Journal Home > Volume 1 , Issue 1
Nano TransMed 2022, 1(1): 9130001 https://doi.org/10.26599/NTM.2022.9130001
Review Article | Open Access | Issue | Published: 06 February 2022

Evoking pyroptosis with nanomaterials for cancer immunotherapy: Current boom and novel outlook

Show Author's Information Wen-Da Wang1,  Zhi-Jun Sun1,2 ( )
The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, Wuhan 430079, China
Department of Oral Maxillofacial-Head Neck Oncology, School & Hospital of Stomatology, Wuhan University, Wuhan 430079, China
Keywords:
nanomaterials, cancer immunotherapy, pyroptosis
Cite this article:
Wang W-D, Sun Z-J. Evoking pyroptosis with nanomaterials for cancer immunotherapy: Current boom and novel outlook. Nano TransMed, 2022, 1(1): 9130001. https://doi.org/10.26599/NTM.2022.9130001
Download citation
EndNote(RIS)
BibTeX

2894

Views

514

Downloads

Citations

8

Crossref

N/A

WoS

N/A

Scopus

N/A

CSCD

Abstract Full text About this article

Cancer immunotherapy, including immune checkpoint blockade, has emerged as a powerful and effective clinical strategy for the treatment of tumors. However, the low response rates or systemic adverse effects owing to the heterogeneity of the tumor microenvironment limit the efficacy of cancer immunotherapy. Pyroptosis, featuring inflammation and lysis, can promote the release of large amounts of proinflammatory agents that reprogram the tumor microenvironment and is expected to achieve the transition from "cold" tumors to "hot" tumors. Therefore, understanding how to particularly evoke tumor cell pyroptosis is crucial in overcoming the adverse effects associated with the tumor microenvironment. The development of emerging nanotechnology offers an avenue for tumor-targeted drug development. Nanomaterials that can trigger tumor-specific pyroptosis have promising applications in improving the efficacy of cancer immunotherapy while reducing systemic adverse effects. Herein, we review the fundamentals of pyroptosis, and summarize the strategies of pyroptosis-based nanomaterials that have been developed recently, with emphasis on their utility and benefits in cancer immunotherapy. Furthermore, we put forth our viewpoints regarding the investigation of nanomaterials and suggest future directions for this rapidly developing field.


menu
Abstract
Full text
Outline
About this article

Evoking pyroptosis with nanomaterials for cancer immunotherapy: Current boom and novel outlook

Show Author's information Wen-Da Wang1, Zhi-Jun Sun1,2 ( )
The State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) & Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Wuhan University, Wuhan 430079, China
Department of Oral Maxillofacial-Head Neck Oncology, School & Hospital of Stomatology, Wuhan University, Wuhan 430079, China

Abstract

Cancer immunotherapy, including immune checkpoint blockade, has emerged as a powerful and effective clinical strategy for the treatment of tumors. However, the low response rates or systemic adverse effects owing to the heterogeneity of the tumor microenvironment limit the efficacy of cancer immunotherapy. Pyroptosis, featuring inflammation and lysis, can promote the release of large amounts of proinflammatory agents that reprogram the tumor microenvironment and is expected to achieve the transition from "cold" tumors to "hot" tumors. Therefore, understanding how to particularly evoke tumor cell pyroptosis is crucial in overcoming the adverse effects associated with the tumor microenvironment. The development of emerging nanotechnology offers an avenue for tumor-targeted drug development. Nanomaterials that can trigger tumor-specific pyroptosis have promising applications in improving the efficacy of cancer immunotherapy while reducing systemic adverse effects. Herein, we review the fundamentals of pyroptosis, and summarize the strategies of pyroptosis-based nanomaterials that have been developed recently, with emphasis on their utility and benefits in cancer immunotherapy. Furthermore, we put forth our viewpoints regarding the investigation of nanomaterials and suggest future directions for this rapidly developing field.

Keywords: nanomaterials, cancer immunotherapy, pyroptosis

References(131)

1

Duan, X. P.; Chan, C.; Lin, W. B. Nanoparticle-mediated immunogenic cell death enables and potentiates cancer immunotherapy. Angew. Chem., Int. Ed. 2019, 58, 670–680.
DOI Google Scholar
2

Yang, Y. P. Cancer immunotherapy: Harnessing the immune system to battle cancer. J. Clin. Invest. 2015, 125, 3335–3337.
DOI Google Scholar
3

Kubli, S. P.; Berger, T.; Araujo, D. V.; Siu, L. L.; Mak, T. W. Beyond immune checkpoint blockade: Emerging immunological strategies. Nat. Rev. Drug Dis. 2021, 20, 899–919.
DOI Google Scholar
4

Couzin-Frankel, J. Cancer immunotherapy. Science 2013, 342, 1432–1433.
DOI Google Scholar
5

Ribas, A.; Wolchok, J. D. Cancer immunotherapy using checkpoint blockade. Science 2018, 359, 1350–1355.
DOI Google Scholar
6

Wei, S. C.; Duffy, C. R.; Allison, J. P. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018, 8, 1069–1086.
DOI Google Scholar
7

Morad, G.; Helmink, B. A.; Sharma, P.; Wargo, J. A. Hallmarks of response, resistance, and toxicity to immune checkpoint blockade. Cell 2021, 184, 5309–5337.
DOI Google Scholar
8

Hegde, P. S.; Chen, D. S. Top 10 challenges in cancer immunotherapy. Immunity 2020, 52, 17–35.
DOI Google Scholar
9

Menon, S.; Shin, S.; Dy, G. Advances in cancer immunotherapy in solid tumors. Cancers 2016, 8, 106.
DOI Google Scholar
10

Musetti, S.; Huang, L. Nanoparticle-mediated remodeling of the tumor microenvironment to enhance immunotherapy. ACS Nano 2018, 12, 11740–11755.
DOI Google Scholar
11

Suarez-Lopez, L.; Sriram, G.; Kong, Y. W.; Morandell, S.; Merrick, K. A.; Hernandez, Y.; Haigis, K, M.; Yaffe, M. B. MK2 contributes to tumor progression by promoting M2 macrophage polarization and tumor angiogenesis. Proc. Natl. Acad. Sci. USA 2018, 115, E4236–E4244.
DOI Google Scholar
12

Veglia, F.; Perego, M.; Gabrilovich, D. Myeloid-derived suppressor cells coming of age. Nat. Immunol. 2018, 19, 108–119.
DOI Google Scholar
13

Wing, J. B.; Tanaka, A.; Sakaguchi, S. Human FOXP3+ regulatory T cell heterogeneity and function in autoimmunity and cancer. Immunity 2019, 50, 302–316.
DOI Google Scholar
14

Liu, Y. T.; Sun, Z. J. Turning cold tumors into hot tumors by improving T-cell infiltration. Theranostics 2021, 11, 5365–5386.
DOI Google Scholar
15

Shao, F. Gasdermins: Making pores for pyroptosis. Nat. Rev. Immunol. 2021, 21, 620–621.
DOI Google Scholar
16

Broz, P.; Pelegrín, P.; Shao, F. The gasdermins, a protein family executing cell death and inflammation. Nat. Rev. Immunol. 2020, 20, 143–157.
DOI Google Scholar
17

Galluzzi, L.; Vitale, I.; Aaronson, S. A.; Abrams, J. M.; Adam, D.; Agostinis, P.; Alnemri, E. S.; Altucci, L.; Amelio, I.; Andrews, D. W. et al. Molecular mechanisms of cell death: Recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018, 25, 486–541.
DOI Google Scholar
18

Mulvihill, E.; Sborgi, L.; Mari, S. A.; Pfreundschuh, M.; Hiller, S.; Müller, D. J. Mechanism of membrane pore formation by human gasdermin-D. EMBO J. 2018, 37, e98321.
DOI Google Scholar
19

Ding, J. J.; Wang, K.; Liu, W.; She, Y.; Sun, Q.; Shi, J. J.; Sun, H. Z.; Wang, D. C.; Shao, F. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 2016, 535, 111–116.
DOI Google Scholar
20

Evavold, C. L.; Hafner-Bratkovič, I.; Devant, P.; D'Andrea, J. M.; Ngwa, E. M.; Boršić, E.; Doench, J. G.; LaFleur, M. W.; Sharpe, A. H.; Thiagarajah, J. R. et al. Control of gasdermin D oligomerization and pyroptosis by the Ragulator-Rag-mTORC1 pathway. Cell 2021, 184, 4495–4511. e19.
DOI Google Scholar
21

Shi, J. J.; Gao, W. Q.; Shao, F. Pyroptosis: Gasdermin-mediated programmed necrotic cell death. Trends Biochem. Sci. 2017, 42, 245–254.
DOI Google Scholar
22

Jorgensen, I.; Miao, E. A. Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev. 2015, 265, 130–142.
DOI Google Scholar
23

Gajewski, T. F.; Woo, S. R.; Zha, Y. Y.; Spaapen, R.; Zheng, Y.; Corrales, L.; Spranger, S. Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment. Curr. Opin. Immunol. 2013, 25, 268–276.
DOI Google Scholar
24

Schumacher, T. N.; Schreiber, R. D. Neoantigens in cancer immunotherapy. Science 2015, 348, 69–74.
DOI Google Scholar
25

Su, F.; Duan, J. Z.; Zhu, J.; Fu, H. J.; Zheng, X. F.; Ge, C. H. Long non-coding RNA nuclear paraspeckle assembly transcript 1 regulates ionizing radiation-induced pyroptosis via microRNA-448/gasdermin E in colorectal cancer cells. Int. J. Oncol. 2021, 59, 79.
DOI Google Scholar
26

Liu, Y. G.; Chen, J. K.; Zhang, Z. T.; Ma, X. J.; Chen, Y. C.; Du, X. M.; Liu, H.; Zong, Y.; Lu, G. C. NLRP3 inflammasome activation mediates radiation-induced pyroptosis in bone marrow-derived macrophages. Cell Death Dis. 2017, 8, e2579.
DOI Google Scholar
27

Yan, H. L.; Luo, B.; Wu, X. Y.; Guan, F.; Yu, X. X.; Zhao, L. N.; Ke, X. K.; Wu, J.; Yuan, J. P. Cisplatin induces pyroptosis via activation of MEG3/NLRP3/caspase-1/GSDMD pathway in triple-negative breast cancer. Int. J. Biol. Sci. 2021, 17, 2606–2621.
DOI Google Scholar
28

Hu, L.; Chen, M.; Chen, X. R.; Zhao, C. G.; Fang, Z. Y.; Wang, H. Z.; Dai, H. M. Chemotherapy-induced pyroptosis is mediated by BAK/ BAX-caspase-3-GSDME pathway and inhibited by 2-bromopalmitate. Cell Death Dis. 2020, 11, 281.
DOI Google Scholar
29

Wang, L.; Li, K.; Lin, X. J.; Yao, Z. M.; Wang, S. H.; Xiong, X.; Ning, Z. F.; Wang, J.; Xu, X. Z.; Jiang, Y. et al. Metformin induces human esophageal carcinoma cell pyroptosis by targeting the miR-497/PELP1 axis. Cancer Lett. 2019, 450, 22–31.
DOI Google Scholar
30

Wang, Y. P.; Gao, W. Q.; Shi, X. Y.; Ding, J. J.; Liu, W.; He, H. B.; Wang, K.; Shao, F. Chemotherapy drugs induce pyroptosis through caspase-3 cleavage of a gasdermin. Nature 2017, 547, 99–103.
DOI Google Scholar
31

Hage, C.; Hoves, S.; Strauss, L.; Bissinger, S.; Prinz, Y.; Pöschinger, T.; Kiessling, F.; Ries, C. H. Sorafenib induces pyroptosis in macrophages and triggers natural killer cell-mediated cytotoxicity against hepatocellular carcinoma. Hepatology 2019, 70, 1280–1297.
DOI Google Scholar
32

Lu, Y.; Xu, F.; Wang, Y.; Shi, C.; Sha, Y. Z.; He, G. L.; Yao, Q. C.; Shao, K.; Sun, W.; Du, J. J. et al. Cancer immunogenic cell death via photo-pyroptosis with light-sensitive indoleamine, 2, 3-dioxygenase inhibitor conjugate. Biomaterials 2021, 278, 121167.
DOI Google Scholar
33

Bollino, D.; Colunga, A.; Li, B. Q.; Aurelian, L. ΔPK oncolytic activity includes modulation of the tumour cell milieu. J. Gen. Virol. 2016, 97, 496–508.
DOI Google Scholar
34

Douzandegan, Y.; Tahamtan, A.; Gray, Z.; Nikoo, H. R.; Tabarraei, A.; Moradi, A. Cell death mechanisms in esophageal squamous cell carcinoma induced by vesicular stomatitis virus matrix protein. Osong Public Health Res. Perspect. 2019, 10, 246–252.
DOI Google Scholar
35

Zhao, P. F.; Wang, M.; Chen, M.; Chen, Z.; Peng, X.; Zhou, F. F.; Song, J.; Qu, J. L. Programming cell pyroptosis with biomimetic nanoparticles for solid tumor immunotherapy. Biomaterials 2020, 254, 120142.
DOI Google Scholar
36

Wu, M.; Liu, X. G.; Chen, H.; Duan, Y. K.; Liu, J. J.; Pan, Y. T.; Liu, B. Activation of pyroptosis by membrane-anchoring AIE photosensitizer design: New prospect for photodynamic cancer cell ablation. Angew. Chem., Int. Ed. 2021, 60, 9093–9098.
DOI Google Scholar
37

Li, L. S.; Song, D. F.; Qi, L.; Jiang, M. X.; Wu, Y. M.; Gan, J. Q.; Cao, K.; Li, Y. J.; Bai, Y. X.; Zheng, T. S. Photodynamic therapy induces human esophageal carcinoma cell pyroptosis by targeting the PKM2/caspase-8/caspase-3/GSDME axis. Cancer Lett. 2021, 520, 143–159.
DOI Google Scholar
38

Yang, W.; Xu, H. T.; Liu, Q. H.; Liu, C. X.; Hu, J. H.; Liu, P.; Fang, T. Y.; Bai, Y. X.; Zhu, J. X.; Xie, R. 5-Aminolevulinic acid hydrochloride loaded microbubbles-mediated sonodynamic therapy in pancreatic cancer cells. Artif. Cells Nanomed. Biotechnol. 2020, 48, 1178–1188.
DOI Google Scholar
39

Zhu, J. X.; Zhu, W. T.; Hu, J. H.; Yang, W.; Liu, P.; Liu, Q. H.; Bai, Y. X.; Xie, R. Curcumin-loaded poly(L-lactide-co-glycolide) microbubble- mediated sono-photodynamic therapy in liver cancer cells. Ultrasound Med. Biol. 2020, 46, 2030–2043.
DOI Google Scholar
40

Liu, Y.; Zhen, W. Y.; Wang, Y. H.; Song, S. Y.; Zhang, H. J. Na2S2O8 nanoparticles trigger antitumor immunotherapy through reactive oxygen species storm and surge of tumor osmolarity. J. Am. Chem. Soc. 2020, 142, 21751–21757.
DOI Google Scholar
41

Yang, Y.; Liu, P. Y.; Bao, W.; Chen, S. J.; Wu, F. S.; Zhu, P. Y. Hydrogen inhibits endometrial cancer growth via a ROS/NLRP3/caspase-1/ GSDMD-mediated pyroptotic pathway. BMC Cancer 2020, 20, 28.
DOI Google Scholar
42

Song, N.; Li, X. J.; Cui, Y.; Zhang, T. Y.; Xu, S. W.; Li, S. Hydrogen sulfide exposure induces pyroptosis in the trachea of broilers via the regulatory effect of circRNA-17828/miR-6631-5p/DUSP6 crosstalk on ROS production. J. Hazard. Mater. 2021, 418, 126172.
DOI Google Scholar
43

Xiong, H. G.; Ma, X. B.; Wang, X. L.; Su, W.; Wu, L.; Zhang, T.; Xu, Z. G.; Sun, Z. J. Inspired epigenetic modulation synergy with adenosine inhibition elicits pyroptosis and potentiates cancer immunotherapy. Adv. Funct. Mater. 2021, 31, 2100007.
DOI Google Scholar
44

Bazak, R.; Houri, M.; El Achy, S.; Hussein, W.; Refaat, T. Passive targeting of nanoparticles to cancer: A comprehensive review of the literature. Mol. Clin. Oncol. 2014, 2, 904–908.
DOI Google Scholar
45

Shen, Z. Y.; Wu, H.; Yang, S.; Ma, X. H.; Li, Z. H.; Tan, M. Q.; Wu, A. G. A novel Trojan-horse targeting strategy to reduce the non- specific uptake of nanocarriers by non-cancerous cells. Biomaterials 2015, 70, 1–11.
DOI Google Scholar
46

Chu, C. C.; Lin, H. R.; Liu, H.; Wang, X. Y.; Wang, J. Q.; Zhang, P. F.; Gao, H. Y.; Huang, C.; Zeng, Y.; Tan, Y. Z. et al. Tumor microenvironment-triggered supramolecular system as an in situ nanotheranostic generator for cancer phototherapy. Adv. Mater. 2017, 29, 1605928.
DOI Google Scholar
47

Dong, R. J.; Zhou, Y. F.; Huang, X. H.; Zhu, X. Y.; Lu, Y. F.; Shen, J. Functional supramolecular polymers for biomedical applications. Adv. Mater. 2015, 27, 498–526.
DOI Google Scholar
48

Wang, L.; Li, L. L.; Fan, Y. S.; Wang, H. Host–guest supramolecular nanosystems for cancer diagnostics and therapeutics. Adv. Mater. 2013, 25, 3888–3898.
DOI Google Scholar
49

Yu, G. C.; Yang, Z.; Fu, X.; Yung, B. C.; Yang, J.; Mao, Z. W.; Shao, L.; Hua, B.; Liu, Y. J.; Zhang, F. W. et al. Polyrotaxane-based supramolecular theranostics. Nat. Commun. 2018, 9, 766.
DOI Google Scholar
50

Yu, G. C.; Zhao, X. L.; Zhou, J.; Mao, Z. W.; Huang, X. L.; Wang, Z. T.; Hua, B.; Liu, Y. J.; Zhang, F. W.; He, Z. M. et al. Supramolecular polymer-based nanomedicine: High therapeutic performance and negligible long-term immunotoxicity. J. Am. Chem. Soc. 2018, 140, 8005–8019.
DOI Google Scholar
51

Gallo, P. M.; Gallucci, S. The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front. Immunol. 2013, 4, 138.
DOI Google Scholar
52

Pallardy, M. J.; Turbica, I.; Biola-Vidamment, A. Why the immune system should be concerned by nanomaterials?. Front. Immunol. 2017, 8, 544.
DOI Google Scholar
53

Kayagaki, N.; Stowe, I. B.; Lee, B. L.; O'Rourke, K.; Anderson, K.; Warming, S.; Cuellar, T.; Haley, B.; Roose-Girma, M.; Phung, Q. T. et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 2015, 526, 666–671.
DOI Google Scholar
54

Shi, J. J.; Zhao, Y.; Wang, K.; Shi, X. Y.; Wang, Y.; Huang, H. W.; Zhuang, Y. H.; Cai, T.; Wang, F. C.; Shao, F. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015, 526, 660–665.
DOI Google Scholar
55

He, W. T.; Wan, H. Q.; Hu, L. C.; Chen, P. D.; Wang, X.; Huang, Z.; Yang, Z. H.; Zhong, C. Q.; Han, J. H. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 2015, 25, 1285–1298.
DOI Google Scholar
56

Tsuchiya, K. Inflammasome-associated cell death: Pyroptosis, apoptosis, and physiological implications. Microbiol. Immunol. 2020, 64, 252–269.
DOI Google Scholar
57

Tsuchiya, K.; Nakajima, S.; Hosojima, S.; Nguyen, D. T.; Hattori, T.; Le, T. M.; Hori, O.; Mahib, M. R.; Yamaguchi, Y.; Miura, M. et al. Caspase-1 initiates apoptosis in the absence of gasdermin D. Nat. Commun. 2019, 10, 2091.
DOI Google Scholar
58

Wang, Q.; Imamura, R.; Motani, K.; Kushiyama, H.; Nagata, S.; Suda, T. Pyroptotic cells externalize eat-me and release find-me signals and are efficiently engulfed by macrophages. Int. Immunol. 2013, 25, 363–372.
DOI Google Scholar
59

Tsuchiya, K. Switching from apoptosis to pyroptosis: Gasdermin- elicited inflammation and antitumor immunity. Int. J. Mol. Sci. 2021, 22, 426.
DOI Google Scholar
60

Volchuk, A.; Ye, A. N.; Chi, L.; Steinberg, B. E.; Goldenberg, N. M. Indirect regulation of HMGB1 release by gasdermin D. Nat. Commun. 2020, 11, 4561.
DOI Google Scholar
61

Franklin, B. S.; Bossaller, L.; De Nardo, D.; Ratter, J. M.; Stutz, A.; Engels, G.; Brenker, C.; Nordhoff, M.; Mirandola, S. R.; Al-Amoudi, A. et al. The adaptor ASC has extracellular and "prionoid" activities that propagate inflammation. Nat. Immunol. 2014, 15, 727–737.
DOI Google Scholar
62

Davis, M. A.; Fairgrieve, M. R.; Den Hartigh, A.; Yakovenko, O.; Duvvuri, B.; Lood, C.; Thomas, W. E.; Fink, S. L.; Gale, M. Jr. Calpain drives pyroptotic vimentin cleavage, intermediate filament loss, and cell rupture that mediates immunostimulation. Proc. Natl. Acad. Sci. USA 2019, 116, 5061–5070.
DOI Google Scholar
63

Rühl, S.; Shkarina, K.; Demarco, B.; Heilig, R.; Santos, J. C.; Broz, P. ESCRT-dependent membrane repair negatively regulates pyroptosis downstream of GSDMD activation. Science 2018, 362, 956–960.
DOI Google Scholar
64

Knodler, L. A.; Crowley, S. M.; Sham, H. P.; Yang, H.; Wrande, M.; Ma, C. X.; Ernst, R. K.; Steele-Mortimer, O.; Celli, J.; Vallance, B. A. Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 2014, 16, 249–256.
DOI Google Scholar
65

Kayagaki, N.; Warming, S.; Lamkanfi, M.; Walle, L. V.; Louie, S.; Dong, J.; Newton, K.; Qu, Y.; Liu, J. F.; Heldens, S. et al. Non- canonical inflammasome activation targets caspase-11. Nature 2011, 479, 117–121.
DOI Google Scholar
66

Shi, J. J.; Zhao, Y.; Wang, Y. P.; Gao, W. Q.; Ding, J. J.; Li, P.; Hu, L. Y.; Shao, F. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 2014, 514, 187–192.
DOI Google Scholar
67

Vanaja, S. K.; Russo, A. J.; Behl, B.; Banerjee, I.; Yankova, M.; Deshmukh, S. D.; Rathinam, V. A. K. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 2016, 165, 1106–1119.
DOI Google Scholar
68

Deng, M. H.; Tang, Y. T.; Li, W. B.; Wang, X. Y.; Zhang, R.; Zhang, X. Y.; Zhao, X.; Liu, J.; Tang, C.; Liu, Z. H. et al. The endotoxin delivery protein HMGB1 mediates caspase-11-dependent lethality in sepsis. Immunity 2018, 49, 740–753. e7.
DOI Google Scholar
69

Kayagaki, N.; Wong, M. T.; Stowe, I. B.; Ramani, S. R.; Gonzalez, L. C.; Akashi-Takamura, S.; Miyake, K.; Zhang, J.; Lee, W. P.; Muszyński, A. et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013, 341, 1246–1249.
DOI Google Scholar
70

Tamura, M.; Tanaka, S.; Fujii, T.; Aoki, A.; Komiyama, H.; Ezawa, K.; Sumiyama, K.; Sagai, T.; Shiroishi, T. Members of a novel gene family, Gsdm, are expressed exclusively in the epithelium of the skin and gastrointestinal tract in a highly tissue-specific manner. Genomics 2007, 89, 618–629.
DOI Google Scholar
71

Fujikane, T.; Nishikawa, N.; Toyota, M.; Suzuki, H.; Nojima, M.; Maruyama, R.; Ashida, M.; Ohe-Toyota, M.; Kai, M.; Nishidate, T. et al. Genomic screening for genes upregulated by demethylation revealed novel targets of epigenetic silencing in breast cancer. Breast Cancer Res. Treat. 2010, 122, 699–710.
DOI Google Scholar
72

Nagata, S.; Tanaka, M. Programmed cell death and the immune system. Nat. Rev. Immunol. 2017, 17, 333–340.
DOI Google Scholar
73

Zhang, Z. B.; Zhang, Y.; Xia, S. Y.; Kong, Q.; Li, S. Y.; Liu, X.; Junqueira, C.; Meza-Sosa, K. F.; Mok, T. M. Y.; Ansara, J. et al. Gasdermin E suppresses tumour growth by activating anti-tumour immunity. Nature 2020, 579, 415–420.
DOI Google Scholar
74

Voskoboinik, I.; Whisstock, J. C.; Trapani, J. A. Perforin and granzymes: Function, dysfunction and human pathology. Nat. Rev. Immunol. 2015, 15, 388–400.
DOI Google Scholar
75

Chowdhury, D.; Lieberman, J. Death by a thousand cuts: Granzyme pathways of programmed cell death. Annu. Rev. Immunol. 2008, 26, 389–420.
DOI Google Scholar
76

Chao, K. L.; Kulakova, L.; Herzberg, O. Gene polymorphism linked to increased asthma and IBD risk alters gasdermin-B structure, a sulfatide and phosphoinositide binding protein. Proc. Natl. Acad. Sci. USA 2017, 114, E1128–E1137.
DOI Google Scholar
77

Zhou, Z. W.; He, H. B.; Wang, K.; Shi, X. Y.; Wang, Y. P.; Su, Y.; Wang, Y.; Li, D.; Liu, W.; Zhang, Y. L. et al. Granzyme A from cytotoxic lymphocytes cleaves GSDMB to trigger pyroptosis in target cells. Science 2020, 368, eaaz7548.
DOI Google Scholar
78

Watabe, K.; Ito, A.; Asada, H.; Endo, Y.; Kobayashi, T.; Nakamoto, K.; Itami, S.; Takao, S.; Shinomura, Y.; Aikou, T. et al. Structure, expression and chromosome mapping of MLZE, a novel gene which is preferentially expressed in metastatic melanoma cells. Jpn. J. Cancer Res. 2001, 92, 140–151.
DOI Google Scholar
79

Orning, P.; Weng, D.; Starheim, K.; Ratner, D.; Best, Z.; Lee, B.; Brooks, A.; Xia, S. Y.; Wu, H.; Kelliher, M. A. et al. Pathogen blockade of TAK1 triggers caspase-8-dependent cleavage of gasdermin D and cell death. Science 2018, 362, 1064–1069.
DOI Google Scholar
80

Sollberger, G.; Choidas, A.; Burn, G. L.; Habenberger, P.; Di Lucrezia, R.; Kordes, S.; Menninger, S.; Eickhoff, J.; Nussbaumer, P.; Klebl, B. et al. Gasdermin D plays a vital role in the generation of neutrophil extracellular traps. Sci. Immunol. 2018, 3, eaar6689.
DOI Google Scholar
81

Kambara, H.; Liu, F.; Zhang, X. Y.; Liu, P.; Bajrami, B.; Teng, Y.; Zhao, L.; Zhou, S. Y.; Yu, H. B.; Zhou, W. D. et al. Gasdermin D exerts anti-inflammatory effects by promoting neutrophil death. Cell Rep. 2018, 22, 2924–2936.
DOI Google Scholar
82

Ye, Y. Q.; Wang, C.; Zhang, X. D.; Hu, Q. Y.; Zhang, Y. Q.; Liu, Q.; Wen, D.; Milligan, J.; Bellotti, A.; Huang, L. et al. A melanin-mediated cancer immunotherapy patch. Sci. Immunol. 2017, 2, eaan5692.
DOI Google Scholar
83

Cheng, L.; Wang, C.; Feng, L. Z.; Yang, K.; Liu, Z. Functional nanomaterials for phototherapies of cancer. Chem. Rev. 2014, 114, 10869–10939.
DOI Google Scholar
84

Chen, Q.; Hu, Q. Y.; Dukhovlinova, E.; Chen, G. J.; Ahn, S.; Wang, C.; Ogunnaike, E. A.; Ligler, F. S.; Dotti, G.; Gu, Z. Photothermal therapy promotes tumor infiltration and antitumor activity of CAR T cells. Adv. Mater. 2019, 31, 1900192.
DOI Google Scholar
85

Agostinis, P.; Berg, K.; Cengel, K. A.; Foster, T. H.; Girotti, A. W.; Gollnick, S. O.; Hahn, S. M.; Hamblin, M. R.; Juzeniene, A.; Kessel, D. et al. Photodynamic therapy of cancer: An update. CA Cancer J. Clin. 2011, 61, 250–281.
DOI Google Scholar
86

Lucky, S. S.; Soo, K. C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev. 2015, 115, 1990–2042.
DOI Google Scholar
87

Chen, Q.; Wang, C.; Zhan, Z. X.; He, W. W.; Cheng, Z. P.; Li, Y. Y.; Liu, Z. Near-infrared dye bound albumin with separated imaging and therapy wavelength channels for imaging-guided photothermal therapy. Biomaterials 2014, 35, 8206–8214.
DOI Google Scholar
88

Day, E. S.; Morton, J. G.; West, J. L. Nanoparticles for thermal cancer therapy. J. Biomech. Eng. 2009, 131, 074001.
DOI Google Scholar
89

Boni, L.; David, G.; Mangano, A.; Dionigi, G.; Rausei, S.; Spampatti, S.; Cassinotti, E.; Fingerhut, A. Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg. Endosc. 2015, 29, 2046–2055.
DOI Google Scholar
90

Kuo, W. S.; Chang, Y. T.; Cho, K. C.; Chiu, K. C.; Lien, C. H.; Yeh, C. S.; Chen, S. J. Gold nanomaterials conjugated with indocyanine green for dual-modality photodynamic and photothermal therapy. Biomaterials 2012, 33, 3270–3278.
DOI Google Scholar
91

Wang, H. L.; Li, X. X.; Tse, B. W. C.; Yang, H. T.; Thorling, C. A.; Liu, Y. X.; Touraud, M.; Chouane, J. B.; Liu, X.; Roberts, M. S. et al. Indocyanine green-incorporating nanoparticles for cancer theranostics. Theranostics 2018, 8, 1227–1242.
DOI Google Scholar
92
Su, X. X.; Wang, W. J.; Cao, Q.; Zhang, H.; Liu, B.; Ling, Y. Y.; Zhou, X. T.; Mao, Z. W. A carbonic anhydrase IX (CAIX)-anchored rhenium(I) photosensitizer evokes pyroptosis for enhanced anti- tumor immunity. Angew. Chem., Int. Ed. 2021, e202115800, in press, https://doi.org/10.1002/ange.202115800.
DOI
93

Wu, L. H.; Mendoza-Garcia, A.; Li, Q.; Sun, S. H. Organic phase syntheses of magnetic nanoparticles and their applications. Chem. Rev. 2016, 116, 10473–10512.
DOI Google Scholar
94

Gavilán, H.; Avugadda, S. K.; Fernández-Cabada, T.; Soni, N.; Cassani, M.; Mai, B. T.; Chantrell, R.; Pellegrino, T. Magnetic nanoparticles and clusters for magnetic hyperthermia: Optimizing their heat performance and developing combinatorial therapies to tackle cancer. Chem. Soc. Rev. 2021, 50, 11614–11667.
DOI Google Scholar
95

Clerc, P.; Jeanjean, P.; Hallali, N.; Gougeon, M.; Pipy, B.; Carrey, J.; Fourmy, D.; Gigoux, V. Targeted magnetic intra-lysosomal hyperthermia produces lysosomal reactive oxygen species and causes caspase-1 dependent cell death. J. Control. Release 2018, 270, 120–134.
DOI Google Scholar
96

Muckenthaler, M. U.; Rivella, S.; Hentze, M. W.; Galy, B. A red carpet for iron metabolism. Cell 2017, 168, 344–361.
DOI Google Scholar
97

Dixon, S. J.; Lemberg, K. M.; Lamprecht, M. R.; Skouta, R.; Zaitsev, E. M.; Gleason, C. E.; Patel, D. N.; Bauer, A. J.; Cantley, A. M.; Yang, W. S. et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012, 149, 1060–1072.
DOI Google Scholar
98

Furukawa, H.; Cordova, K. E.; O'Keeffe, M.; Yaghi, O. M. The chemistry and applications of metal-organic frameworks. Science 2013, 341, 1230444.
DOI Google Scholar
99

Freund, R.; Zaremba, O.; Arnauts, G.; Ameloot, R.; Skorupskii, G.; Dincă, M.; Bavykina, A.; Gascon, J.; Ejsmont, A.; Goscianska, J. et al. The current status of MOF and COF applications. Angew. Chem., Int. Ed. 2021, 60, 23975–24001.
DOI Google Scholar
100

Ploetz, E.; Zimpel, A.; Cauda, V.; Bauer, D.; Lamb, D. C.; Haisch, C.; Zahler, S.; Vollmar, A. M.; Wuttke, S.; Engelke, H. Metal–organic framework nanoparticles induce pyroptosis in cells controlled by the extracellular pH. Adv. Mater. 2020, 32, 1907267.
DOI Google Scholar
101

Xu, R.; Yang, J.; Qian, Y.; Deng, H. Z.; Wang, Z. H.; Ma, S. Y.; Wei, Y. W.; Yang, N.; Shen, Q. Ferroptosis/pyroptosis dual-inductive combinational anti-cancer therapy achieved by transferrin decorated nanoMOF. Nanoscale Horiz. 2021, 6. 348–356.
DOI Google Scholar
102

Rongvaux, A.; Jackson, R.; Harman, C. C. D.; Li, T.; West, A. P.; de Zoete, M. R.; Wu, Y. T.; Yordy, B.; Lakhani, S. A.; Kuan, C. Y. et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 2014, 159, 1563–1577.
DOI Google Scholar
103

Zhou, S. Y.; Shang, Q.; Ji, J. B.; Luan, Y. X. A nanoplatform to amplify apoptosis-to-pyroptosis immunotherapy via immunomodulation of myeloid-derived suppressor cells. ACS Appl. Mater. Interfaces 2021, 13, 47407–47417.
DOI Google Scholar
104

Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach?. Nat. Rev. Drug Discov. 2009, 8, 579–591.
DOI Google Scholar
105

Szatrowski, T. P.; Nathan, C. F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51, 794–798.
Google Scholar
106

Lee, S. H.; Gupta, M. K.; Bang, J. B.; Bae, H.; Sung, H. J. Current progress in reactive oxygen species (ROS)-responsive materials for biomedical applications. Adv. Healthc. Mater. 2013, 2, 908–915.
DOI Google Scholar
107

Zhang, D. L.; Wei, Y. L.; Chen, K.; Zhang, X. J.; Xu, X. Q.; Shi, Q.; Han, S. L.; Chen, X.; Gong, H.; Li, X. H. et al. Biocompatible reactive oxygen species (ROS)-responsive nanoparticles as superior drug delivery vehicles. Adv. Healthc. Mater. 2015, 4, 69–76.
DOI Google Scholar
108

Xu, X. D.; Saw, P. E.; Tao, W.; Li, Y. J.; Ji, X. Y.; Bhasin, S.; Liu, Y. L.; Ayyash, D.; Rasmussen, J.; Huo, M. et al. ROS-responsive polyprodrug nanoparticles for triggered drug delivery and effective cancer therapy. Adv. Mater. 2017, 29, 1700141.
DOI Google Scholar
109

Li, J. J.; Anraku, Y.; Kataoka, K. Self-boosting catalytic nanoreactors integrated with triggerable crosslinking membrane networks for initiation of immunogenic cell death by pyroptosis. Angew. Chem., Int. Ed. 2020, 59, 13526–13530.
DOI Google Scholar
110

Wang, K. W.; Xiao, X.; Jiang, M. L.; Li, J. S.; Zhou, J. L.; Yuan, Y. Y. An NIR-fluorophore-based theranostic for selective initiation of tumor pyroptosis-induced immunotherapy. Small 2021, 17, 2102610.
DOI Google Scholar
111

Xiao, Y.; Zhang, T.; Ma, X. B.; Yang, Q. C.; Yang, L. L.; Yang, S. C.; Liang, M. Y.; Xu, Z. G.; Sun, Z. J. Microenvironment-responsive prodrug-induced pyroptosis boosts cancer immunotherapy. Adv. Sci. 2021, 8, 2101840.
DOI Google Scholar
112
Zhou, J. J.; Ma, X. B.; Li, H.; Chen, D. R.; Mao, L.; Yang, L. L.; Zhang, T.; Qiu, W.; Xu, Z. G.; Sun, Z. J. Inspired heat shock protein alleviating prodrug enforces immunogenic photodynamic therapy by eliciting pyroptosis. Nano Res., in press, https://doi.org/10.1007/s12274-021-3946-2.
DOI
113

Tanner, P.; Baumann, P.; Enea, R.; Onaca, O.; Palivan, C.; Meier, W. Polymeric vesicles: From drug carriers to nanoreactors and artificial organelles. Acc. Chem. Res. 2011, 44, 1039–1049.
DOI Google Scholar
114

Ahmed, K. S.; Hussein, S. A.; Ali, A. H.; Korma, S. A.; Qiu, L. P.; Chen, J. H. Liposome: Composition, characterisation, preparation, and recent innovation in clinical applications. J. Drug Target. 2019, 27, 742–761.
DOI Google Scholar
115

Zahednezhad, F.; Saadat, M.; Valizadeh, H.; Zakeri-Milani, P.; Baradaran, B. Liposome and immune system interplay: Challenges and potentials. J. Control. Release 2019, 305, 194–209.
DOI Google Scholar
116

Akino, K.; Toyota, M.; Suzuki, H.; Imai, T.; Maruyama, R.; Kusano, M.; Nishikawa, N.; Watanabe, Y.; Sasaki, Y.; Abe, T. et al. Identification of DFNA5 as a target of epigenetic inactivation in gastric cancer. Cancer Sci. 2007, 98, 88–95.
DOI Google Scholar
117

Kim, M. S.; Chang, X.; Yamashita, K.; Nagpal, J. K.; Baek, J. H.; Wu, G.; Trink, B.; Ratovitski, E. A.; Mori, M.; Sidransky, D. Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene 2008, 27, 3624–3634.
DOI Google Scholar
118

Fan, J. X.; Deng, R. H.; Wang, H.; Liu, X. H.; Wang, X. N.; Qin, R.; Jin, X.; Lei, T. R.; Zheng, D. W.; Zhou, P. H. et al. Epigenetics-based tumor cells pyroptosis for enhancing the immunological effect of chemotherapeutic nanocarriers. Nano Lett. 2019, 19, 8049–8058.
DOI Google Scholar
119

Song, M. M.; Xia, W. T.; Tao, Z. X.; Zhu, B.; Zhang, W. X.; Liu, C.; Chen, S. Y. Self-assembled polymeric nanocarrier-mediated co-delivery of metformin and doxorubicin for melanoma therapy. Drug Deliv. 2021, 28, 594–606.
DOI Google Scholar
120

Serna, N.; Sánchez-García, L.; Unzueta, U.; Díaz, R.; Vázquez, E.; Mangues, R. Protein-based therapeutic killing for cancer therapies. Trends Biotechnol. 2018, 36, 318–335.
DOI Google Scholar
121

Serna, N.; Álamo, P.; Ramesh, P.; Vinokurova, D.; Sánchez-García, L.; Unzueta, U.; Gallardo, A.; Céspedes, M. V.; Vázquez, E.; Villaverde, A. et al. Nanostructured toxins for the selective destruction of drug-resistant human CXCR4+ colorectal cancer stem cells. J. Control. Release 2020, 320, 96–104.
DOI Google Scholar
122

Wang, Q. Y.; Wang, Y. P.; Ding, J. J.; Wang, C. H.; Zhou, X. H.; Gao, W. Q.; Huang, H. W.; Shao, F.; Liu, Z. B. A bioorthogonal system reveals antitumour immune function of pyroptosis. Nature 2020, 579, 421–426.
DOI Google Scholar
123

Elion, D. L.; Jacobson, M. E.; Hicks, D. J.; Rahman, B.; Sanchez, V.; Gonzales-Ericsson, P. I.; Fedorova, O.; Pyle, A. M.; Wilson, J. T.; Cook, R. S. Therapeutically active RIG-I agonist induces immunogenic tumor cell killing in breast cancers. Cancer Res. 2018, 78, 6183–6195.
DOI Google Scholar
124

Hu, J.; Dong, Y.; Ding, L.; Dong, Y.; Wu, Z. H.; Wang, W. P.; Shen, M.; Duan, Y. R. Local delivery of arsenic trioxide nanoparticles for hepatocellular carcinoma treatment. Signal Transduct. Target. Ther. 2019, 4, 28.
DOI Google Scholar
125

Nadeem, S.; Yang, C.; Du, Y.; Li, F. Y.; Chen, Z.; Zhou, Y.; Lee, J. Y.; Ding, Q.; Ling, D. S. A virus-spike tumor-activatable pyroptotic agent. Small 2021, 17, 2006599.
DOI Google Scholar
126

Ding, B. B.; Sheng, J. Y.; Zheng, P.; Li, C. X.; Li, D.; Cheng, Z. Y.; Ma, P. A.; Lin, J. Biodegradable upconversion nanoparticles induce pyroptosis for cancer immunotherapy. Nano Lett. 2021, 21, 8281–8289.
DOI Google Scholar
127

Grivennikov, S. I.; Greten, F. R.; Karin, M. Immunity, inflammation, and cancer. Cell 2010, 140, 883–899.
DOI Google Scholar
128

Vakkila, J.; Lotze, M. T. Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 2004, 4, 641–648.
DOI Google Scholar
129

Xia, X. J.; Wang, X.; Cheng, Z.; Qin, W. H.; Lei, L. C.; Jiang, J. Q.; Hu, J. H. The role of pyroptosis in cancer: Pro-cancer or pro-"host"?. Cell Death Dis. 2019, 10, 650.
DOI Google Scholar
130

Segovia, M.; Russo, S.; Jeldres, M.; Mahmoud, Y. D.; Perez, V.; Duhalde, M.; Charnet, P.; Rousset, M.; Victoria, S.; Veigas, F. et al. Targeting TMEM176B enhances antitumor immunity and augments the efficacy of immune checkpoint blockers by unleashing inflammasome activation. Cancer Cell 2019, 35, 767–781. e6.
DOI Google Scholar
131

Zhang, M.; Xin, W.; Yu, Y.; Yang, X. Y.; Ma, C.; Zhang, H. Y.; Liu, Y.; Zhao, X. J.; Guan, X.; Wang, X. Y. et al. Programmed death-ligand 1 triggers PASMCs pyroptosis and pulmonary vascular fibrosis in pulmonary hypertension. J. Mol. Cell. Cardiol. 2020, 138, 23–33.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 01 January 2022
Revised: 26 January 2022
Accepted: 26 January 2022
Published: 06 February 2022
Issue date: March 2022

Copyright

© The Author(s) 2022. Nano TransMed published by Tsinghua University Press.

Acknowledgements

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 82072996 and 81874131), and the Fundamental Research Funds for the Central Universities (No. 2042021kf0216).

Rights and permissions

The articles published in this open access journal are distributedunder the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use,distribution and reproduction in any medium, provided the original work is properly cited.

Return