Recent Insights into the Molecular Mechanisms Underlying Pyroptosis and Gasdermin Family Functions

Trends in Immunology

Volumn 38, Issue 4, 2017, Pages 261-271

  Aglietti, Robin A ^a   Dueber, Erin C ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CELL PROTEIN; GASDERMIN D PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; UNCLASSIFIED DRUG; CASP11 PROTEIN, MOUSE; CASPASE; GSDMD PROTEIN, HUMAN; TUMOR PROTEIN;

AMINO TERMINAL SEQUENCE; CANONICAL INFLAMMASOME SIGNALING; CELL DIFFERENTIATION; CELL MEMBRANE; CELL PROLIFERATION; CHANNEL GATING; COMPARATIVE STUDY; COMPLEX FORMATION; CYTOSOL; CYTOTOXICITY; EFFECTOR CELL; ENZYME SUBSTRATE; HUMAN; LIPID BILAYER; MOLECULAR BIOLOGY; NONCANONICAL INFLAMMASOME SIGNALING; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN FAMILY; PROTEIN FUNCTION; PYROPTOSIS; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; IMMUNOLOGY; INFECTION; INFLAMMATION; METABOLISM; MOUSE; SEPTIC SHOCK;

ANIMALS; CASPASE 1; CASPASES; HUMANS; INFECTION; INFLAMMATION; MICE; NEOPLASM PROTEINS; PYROPTOSIS; SHOCK, SEPTIC;

EID: 85012024592     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2017.01.003     Document Type: Review

References (86)

1. 1 Hennessy, E.J., et al. Targeting Toll-like receptors: emerging therapeutics?. Nat. Rev. Drug Discov. 9 (2010), 293–307.
2. 2 Hagar, J.A., et al. Cytoplasmic LPS activates Caspase-11: implications in TLR4-independent endotoxic shock. Science 341 (2013), 1250–1253.
3. 3 Kayagaki, N., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341 (2013), 1246–1249.
4. 4 Kayagaki, N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479 (2011), 117–121.
5. 5 Shi, J., et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514 (2014), 187–192.
6. 6 Aachoui, Y., et al. Caspase-11 protects against bacteria that escape the vacuole. Science 339 (2013), 975–978.
7. 7 Knodler, L.A., et al. Noncanonical inflammasome activation of Caspase-4/Caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe. 16 (2014), 249–256.
8. 8 Kayagaki, N., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signaling. Nature 526 (2015), 666–671.
9. 9 Shi, J., et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526 (2015), 660–665.
10. 10 Aglietti, R.A., et al. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 7858–7863.
11. 11 Ding, J., et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535 (2016), 111–116.
12. 12 Liu, X., et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535 (2016), 153–158.
13. 13 Sborgi, L., et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35 (2016), 1766–1778.
14. 14 Chen, X., et al. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis. Cell Res. 26 (2016), 1007–1020.
15. 15 Heimburg, T., Marsh, D., Thermodynamics of the interaction of proteins with lipid membranes. Merz, J.K., Roux, B., (eds.) Biological Membranes, 1996, Birkhäuser, 405–462.
16. 16 Andersen, O.S., Koeppe, R.E., Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36 (2007), 107–130.
17. 17 Jurkiewicz, P., et al. Biophysics of lipid bilayers containing oxidatively modified phospholipids: Insights from fluorescence and EPR experiments and from MD simulations. Biochim. Biophys. Acta 1818 (2012), 2388–2402.
18. 18 Nicolson, G.L., The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim. Biophys. Acta 1838 (2014), 1451–1466.
19. 19 Brown, D.A., Rose, J.K., Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68 (1992), 533–544.
20. 20 Zech, T., et al. Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J. 28 (2009), 466–476.
21. 21 Lingwood, D., Simons, K., Lipid rafts as a membrane-organizing principle. Science 327 (2010), 46–50.
22. 22 Tilley, S.J., et al. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121 (2005), 247–256.
23. 23 Peraro, M.D., van der Goot, F.G., Pore-forming toxins: ancient, but never really out of fashion. Nat. Rev. Microbiol. 14 (2016), 77–92.
24. 24 Wade, K.R., et al. An intermolecular electrostatic interaction controls the prepore-to-pore transition in a cholesterol-dependent cytolysin. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 2204–2209.
25. 25 Yamashita, D., et al. Molecular basis of transmembrane beta-barrel formation of staphylococcal pore-forming toxins. Nat. Commun., 5, 2014, 4897.
26. 26 Agard, N.J., et al. Inflammatory stimuli regulate caspase substrate profiles. Mol. Cell Proteomics 9 (2010), 880–893.
27. 27 Okondo, M.C., et al. DPP8 and DPP9 inhibition induces pro-caspase-1-dependent monocyte and macrophage pyroptosis. Nat. Chem. Biol. 13 (2017), 46–53.
28. 28 Tamura, M., et al. 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 89 (2007), 618–629.
29. 29 Sakamaki, K., Satou, Y., Caspases: evolutionary aspects of their functions in vertebrates. J. Fish Biol. 74 (2009), 727–753.
30. 30 Angosto, D., et al. Evolution of inflammasome functions in vertebrates: inflammasome and caspase-1 trigger fish macrophage cell death but are dispensable for the processing of IL-1β. Innate Immun. 18 (2012), 815–824.
31. 31 Latz, E., et al. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13 (2013), 397–411.
32. 32 Muñoz-Planillo, R., et al. K+ efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38 (2013), 1142–1153.
33. 33 Petrilli, V., et al. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14 (2007), 1583–1589.
34. 34 Rühl, S., Broz, P., Caspase-11 activates a canonical NLRP3 inflammasome by promoting K+ efflux. Eur. J Immunol. 45 (2015), 2927–2936.
35. 35 Van Laer, L., et al. Nonsyndromic hearing impairment is associated with a mutation in DFNA5. Nat. Genetics 20 (1998), 194–197.
36. 36 Delmaghani, S., et al. Mutations in the gene encoding pejvakin, a newly identified protein of the afferent auditory pathway, cause DFNB59 auditory neuropathy. Nat. Genetics 38 (2006), 770–778.
37. 37 Saeki, N., Sasaki, H., Gasdermin superfamily: a novel gene family functioning in epithelial cells. Carrasco, J., Mota, M., (eds.) Endothelium and Epithelium, 2012, Nova Science Publishers, 193–211.
38. 38 Liu, W., et al. Distribution of pejvakin in human spiral ganglion: an immunohistochemical study. Cochlear Implants Int. 14 (2013), 225–231.
39. 39 Hosoya, M., et al. Distinct expression patterns of causative genes responsible for hereditary progressive hearing loss in non-human primate cochlea. Sci. Rep., 6, 2016, 22250.
40. 40 Lin, P.-H., et al. N-terminal functional domain of Gasdermin A3 regulates mitochondrial homeostasis via mitochondrial targeting. J. Biomed. Sci. 22 (2015), 1–18.
41. 41 Van Laer, L., et al. DFNA5: hearing impairment exon instead of hearing impairment gene?. J. Med. Genet. 41 (2004), 401–406.
42. 42 de Beeck, K.O., The DFNA5 gene, responsible for hearing loss and involved in cancer, encodes a novel apoptosis-inducing protein. Eur. J. Hum. Genet. 19 (2011), 965–973.
43. 43 de Beeck, K.O., et al. DFNA5, a gene involved in hearing loss and cancer: a review. Ann. Otol. Rhinol. Laryngol. 121 (2012), 197–207.
44. 44 Van Rossom, S., et al. The deafness gene DFNA5 induces programmed cell death through mitochondria and MAPK-related pathways. Front. Cell Neurosci. 9 (2015), 1–15.
45. 45 Delmaghani, S., et al. Hypervulnerability to sound exposure through impaired adaptive proliferation of peroxisomes. Cell 163 (2015), 894–906.
46. 46 Saeki, N., et al. Distinctive expression and function of four GSDM family genes (GSDMA-D) in normal and malignant upper gastrointestinal epithelium. Genes Chromosomes Cancer 48 (2009), 261–271.
47. 47 Saeki, N., et al. GASDERMIN suppressed frequently in gastric cancer, is a target of LMO1 in TGF-|[beta]|-dependent apoptotic signalling. Oncogene 26 (2007), 6488–6498.
48. 48 Wu, H., et al. Genetic variation in ORM1-like 3 (ORMDL3) and gasdermin-like (GSDML) and childhood asthma. Allergy 64 (2009), 629–635.
49. 49 Sun, Q., et al. Expression of GSDML associates with tumor progression in uterine cervix cancer. Transl. Oncol. 1 (2008), 73–83.
50. 50 Hergueta-Redondo, M., Gasdermin-B promotes invasion and metastasis in breast cancer cells. PLoS One, 9, 2014, e90099.
51. 51 Hergueta-Redondo, M., et al. Gasdermin B expression predicts poor clinical outcome in HER2-positive breast cancer. Oncotarget 7 (2016), 56295–56308.
52. 52 Watabe, K., et al. Structure, expression and chromosome mapping of MLZE, a novel gene which is preferentially expressed in metastatic melanoma cells. Cancer Sci. 92 (2001), 140–151.
53. 53 Cookson, B.T., Brennan, M.A., Pro-inflammatory programmed cell death. Trends Microbiol. 9 (2001), 113–114.
54. 54 Jorgensen, I., Miao, E.A., Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev. 265 (2015), 130–142.
55. 55 Bergsbaken, T., et al. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7 (2009), 99–109.
56. 56 Miao, E.A., et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11 (2010), 1136–1142.
57. 57 Aziz, M., et al. Revisiting caspases in sepsis. Cell Death Dis., 5, 2014, e1526.
58. 58 Aziz, M., et al. Current trends in inflammatory and immunomodulatory mediators in sepsis. J. Leukoc. Biol. 93 (2013), 329–342.
59. 59 Aachoui, Y., et al. Inflammasome-mediated pyroptotic and apoptotic cell death, and defense against infection. Curr. Opin. Microbiol. 16 (2013), 319–326.
60. 60 Fink, S.L., Cookson, B.T., Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8 (2006), 1812–1825.
61. 61 Shalini, S., et al. Old, new and emerging functions of caspases. Cell Death Differ. 22 (2015), 526–539.
62. 62 Yazdi, A.S., et al. Inflammatory caspases in innate immunity and inflammation. J. Innate Immun. 2 (2010), 228–237.
63. 63 Fernández, D.J., Lamkanfi, M., Inflammatory caspases: key regulators of inflammation and cell death. Biol. Chem. 396 (2015), 193–203.
64. 64 Kersse, K., et al. A phylogenetic and functional overview of inflammatory caspases and caspase-1-related CARD-only proteins. Biochem. Soc. Trans. 35 (2007), 1508–1511.
65. 65 Martinon, F., Tschopp, J., Inflammatory caspases. Cell 117 (2004), 561–574.
66. 66 Casson, C.N., et al. Human caspase-4 mediates noncanonical inflammasome activation against gram-negative bacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 6688–6693.
67. 67 Fischer, H., et al. Human caspase 12 has acquired deleterious mutations. Biochem. Biophys. Res. Commun. 293 (2002), 722–726.
68. 68 Lemmers, B., et al. Essential role for caspase-8 in Toll-like receptors and NFκB signaling. J. Biol. Chem. 282 (2007), 7416–7423.
69. 69 Gurung, P., et al. FADD and Caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes. J. Immunol. 192 (2014), 1835–1846.
70. 70 Gurung, P., Kanneganti, T.-D., Novel roles for caspase-8 in IL-1β and inflammasome regulation. Am. J. Pathol. 185 (2015), 17–25.
71. 71 Monie, T.P., Bryant, C.E., Caspase-8 functions as a key mediator of inflammation and pro-IL-1β processing via both canonical and non-canonical pathways. Immunol. Rev. 265 (2015), 181–193.
72. 72 Feltham, R., et al. Caspase-8: not so silently deadly. Clin. Transl. Immunol., 6, 2017, e124.
73. 73 Lamkanfi, M., et al. Targeted peptidecentric proteomics reveals Caspase-7 as a substrate of the Caspase-1 inflammasomes. Mol. Cell Proteomics 7 (2008), 2350–2363.
74. 74 Akhter, A., et al. Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog, 5, 2009, e1000361.
75. 75 Erener, S., et al. Inflammasome-Activated Caspase 7 cleaves PARP1 to enhance the expression of a subset of NF-κB target genes. Mol. Cell 46 (2012), 200–211.
76. 76 Martinon, F., et al. The inflammasome. Mol. Cell 10 (2002), 417–426.
77. 77 Broz, P., Dixit, V.M., Inflammasomes: mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 16 (2016), 407–420.
78. 78 Chavarría Smith, J., Vance, R.E., The NLRP1 inflammasomes. Immunol. Rev. 265 (2015), 22–34.
79. 79 Abderrazak, A., et al. NLRP3 inflammasome: from a danger signal sensor to a regulatory node of oxidative stress and inflammatory diseases. Redox Biol. 4 (2015), 296–307.
80. 80 Elliott, E.I., Sutterwala, F.S., Initiation and perpetuation of NLRP3 inflammasome activation and assembly. Immunol. Rev. 265 (2015), 35–52.
81. 81 Vance, R.E., The NAIP/NLRC4 inflammasomes. Curr. Opin. Immunol. 32 (2015), 84–89.
82. 82 Hornung, V., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 (2009), 514–518.
83. 83 Jones, J.W., et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 9771–9776.
84. 84 Xu, H., et al. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513 (2014), 237–241.
85. 85 de Alba, E., Structure and interdomain dynamics of apoptosis-associated speck-like protein containing a CARD (ASC). J. Biol. Chem. 284 (2009), 32932–32941.
86. 86 Man, S.M., Kanneganti, T.-D., Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat. Rev. Immunol. 16 (2016), 7–21.