Pyroptosis: Gasdermin-Mediated Programmed Necrotic Cell Death

Trends in Biochemical Sciences

Volumn 42, Issue 4, 2017, Pages 245-254

  Shi, Jianjin ^a   Gao, Wenqing ^a   Shao, Feng ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

caspase; gasdermin; innate immunity; necrosis; pore forming protein; pyroptosis

Indexed keywords

CASPASE 11; CASPASE 4; CASPASE 5; GASDERMIN; GASDERMIN D; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; GSDMD PROTEIN, HUMAN; TUMOR PROTEIN;

BACTERIUM; CELL DEATH; ENZYME ACTIVATION; ENZYME SUBSTRATE; HUMAN; IMMUNE RESPONSE; INFECTION; MONOCYTE; NONHUMAN; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PYROPTOSIS; REVIEW; METABOLISM; NECROSIS;

HUMANS; NECROSIS; NEOPLASM PROTEINS; PYROPTOSIS;

EID: 85007439966     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.10.004     Document Type: Review

References (77)

1. 1 Wallach, D., et al. Programmed necrosis in inflammation: toward identification of the effector molecules. Science, 352, 2016, aaf2154.
2. 2 Wang, H., et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54 (2014), 133–146.
3. 3 Cai, Z., et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16 (2014), 55–65.
4. 4 Chen, X., et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 24 (2014), 105–121.
5. 5 Dondelinger, Y., et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7 (2014), 971–981.
6. 6 Jorgensen, I., Miao, E.A., Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev. 265 (2015), 130–142.
7. 7 Miao, E.A., et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11 (2010), 1136–1142.
8. 8 Jorgensen, I., et al. Pyroptosis triggers pore-induced intracellular traps (PITs) that capture bacteria and lead to their clearance by efferocytosis. J. Exp. Med. 213 (2016), 2113–2128.
9. 9 Bergsbaken, T., et al. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7 (2009), 99–109.
10. 10 Thornberry, N.A., et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356 (1992), 768–774.
11. 11 Cerretti, D.P., et al. Molecular cloning of the interleukin-1 beta converting enzyme. Science 256 (1992), 97–100.
12. 12 Martinon, F., et al. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10 (2002), 417–426.
13. 13 Broz, P., Dixit, V.M., Inflammasomes: mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 16 (2016), 407–420.
14. 14 Zhao, Y., Shao, F., Diverse mechanisms for inflammasome sensing of cytosolic bacteria and bacterial virulence. Curr. Opin. Microbiol. 29 (2015), 37–42.
15. 15 Li, P., et al. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80 (1995), 401–411.
16. 16 Wang, S., et al. Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE. J. Biol. Chem. 271 (1996), 20580–20587.
17. 17 Wang, S., et al. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92 (1998), 501–509.
18. 18 Kang, S.J., et al. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 149 (2000), 613–622.
19. 19 Kayagaki, N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479 (2011), 117–121.
20. 20 Ng, T.M., Monack, D.M., Revisiting caspase-11 function in host defense. Cell Host Microbe 14 (2013), 9–14.
21. 21 Yang, J., et al. Non-canonical activation of inflammatory caspases by cytosolic LPS in innate immunity. Curr. Opin. Immunol. 32 (2015), 78–83.
22. 22 Kayagaki, N., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341 (2013), 1246–1249.
23. 23 Hagar, J.A., et al. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341 (2013), 1250–1253.
24. 24 Aachoui, Y., et al. Caspase-11 protects against bacteria that escape the vacuole. Science 339 (2013), 975–978.
25. 25 Shi, J., et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514 (2014), 187–192.
26. 26 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.
27. 27 Sellin, M.E., et al. Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe 16 (2014), 237–248.
28. 28 Kayagaki, N., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signaling. Nature 526 (2015), 666–671.
29. 29 Shi, J., et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526 (2015), 660–665.
30. 30 Saeki, N., et al. Gasdermin (Gsdm) localizing to mouse chromosome 11 is predominantly expressed in upper gastrointestinal tract but significantly suppressed in human gastric cancer cells. Mamm. Genome 11 (2000), 718–724.
31. 31 Saeki, N., Sasaki, H., Gasdermin superfamily: a novel gene family functioning in epithelial cells. Carrasco, J., Matheus, M., (eds.) Endothelium and Epithelium: Composition, Functions, and Pathology, 2011, Nova Science Publishers, 193–211.
32. 32 Fujii, T., et al. Gasdermin D (Gsdmd) is dispensable for mouse intestinal epithelium development. Genesis 46 (2008), 418–423.
33. 33 Akhter, A., et al. Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog., 5, 2009, e1000361.
34. 34 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.
35. 35 Ding, J., et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535 (2016), 111–116.
36. 36 Liu, X., et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535 (2016), 153–158.
37. 37 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.
38. 38 Sborgi, L., et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35 (2016), 1766–1778.
39. 39 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.
40. 40 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.
41. 41 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.
42. 42 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.
43. 43 Sato, H., et al. A new mutation Rim3 resembling Re(den) is mapped close to retinoic acid receptor alpha (Rara) gene on mouse chromosome 11. Mamm. Genome 9 (1998), 20–25.
44. 44 Porter, R.M., et al. Defolliculated (dfl): a dominant mouse mutation leading to poor sebaceous gland differentiation and total elimination of pelage follicles. J. Invest. Dermatol. 119 (2002), 32–37.
45. 45 Runkel, F., et al. The dominant alopecia phenotypes Bareskin, Rex-denuded, and Reduced Coat 2 are caused by mutations in gasdermin 3. Genomics 84 (2004), 824–835.
46. 46 Shi, P., et al. Loss of conserved Gsdma3 self-regulation causes autophagy and cell death. Biochem. J. 468 (2015), 325–336.
47. 47 Tanaka, S., et al. Functional conservation of Gsdma cluster genes specifically duplicated in the mouse genome. G3 (Bethesda) 3 (2013), 1843–1850.
48. 48 Ruge, F., et al. Delineating immune-mediated mechanisms underlying hair follicle destruction in the mouse mutant defolliculated. J. Invest. Dermatol. 131 (2011), 572–579.
49. 49 Zhou, Y., et al. Gsdma3 mutation causes bulge stem cell depletion and alopecia mediated by skin inflammation. Am. J. Pathol. 180 (2012), 763–774.
50. 50 Moffatt, M.F., et al. A large-scale, consortium-based genomewide association study of asthma. N. Engl. J. Med. 363 (2010), 1211–1221.
51. 51 Zhao, C.N., et al. The association of GSDMB and ORMDL3 gene polymorphisms with asthma: a meta-analysis. Allergy Asthma Immunol. Res. 7 (2015), 175–185.
52. 52 Kang, M.J., et al. GSDMB/ORMDL3 variants contribute to asthma susceptibility and eosinophil-mediated bronchial hyperresponsiveness. Hum. Immunol. 73 (2012), 954–959.
53. 53 Hergueta-Redondo, M., et al. Gasdermin-B promotes invasion and metastasis in breast cancer cells. PLoS One, 9, 2014, e90099.
54. 54 Van Laer, L., et al. Nonsyndromic hearing impairment is associated with a mutation in DFNA5. Nat. Genet. 20 (1998), 194–197.
55. 55 Delmaghani, S., et al. Mutations in the gene encoding pejvakin, a newly identified protein of the afferent auditory pathway, cause DFNB59 auditory neuropathy. Nat. Genet. 38 (2006), 770–778.
56. 56 Gregan, J., et al. A yeast model for the study of human DFNA5, a gene mutated in nonsyndromic hearing impairment. Biochim. Biophys. Acta 1638 (2003), 179–186.
57. 57 Van Laer, L., et al. Mice lacking Dfna5 show a diverging number of cochlear fourth row outer hair cells. Neurobiol. Dis. 19 (2005), 386–399.
58. 58 Masuda, Y., et al. The potential role of DFNA5, a hearing impairment gene, in p53-mediated cellular response to DNA damage. J. Hum. Genet. 51 (2006), 652–664.
59. 59 Kim, M.S., et al. Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene 27 (2008), 3624–3634.
60. 60 Akino, K., et al. Identification of DFNA5 as a target of epigenetic inactivation in gastric cancer. Cancer Sci. 98 (2007), 88–95.
61. 61 Collin, R.W., et al. Involvement of DFNB59 mutations in autosomal recessive nonsyndromic hearing impairment. Hum. Mutat. 28 (2007), 718–723.
62. 62 Ebermann, I., et al. Truncating mutation of the DFNB59 gene causes cochlear hearing impairment and central vestibular dysfunction. Hum. Mutat. 28 (2007), 571–577.
63. 63 Schwander, M., et al. A forward genetics screen in mice identifies recessive deafness traits and reveals that pejvakin is essential for outer hair cell function. J. Neurosci. 27 (2007), 2163–2175.
64. 64 Mujtaba, G., et al. A p.C343S missense mutation in PJVK causes progressive hearing loss. Gene 504 (2012), 98–101.
65. 65 Delmaghani, S., et al. Hypervulnerability to sound exposure through impaired adaptive proliferation of peroxisomes. Cell 163 (2015), 894–906.
66. 66 Friedlander, A.M., Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J. Biol. Chem. 261 (1986), 7123–7126.
67. 67 Cordoba-Rodriguez, R., et al. Anthrax lethal toxin rapidly activates caspase-1/ICE and induces extracellular release of interleukin (IL)-1beta and IL-18. J. Biol. Chem. 279 (2004), 20563–20566.
68. 68 Boyden, E.D., Dietrich, W.F., Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38 (2006), 240–244.
69. 69 Zychlinsky, A., et al. Shigella flexneri induces apoptosis in infected macrophages. Nature 358 (1992), 167–169.
70. 70 Hilbi, H., et al. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 273 (1998), 32895–32900.
71. 71 Zychlinsky, A., et al. Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J. Clin. Invest. 94 (1994), 1328–1332.
72. 72 Fernandez-Prada, C.M., et al. Human monocyte-derived macrophages infected with virulent Shigella flexneri in vitro undergo a rapid cytolytic event similar to oncosis but not apoptosis. Infect. Immun. 65 (1997), 1486–1496.
73. 73 Brennan, M.A., Cookson, B.T., Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol. 38 (2000), 31–40.
74. 74 Cookson, B.T., Brennan, M.A., Pro-inflammatory programmed cell death. Trends Microbiol. 9 (2001), 113–114.
75. 75 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.
76. 76 Fink, S.L., et al. Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 4312–4317.
77. 77 Kroemer, G., et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16 (2009), 3–11.