Research development of inflammasome in glioma

doi:10.3969/j.issn.1000-1565.2024.04.007

Abstract

Abstract: Inflammasome is composed of apoptosis-associated speckle-like protein(ASC), caspase-1 and pattern recognition receptors(PRR). Inflammasome plays an important role in the process of tumorigenesis, including the regulation of tumor biological behavior, pyroptosis and immunity. Targeting inflammasome may provide new ideas for tumor treatment and prognosis improvement. Gliomas are highly malignant brain tumors with poor prognosis in the central nervous system. This article reviews the composition, activation mechanism and the role of inflammasome in gliomas.

Key words: inflammasome, glioma, pyroptosis, immunotherapy, IL-1β

CLC Number:

R739.4

TAN Yanli, LI Xiang, LI Zirui, YU Jia. Research development of inflammasome in glioma[J]. Journal of Hebei University(Natural Science Edition), 2024, 44(4): 390-398.

References

[1] YI K K, ZHAN Q, WANG Q X, et al. PTRF/cavin-1 remodels phospholipid metabolism to promote tumor proliferation and suppress immune responses in glioblastoma by stabilizing cPLA2[J]. Neuro-oncology, 2021, 23(3): 387-399. DOI: 10.1093/neuonc/noaa255.
[2] ZHANG R, SONG Q, LIN X,et al. GSDMA at the crossroads between pyroptosis and tumor immune evasion in glioma[J].Biochem Biophys Res Commun,2023,686:149181. DOI:10.1016/j.bbrc.2023.149181.
[3] MARTINON F, BURNS K, TSCHOPP J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta[J]. Mol Cell, 2002, 10(2): 417-426. DOI: 10.1016/s1097-2765(02)00599-3.
[4] LIU S W, SONG W J, MA G K, et al. Pyroptosis and its role in cancer[J]. World J Clin Cases, 2023, 11(11): 2386-2395. DOI: 10.12998/wjcc.v11.i11.2386.
[5] SUNDARAM B, KANNEGANTI T D. Advances in understanding activation and function of the NLRC4 inflammasome[J]. Int J Mol Sci, 2021, 22(3): 1048. DOI: 10.3390/ijms22031048.
[6] 王文连,林欣,胡俊锋.炎性小体在肺部疾病中的作用[J].中国呼吸与危重监护杂志, 2019,18(4): 404-408. DOI: 10.7507/1671-6205.201805056.
[7] 王变丽,王天怡,张露丹,等.炎性小体及细胞焦亡在肠道稳态中的研究进展[J]. 中国免疫学杂志, 2023, 39(6): 1337-1341. DOI: 10.3969/j.issn.1000-484X.2023.06.046.
[8] 耿晋,朱永杰,耿蕴琦,等.炎性小体及其与结直肠癌关系的研究进展[J].军事医学, 2018, 42(6): 471-475. DOI:10.7644/j.issn.1674-9960.2018.06.016.
[9] CHEW Z H, CUI J Z, SACHAPHIBULKIJ K, et al. Macrophage IL-1β contributes to tumorigenesis through paracrine AIM2 inflammasome activation in the tumor microenvironment[J]. Front Immunol, 2023, 14: 1211730. DOI: 10.3389/fimmu.2023.1211730.
[10] BURDETTE B E, ESPARZA A N, ZHU H,et al. Gasdermin D in pyroptosis[J]. Acta Pharm Sin B, 2021;11(9):2768-2782. DOI:10.1016/j.apsb.2021.02.006
[11] CHRISTGEN S, PLACE D E, KANNEGANTI T D. Toward targeting inflammasomes: insights into their regulation and activation[J]. Cell Res, 2020, 30(4): 315-327. DOI: 10.1038/s41422-020-0295-8.
[12] ROSS C, CHAN A H, VON PEIN J B, et al. Inflammatory caspases: toward a unified model for caspase activation by inflammasomes[J]. Annu Rev Immunol, 2022, 40: 249-269. DOI: 10.1146/annurev-immunol-101220-030653.
[13] CHAUHAN D, VANDE WALLE L, LAMKANFI M. Therapeutic modulation of inflammasome pathways[J]. Immunol Rev, 2020, 297(1): 123-138. DOI: 10.1111/imr.12908.
[14] SHI J J, ZHAO Y, WANG K, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death[J]. Nature, 2015, 526(7575): 660-665. DOI: 10.1038/nature15514.
[15] TAPIA-ABELLÁN A, ANGOSTO-BAZARRA D, ALARCÓN-VILA C, et al. Sensing low intracellular potassium by NLRP3 results in a stable open structure that promotes inflammasome activation[J]. Sci Adv, 2021, 7(38): eabf4468. DOI: 10.1126/sciadv.abf4468.
[16] PENG L C, TIAN H L, LU Y, et al. Chicken cathelicidin-2 promotes NLRP3 inflammasome activation in macrophages[J]. Vet Res, 2022, 53(1): 69. DOI: 10.1186/s13567-022-01083-4.
[17] MURAKAMI T, OCKINGER J, YU J J, et al. Critical role for calcium mobilization in activation of the NLRP3 inflammasome[J]. Proc Natl Acad Sci USA, 2012, 109(28): 11282-11287. DOI: 10.1073/pnas.1117765109.
[18] LIU Q Y, WANG D D, YANG X D, et al. The mechanosensitive ion channel PIEZO1 in intestinal epithelial cells mediates inflammation through the NOD-like receptor 3 pathway in Crohn’s disease[J]. Inflamm Bowel Dis, 2023, 29(1): 103-115. DOI: 10.1093/ibd/izac152.
[19] ZHANG Z, XIE S J, QIAN J, et al. Targeting macrophagic PIM-1 alleviates osteoarthritis by inhibiting NLRP3 inflammasome activation via suppressing mitochondrial ROS/Cl- efflux signaling pathway[J]. J Transl Med, 2023, 21(1): 452. DOI: 10.1186/s12967-023-04313-1.
[20] GREEN J P, YU S, MARTÍN-SÁNCHEZ F, et al. Chloride regulates dynamic NLRP3-dependent ASC oligomerization and inflammasome priming[J]. Proc Natl Acad Sci USA, 2018, 115(40): E9371-E9380. DOI: 10.1073/pnas.1812744115.
[21] CHEN F, FENG L, ZHENG Y L, et al. 2, 2', 4, 4'-tetrabromodiphenyl ether(BDE-47)induces mitochondrial dysfunction and related liver injury via eliciting miR-34a-5p-mediated mitophagy impairment[J]. Environ Pollut, 2020, 258: 113693. DOI: 10.1016/j.envpol.2019.113693.
[22] AN C, SUN F, LIU C, et al. IQGAP1 promotes mitochondrial damage and activation of the mtDNA sensor cGAS-STING pathway to induce endothelial cell pyroptosis leading to atherosclerosis[J]. Int Immunopharmacol, 2023, 123: 110795. DOI: 10.1016/j.intimp.2023.110795.
[23] YANG B W, WANG Y T, FANG C Y, et al. Polybrominated diphenyl ether quinone exposure leads to ROS-driven lysosomal damage, mitochondrial dysfunction and NLRP3 inflammasome activation[J]. Environ Pollut, 2022, 311: 119846. DOI: 10.1016/j.envpol.2022.119846.
[24] HOU Y T, HE H B, MA M, et al. Apilimod activates the NLRP3 inflammasome through lysosome-mediated mitochondrial damage[J]. Front Immunol, 2023, 14: 1128700. DOI: 10.3389/fimmu.2023.1128700.
[25] NEUWIRT E, MAGNANI G, C^'IKOVI T, et al. Tyrosine kinase inhibitors can activate the NLRP3 inflammasome in myeloid cells through lysosomal damage and cell lysis[J]. Sci Signal, 2023, 16(768): eabh1083. DOI: 10.1126/scisignal.abh1083.
[26] WANG W Q, CHANG R, WANG Y, et al. Mitophagy-dependent mitochondrial ROS mediates 2, 5-hexanedione-induced NLRP3 inflammasome activation in BV2 microglia[J]. Neurotoxicology, 2023, 99: 50-58. DOI: 10.1016/j.neuro.2023.09.008.
[27] GAI Y, BAI C, ZHANG W, et al. Nootkatone attenuates airway inflammation in asthmatic mice through repressing ROS-induced NLRP3 inflammasome activation[J]. Biochem Cell Biol, 2023, 101(6): 513-522. DOI: 10.1139/bcb-2023-0009.
[28] SU W J, LI J M, ZHANG T, et al. Microglial NLRP3 inflammasome activation mediates diabetes-induced depression-like behavior via triggering neuroinflammation[J]. Prog Neuropsychopharmacol Biol Psychiatry, 2023, 126: 110796. DOI: 10.1016/j.pnpbp.2023.110796.
[29] ROSA C P, BELO T C A, SANTOS N C M, et al. Reactive oxygen species trigger inflammasome activation after intracellular microbial interaction[J]. Life Sci, 2023, 331: 122076. DOI: 10.1016/j.lfs.2023.122076.
[30] TURTON K, PARKS H J, ZARODKIEWICZ P, et al. The Achromobacter type 3 secretion system drives pyroptosis and immunopathology via independent activation of NLRC4 and NLRP3 inflammasomes[J]. Cell Rep, 2023, 42(8): 113012. DOI: 10.1016/j.celrep.2023.113012.
[31] KOIZUMI Y, TOMA C, HIGA N, et al. Inflammasome activation via intracellular NLRs triggered by bacterial infection[J]. Cell Microbiol, 2012, 14(2): 149-154. DOI: 10.1111/j.1462-5822.2011.01707.x.
[32] TIBBLE R, YONEMITSU M A, MITCHELL P S. Stalled but not forgotten: bacterial exotoxins inhibit translation to activate NLRP1[J]. J Exp Med, 2023, 220(10): e20231160. DOI: 10.1084/jem.20231160.
[33] ZHENG D P, KERN L, ELINAV E. The NLRP6 inflammasome[J]. Immunology, 2021, 162(3): 281-289. DOI: 10.1111/imm.13293.
[34] ZHOU Y, SHAH S Z, YANG L F, et al. Virulent mycobacterium bovis Beijing strain activates the NLRP7 inflammasome in THP-1 macrophages[J]. PLoS One, 2016, 11(4): e0152853. DOI: 10.1371/journal.pone.0152853.
[35] JING X, YUN Y H, JI X, et al. Pyroptosis and inflammasome-related genes- NLRP3, NLRC4 and NLRP7 polymorphisms were associated with risk of lung cancer[J]. Pharmgenomics Pers Med, 2023, 16: 795-804. DOI: 10.2147/PGPM.S424326.
[36] CASILI G, SCUDERI S A, LANZA M, et al. Therapeutic potential of BAY-117082, a selective NLRP3 inflammasome inhibitor, on metastatic evolution in human oral squamous cell carcinoma(OSCC)[J]. Cancers, 2023, 15(10): 2796. DOI: 10.3390/cancers15102796.
[37] LI W J, ZHAO X B, ZHANG R J, et al. Silencing of NLRP3 sensitizes chemoresistant ovarian cancer cells to cisplatin[J]. Mediators Inflamm, 2023, 2023: 7700673. DOI: 10.1155/2023/7700673.
[38] LIU H D, LI W, CHEN Z R, et al. Expression of the NLRP3 inflammasome in cerebral cortex after traumatic brain injury in a rat model[J]. Neurochem Res, 2013, 38(10): 2072-2083. DOI: 10.1007/s11064-013-1115-z.
[39] 樊明德,张源,苗保旺,等.Nod样受体热蛋白结构域相关蛋白3在人脑胶质瘤中的表达[J].山东大学学报(医学版), 2013, 51(4): 51-54. DOI: 10.6040/j.issn.1671-7554.2013.04.012.
[40] HAN S Y, ZHANG Z M, MA W B, et al. Nucleotide-binding oligomerization domain(NOD)-like receptor subfamily C(NLRC)as a prognostic biomarker for glioblastoma multiforme linked to tumor microenvironment: a bioinformatics, immunohistochemistry, and machine learning-based study[J]. J Inflamm Res, 2023, 16: 523-537. DOI: 10.2147/JIR.S397305.
[41] LIM J, KIM M J, PARK Y, et al. Upregulation of the NLRC4 inflammasome contributes to poor prognosis in glioma patients[J]. Sci Rep, 2019, 9(1): 7895. DOI: 10.1038/s41598-019-44261-9.
[42] ZHANG L, JIAO C, LIU L J, et al. NLRC5: a potential target for central nervous system disorders[J]. Front Immunol, 2021, 12: 704989. DOI: 10.3389/fimmu.2021.704989.
[43] VIJAYAN S, SIDIQ T, YOUSUF S, et al. Class I transactivator, NLRC5: a central player in the MHC class I pathway and cancer immune surveillance[J]. Immunogenetics, 2019,71(3):273-282.DOI:10.1007/s00251-019-01106-z.
[44] YIN X F, ZHANG Q, CHEN Z Y, et al. NLRP3 in human glioma is correlated with increased WHO grade, and regulates cellular proliferation, apoptosis and metastasis via epithelial-mesenchymal transition and the PTEN/AKT signaling pathway[J]. Int J Oncol, 2018, 53(3): 973-986. DOI: 10.3892/ijo.2018.4480.
[45] ZHU C, ZOU C Y, GUAN G F, et al. Development and validation of an interferon signature predicting prognosis and treatment response for glioblastoma[J]. Oncoimmunology, 2019, 8(9): e1621677. DOI: 10.1080/2162402X.2019.1621677.
[46] 殷小凤.NLRP3在人胶质瘤中的表达及其对胶质瘤细胞生物学行为的作用研究[D].广州:南方医科大学, 2017
[47] BELLUT M, PAPP L, BIEBER M, et al. NLPR3 inflammasome inhibition alleviates hypoxic endothelial cell death in vitro and protects blood-brain barrier integrity in murine stroke[J]. Cell Death Dis, 2021, 13(1): 20. DOI: 10.1038/s41419-021-04379-z.
[48] XUE L, LU B, GAO B, et al. NLRP3 promotes glioma cell proliferation and invasion via the interleukin-1β/NF-κB p65 signals[J].Oncol Res,2019;27(5):557-564. DOI:10.3727/096504018X15264647024196.
[49] XUE L P, LU B, GAO B B, et al. NLRP3 promotes glioma cell proliferation and invasion via the interleukin-1β/NF-κB p65 signals[J]. Oncol Res, 2019, 27(5): 557-564. DOI: 10.3727/096504018X15264647024196.
[50] XIE K, ZHOU D M, FANG C, et al. Inhibition of NF-κB activation by BAY 11-7821 suppresses the proliferation and inflammation of glioma cells through inducing autophagy[J]. Transl Cancer Res TCR, 2022, 11(2): 403-413. DOI: 10.21037/tcr-21-2914.
[51] ZONG Z Q, SONG Y C, XUE Y X, et al. Knockdown of LncRNA SCAMP1 suppressed malignant biological behaviours of glioma cells via modulating miR-499a-5p/LMX1A/NLRC5 pathway[J]. J Cell Mol Med, 2019, 23(8): 5048-5062. DOI: 10.1111/jcmm.14362.
[52] WANG H B, XU G X, HUANG Z J, et al. LRP6 targeting suppresses gastric tumorigenesis via P14ARF-Mdm2-p53-dependent cellular senescence[J]. Oncotarget, 2017, 8(67): 111597-111607. DOI: 10.18632/oncotarget.22876.
[53] YU Y H, CAO F, XIONG Y Q, et al. SP1 transcriptionally activates NLRP6 inflammasome and induces immune evasion and radioresistance in glioma cells[J]. Int Immunopharmacol, 2021, 98: 107858. DOI: 10.1016/j.intimp.2021.107858.
[54] WAN S C, ZHANG G H, LIU R C, et al. Pyroptosis, ferroptosis, and autophagy cross-talk in glioblastoma opens up new avenues for glioblastoma treatment[J]. Cell Commun Signal, 2023, 21(1): 115. DOI: 10.1186/s12964-023-01108-1.
[55] TANG N, ZHU Y, YU J. Xihuang pill facilitates glioma cell pyroptosis via the POU4F1/STAT3 axis[J]. Funct Integr Genomics,2023;23(4):334. DOI:10.1007/s10142-023-01263-1.
[56] ZHAO X, CHEN C, HAN W, et al. EEBR induces Caspase-1-dependent pyroptosis through the NF-κB/NLRP3 signalling cascade in non-small cell lung cancer[J].J Cell Mol Med,2024;28(3):e18094. DOI:10.1111/jcmm.18094.
[57] 陈健,郭志娟,裴美娟,等.HIF-1α对人脑胶质瘤SHG44细胞恶性度的影响及其机制[J].武警医学, 2022, 33(6): 484-488. DOI: 10.3969/j.issn.1004-3594.2022.06.007.
[58] FENG X Q, CHEN Y H, LIU X Y, et al. Construction and verification of a novel pyroptosis-related lncRNA signature associated with immune landscape in gliomas[J]. J Oncol, 2022, 2022: 7043431. DOI: 10.1155/2022/7043431.
[59] YANG S, XIE C, GUO T, et al. Simvastatin inhibits tumor growth and migration by mediating caspase-1-dependent pyroptosis in glioblastoma multiforme[J].World Neurosurg,2022;165:e12-e21. DOI:10.1016/j.wneu.2022.03.089
[60] 杜洋,邱鹏程,王媛媛,等.海星皂苷CN-3激活NLRP3/Caspase-1/GSDMD信号通路诱导胶质瘤细胞焦亡的作用[J].环球中医药, 2022, 15(11): 2022-2029. DOI: 10.3969/j.issn.1674-1749.2022.11.006.
[61] WU Y S, CHANG J, GE J J, et al. Isobavachalcone’s alleviation of pyroptosis contributes to enhanced apoptosis in glioblastoma: possible involvement of NLRP3[J]. Mol Neurobiol, 2022, 59(11): 6934-6955. DOI: 10.1007/s12035-022-03010-2.
[62] LIANG Q Y, WU J Q, ZHAO X, et al. Establishment of tumor inflammasome clusters with distinct immunogenomic landscape aids immunotherapy[J]. Theranostics, 2021, 11(20): 9884-9903. DOI: 10.7150/thno.63202.
[63] LI Z, FU W J, CHEN X Q, et al. Autophagy-based unconventional secretion of HMGB1 in glioblastoma promotes chemosensitivity to temozolomide through macrophage M1-like polarization[J]. J Exp Clin Cancer Res, 2022, 41(1): 74. DOI: 10.1186/s13046-022-02291-8.
[64] KIM S M, JEON Y, JANG J Y, et al. NR1D1 deficiency in the tumor microenvironment promotes lung tumor development by activating the NLRP3 inflammasome[J]. Cell Death Discov, 2023, 9(1): 278. DOI: 10.1038/s41420-023-01554-3.
[65] DALEY D, MANI V R, MOHAN N, et al. NLRP3 signaling drives macrophage-induced adaptive immune suppression in pancreatic carcinoma[J].J Exp Med, 2017;214(6):1711-1724. DOI:10.1084/jem.20161707.
[66] TENGESDAL I W, MENON D R, OSBORNE D G, et al. Targeting tumor-derived NLRP3 reduces melanoma progression by limiting MDSCs expansion[J]. Proc Natl Acad Sci USA, 2021;118(10):e2000915118. DOI:10.1073/pnas.2000915118.
[67] CHEN Z, GIOTTI B, KALUZOVA M, et al. A paracrine circuit of IL-1β/IL-1R1 between myeloid and tumor cells drives genotype-dependent glioblastoma progression[J].J Clin Invest, 2023;133(22):e163802. DOI:10.1172/JCI163802.
[68] GELFO V, ROMANIELLO D, MAZZESCHI M, et al. Roles of IL-1 in cancer: from tumor progression to resistance to targeted therapies[J].Int J Mol Sci, 2020;21(17):6009. DOI:10.3390/ijms21176009.
[69] LIU J H, GAO L, ZHU X N, et al. Gasdermin D is a novel prognostic biomarker and relates to TMZ response in glioblastoma[J]. Cancers, 2021, 13(22): 5620. DOI: 10.3390/cancers13225620.
[70] TONG L, XIE C C, WEI Y F, et al. Antitumor effects of berberine on gliomas via inactivation of caspase-1-mediated IL-1β and IL-18 release[J]. Front Oncol, 2019, 9: 364. DOI: 10.3389/fonc.2019.00364.
[71] SHANG S, WANG L L, ZHANG Y L, et al. The beta-hydroxybutyrate suppresses the migration of glioma cells by inhibition of NLRP3 inflammasome[J]. Cell Mol Neurobiol, 2018, 38(8): 1479-1489. DOI: 10.1007/s10571-018-0617-2.
[72] HONDA S, SADATOMI D, YAMAMURA Y, et al. WP1066 suppresses macrophage cell death induced by inflammasome agonists independently of its inhibitory effect on STAT3[J]. Cancer Sci, 2017, 108(3): 520-527. DOI: 10.1111/cas.13154.
[73] DOS SANTOS DC, RAFIQUE J, SABA S, et al. IP-Se-06, a selenylated imidazo[1, 2- a] pyridine, modulates intracellular redox state and causes akt/mTOR/HIF-1 α and MAPK signaling inhibition, promoting antiproliferative effect and apoptosis in glioblastoma cells[J]. Oxid Med Cell Longev, 2022, 2022: 3710449. DOI: 10.1155/2022/3710449.
[74] CELESTI F, GATTA A, SHALLAK M, et al. Protective anti-tumor vaccination against glioblastoma expressing the MHC class II transactivator CIITA[J]. Front Immunol, 2023, 14: 1133177. DOI: 10.3389/fimmu.2023.1133177. (