Abstract
Bacterial infection is the leading cause of many severe inflammation diseases. The development of novel and effective therapeutic approaches to counter bacterial infections, especially for drug-resistant bacteria, is essential. Herein, we have successfully developed an ultrasound-active tricarbonyl rhenium(I) complex with tetraphenylethylene (TPE) modification (RePy-TPE) for CO gas therapy and sonodynamic therapy of bacterial infections. RePy-TPE produced reactive oxygen species and released CO under ultrasound irradiation. In addition, RePy-TPE showed aggregation-induced emission in water due to the introduction of TPE, which enhanced the yield of 1O2 generation in a biological aqueous solution. The produced 1O2 and released CO killed mycobacterium smegmatis (M. smegmatis) and Escherichia coli (E. coli), as shown by bacterial membrane damage and biofilm elimination. Furthermore, ultrasound-active RePy-TPE perturbed the purine metabolism of the bacteria, which disturbed the biosynthesis of DNA and energy metabolism, eventually reducing the vitality of bacteria. This article provides a novel strategy for the development of ultrasound-active metal-based antibiotics.
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Stokes JM, Yang K, Swanson K, Jin W, Cubillos-Ruiz A, Donghia NM, MacNair CR, French S, Carfrae LA, Bloom-Ackermann Z, Tran VM, Chiappino-Pepe A, Badran AH, Andrews IW, Chory EJ, Church GM, Brown ED, Jaakkola TS, Barzilay R, Collins JJ. Cell, 2020, 180: 688–702.e13
Burki TK. Lancet Respir Med, 2021, 9: e54
Wallis RS, O’Garra A, Sher A, Wack A. Nat Rev Immunol, 2023, 23: 121–133
Ravesloot-Chávez MM, Van Dis E, Stanley SA. Annu Rev Immunol, 2021, 39: 611–637
Furin J, Cox H, Pai M. Lancet, 2019, 393: 1642–1656
Chakaya J, Petersen E, Nantanda R, Mungai BN, Migliori GB, Amanullah F, Lungu P, Ntoumi F, Kumarasamy N, Maeurer M, Zumla A. Int J Infect Dis, 2022, 124: S26–S29
Blot M, Dinh A. Clin Infect Dis, 2022, 74: 749–750
Li L, Chen L, Lu Y, Li B, Hu R, Huang L, Zhang T, Wei X, Yang Z, Mao C. Aggregate, 2023, 4: 200
Fan W, Lu N, Shen Z, Tang W, Shen B, Cui Z, Shan L, Yang Z, Wang Z, Jacobson O, Zhou Z, Liu Y, Hu P, Yang W, Song J, Zhang Y, Zhang L, Khashab NM, Aronova MA, Lu G, Chen X. Nat Commun, 2019, 10: 1241
Ye J, Fu Q, Liu L, Chen L, Zhang X, Li Q, Li Z, Su L, Zhu R, Song J, Yang H. Sci China Chem, 2021, 64: 2218–2229
Wu CG, Liang JL, Wang X, Zhou X, Cai X, Xu J, Wang M, Wang WB, Ma D, Xue W. Sci China Chem, 2021, 64: 1796–1810
Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AMK. Nat Med, 2000, 6: 422–428
Motterlini R, Otterbein LE. Nat Rev Drug Discov, 2010, 9: 728–743
Wegiel B, Gallo D, Csizmadia E, Harris C, Belcher J, Vercellotti GM, Penacho N, Seth P, Sukhatme V, Ahmed A, Pandolfi PP, Helczynski L, Bjartell A, Persson JL, Otterbein LE. Cancer Res, 2013, 73: 7009–7021
Wang Y, Yang T, He Q. Natl Sci Rev, 2020, 7: 1485–1512
Zheng DW, Li B, Li CX, Xu L, Fan JX, Lei Q, Zhang XZ. Adv Mater, 2017, 29: 1703822
Li WP, Su CH, Tsao LC, Chang CT, Hsu YP, Yeh CS. ACS Nano, 2016, 10: 11027–11036
Liu J, Li RS, He M, Xu Z, Xu LQ, Kang Y, Xue P. Biomaterials, 2021, 277: 121084
Cheng J, Gan G, Shen Z, Gao L, Zhang G, Hu J. Angew Chem Int Ed, 2021, 60: 13513–13520
Jiang X, Xiao Z, Zhong W, Liu X. Coord Chem Rev, 2021, 429: 213634
Garcia-Gallego S, Bernardes GJL. Angew Chem Int Ed, 2014, 53: 9712–9721
Ling K, Men F, Wang WC, Zhou YQ, Zhang HW, Ye DW. J Med Chem, 2018, 61: 2611–2635
Li Y, Lu N, Lin Q, Wang H, Liang Z, Lu Y, Zhang P. Chin Chem Lett, 2023, 34: 107653
Zhu J, Ouyang A, He J, Xie J, Banerjee S, Zhang Q, Zhang P. Chem Commun, 2022, 58: 3314–3317
Schatzschneider U. Inorg Chim Acta, 2011, 374: 19–23
Southam HM, Smith TW, Lyon RL, Liao C, Trevitt CR, Middlemiss LA, Cox FL, Chapman JA, El-Khamisy SF, Hippler M, Williamson MP, Henderson PJF, Poole RK. Redox Biol, 2018, 18: 114–123
Kunz PC, Huber W, Rojas A, Schatzschneider U, Spingler B. Eur J Inorg Chem, 2009, 35: 5358–5366
Govender P, Pai S, Schatzschneider U, Smith GS. Inorg Chem, 2013, 52: 5470–5478
Pierri AE, Pallaoro A, Wu G, Ford PC. J Am Chem Soc, 2012, 134: 18197–18200
Su X, Wang W, Cao Q, Zhang H, Liu B, Ling Y, Zhou X, Mao Z. Angew Chem Int Ed, 2022, 61: e202115800
Tan CP, Zhong YM, Ji LN, Mao ZW. Chem Sci, 2021, 12: 2357–2367
Pan Z, Tan C, Rao L, Zhang H, Zheng Y, Hao L, Ji L, Mao Z. Angew Chem Int Ed, 2020, 59: 18755–18762
Heinemann F, Karges J, Gasser G. Acc Chem Res, 2017, 50: 2727–2736
Hess J, Huang H, Kaiser A, Pierroz V, Blacque O, Chao H, Gasser G. Chem Eur J, 2017, 23: 9888–9896
Shen Y, Shuhendler AJ, Ye D, Xu JJ, Chen HY. Chem Soc Rev, 2016, 45: 6725–6741
Cox B, Beard P. Nature, 2015, 527: 451–452
Xing X, Zhao S, Xu T, Huang L, Zhang Y, Lan M, Lin C, Zheng X, Wang P. Coord Chem Rev, 2021, 445: 214087
Lai Y, Lu N, Ouyang A, Zhang Q, Zhang P. Chem Sci, 2022, 13: 9921–9926
Liang C, Xie J, Luo S, Huang C, Zhang Q, Huang H, Zhang P. Nat Commun, 2021, 12: 5001
Yang H, Tu L, Li J, Bai S, Hu Z, Yin P, Lin H, Yu Q, Zhu H, Sun Y. Coord Chem Rev, 2022, 453: 214333
Zhang H, Pan X, Wu Q, Guo J, Wang C, Liu H. Exploration, 2021, 1: 20210010
Wu Q, Zhang H, Liu H. BMEMat, 2023, 1: e12010
Ismail NA, Shameli K, Wong MMT, Teow SY, Chew J, Sukri SNAM. Mater Sci Eng-C, 2019, 104: 109899
Sun D, Pang X, Cheng Y, Ming J, Xiang S, Zhang C, Lv P, Chu C, Chen X, Liu G, Zheng N. ACS Nano, 2020, 14: 2063–2076
Song M, Cheng Y, Tian Y, Chu C, Zhang C, Lu Z, Chen X, Pang X, Liu G. Adv Funct Mater, 2020, 30: 2003587
Yu Y, Tan L, Li Z, Liu X, Zheng Y, Feng X, Liang Y, Cui Z, Zhu S, Wu S. ACS Nano, 2021, 15: 10628–10639
Zhang Y, Zhang X, Yang H, Yu L, Xu Y, Sharma A, Yin P, Li X, Kim JS, Sun Y. Chem Soc Rev, 2021, 50: 11227–11248
Huo J, Jia Q, Huang H, Zhang J, Li P, Dong X, Huang W. Chem Soc Rev, 2021, 50: 8762–8789
Zhou T, Hu R, Wang L, Qiu Y, Zhang G, Deng Q, Zhang H, Yin P, Situ B, Zhan C, Qin A, Tang BZ. Angew Chem Int Ed, 2020, 59: 9952–9956
Wan Q, Zhang R, Zhuang Z, Li Y, Huang Y, Wang Z, Zhang W, Hou J, Tang BZ. Adv Funct Mater, 2020, 30: 2002057
Li Q, Li Y, Min T, Gong J, Du L, Phillips DL, Liu J, Lam JWY, Sung HHY, Williams ID, Kwok RTK, Ho CL, Li K, Wang J, Tang BZ. Angew Chem Int Ed, 2020, 59: 9470–9477
Polo AS, Itokazu MK, Frin KM, de Toledo Patrocinio AO, Murakami Iha NY. Coord Chem Rev, 2006, 250: 1669–1680
Son S, Kim JH, Wang X, Zhang C, Yoon SA, Shin J, Sharma A, Lee MH, Cheng L, Wu J, Kim JS. Chem Soc Rev, 2020, 49: 3244–3261
Beguin E, Shrivastava S, Dezhkunov NV, McHale AP, Callan JF, Stride E. ACS Appl Mater Interfaces, 2019, 11: 19913–19919
Sharipov GL, Abdrakhmanov AM, Gareev BM, Yakshembetova LR. Ultrasons SonoChem, 2018, 42: 526–531
Fan Z, Rong Y, Sadhukhan T, Liang S, Li W, Yuan Z, Zhu Z, Guo S, Ji S, Wang J, Kushwaha R, Banerjee S, Raghavachari K, Huang H. Angew Chem Int Ed, 2022, 61: e202202098
Judzewitsch PR, Corrigan N, Wong EHH, Boyer C. Angew Chem Int Ed, 2021, 60: 24248–24256
Lai Y, Lu N, Luo S, Wang H, Zhang P. J Med Chem, 2022, 65: 13041–13051
Michel BW, Lippert AR, Chang CJ. J Am Chem Soc, 2012, 134: 15668–15671
Pang X, Liu X, Cheng Y, Zhang C, Ren E, Liu C, Zhang Y, Zhu J, Chen X, Liu G. Adv Mater, 2019, 31: 1902530
Stewart PS, William Costerton J. Lancet, 2001, 358: 135–138
Feng X, Ma L, Lei J, Ouyang Q, Zeng Y, Luo Y, Zhang X, Song Y, Li G, Tan L, Liu X, Yang C. ACS Nano, 2022, 16: 2546–2557
Zhou H, Tang D, Kang X, Yuan H, Yu Y, Xiong X, Wu N, Chen F, Wang X, Xiao H, Zhou D. Adv Sci, 2022, 9: 2200732
Yu X, Jin X, Tang J, Wang N, Yu Y, Sun R, Deng F, Huang C, Sun J, Zhu L. Chemosphere, 2022, 291: 133125
Pedley AM, Benkovic SJ. Trends Biochem Sci, 2017, 42: 141–154
Acknowledgements
This work was supported by the Natural Science Foundation of Guangdong Province (2023B1515020060, 2021B1515020050), the Science and Technology Foundation of Shenzhen (RCYX20221008-092906021, JCYJ20210324095200002, JCYJ20220531103405012), the National Natural Science Foundation of China (22077085, 22177078, 22277153). We appreciate the UPLC-MS system of Shenzhen Bay Laboratory and the Instrumental Analysis Center of Shenzhen University.
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Supporting information The supporting information is available online at https://chem.scichina.com and https://link.springer.com/journal/11426. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.
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Li, Y., Wang, H., Lin, Q. et al. Ultrasound-active ReCORM-AIEgen for gas and sonodynamic therapy of mycobacterium biofilms. Sci. China Chem. 66, 2645–2653 (2023). https://doi.org/10.1007/s11426-023-1696-5
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DOI: https://doi.org/10.1007/s11426-023-1696-5