C. You, Y. Li, Y. Dong, L. Ning, Y. Zhang, L. Yao, F. Wang, ACS Biomater. Sci. Eng. 2020, 6, 1535.
- 26T. K. Sau, C. J. Murphy, Langmuir 2004, 20, 6414.
- 27X. Zhang, P. P. Yang, Y. L. Dai, P. A. Ma, X. J. Li, Z. Y. Cheng, Z. Y. Hou, X. J. Kang, C. X. Li, J. Lin, Adv. Funct. Mater. 2013, 23, 4067.
- 28P. Xue, M. Hou, L. Sun, Q. Li, L. Zhang, Z. Xu, Y. Kang, Acta Biomater. 2018, 81, 242.
- 29J. Chen, L. Liu, S. M. Motevalli, X. L. Wu, X. H. Yang, X. L. Li, L. Han, A. Magrini, W. S. Guo, J. Chang, M. Bottini, X. J. Liang, Adv. Funct. Mater. 2018, 28, 1707291.
- 30W. Fan, B. C. Yung, X. Chen, Angew. Chem., Int. Ed. 2018, 57, 8383.
- 31P. G. Wang, M. Xian, X. P. Tang, X. J. Wu, Z. Wen, T. W. Cai, A. J. Janczuk, Chem. Rev. 2002, 102, 1091.
- 32M. M. Wan, H. Chen, Q. Wang, Q. Niu, P. Xu, Y. Q. Yu, T. Y. Zhu, C. Mao, J. Shen, Nat. Commun. 2019, 10, 966.
- 33S. Kudo, Y. Nagasaki, J. Control. Release 2015, 217, 256.
- 34C. Youn, C. Pontaza, Y. Wang, D. A. Dikeman, D. P. Joyce, M. P. Alphonse, M.-J. Wu, S. J. Nolan, M. A. Anany, M. Ahmadi, J. Young, A. Tocaj, L. A. Garza, H. Wajant, L. S. Miller, N. K. Archer, Sci. Adv. 2023, 9, eadf8748.
- 35A. York, Nat. Rev. Microbiol. 2023, 21, 345.
- 36M. Li, L. Li, K. Su, X. Liu, T. Zhang, Y. Liang, D. Jing, X. Yang, D. Zheng, Z. Cui, Z. Li, S. Zhu, K. W. K. Yeung, Y. Zheng, X. Wang, S. Wu, Adv. Sci. 2019, 6, 1900599.
- 37Z. Yuan, B. L. Tao, Y. He, C. Y. Mu, G. H. Liu, J. X. Zhang, Q. Liao, P. Liu, K. Y. Cai, Biomaterials 2019, 223, 119479.
- 38L. J. Zhang, C. Y. Hu, M. Z. Sun, X. K. Ding, H. B. Cheng, S. Duan, F. J. Xu, Adv. Sci. 2023, 10, 14.
- 39A. G. Lin, Y. A. Liu, X. F. Zhu, X. Chen, J. W. Liu, Y. H. Zhou, X. Y. Qin, J. Liu, ACS Nano 2019, 13, 13965.
- 40E. M. Hetrick, J. H. Shin, N. A. Stasko, C. B. Johnson, D. A. Wespe, E. Holmuhamedov, M. H. Schoenfisch, ACS Nano 2008, 2, 235.
- 41J. Gehring, B. Trepka, N. Klinkenberg, H. Bronner, D. Schleheck, S. Polarz, J. Am. Chem. Soc. 2016, 138, 3076.
- 42A. Denicola, J. M. Souza, R. Radi, E. Lissi, Arch. Biochem. Biophys. 1996, 328, 208.
- 43M. N. Moller, Q. Li, J. R. Lancaster, A. Denicola, IUBMB Life 2007, 59, 243.
- 44H. Koo, R. N. Allan, R. P. Howlin, P. Stoodley, L. Hall-Stoodley, Nat. Rev. Microbiol. 2017, 15, 740.
- 45Y. Z. Guo, S. T. Liu, X. Tang, C. Wang, Z. Niu, Y. Feng, Environ. Sci. Technol. 2017, 51, 9155.
- 46Y.-m. Cai, J. S. Webb, Appl. Microbiol. Biot. 2020, 104, 8859.
- 47L. Tan, J. Li, X. M. Liu, Z. D. Cui, X. J. Yang, S. L. Zhu, Z. Y. Li, X. B. Yuan, Y. F. Zheng, K. W. K. Yeung, H. B. Pan, X. B. Wang, S. L. Wu, Adv. Mater. 2018, 30, 1801808.
- 48S. Zwirowski, A. Klosowska, I. Obuchowski, N. B. Nillegoda, A. Pirog, S. Zietkiewicz, B. Bukau, A. Mogk, K. Liberek, EMBO J. 2017, 36, 783.
- 49H. Morita, H. Yoshikawa, T. Suzuki, S. Hisamatsu, Y. Kato, R. Sakata, Y. Nagata, T. Yoshimura, Biosci Biotechnol Biochem 2004, 68, 1027.
- 50X. J. Cai, J. Tian, J. W. Zhu, J. P. Chen, L. Li, C. Yang, J. L. Chen, D. F. Chen, Chem. Eng. J. 2021, 426, 131919.
- 51Z. Q. Chen, S. F. Li, F. Z. Li, C. Qin, X. L. Li, G. C. Qing, J. J. Wang, B. Z. Xia, F. X. Zhang, L. L. Meng, X. J. Liang, Y. Y. Xiao, Adv. Sci. 2023, 10, 2206707.
- 52B. B. Mishra, V. A. K. Rathinam, G. W. Martens, A. J. Martinot, H. Kornfeld, K. A. Fitzgerald, C. M. Sassetti, Nat. Immun. 2013, 14, 52.