Regulating gut microbiota with nanomaterials for cancer immunotherapy

Abstract

Gut microbiota play a key role in cancer immunotherapy and regulating gut microbiota provides new strategies with great potential for cancer therapeutics. Several gut microbiota-based strategies, such as antibiotic treatment and fecal microbiota transplantation, have gained certain achievements in enhancing cancer immunotherapy, while the potential risk of biosafety and the destruction of commensal microbiota limit their further applications. Nanomaterials with excellent capabilities in delivering drugs and modulating bacteria may provide specific solutions for these limitations, and have shown promising potential in manipulating the gut microbiota to boost cancer immunotherapy. In this perspective, we reviewed the breakthroughs of nanomaterials in modulating the gut microbiota and their metabolites to enhance cancer immunotherapy, and further discussed the challenges and opportunities in this emerging field. It is anticipated that this perspective will offer new insights on the rational design of nanomaterials to regulate the gut microbiota for enhanced cancer immunotherapy, fostering clinical translation and ultimately benefiting patients.

Keywords

biotechnology / cancer immunotherapy / drug delivery / gut microbiota / nanomaterials

References

[1] G. D. Sepich-Poore, L. Zitvogel, R. Straussman, J. Hasty, J. A. Wargo, R. Knight, Science 2021, 371, eabc4552.

[2] R. Zhu, T. Lang, W. Yan, X. Zhu, X. Huang, Q. Yin, Y. Li, Adv. Sci. 2021, 8, 2003542.

[3] C. P. Kelly, N. Engl. J. Med. 2013, 368, 474.

[4] J. Hahn, S. Ding, J. Im, T. Harimoto, K. W. Leong, T. Danino, Nat. Rev. Bioeng. 2024, 2, 120.

[5] C. H. Woelk, A. Snyder, Science 2021, 371, 573.

[6] E. M. Park, M. Chelvanambi, N. Bhutiani, G. Kroemer, L. Zitvogel, J. A. Wargo, Nat. Med. 2022, 28, 690.

[7] C. C. Wong, J. Yu, Nat. Rev. Clin. Oncol. 2023, 20, 429.

[8] S. Han, W. Van Treuren, C. R. Fischer, B. D. Merrill, B. C. DeFelice, J. M. Sanchez, S. K. Higginbottom, L. Guthrie, L. A. Fall, D. Dodd, M. A. Fischbach, J. L. Sonnenburg, Nature 2021, 595, 415.

[9] C. M. Paulos, C. Wrzesinski, Andrew Kaiser, C. S. Hinrichs, M. Chieppa, L. Cassard, D. C. Palmer, A. Boni, P. Muranski, Z. Yu, L. Gattinoni, P. A. Antony, S. A. Rosenberg, N. P. Restifo, J. Clin, Invest 2007, 117, 2197.

[10] Y. Wang, F.-C. Zhang, Y.-J. Wang, Asian Pac. J. Cancer Prev. 2014, 15, 4449.

[11] B. Mekuye, B. Abera, Nano Select 2023, 4, 486.

[12] D. A. Schupack, R. A. T. Mars, D. H. Voelker, J. P. Abeykoon, P. C. Kashyap, Nat. Rev. Gastroenterol. Hepatol. 2022, 19, 7.

[13] L. Rao, Y. Yuan, X. Shen, G. Yu, X. Chen, Nat. Nanotechnol. 2024, 19, 1769.

[14] K. Strebhardt, A. Ullrich, Nat. Rev. Cancer 2008, 8, 473.

[15] S. Hussain, J. Joo, J. Kang, B. Kim, G. B. Braun, Z.-G. She, D. Kim, A. P. Mann, T. Mölder, T. Teesalu, S. Carnazza, S. Guglielmino, M. J. Sailor, E. Ruoslahti, Nat. Biomed. Eng. 2018, 2, 95.

[16] Y. Jiang, W. Zheng, K. Tran, E. Kamilar, J. Bariwal, H. Ma, H. Liang, Nat. Commun. 2022, 13, 197.

[17] L. Chen, R. Zhao, J. Shen, N. Liu, Z. Zheng, Y. Miao, J. Zhu, L. Zhang, Y. Wang, H. Fang, J. Zhou, M. Li, Y. Yang, Z. Liu, Q. Chen, Adv. Mater. 2023, 35, 2306281.

[18] X. Dong, P. Pan, D.-W. Zheng, P. Bao, X. Zeng, X.-Z. Zhang, Sci. Adv. 2020, 6, eaba1590.

[19] G. Zhang, Q. Wang, W. Tao, W. Jiang, E. Elinav, Y. Wang, S. Zhu, Nat. Biomed. Eng. 2022, 6, 867.

[20] M.-G. Alameh, A. Semon, N. U. Bayard, Y.-G. Pan, G. Dwivedi, J. Knox, R. C. Glover, P. C. Rangel, C. Tanes, K. Bittinger, Q. She, H. Hu, S. R. Bonam, J. R. Maslanka, P. J. Planet, A. M. Moustafa, B. Davis, A. Chevrier, M. Beattie, H. Ni, G. Blizard, E. E. Furth, R. H. Mach, M. Lavertu, M. A. Sellmyer, Y. Tam, M. C. Abt, D. Weissman, J. P. Zackular, Science 2024, 386, 69.

[21] W. Song, A. C. Anselmo, L. Huang, Nat. Nanotechnol. 2019, 14, 1093.

[22] D. H. Dapito, A. Mencin, G.-Y. Gwak, J.-P. Pradere, M.-K. Jang, I. Mederacke, J. M. Caviglia, H. Khiabanian, A. Adeyemi, R. Bataller, J. H. Lefkowitch, M. Bower, R. Friedman, R. B. Sartor, R. Rabadan, R. F. Schwabe, Cancer Cell 2012, 21, 504.

[23] W. Song, K. Tiruthani, Y. Wang, L. Shen, M. Hu, O. Dorosheva, K. Qiu, K. A. Kinghorn, R. Liu, L. Huang, Adv. Mater. 2018, 30, 1805007.

[24] C. Ma, M. Han, B. Heinrich, Q. Fu, Q. Zhang, M. Sandhu, D. Agdashian, M. Terabe, J. A. Berzofsky, V. Fako, T. Ritz, T. Longerich, C. M. Theriot, J. A. McCulloch, S. Roy, W. Yuan, V. Thovarai, S. K. Sen, M. Ruchirawat, F. Korangy, X. W. Wang, G. Trinchieri, T. F. Greten, Science 2018, 360, eaan5931.

[25] G. Ji, X. Si, S. Dong, Y. Xu, M. Li, B. Yang, Z. Tang, X. Fang, L. Huang, W. Song, X. Chen, Nano Lett. 2021, 21, 6781.

[26] K. Han, J. Nam, J. Xu, X. Sun, X. Huang, O. Animasahun, A. Achreja, J. H. Jeon, B. Pursley, N. Kamada, G. Y. Chen, D. Nagrath, J. J. Moon, Nat. Biomed. Eng. 2021, 5, 1377.

[27] T. Lang, R. Zhu, X. Zhu, W. Yan, Y. Li, Y. Zhai, T. Wu, X. Huang, Q. Yin, Y. Li, Nat. Commun. 2023, 14, 4746.

[28] M. R. Fernandes, P. Aggarwal, R. G. F. Costa, A. M. Cole, G. Trinchieri, Nat. Rev. Cancer 2022, 22, 703.

[29] J. A. McCulloch, D. Davar, R. R. Rodrigues, J. H. Badger, J. R. Fang, A. M. Cole, A. K. Balaji, M. Vetizou, S. M. Prescott, M. R. Fernandes, R. G. F. Costa, W. Yuan, R. Salcedo, E. Bahadiroglu, S. Roy, R. N. DeBlasio, R. M. Morrison, J.-M. Chauvin, Q. Ding, B. Zidi, A. Lowin, S. Chakka, W. Gao, O. Pagliano, S. J. Ernst, A. Rose, N. K. Newman, A. Morgun, H. M. Zarour, G. Trinchieri, A. K. Dzutsev, Nat. Med. 2022, 28, 545.

[30] G. Cammarota, G. Ianiro, A. Ahern, C. Carbone, A. Temko, M. J. Claesson, A. Gasbarrini, G. Tortora, Nat. Rev. Gastroenterol. Hepatol. 2020, 17, 635.

RIGHTS & PERMISSIONS

2025 The Author(s). Interdisciplinary Medicine published by Wiley-VCH GmbH on behalf of Nanfang Hospital, Southern Medical University.