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Ultrasound-active ReCORM-AIEgen for gas and sonodynamic therapy of mycobacterium biofilms

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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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References

  1. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Burki TK. Lancet Respir Med, 2021, 9: e54

    Article  PubMed  Google Scholar 

  3. Wallis RS, O’Garra A, Sher A, Wack A. Nat Rev Immunol, 2023, 23: 121–133

    Article  CAS  PubMed  Google Scholar 

  4. Ravesloot-Chávez MM, Van Dis E, Stanley SA. Annu Rev Immunol, 2021, 39: 611–637

    Article  PubMed  Google Scholar 

  5. Furin J, Cox H, Pai M. Lancet, 2019, 393: 1642–1656

    Article  PubMed  Google Scholar 

  6. 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

    Article  PubMed  PubMed Central  Google Scholar 

  7. Blot M, Dinh A. Clin Infect Dis, 2022, 74: 749–750

    Article  CAS  PubMed  Google Scholar 

  8. Li L, Chen L, Lu Y, Li B, Hu R, Huang L, Zhang T, Wei X, Yang Z, Mao C. Aggregate, 2023, 4: 200

    Article  Google Scholar 

  9. 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

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. Motterlini R, Otterbein LE. Nat Rev Drug Discov, 2010, 9: 728–743

    Article  CAS  PubMed  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. Wang Y, Yang T, He Q. Natl Sci Rev, 2020, 7: 1485–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zheng DW, Li B, Li CX, Xu L, Fan JX, Lei Q, Zhang XZ. Adv Mater, 2017, 29: 1703822

    Article  Google Scholar 

  17. Li WP, Su CH, Tsao LC, Chang CT, Hsu YP, Yeh CS. ACS Nano, 2016, 10: 11027–11036

    Article  CAS  PubMed  Google Scholar 

  18. Liu J, Li RS, He M, Xu Z, Xu LQ, Kang Y, Xue P. Biomaterials, 2021, 277: 121084

    Article  CAS  PubMed  Google Scholar 

  19. Cheng J, Gan G, Shen Z, Gao L, Zhang G, Hu J. Angew Chem Int Ed, 2021, 60: 13513–13520

    Article  CAS  Google Scholar 

  20. Jiang X, Xiao Z, Zhong W, Liu X. Coord Chem Rev, 2021, 429: 213634

    Article  CAS  Google Scholar 

  21. Garcia-Gallego S, Bernardes GJL. Angew Chem Int Ed, 2014, 53: 9712–9721

    Article  CAS  Google Scholar 

  22. Ling K, Men F, Wang WC, Zhou YQ, Zhang HW, Ye DW. J Med Chem, 2018, 61: 2611–2635

    Article  CAS  PubMed  Google Scholar 

  23. Li Y, Lu N, Lin Q, Wang H, Liang Z, Lu Y, Zhang P. Chin Chem Lett, 2023, 34: 107653

    Article  CAS  Google Scholar 

  24. Zhu J, Ouyang A, He J, Xie J, Banerjee S, Zhang Q, Zhang P. Chem Commun, 2022, 58: 3314–3317

    Article  CAS  Google Scholar 

  25. Schatzschneider U. Inorg Chim Acta, 2011, 374: 19–23

    Article  CAS  Google Scholar 

  26. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kunz PC, Huber W, Rojas A, Schatzschneider U, Spingler B. Eur J Inorg Chem, 2009, 35: 5358–5366

    Article  Google Scholar 

  28. Govender P, Pai S, Schatzschneider U, Smith GS. Inorg Chem, 2013, 52: 5470–5478

    Article  CAS  PubMed  Google Scholar 

  29. Pierri AE, Pallaoro A, Wu G, Ford PC. J Am Chem Soc, 2012, 134: 18197–18200

    Article  CAS  PubMed  Google Scholar 

  30. Su X, Wang W, Cao Q, Zhang H, Liu B, Ling Y, Zhou X, Mao Z. Angew Chem Int Ed, 2022, 61: e202115800

    Article  CAS  Google Scholar 

  31. Tan CP, Zhong YM, Ji LN, Mao ZW. Chem Sci, 2021, 12: 2357–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pan Z, Tan C, Rao L, Zhang H, Zheng Y, Hao L, Ji L, Mao Z. Angew Chem Int Ed, 2020, 59: 18755–18762

    Article  CAS  Google Scholar 

  33. Heinemann F, Karges J, Gasser G. Acc Chem Res, 2017, 50: 2727–2736

    Article  CAS  PubMed  Google Scholar 

  34. Hess J, Huang H, Kaiser A, Pierroz V, Blacque O, Chao H, Gasser G. Chem Eur J, 2017, 23: 9888–9896

    Article  CAS  PubMed  Google Scholar 

  35. Shen Y, Shuhendler AJ, Ye D, Xu JJ, Chen HY. Chem Soc Rev, 2016, 45: 6725–6741

    Article  CAS  PubMed  Google Scholar 

  36. Cox B, Beard P. Nature, 2015, 527: 451–452

    Article  CAS  PubMed  Google Scholar 

  37. Xing X, Zhao S, Xu T, Huang L, Zhang Y, Lan M, Lin C, Zheng X, Wang P. Coord Chem Rev, 2021, 445: 214087

    Article  CAS  Google Scholar 

  38. Lai Y, Lu N, Ouyang A, Zhang Q, Zhang P. Chem Sci, 2022, 13: 9921–9926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liang C, Xie J, Luo S, Huang C, Zhang Q, Huang H, Zhang P. Nat Commun, 2021, 12: 5001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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

    Article  CAS  Google Scholar 

  41. Zhang H, Pan X, Wu Q, Guo J, Wang C, Liu H. Exploration, 2021, 1: 20210010

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wu Q, Zhang H, Liu H. BMEMat, 2023, 1: e12010

    Article  Google Scholar 

  43. Ismail NA, Shameli K, Wong MMT, Teow SY, Chew J, Sukri SNAM. Mater Sci Eng-C, 2019, 104: 109899

    Article  CAS  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. Song M, Cheng Y, Tian Y, Chu C, Zhang C, Lu Z, Chen X, Pang X, Liu G. Adv Funct Mater, 2020, 30: 2003587

    Article  CAS  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. Huo J, Jia Q, Huang H, Zhang J, Li P, Dong X, Huang W. Chem Soc Rev, 2021, 50: 8762–8789

    Article  CAS  PubMed  Google Scholar 

  49. 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

    Article  CAS  Google Scholar 

  50. Wan Q, Zhang R, Zhuang Z, Li Y, Huang Y, Wang Z, Zhang W, Hou J, Tang BZ. Adv Funct Mater, 2020, 30: 2002057

    Article  CAS  Google Scholar 

  51. 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

    Article  CAS  Google Scholar 

  52. Polo AS, Itokazu MK, Frin KM, de Toledo Patrocinio AO, Murakami Iha NY. Coord Chem Rev, 2006, 250: 1669–1680

    Article  CAS  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. Beguin E, Shrivastava S, Dezhkunov NV, McHale AP, Callan JF, Stride E. ACS Appl Mater Interfaces, 2019, 11: 19913–19919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sharipov GL, Abdrakhmanov AM, Gareev BM, Yakshembetova LR. Ultrasons SonoChem, 2018, 42: 526–531

    Article  CAS  Google Scholar 

  56. 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

    Article  CAS  Google Scholar 

  57. Judzewitsch PR, Corrigan N, Wong EHH, Boyer C. Angew Chem Int Ed, 2021, 60: 24248–24256

    Article  CAS  Google Scholar 

  58. Lai Y, Lu N, Luo S, Wang H, Zhang P. J Med Chem, 2022, 65: 13041–13051

    Article  CAS  PubMed  Google Scholar 

  59. Michel BW, Lippert AR, Chang CJ. J Am Chem Soc, 2012, 134: 15668–15671

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. Stewart PS, William Costerton J. Lancet, 2001, 358: 135–138

    Article  CAS  PubMed  Google Scholar 

  62. 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

    Article  CAS  PubMed  Google Scholar 

  63. 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

    Article  CAS  Google Scholar 

  64. Yu X, Jin X, Tang J, Wang N, Yu Y, Sun R, Deng F, Huang C, Sun J, Zhu L. Chemosphere, 2022, 291: 133125

    Article  CAS  PubMed  Google Scholar 

  65. Pedley AM, Benkovic SJ. Trends Biochem Sci, 2017, 42: 141–154

    Article  CAS  PubMed  Google Scholar 

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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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Correspondence to Pingyu Zhang.

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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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