Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death

Nature Communications

Volumn 8, Issue , 2017, Pages

  Rogers, Corey ^a   Fernandes Alnemri, Teresa ^a   Mayes, Lindsey ^a   Alnemri, Diana ^b   Cingolani, Gino ^a   Alnemri, Emad S ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CASPASE 3; DFNA5 PROTEIN; ETOPOSIDE; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CASP3 PROTEIN, MOUSE; DFNA5H PROTEIN, MOUSE; ESTROGEN RECEPTOR; GSDMD PROTEIN, MOUSE;

APOPTOSIS; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; INFECTIOUS DISEASE; INFECTIVITY; PROTEIN; VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL MEMBRANE; CONTROLLED STUDY; DISEASE COURSE; EMBRYO; ENZYME ACTIVATION; GENE; HEK293 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NECROSIS; NONHUMAN; PROTEIN CLEAVAGE; PYROPTOSIS; VESICULAR STOMATITIS; VESICULOVIRUS; ANIMAL; APOPTOSIS; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEP-G2 CELL LINE; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOGENICITY; PRIMARY CELL CULTURE; VESICULAR STOMATITIS INDIANA VIRUS; VIROLOGY;

VESICULAR STOMATITIS VIRUS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; CELL MEMBRANE; ETOPOSIDE; GENE EXPRESSION REGULATION; HEK293 CELLS; HEP G2 CELLS; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; PRIMARY CELL CULTURE; PYROPTOSIS; RECEPTORS, ESTROGEN; VESICULAR STOMATITIS INDIANA VIRUS;

EID: 85008419254     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14128     Document Type: Article

References (64)

1. Wallach, D., Kang, T. B., Dillon, C. P. & Green, D. R. Programmed necrosis in inflammation: toward identification of the effector molecules. Science 352, aaf2154 (2016).
2. Linkermann, A. & Green, D. R. Necroptosis. N. Engl. J. Med. 370, 455-465 (2014).
3. Miao, E. A., Rajan, J. V. & Aderem, A. Caspase-1-induced pyroptotic cell death. Immunol. Rev. 243, 206-214 (2011).
4. Shi, J. et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187-192 (2014).
5. Guo, H., Callaway, J. B. & Ting, J. P. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21, 677-687 (2015).
6. Kayagaki, N. et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666-671 (2015).
7. Shi, J. et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660-665 (2015).
8. He, W. T. et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res. 25, 1285-1298 (2015).
9. Aglietti, R. A. et al. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc. Natl Acad. Sci. USA 113, 7858-7863 (2016).
10. Ding, J. et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535, 111-116 (2016).
11. Liu, X. et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153-158 (2016).
12. Sborgi, L. et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35, 1766-1778 (2016).
13. Barber, G. N. Host defense, viruses and apoptosis. Cell Death Differ. 8, 113-126 (2001).
14. Taylor, R. C., Cullen, S. P. & Martin, S. J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9, 231-241 (2008).
15. Silva, M. T., do Vale, A. & dos Santos, N. M. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis: Int. J. Programmed Cell Death 13, 463-482 (2008).
16. Vanden Berghe, T. et al. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death. Differ. 17, 922-930 (2010).
17. 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, 618-629 (2007).
18. Op de Beeck, K. et al. The DFNA5 gene, responsible for hearing loss and involved in cancer, encodes a novel apoptosis-inducing protein. Eur. J. Hum. Genet. 19, 965-973 (2011).
19. Van Rossom, S. et al. The splicing mutant of the human tumor suppressor protein DFNA5 induces programmed cell death when expressed in the yeast Saccharomyces cerevisiae. Front. Oncol. 2, 77 (2012).
20. Bischoff, A. M. et al. A novel mutation identified in the DFNA5 gene in a Dutch family: a clinical and genetic evaluation. Audiol. Neurootol. 9, 34-46 (2004).
21. Van Laer, L. et al. Nonsyndromic hearing impairment is associated with a mutation in DFNA5. Nat. Genet. 20, 194-197 (1998).
22. Akino, K. et al. Identification of DFNA5 as a target of epigenetic inactivation in gastric cancer. Cancer Sci. 98, 88-95 (2007).
23. 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, 652-664 (2006).
24. Kang, S. et al. Caspase-8 scaffolding function and MLKL regulate NLRP3 inflammasome activation downstream of TLR3. Nat. Commun. 6, 7515 (2015).
25. Crawford, E. D. et al. The DegraBase: a database of proteolysis in healthy and apoptotic human cells. Mol. Cell. Proteom 12, 813-824 (2013).
26. Janicke, R. U., Sprengart, M. L., Wati, M. R. & Porter, A. G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273, 9357-9360 (1998).
27. Biasini, M. et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids. Res. 42, W252-W258 (2014).
28. Lukoyanova, N. et al. Conformational changes during pore formation by the perforin-related protein pleurotolysin. PLOS Biol. 13, e1002049 (2015).
29. Hadders, M. A., Beringer, D. X. & Gros, P. Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317, 1552-1554 (2007).
30. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
31. Dudkina, N. V. et al. Structure of the poly-C9 component of the complement membrane attack complex. Nat. Commun. 7, 10588 (2016).
32. Serna, M., Giles, J. L., Morgan, B. P. & Bubeck, D. Structural basis of complement membrane attack complex formation. Nat. Commun. 7, 10587 (2016).
33. Dal Peraro, M. & van der Goot, F. G. Pore-forming toxins: ancient, but never really out of fashion. Nat. Rev. Microbiol. 14, 77-92 (2016).
34. Silva, M. T. Secondary necrosis: the natural outcome of the complete apoptotic program. FEBS Lett. 584, 4491-4499 (2010).
35. Bergsbaken, T., Fink, S. L. & Cookson, B. T. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7, 99-109 (2009).
36. Fink, S. L. & Cookson, B. T. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8, 1812-1825 (2006).
37. Srinivasula, S. M. et al. Generation of constitutively active recombinant caspases-3 and-6 by rearrangement of their subunits. J. Biol. Chem. 273, 10107-10111 (1998).
38. Hobbs, J. A., Schloemer, R. H., Hommel-Berrey, G. & Brahmi, Z. Caspase-3-like proteases are activated by infection but are not required for replication of vesicular stomatitis virus. Virus Res. 80, 53-65 (2001).
39. Ohguchi, A. et al. Encepalomyocarditis virus-induced apoptosis and ultrastructural changes in the lacrimal and parotid glands of mice. Exp. Mol. Pathol. 80, 201-207 (2006).
40. Denecker, G. et al. Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ. 8, 829-840 (2001).
41. Krysko, D. V., Vanden Berghe, T., D'Herde, K. & Vandenabeele, P. Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44, 205-221 (2008).
42. Berg, R. D. et al. Lysosomal disorders drive susceptibility to tuberculosis by compromising macrophage migration. Cell 165, 139-152 (2016).
43. Jorgensen, I., Zhang, Y., Krantz, B. A. & Miao, E. A. Pyroptosis triggers pore-induced intracellular traps (PITs) that capture bacteria and lead to their clearance by efferocytosis. J. Exp. Med. 213, 2113-2128 (2016).
44. Stewart, M. K. & Cookson, B. T. Evasion and interference: intracellular pathogens modulate caspase-dependent inflammatory responses. Nat. Rev. Microbiol. 14, 346-359 (2016).
45. Ulland, T. K., Ferguson, P. J. & Sutterwala, F. S. Evasion of inflammasome activation by microbial pathogens. J. Clin. Invest. 125, 469-477 (2015).
46. Best, S. M. Viral subversion of apoptotic enzymes: escape from death row. Annu. Rev. Microbiol. 62, 171-192 (2008).
47. Dobbelstein, M. & Shenk, T. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J. Virol. 70, 6479-6485 (1996).
48. Macen, J. L. et al. Differential inhibition of the Fas-and granule-mediated cytolysis pathways by the orthopoxvirus cytokine response modifier A/SPI-2 and SPI-1 protein. Proc. Natl Acad. Sci. USA 93, 9108-9113 (1996).
49. Turner, S. J., Silke, J., Kenshole, B. & Ruby, J. Characterization of the ectromelia virus serpin, SPI-2. J. Gen. Virol. 81, 2425-2430 (2000).
50. Lamkanfi, M. & Dixit, V. M. Modulation of inflammasome pathways by bacterial and viral pathogens. J. Immunol. 187, 597-602 (2011).
51. de Beeck, K. O., Van Laer, L. & Van Camp, G. DFNA5, a gene involved in hearing loss and cancer: a review. Ann. Otol. Rhinol. Laryngol. 121, 197-207 (2012).
52. Kim, M. S. et al. Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene 27, 3624-3634 (2008).
53. Kim, M. S. et al. Methylation of the DFNA5 increases risk of lymph node metastasis in human breast cancer. Biochem. Biophys. Res. Commun. 370, 38-43 (2008).
54. Lage, H., Helmbach, H., Grottke, C., Dietel, M. & Schadendorf, D. DFNA5 (ICERE-1) contributes to acquired etoposide resistance in melanoma cells. FEBS Lett. 494, 54-59 (2001).
55. Fujikane, T. et al. Genomic screening for genes upregulated by demethylation revealed novel targets of epigenetic silencing in breast cancer. Breast Cancer Res. Treat. 122, 699-710 (2010).
56. Bauernfeind, F. G. et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183, 787-791 (2009).
57. Fernandes-Alnemri, T. et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 14, 1590-1604 (2007).
58. Yu, J. W. et al. Pyrin activates the ASC pyroptosome in response to engagement by autoinflammatory PSTPIP1 mutants. Mol. Cell 28, 214-227 (2007).
59. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J. & Alnemri, E. S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513 (2009).
60. Skarnes, W. C. et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342 (2011).
61. White, J. K. et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154, 452-464 (2013).
62. Ryder, E. et al. Rapid conversion of EUCOMM/KOMP-CSD alleles in mouse embryos using a cell-permeable Cre recombinase. Transgenic Res. 23, 177-185 (2014).
63. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta. Crystallogr. D. Biol. Crystallogr. 60, 2126-2132 (2004).
64. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).