Regulation of Tumor Microenvironment Under Malignant Conditions: Application of nMOFs in Sonodynamic Therapy

doi:10.1007/s40242-024-4108-3

摘要/Abstract

摘要： In this review, we delve into the intricate regulation of the tumor microenvironment (TME) under malignant conditions and explore the transformative potential of nanoscale metal-organic frameworks (nMOFs) in the realm of sonodynamic therapy (SDT). The TME serves as a dynamic milieu influencing tumor progression and therapeutic response, presenting formidable challenges, such as hypoxia, acidity, excess hydrogen peroxide, high expression of glutathione, and immunosuppression. Utilizing the exceptional attributes of nMOFs, including their tunable structures and biocompatibility, holds immense promise for enhancing SDT efficacy and reshaping the TME landscape. By integrating nMOFs with SDT, researchers aim to assemble multiple functionalities in a single platform that enhance tumor cell eradication while counteracting unfavorable TME conditions and immune resistance. The potential of nMOFs to revolutionize tumor therapies by precisely targeting TME and overcoming therapeutic barriers is underscored by an in-depth analysis of recent breakthroughs in the use of nMOFs-based sonosensitizers to remodulate TME to amplify the efficacy of SDT.

关键词: Sonodynamic therapy, Metal-organic framework, Tumor microenvironment, Modification of sonosensitizer

Abstract: In this review, we delve into the intricate regulation of the tumor microenvironment (TME) under malignant conditions and explore the transformative potential of nanoscale metal-organic frameworks (nMOFs) in the realm of sonodynamic therapy (SDT). The TME serves as a dynamic milieu influencing tumor progression and therapeutic response, presenting formidable challenges, such as hypoxia, acidity, excess hydrogen peroxide, high expression of glutathione, and immunosuppression. Utilizing the exceptional attributes of nMOFs, including their tunable structures and biocompatibility, holds immense promise for enhancing SDT efficacy and reshaping the TME landscape. By integrating nMOFs with SDT, researchers aim to assemble multiple functionalities in a single platform that enhance tumor cell eradication while counteracting unfavorable TME conditions and immune resistance. The potential of nMOFs to revolutionize tumor therapies by precisely targeting TME and overcoming therapeutic barriers is underscored by an in-depth analysis of recent breakthroughs in the use of nMOFs-based sonosensitizers to remodulate TME to amplify the efficacy of SDT.

Key words: Sonodynamic therapy, Metal-organic framework, Tumor microenvironment, Modification of sonosensitizer

YANG Yilin, YAN Fei, SHI Zhan. Regulation of Tumor Microenvironment Under Malignant Conditions: Application of nMOFs in Sonodynamic Therapy[J]. 高等学校化学研究, 2024, 40(4): 611-626.

YANG Yilin, YAN Fei, SHI Zhan. Regulation of Tumor Microenvironment Under Malignant Conditions: Application of nMOFs in Sonodynamic Therapy[J]. Chemical Research in Chinese Universities, 2024, 40(4): 611-626.

参考文献

[1] Martínez-Jiménez F., Muiños F., Sentís I., Deu-Pons J., Reyes-Salazar I., Arnedo-Pac C., Mularoni L., Pich O., Bonet J., Kranas H., Gonzalez-Perez A., Lopez-Bigas N., Nat. Rev. Cancer, 2020, 20, 555.
[2] Ugai T., Sasamoto N., Lee H. -Y., Ando M., Song M., Tamimi R. M., Kawachi I., Campbell P. T., Giovannucci E. L., Weiderpass E., Rebbeck T. R., Ogino S., Nat. Rev. Clin. Oncol., 2022, 19, 656.
[3] Shi J., Kantoff P. W., Wooster R., Farokhzad O. C., Nat. Rev. Cancer, 2017, 17, 20.
[4] Faguet G. B., Int. J. Cancer, 2015, 136, 2022.
[5] Guo Q., Dai X., Yin M., Cheng H., Qian H., Wang H., Zhu D., Wang X., Military Med. Res., 2022, 9, 26.
[6] Xu M., Zhou L., Zheng L., Zhou Q., Liu K., Mao Y., Song S., Cancer Lett., 2021, 497, 229.
[7] Canaparo R., Foglietta F., Barbero N., Serpe L., Adv. Drug Deliv. Rev., 2022, 189, 114495.
[8] Qian X., Zheng Y., Chen Y., Adv. Mater., 2016, 28, 8097.
[9] Trachootham D., Alexandre J., Huang P., Nat. Rev. Drug. Discov., 2009, 8, 579.
[10] Fan H., Guo Z., Coord. Chem. Rev., 2023, 480, 215027.
[11] Wang S., Song Y., Cao K., Zhang L., Fang X., Chen F., Feng S., Yan F., Acta Biomater., 2021, 134, 621.
[12] Visser K. E. D., Joyce J. A., Cancer cell, 2023, 41, 374.
[13] Chao Y., Liu Z., Nat. Rev. Bioeng, 2023, 1, 125.
[14] Song L., Lu L., Pu Y., Yin H., Zhang K., Acc. Mater. Res., 2022, 3, 971.
[15] Tao N., Li H., Deng L., Zhao S., Ouyang J., Wen M., Chen W., Zeng K., Wei C., Liu Y., ACS Nano, 2022, 16, 485.
[16] Wang T., Peng W., Du M., Chen Z., Front. Oncol., 2023, 13, 1167105.
[17] Yuan H., Ma J., Huang W., Gong P., Shi F., Xu X., Fu C., Wang X., Wong Y. K., Long Y., Sun X., Li W., Li Z., Wang J., JACS Au, 2023, 3, 1507.
[18] Zhang Z., Li B., Xie L., Sang W., Tian H., Li J., Wang G., Dai Y., ACS Nano, 2021, 15, 16934.
[19] Umemura S., Yumita N., Nishigaki R., Umemura K., Jpn. J. Cancer Res., 1990, 81, 962.
[20] Son S., Kim J. H., Wang X., Zhang C., Yoon S. A., Shin J., Sharma A., Lee M. H., Cheng L., Wu J., Kim J. S., Chem. Soc. Rev., 2020, 49, 3244.
[21] Bindra A. K., Wang D., Zhao Y., Adv. Mater., 2023, 35, 2300700.
[22] Gao P., Chen Y., Pan W., Li N., Liu Z., Tang B., Angew. Chem. Int. Ed., 2021, 60, 2.
[23] Sun Y., Zheng L., Yang Y., Qian X., Fu T., Li X., Yang Z., Yan H., Cui C., Tan W., Nano-Micro Lett., 2020, 12, 103.
[24] Huang S., Kou X., Shen J., Chen G., Ouyang G., Angew. Chem. Int. Ed., 2020, 590, 59.
[25] Yang F., Dong J., Li Z., Wang Z., ACS Nano, 2023, 17, 4102.
[26] Jiang Q., Gao X., Zhang W., Chen Z., Biomater. Sci., 2023, 11, 4452.
[27] Tang J., Huang C., Liu Y., Wang T., Yu M., Hao H., Zeng W., Huang W., Wang J., Wu M., Coord. Chem. Rev., 2023, 490, 215211.
[28] Ge X., Wong R., Anisa A., Ma S., Biomaterials, 2022, 281, 121322.
[29] Guo W., Wang Y., Zhang K., Dai X., Qiao Z., Liu Z., Yu B., Zhao N., Xu F., Chem. Mater., 2023, 35, 6853.
[30] Liao D., Huang J., Jiang C., Zhou L., Zheng M., Pharmaceutics, 2023, 15, 2071.
[31] Ravi K., Manoharan T. J. M., Wang K., Pockaj B., Nikkhah M., Biomaterials, 2024, 305, 122428.
[32] Zhang Z., Ding C., Sun T., Wang L., Chen C., Adv. Healthc. Mater., 2023, 12, 2300153.
[33] Coluccia M., Parisse V., Guglielmi P., Giannini G., Secci D., Eur. J. Med. Chem., 2022, 244, 114801.
[34] Ouyang J., Tang Z., Farokhzad N., Kong N., Kim N. Y., Feng C., Blake S., Xiao Y., Liu C., Xie T., Tao W., Naonotoday, 2020, 35, 100949.
[35] Lentacker I., Cock D., Deckers R., Smedt S. C. D., Moonen C. T. W., Adv. Drug Deliv. Rev., 2014, 72, 49.
[36] Chowdhury S. M., Abou-Elkacem L., Lee T., Dahl J., Lutz A. M., J. Control. Release, 2020, 326, 75.
[37] Kooiman K., Roovers S., Langeveld S. A. G., Kleven R. T., Dewitte H., O'Reilly M. A., Escoffre J.-M., Bouakaz A., Verweij M. D., Hynynen K., Lentacke I., Stride E., Holland C. K., Ultrasound Med. Biol., 2020, 44, 1296.
[38] Yang H., Villani R. M., Wang H., Simpson M. J., Roberts M. S., Tang M., Liang X., J. Exp. Clin. Cancer Res., 2018, 37, 266.
[39] Cheung E. C., Vousden K. H., Nat. Rev. Cancer, 2022, 22, 280.
[40] Dong Y., Dong S., Liu B., Yu C., Liu J., Yang D., Yang P., Lin J., Adv. Mater., 2021, 33, 2106838.
[41] Hiam-Galvez K. J., Allen B. M., Spitzer M. H., Nat. Rev. Cancer, 2021, 21, 345.
[42] Zhu S., Zhang T., Zheng L., Liu H., Song W., Liu D., Li Z., Pan C., J. Hematol. Oncol., 2021, 114, 156.
[43] Yin Y., Jiang X., Sun L., Li H., Su C., Zhang Y., Xu G., Li X., Zhao C., Chen Y., Xu H., Zhang K., Nanotoday, 2021, 36, 101009.
[44] Yang Y., Huang J., Liu M., Qiu Y., Chen Q., Zhao T., Xiao Z., Yang Y., Jiang Y., Huang Q., Ai K., Adv. Sci., 2023, 10, 2204365.
[45] Wang T., Peng W., Du M., Chen Z., Front. Oncol., 2023, 13, 1167105.
[46] Li D., Yang Y., Li D., Pan J., Chu C., Liu G., Small, 2021, 17, 2101976.
[47] Lin X., Song J., Chen X., Yang H., Angew. Chem. Int. Ed., 2019, 59, 14212.
[48] Xing X., Zhao S., Xu T., Huang L., Zhang Y., Lan M., Lin C., Zheng X., Wang P., Coord. Chem. Rev., 2021, 445, 214087.
[49] Liu K., Jiang Z., Zhao F., Wang W., Jäkle F., Wang N., Tang X., Yin X., Chen P., Adv. Mater., 2022, 34, 2206594.
[50] Qian X., Zheng Y., Chen Y., Adv. Mater., 2016, 28, 8097.
[51] Chewn H., Liu L., Ma A., Yin T., Chen Z., Liang R., Qiu Y., Zheng M., Cai L., Biomaterials, 2021, 269, 120639.
[52] Teranishi R., Matsuda T., Yuba E., Kono K., Harada A., Macromol. Biosci., 2019, 19, 1800365.
[53] Zhang D., Chen B. Pan Y., Liu H., Shi Y., Chen L., Kankala R. K., Wang S., Chen A., Mater. Des., 2023, 227, 111794.
[54] Li Y., Huang C., Xu Y., Front. Bioeng. Biotechnol., 2022, 10, 1069676.
[55] Hu W., Wang S., Jiang C., Zheng M., Bai Z., Srivastava D., Kumar A., Liu J., Dyes Pigment., 2023, 219, 111596.
[56] Wang X., Zhong X., Bai L., Xu J., Gong F., Dong Z., Yang Z., Zeng Z., Liu Z., Cheng L., J. Am. Chem. Soc., 2020, 142, 6527.
[57] Liu Y., Wang Y., Zhen W., Wang Y., Zhang S., Zhao Y., Song S., Wu Z., Zhang H., Biomaterials, 2020, 251, 120075.
[58] Deepagan V. G., You D. G., Um W., Ko H., Kwon S., Choi K. Y., Yi G., Lee J. Y., Lee D. S., Kim K., Kwon I. C., Park J. H., Nano Lett., 2016, 16, 6257.
[59] Xu T., Zhao S., Lin C., Zheng X., Lan M., Nano Res., 2020, 13, 2898.
[60] Qiao X., Xue L., Huang H., Dai X., Chen Y., Ding H., J. Nanobiotechnol., 2022, 20, 186.
[61] Cao Z., Yuan G., Zeng L., Bai L., Liu X., Wu M., Sun R., Chen Z., Jiang Y., Gao Q., Chen Y., Zhang Y., Pan Y., Wang J., ACS Nano 2022, 16, 10608.
[62] Pandey A., Dhas N., Deshmukh P., Caro C., Patil P., García-Martín M. L., Padya B., Nikam A., Mehta T., Mutalik S., Coord. Chem. Rev., 2020, 409, 213212.
[63] Cao J., Huang D., Peppas N. A., Adv. Drug Deliv., 2020, 167, 170.
[64] Wang Z., Sun Q., Liu B., Kuang Y., Gulzar A., He F., Gai S., Yang P., Lin J., Coord. Chem. Rev., 2021, 439, 213945.
[65] Ye Y., Zhao Y., Sun Y., Cao J., Int. J. Nanomed., 2022, 17, 2367.
[66] Hu W., Wang S., Jiang C., Zheng M., Bai Z., Srivastava D., Kumar A., Liu J., Dyes Pigm., 2023, 219, 111596.
[67] Anderson S. L., Stylianou K. C., Coord. Chem. Rev., 2017, 349, 102.
[68] Zhang Y., Wang F., Liu C., Wang Z., Kang L., Huang Y., Dong K., Ren J., Qu X., ACS Nano, 2018, 12, 651.
[69] Zheng Y., Zhang X., Su Z., Nanoscale, 2021, 13, 12102.
[70] Song Y., Zhang L., Wang Y., Han M., Wang Z., Wang N., Shao B., Li R., Cao K., Song M., Du Y., Yan F., Adv. Mater., 2023, 35, 2210895.
[71] Zeng Y., Ouyang Q., Yu Y., Tan L., Liu X., Zheng Y., Wu S., Small Methods, 2022, 7, 2201248.
[72] Liang S., Xiao X., Bai L., Liu B., Yuan M., Ma P., Pang M., Cheng Z., Lin J., Adv. Mater., 2021, 33, 2100333.
[73] Liu S., Wen M., Huang M., Wang H., Chen Z., Yu N., J. Colloid Interface Sci., 2022, 616, 23.
[74] Hu C., Wang J., Liu S., Cai L., Zhou Y., Liu X., Wang M., Liu Z., Pang M., ACS Appl. Mater. Interfaces, 2021, 13, 4825.
[75] Lin G., Nash G. T., Luo T., Ghosh I., Sohoni S., Christofferson A. J., Liu G., Engel G. S., Lin W., Adv. Mater., 2023, 35, 2212069.
[76] Meng X., Sun S., Gong C., Yang J., Yang Z., Zhang X., Dong H., ACS Nano, 2023, 17, 1174.
[77] Li H., Zhou L., Zhou J., Li Q., Ji Q., J. Exp. Clin. Cancer Res., 2021, 40, 97.
[78] DePeaux K., Delgoffe G. M., Nat. Rev. Immunol., 2021, 21, 785.
[79] Godet I., Shin Y. J., Ju J. A., Ye I. C., Wang G., Gilkes D. M., Nat. Commun., 2019, 10, 4862.
[80] Zhang T., Sun Y., Cao J., Luo J., Wang J., Jiang Z., Huang P., J. Nanobiotechnol., 2021, 19, 315.
[81] Xu Q., Zhan G., Zhang Z., Yong T., Yang X., Gan L., Theranostics, 2021, 11, 1937.
[82] Liu X., Dong X., Yang S., Lai X., Liu H., Gao Y., Feng H., Zhu M., Yuan Y., Lu Q., Lovell J. F., Chen H., Fang C., Adv. Sci., 2021, 8, 2003679.
[83] Bao Y., Chen J., Qiu H., Zhang C., Huang P., Mao Z., Tong W., ACS Appl. Mater. Interfaces, 2021, 13, 24532.
[84] Sulea T., Rohani N., Baardsnes J., Corbeil C. R., Deprez C., Cepero-Donates Y., Robert A., Schrag J. D., Parat M., Duchesne M., Jaramillo M. L., Purisima E. O., Zwaagstra J. C., Mabs, 2021, 12, 1682866.
[85] Ren Q., Yu N., Wang L., Wen M., Geng P., Jiang Q., Li M., J. Colloid Interface Sci., 2022, 614, 147.
[86] Dong Z., Feng L., Hao Y., Li Q., Chen M., Yang Z., Zhao H., Liu Z., Chem, 2020, 6, 1391.
[87] Chu Z., Yang J., Zheng W., Sun J., Wang W., Qian H., Coord. Chem. Rev., 2023, 481, 215049.
[88] Yang N., Xiao W., Song X., Wang W., Dong X., Nano-Micro Lett., 2020, 12, 15.
[89] Zhang H., Zhang Y., Li Y., Hu M., Rong Z., Meng L., Zhang X., Wen L., Liang X., Chen Z., Liu C., Adv. Therap., 2023, 6, 2300074.
[90] Hang L., Li M., Zhang Y., Li W., Fang L., Chen Y., Zhou C., Qu H., Shao L., Jiang G., Small, 2023, 2306364.
[91] Wang Y., Huang K., Wang T., Liu L., Yu F., Sun W., Yao W., Xiong H., Liu X., Jiang H., Wang X., Small, 2024, 2310300.
[92] Li M., Huo L., Zeng J., Zhu G., Shi S., Liu X., Zhu X., Huang G., Qiu D., Jia J., Ni K., Zhao Z., Chem. Eng. J., 2022, 440, 135966.
[93] Fang L., Han M., Zhang Y., Song Y., Liu B., Cai M., Jiang M., Hu L., Zheng R., Lian X., Yan F., Huang K., Feng S., Adv. Healthc. Mater., 2023, 12, 2300134.
[94] Jiang S., He Q., Li C., Dang K., Ye L., Zhang W., Tian Y., Sci. China Mater., 2022, 65, 1112.
[95] Zhang K., Meng X., Yang Z., Dong H., Zhang X., Biomaterials, 2020, 258, 120278.
[96] Zhou L., Feng W., Mao Y., Chen Y., Zhang X., Bioact. Mater., 2023, 24, 26.
[97] Jia T., Du J., Yang J., Li Y., Ohulchanskyy T. Y., Fang X., Chen G., Adv. Funct. Mater., 2023, 34, 2307816.
[98] Xu X., Chen M., Jiang S., Pan Z., Zhao C., Adv. Funct. Mater., 2024, 2314780.
[99] Zhou Y., Jiao J., Yang R., Wen B., Wu Q., Xu L., Tong X., Yan H., Clin. Immunol., 2023, 256, 109772.
[100] Wang T., Peng W., Du M., Chen Z., Front. Oncol., 2023, 13, 1167105.
[101] Wang Y., Gong F., Han Z., Lei H., Zhou Y., Cheng S., Yang X., Wang T., Wang L., Yang N., Liu Z., Cheng L., Angew. Chem. Int. Ed., 2023, 62, e202215467.
[102] Chen C., Song M., Du Y., Yu Y., Li C., Han Y., Yan F., Shi Z., Feng S., Nano Lett., 2021, 21, 5522.
[103] Luo J., Wang X., Shi Z., Zeng Y., He L., Cao J., Sun Y., Zhang T., Huang P., J. Nanobiotechnol, 2022, 20, 228.
[104] Lu Z., Bai S., Jiang Y., Wu S., Xu D., Zhang J., Peng X., Zhang H., Shi Y., Liu G., Small, 2022, 18, 2203952.
[105] Liu L., Pan Y., Zhao C., Huang P., Chen X., Rao L., ACS Nano, 2023, 17, 3225.
[106] Du Y., Dai X., Han M., Wang Z., Wang Y., Shi Z., Yan F., Feng S., Chem. Eng. J., 2023, 453, 139635.
[107] Li Q., Su R., Bao X., Cao K., Du Y., Wang N., Wang J., Xing F., Yan F., Huang K., Feng S., Acta Biomater., 2022, 144, 109.
[108] Zhou X., Ni Y., Liang X., Lin Y., An B., He X., Zhao X., Front. Immunol., 2022, 13, 915094.
[109] Dai X., Li X., Liu Y., Yan F., Mater. Des., 2022, 217, 110656.
[110] Dan X., Du Y., Li Y., Yan F., Mater. Today Bio, 2023, 23, 100796.
[111] Heinhuis K. M., Ros W., Kok M., Steeghs N., Beijnen J. H., Schellens J. H. M., Ann. Oncol., 2019, 30, 219.
[112] Yang Y., Wang N., Wang Z., Han M., Yan F., Shi Z., Feng S., Chem. Eng. J., 2023, 474, 145764.
[113] Jiang S., Liu C., He Q., Dang K., Zhang W., Tian Y., Nano Res., 2023, 16, 9633.
[114] Liu Q., Chen G., Liu X., Tao L., Fan Y., Xia T., ACS Nano, 2024, 18, 5219.
[115] Zhan G., Xua Q., Zhang Z., Wei Z., Yong T., Bie N., Zhang X., Li X., Li J., Gan L., Yang X., Nanotoday, 2021, 38, 101195.
[110] Dan X., Du Y., Li Y., Yan F., Mater. Today Bio, 2023, 23, 100796.
[111] Heinhuis K. M., Ros W., Kok M., Steeghs N., Beijnen J. H., Schellens J. H. M., Ann. Oncol., 2019, 30, 219.
[112] Yang Y., Wang N., Wang Z., Han M., Yan F., Shi Z., Feng S., Chem. Eng. J., 2023, 474, 145764.
[113] Jiang S., Liu C., He Q., Dang K., Zhang W., Tian Y., Nano Res., 2023, 16, 9633.
[114] Liu Q., Chen G., Liu X., Tao L., Fan Y., Xia T., ACS Nano, 2024, 18, 5219.
[115] Zhan G., Xua Q., Zhang Z., Wei Z., Yong T., Bie N., Zhang X., Li X., Li J., Gan L., Yang X., Nanotoday, 2021, 38, 101195.