Advances in the regulation of inflammasome activation by GBP family in infectious diseases
Received date: 2023-06-15
Revised date: 2023-08-22
Online published: 2023-09-14
Supported by
National Natural Science Foundation of China(81871617);National Natural Science Foundation of China(81701971);National Natural Science Foundation of China(82172280);National Natural Science Foundation of China(82100010);CAS Key Laboratory of Pathogenic Microbiology and Immunology Open Project(CASPMI202201);Baoding Science and Technology Plan(2272P012);Training Plan for High-Level Public Health Technical Talents of Beijing Municipal Health Commission(2022-3-041)
Guanylate-binding proteins (GBPs) are a subfamily of interferon-inducible proteins that undertake distinct roles in the the context of bacteria, virus, chlamydia and parasites infections. These proteins exert a notable influence on the progression and outcomes of infectious diseases. Within the realm of host cell-autonomous immunity against pathogens, GBPs have been identified as the regulators of pyroptosis through canonical and noncanonical inflammasome activation pathways. In this review, we summarize the structure and evolution of GBP family members, the canonical and noncanonical inflammasome activation pathways, the roles of GBPs in regulating inflammasome activation, and the mechanisms of GBPs affecting infections induced by different pathogens. We hope to provide new basic research clues for the pathogenesis and diagnosis and treatment of infectious diseases.
Shuting Quan, Weiwei Jiao, Fang Xu, Lin Sun, Hui Qi, Adong Shen . Advances in the regulation of inflammasome activation by GBP family in infectious diseases[J]. Hereditas(Beijing), 2023 , 45(11) : 1007 -1017 . DOI: 10.16288/j.yczz.23-119
| [1] | Kutsch M, Coers J. Human guanylate binding proteins: nanomachines orchestrating host defense. FEBS J, 2021, 288(20): 5826-5849. |
| [2] | Macmicking JD. IFN-inducible GTPases and immunity to intracellular pathogens. Trends Immunol, 2004, 25(11): 601-609. |
| [3] | Martens S, Howard J. The interferon-inducible GTPases. Annu Rev Cell Dev Biol, 2006, 22: 559-589. |
| [4] | Man SM, Place DE, Kuriakose T, Kanneganti TD. Interferon-inducible guanylate-binding proteins at the interface of cell-autonomous immunity and inflammasome activation. J Leukoc Biol, 2017, 101(1): 143-150. |
| [5] | Krapp C, Hotter D, Gawanbacht A, Mclaren PJ, Kluge SF, Stürzel CM, Mack K, Reith E, Engelhart S, Ciuffi A, Hornung V, Sauter D, Telenti A, Kirchhoff F. Guanylate binding protein (GBP) 5 is an interferon-inducible inhibitor of HIV-1 infectivity. Cell Host Microbe, 2016, 19(4): 504-514. |
| [6] | Kim BH, Chee JD, Bradfield CJ, Park ES, Kumar P, Macmicking JD. Interferon-induced guanylate-binding proteins in inflammasome activation and host defense. Nat Immunol, 2016, 17(5): 481-489. |
| [7] | Randow F, Macmicking JD, James LC. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science, 2013, 340(6133): 701-706. |
| [8] | Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science, 2013, 341(6151): 1250-1253. |
| [9] | Praefcke GJK. Regulation of innate immune functions by guanylate-binding proteins. Int J Med Microbiol, 2018, 308(1): 237-245. |
| [10] | Schwemmle M, Staeheli P. The interferon-induced 67-kDa guanylate-binding protein (hGBP1) is a GTPase that converts GTP to GMP. J Biol Chem, 1994, 269(15): 11299-11305. |
| [11] | Ghosh A, Praefcke GJK, Renault L, Wittinghofer A, Herrmann C. How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature, 2006, 440(7080): 101-104. |
| [12] | Cui W, Braun E, Wang W, Tang JH, Zheng YY, Slater B, Li N, Chen C, Liu QX, Wang B, Li X, Duan YK, Xiao YJ, Ti RJ, Hotter D, Ji XY, Zhang L, Cui J, Xiong Y, Sauter D, Wang ZF, Kirchhoff F, Yang HT. Structural basis for GTP-induced dimerization and antiviral function of guanylate-binding proteins. Proc Natl Acad Sci USA, 2021, 118(15): e2022269118. |
| [13] | Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, Cresswell P, Macmicking JD. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science, 2012, 336(6080): 481-485. |
| [14] | Resh MD. Trafficking and signaling by fatty-acylated and prenylated proteins. Nat Chem Biol, 2006, 2(11): 584-590. |
| [15] | Konstantinopoulos PA, Karamouzis MV, Papavassiliou AG. Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets. Nat Rev Drug Discov, 2007, 6(7): 541-555. |
| [16] | Tretina K, Park E S, Maminska A, Macmicking J D. Interferon-induced guanylate-binding proteins: guardians of host defense in health and disease. J Exp Med, 2019, 216(3): 482-500. |
| [17] | Britzen-Laurent N, Bauer M, Berton V, Fischer N, Syguda A, Reipschl?ger S, Naschberger E, Herrmann C, Stürzl M. Intracellular trafficking of guanylate-binding proteins is regulated by heterodimerization in a hierarchical manner. PLoS One, 2010, 5(12): e14246. |
| [18] | Honkala AT, Tailor D, Malhotra SV. Guanylate-binding protein 1: an emerging target in inflammation and cancer. Front Immunol, 2019, 10: 3139. |
| [19] | Syguda A, Bauer M, Benscheid U, Ostler N, Naschberger E, Ince S, Sturzl M, Herrmann C. Tetramerization of human guanylate-binding protein 1 is mediated by coiled-coil formation of the C-terminal alpha-helices. FEBS J, 2012, 279(14): 2544-2554. |
| [20] | Olszewski MA, Gray J, Vestal DJ. In silico genomic analysis of the human and murine guanylate-binding protein (GBP) gene clusters. J Interferon Cytokine Res, 2006, 26(5): 328-352. |
| [21] | Kresse A, Konermann C, Degrandi D, Beuter-Gunia C, Wuerthner J, Pfeffer K, Beer S. Analyses of murine GBP homology clusters based on in silico, in vitro and in vivo studies. BMC Genomics, 2008, 9: 158. |
| [22] | EMBL-EBI.https://www.ebi.ac.uk/pdbe/pdbe-kb/proteins/P32455/structures. |
| [23] | Nei M, Gu X, Sitnikova T. Evolution by the birth- and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA, 1997, 94(15): 7799-7806. |
| [24] | Wandel MP, Kim BH, Park ES, Boyle KB, Nayak K, Lagrange B, Herod A, Henry T, Zilbauer M, Rohde J, Macmicking JD, Randow F. Guanylate-binding proteins convert cytosolic bacteria into caspase-4 signaling platforms. Nat Immunol, 2020, 21(8): 880-891. |
| [25] | Corte-Real J V, Baldauf H M, Abrantes J, Esteves P J. Evolution of the guanylate binding protein (GBP) genes: emergence of GBP7 genes in primates and further acquisition of a unique GBP3 gene in simians. Mol Immunol, 2021, 132: 79-81. |
| [26] | Li G, Zhang JY, Sun Y, Wang H, Wang YQ. The evolutionarily dynamic IFN-inducible GTPase proteins play conserved immune functions in vertebrates and cephalochordates. Mol Biol Evol, 2009, 26(7): 1619-1630. |
| [27] | Agostini L, Martinon F, Burns K, Mcdermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta- processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity, 2004, 20(3): 319-325. |
| [28] | Lugrin J, Martinon F. The AIM2 inflammasome: sensor of pathogens and cellular perturbations. Immunol Rev, 2018, 281(1): 99-114. |
| [29] | Cai X, Chen JQ, Xu H, Liu SQ, Jiang QX, Halfmann R, Chen ZJJ. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell, 2014, 156(6): 1207-1222. |
| [30] | Swanson KV, Deng M, Ting JPY. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol, 2019, 19(8): 477-489. |
| [31] | Sharma D, Kanneganti TD. The cell biology of inflammasomes: mechanisms of inflammasome activation and regulation. J Cell Biol, 2016, 213(6): 617-629. |
| [32] | Yi YS. Dual roles of the caspase-11 non-canonical inflammasome in inflammatory bowel disease. Int Immunopharmacol, 2022, 108: 108739. |
| [33] | Yi YS. Caspase-11 non-canonical inflammasome: a critical sensor of intracellular lipopolysaccharide in macrophage- mediated inflammatory responses. Immunology, 2017, 152(2): 207-217. |
| [34] | Shi JJ, Zhao Y, Wang YP, Gao WQ, Ding JJ, Li P, Hu LY, Shao F. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature, 2014, 514(7521): 187-192. |
| [35] | Yi YS. Functional crosstalk between non-canonical caspase-11 and canonical NLRP3 inflammasomes during infection-mediated inflammation. Immunology, 2020, 159(2): 142-155. |
| [36] | Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu JS, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang YF, Bertram EM, Goodnow CC, Dixit VM. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature, 2015, 526(7575): 666-671. |
| [37] | Shi JJ, Zhao Y, Wang K, Shi XY, Wang Y, Huang HW, Zhuang YH, Cai T, Wang FC, Shao F. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature, 2015, 526(7575): 660-665. |
| [38] | Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, Macmicking J D. A family of IFN-gamma-inducible 65-kD GTPases protects against bacterial infection. Science, 2011, 332(6030): 717-721. |
| [39] | Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW 4th, Macmicking JD, Sibley LD. Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii. PLoS Pathog, 2013, 9(4): e1003320. |
| [40] | Xavier A, Al-Zeer MA, Meyer TF, Daumke O. hGBP1 coordinates Chlamydia restriction and inflammasome activation through sequential GTP hydrolysis. Cell Rep, 2020, 31(7): 107667. |
| [41] | Santos JC, Boucher D, Schneider LK, Demarco B, Dilucca M, Shkarina K, Heilig R, Chen KW, Lim RYH, Broz P. Human GBP1 binds LPS to initiate assembly of a caspase-4 activating platform on cytosolic bacteria. Nat Commun, 2020, 11(1): 3276. |
| [42] | Degrandi D, Kravets E, Konermann C, Beuter-Gunia C, Klümpers V, Lahme S, Rasch E, Mausberg AK, Beer- Hammer S, Pfeffer K. Murine guanylate binding protein 2 (mGBP2) controls Toxoplasma gondii replication. Proc Natl Acad Sci USA, 2013, 110(1): 294-299. |
| [43] | Meunier E, Wallet P, Dreier RF, Costanzo S, Anton L, Rühl S, Dussurgey S, Dick MS, Kistner A, Rigard M, Degrandi D, Pfeffer K, Yamamoto M, Henry T, Broz P. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat Immunol, 2015, 16(5): 476-484. |
| [44] | Feng SY, Man SM. Captain GBP1: inflammasomes assemble, pyroptotic endgame. Nat Immunol, 2020, 21(8): 829-830. |
| [45] | Man SM, Karki R, Malireddi RK, Neale G, Vogel P, Yamamoto M, Lamkanfi M, Kanneganti TD. The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection. Nat Immunol, 2015, 16(5): 467-475. |
| [46] | Yang JM, Hwang I, Lee E, Shin SJ, Lee EJ, Rhee JH, Yu JW. Bacterial outer membrane vesicle-mediated cytosolic delivery of Flagellin triggers host NLRC4 canonical inflammasome signaling. Front Immunol, 2020, 11: 581165. |
| [47] | Virreira WS, Niedelman W, Jensen KD, Rosowski EE, Julien L, Spooner E, Caradonna K, Burleigh BA, Saeij JPJ, Ploegh HL, Frickel EM. Determinants of GBP recruitment to Toxoplasma gondii vacuoles and the parasitic factors that control it. PLoS One, 2011, 6(9): e24434. |
| [48] | Sweeney TE, Braviak L, Tato CM, Khatri P. Genome-wide expression for diagnosis of pulmonary tuberculosis: a multicohort analysis. Lancet Respir Med, 2016, 4(3): 213-224. |
| [49] | Costa LLD, Delcroix M, Dalla Costa ER, Prestes IV, Milano M, Francis SS, Unis G, Silva DR, Riley LW, Rossetti ML. A real-time PCR signature to discriminate between tuberculosis and other pulmonary diseases. Tuberculosis (Edinb), 2015, 95(4): 421-425. |
| [50] | Satproedprai N, Wichukchinda N, Suphankong S, Inunchot W, Kuntima T, Kumpeerasart S, Wattanapokayakit S, Nedsuwan S, Yanai H, Higuchi K, Harada N, Mahasirimongkol S. Diagnostic value of blood gene expression signatures in active tuberculosis in Thais: a pilot study. Genes Immun, 2015, 16(4): 253-260. |
| [51] | Cerqueira DM, Gomes MTR, Silva ALN, Rungue M, Assis NRG, Guimaraes ES, Morais SB, Broz P, Zamboni DS, Oliveira SC. Guanylate-binding protein 5 licenses caspase-11 for Gasdermin-D mediated host resistance to Brucella abortus infection. PLoS Pathog, 2018, 14(12): e1007519. |
| [52] | Liu BCY, Sarhan J, Panda A, Muendlein HI, Ilyukha V, Coers J, Yamamoto M, Isberg RR, Poltorak A. Constitutive interferon maintains GBP expression required for release of bacterial components upstream of pyroptosis and anti-DNA responses. Cell Rep, 2018, 24(1): 155-168. |
| [53] | Fisch D, Bando H, Clough B, Hornung V, Yamamoto M, Shenoy AR, Frickel EM. Human GBP1 is a microbe-specific gatekeeper of macrophage apoptosis and pyroptosis. EMBO J, 2019, 38(13): e100926. |
| [54] | Dickinson MS, Kutsch M, Sistemich L, Hernandez D, Piro AS, Needham D, Lesser CF, Herrmann C, Coers J. LPS-aggregating proteins GBP1 and GBP2 are each sufficient to enhance caspase-4 activation both in cellulo and in vitro. Proc Natl Acad Sci USA, 2023, 120(15): e2078939176. |
| [55] | Wandel MP, Pathe C, Werner EI, Ellison CJ, Boyle KB, von der Malsburg A, Rohde J, Randow F.GBPs inhibit motility of Shigella flexneri but are targeted for degradation by the bacterial ubiquitin Ligase IpaH9.8. Cell Host Microbe, 2017, 22(4): 507-518. |
| [56] | Mesner D, Reuschl AK, Whelan MVX, Bronzovich T, Haider T, Thorne LG, Ragazzini R, Bonfanti P, Towers GJ, Jolly C. SARS-CoV-2 evolution influences GBP and IFITM sensitivity. Proc Natl Acad Sci USA, 2023, 120(5): e2082390176. |
/
| 〈 |
|
〉 |
www.chinagene.cn
备案号：京ICP备09063187号
