Pyroptosis and retinal cell death_Chinese Journal of Ocular Fundus Diseases

Authors：

Guo Yinong ,  Sun Xiaodong

Department of Ophthalmology, The General Hospital of Shanghai, Shanghai JiaoTong University, Shanghai 200080, China;

Corresponding author：

Sun Xiaodong, Email: xdsun@sjtu.edu.cn

Keywords：

Cell death; Retinal diseases; Review

DOI：

10.3760/cma.j.issn.1005-1015.2018.02.027

Video：

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Abstract Full text Figures/Tables Video References Cited by

Pyroptosis is a newly discovered form of cell death. Through the activation of inflammasome complexes, pyroptosis induces the production of interleukin (IL) -1β and IL-18, and the osmotic swelling of cells, thus induces cellular rupture and death. It plays a role in the pathological process of a variety of human diseases. The death of retinal cells including photoreceptor cells and retinal pigment epithelium (RPE) cells is the main reason leading to visual dysfunction in the pathogenesis in ocular fundus diseases. Researches have demonstrated that pyroptosis is closely related to the onset and progression of various retinal diseases. In age-related macular degeneration, pyroptosis directly causes apoptosis of RPE cells and upregulation of pro-inflammatory factors, enhancing toxic effect of lipofuscin. For retinitis pigmentosa, pyroptosis is the leading manner of death of secondary cone photoreceptor cells. In cytomegalovirus retinitis, pyroptosis is the main responding way to infection. This review presented the molecular mechanism of pyroptosis and its role in age-related macular degeneration, retinitis pigmentosa and cytomegalovirus retinitis and other retinal diseases.

Citation： Guo Yinong, Sun Xiaodong. Pyroptosis and retinal cell death. Chinese Journal of Ocular Fundus Diseases, 2018, 34(2): 201-204. doi: 10.3760/cma.j.issn.1005-1015.2018.02.027 Copy

1.	Galluzzi L, Kroemer G. Necroptosis: a specialized pathway of programmed necrosis[J]. Cell, 2008, 135(7): 1161-1163. DOI: 10.1016/j.cell.2008.12.004.
2.	Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins[J]. Autophagy, 2011, 7(3): 279-296. DOI: 10.4161/auto.7.3.14487.
3.	He Y, Amer AO. Microbial modulation of host apoptosis and pyroptosis[J]. Front Cell Infect Microbiol, 2014, 4: 83. DOI: 10.3389/fcimb.2014.00083.
4.	Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation[J]. Nature, 2015, 517(7534): 311-320. DOI: 10.1038/nature14191.
5.	Zychlinsky A, Prevost MC, Sansonetti PJ. Shigella flexneri induces apoptosis in infected macrophages[J]. Nature, 1992, 358(6382): 167-169. DOI: 10.1038/358167a0.
6.	Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis[J]. Mol Microbiol, 2000, 38(1):31-40. DOI: 10.1038/nrmicro2070.
7.	Cookson BT, Brennan MA.Pro-inflammatory programmed cell death[J].Trends Microbiol, 2001, 9(3):113-114.
8.	Abe J, Morrell C.Pyroptosis as a regulated form of necrosis: PI+/Annexin V-/high Caspase 1/low Caspase 9 activity in cells = pyroptosis?[J].Circ Res, 2016, 118(10):1457-1460 DOI: 10.1161/CIRCRESAHA.116.308699.
9.	Cunha LD, Zamboni DS.Subversion of inflammasome activation and pyroptosis by pathogenic bacteria[J].Front Cell Infect Microbiol, 2013, 3:76. DOI:10.3389/fcimb.2013.00076.
10.	Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death[J]. Immunol Rev, 2011, 243(1):206-214. DOI: 10.1111/j.1600-065X.2011.01044.x.
11.	Lin KM, Hu W, Troutman TD, et al. IRAK-1 bypasses priming and directly links TLRs to rapid NLRP3 inflammasome activation[J]. Proc Natl Acad Sci USA, 2014, 111(2):775-780. DOI:10.1073/pnas.1320294111.
12.	Broz P, Dixit VM. Inflammasomes: mechanism of assembly, regulation and signalling[J]. Nat Rev Immunol, 2016, 16(7):407-420. DOI:10.1038/nri.2016.58.
13.	Qu Y, Misaghi S, Izrael-Tomasevic A, et al. Phosphorylation of NLRC4 is critical for inflammasome activation[J]. Nature, 2012, 490(7421): 539-542. DOI: 10.1038/nature11429.
14.	Sagulenko V, Thygesen SJ, Sester DP, et al. AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC[J]. Cell Death Differ, 2013, 20(9):1149-1160. DOI:10.1038/cdd.2013.37.
15.	Chen X, He W, Hu L, et al. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis[J]. Cell Res, 2016, 26(9):1007-1020. DOI:10.1038/cr.2016.100.
16.	邱珍, 夏中元, 周斌.细胞焦亡的研究进展[J].医学综述, 2016, 22(15):2935-2938. DOI: 10.3969/j.issn.1006-2084.2016.15.007.Qiu Z, Xia ZY, Zhou B.Research advances in pyroptosis[J].Medical Recapitulate, 2016, 22(15): 2935-2938.DOI:10.3969/j.issn.1006-2084.2016.15.007.
17.	董凯, 周恩亮, 朱子诚, 等.实验性视网膜脱离后光感受器细胞的坏死性凋亡[J].中华眼底病杂志, 2014, 30(4):378-380. DOI:10.3760/cma.j.issn.1005-1015.2014.04.011.Dong K, Zhou EL, Zhu ZC, et al.Photoreceptor necroptosis in experimental retinal detachment[J]. Chin J Ocul Fundus Dis, 2014, 30(4):378-380. DOI:10.3760/cma.j.issn.1005-1015.2014.04.011.
18.	McLeod DS, Grebe R, Bhutto I, et al. Relationship between RPE and choriocapillaris in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2009, 50(10): 4982-4991. DOI: 10.1167/iovs.09-3639. Epub 2009 Apr 8.
19.	Klein ML, Ferris FL 3rd, Armstrong J, et al. Retinal precursors and the development of geographic atrophy in age-related macular degeneration[J]. Ophthalmology, 2008, 115(6): 1026-1031. DOI:10.1016/j.ophtha.2007.08.030.
20.	Doyle SL, Campbell M, Ozaki E, et al. NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components[J]. Nat Med, 2012, 18(5):791-798. DOI:10.1038/nm.2717.
21.	Brandstetter C, Holz FG, Krohne TU. Complement component C5a primes retinal pigment epithelial cells for inflammasome activation by lipofuscin-mediated photooxidative damage[J]. J Biol Chem, 2015, 290(52): 31189-31198. DOI:10.1074/jbc.M115.671180.
22.	Zhao T, Gao J, Van J, et al. Age-related increases in amyloid beta and membrane attack complex: evidence of inflammasome activation in the rodent eye[J]. J Neuroinflammation, 2015, 12(1): 121. DOI: 10.1186/s12974-015-0337-1.
23.	Tarallo V, Hirano Y, Gelfand BD, et al.DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88[J].Cell, 2012, 149(4):847-859.DOI:10.1016/j.cell.2012.03.036.
24.	Brandstetter C, Patt J, Holz FG, et al. Inflammasome priming increases retinal pigment epithelial cell susceptibility to lipofuscin phototoxicity by changing the cell death mechanism from apoptosis to pyroptosis[J]. J Photochem Photobiol B, 2016, 161:177-183. DOI:10.1016/j.jphotobiol.2016.05.018.
25.	Appelbaum T, Santana E, Aguirre GD. Strong upregulation of inflammatory genes accompanies photoreceptor demise in canine models of retinal degeneration[J/OL]. PLoS One, 2017, 12(5): 0177224[2017-05-09]. https://doi.org/10.1371/journal.pone.0177224. DOI: 10.1371/journal.pone.0177224.
26.	Viringipurampeer IA, Metcalfe AL, Bashar AE, et al. NLRP3 inflammasome activation drives bystander cone photoreceptor cell death in a P23H rhodopsin model of retinal degeneration[J]. Hum Mol Genet, 2016, 25(8):1501-1516. DOI:10.1093/hmg/ddw029.
27.	Chien H, Blalock EL, Bush LR, et al. The Caspase-1-induced pyroptotic cell death pathway (Pyroptosis) is upregulated during progression of experimental murine cytomegalovirus (MCMV) retinitis in mice with retrovirus-induced immunosuppression (MAIDS)[J]. IOVS, 2012, 53(14): 6225.
28.	Dix RD, Alston CI, Chien H. Pyroptosis and AIDS-related human cytomegalovirus (HCMV) retinitis: Caspase-1-dependent or caspase-1-independent interleukin-1β expression in response to HCMV infection is cell-type dependent[J]. IOVS, 2014, 55(13): 2818.
29.	Dix RD, Alston CI, Chien H.Both canonical and non-canonical inflammasome systems may operate during development of murine cytomegalovirus (MCMV) retinitis in mice with retrovirus-induced immunodeficiency (MAIDS)[J]. IOVS, 2015, 56(7):1867.
30.	Kataoka K, Matsumoto H, Kaneko H, et al. Macrophage-and RIP3-dependent inflammasome activation exacerbates retinal detachment-induced photoreceptor cell death[J]. Cell Death Dis, 2015, 6:1731. DOI: 10.1038/cddis.2015.73.
31.	Mohr S, Yego EK, Trueblood-Doreian K, et al. Hyperglycemia leads to Müller cell death through induction of pyroptosis-like mechanisms[J]. IOVS, 2009, 50(13): 15.
32.	Rao N, Saraswathy S. In the retinal mitochondrial oxidative stress NLRC4 inflammasome silencing attenuates photoreceptor pyroptosis[J]. IOVS, 2013, 54(15): 1806.

1. Galluzzi L, Kroemer G. Necroptosis: a specialized pathway of programmed necrosis[J]. Cell, 2008, 135(7): 1161-1163. DOI: 10.1016/j.cell.2008.12.004.
2. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins[J]. Autophagy, 2011, 7(3): 279-296. DOI: 10.4161/auto.7.3.14487.
3. He Y, Amer AO. Microbial modulation of host apoptosis and pyroptosis[J]. Front Cell Infect Microbiol, 2014, 4: 83. DOI: 10.3389/fcimb.2014.00083.
4. Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation[J]. Nature, 2015, 517(7534): 311-320. DOI: 10.1038/nature14191.
5. Zychlinsky A, Prevost MC, Sansonetti PJ. Shigella flexneri induces apoptosis in infected macrophages[J]. Nature, 1992, 358(6382): 167-169. DOI: 10.1038/358167a0.
6. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis[J]. Mol Microbiol, 2000, 38(1):31-40. DOI: 10.1038/nrmicro2070.
7. Cookson BT, Brennan MA.Pro-inflammatory programmed cell death[J].Trends Microbiol, 2001, 9(3):113-114.
8. Abe J, Morrell C.Pyroptosis as a regulated form of necrosis: PI+/Annexin V-/high Caspase 1/low Caspase 9 activity in cells = pyroptosis?[J].Circ Res, 2016, 118(10):1457-1460 DOI: 10.1161/CIRCRESAHA.116.308699.
9. Cunha LD, Zamboni DS.Subversion of inflammasome activation and pyroptosis by pathogenic bacteria[J].Front Cell Infect Microbiol, 2013, 3:76. DOI:10.3389/fcimb.2013.00076.
10. Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death[J]. Immunol Rev, 2011, 243(1):206-214. DOI: 10.1111/j.1600-065X.2011.01044.x.
11. Lin KM, Hu W, Troutman TD, et al. IRAK-1 bypasses priming and directly links TLRs to rapid NLRP3 inflammasome activation[J]. Proc Natl Acad Sci USA, 2014, 111(2):775-780. DOI:10.1073/pnas.1320294111.
12. Broz P, Dixit VM. Inflammasomes: mechanism of assembly, regulation and signalling[J]. Nat Rev Immunol, 2016, 16(7):407-420. DOI:10.1038/nri.2016.58.
13. Qu Y, Misaghi S, Izrael-Tomasevic A, et al. Phosphorylation of NLRC4 is critical for inflammasome activation[J]. Nature, 2012, 490(7421): 539-542. DOI: 10.1038/nature11429.
14. Sagulenko V, Thygesen SJ, Sester DP, et al. AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC[J]. Cell Death Differ, 2013, 20(9):1149-1160. DOI:10.1038/cdd.2013.37.
15. Chen X, He W, Hu L, et al. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis[J]. Cell Res, 2016, 26(9):1007-1020. DOI:10.1038/cr.2016.100.
16. 邱珍, 夏中元, 周斌.细胞焦亡的研究进展[J].医学综述, 2016, 22(15):2935-2938. DOI: 10.3969/j.issn.1006-2084.2016.15.007.Qiu Z, Xia ZY, Zhou B.Research advances in pyroptosis[J].Medical Recapitulate, 2016, 22(15): 2935-2938.DOI:10.3969/j.issn.1006-2084.2016.15.007.
17. 董凯, 周恩亮, 朱子诚, 等.实验性视网膜脱离后光感受器细胞的坏死性凋亡[J].中华眼底病杂志, 2014, 30(4):378-380. DOI:10.3760/cma.j.issn.1005-1015.2014.04.011.Dong K, Zhou EL, Zhu ZC, et al.Photoreceptor necroptosis in experimental retinal detachment[J]. Chin J Ocul Fundus Dis, 2014, 30(4):378-380. DOI:10.3760/cma.j.issn.1005-1015.2014.04.011.
18. McLeod DS, Grebe R, Bhutto I, et al. Relationship between RPE and choriocapillaris in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2009, 50(10): 4982-4991. DOI: 10.1167/iovs.09-3639. Epub 2009 Apr 8.
19. Klein ML, Ferris FL 3rd, Armstrong J, et al. Retinal precursors and the development of geographic atrophy in age-related macular degeneration[J]. Ophthalmology, 2008, 115(6): 1026-1031. DOI:10.1016/j.ophtha.2007.08.030.
20. Doyle SL, Campbell M, Ozaki E, et al. NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components[J]. Nat Med, 2012, 18(5):791-798. DOI:10.1038/nm.2717.
21. Brandstetter C, Holz FG, Krohne TU. Complement component C5a primes retinal pigment epithelial cells for inflammasome activation by lipofuscin-mediated photooxidative damage[J]. J Biol Chem, 2015, 290(52): 31189-31198. DOI:10.1074/jbc.M115.671180.
22. Zhao T, Gao J, Van J, et al. Age-related increases in amyloid beta and membrane attack complex: evidence of inflammasome activation in the rodent eye[J]. J Neuroinflammation, 2015, 12(1): 121. DOI: 10.1186/s12974-015-0337-1.
23. Tarallo V, Hirano Y, Gelfand BD, et al.DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88[J].Cell, 2012, 149(4):847-859.DOI:10.1016/j.cell.2012.03.036.
24. Brandstetter C, Patt J, Holz FG, et al. Inflammasome priming increases retinal pigment epithelial cell susceptibility to lipofuscin phototoxicity by changing the cell death mechanism from apoptosis to pyroptosis[J]. J Photochem Photobiol B, 2016, 161:177-183. DOI:10.1016/j.jphotobiol.2016.05.018.
25. Appelbaum T, Santana E, Aguirre GD. Strong upregulation of inflammatory genes accompanies photoreceptor demise in canine models of retinal degeneration[J/OL]. PLoS One, 2017, 12(5): 0177224[2017-05-09]. https://doi.org/10.1371/journal.pone.0177224. DOI: 10.1371/journal.pone.0177224.
26. Viringipurampeer IA, Metcalfe AL, Bashar AE, et al. NLRP3 inflammasome activation drives bystander cone photoreceptor cell death in a P23H rhodopsin model of retinal degeneration[J]. Hum Mol Genet, 2016, 25(8):1501-1516. DOI:10.1093/hmg/ddw029.
27. Chien H, Blalock EL, Bush LR, et al. The Caspase-1-induced pyroptotic cell death pathway (Pyroptosis) is upregulated during progression of experimental murine cytomegalovirus (MCMV) retinitis in mice with retrovirus-induced immunosuppression (MAIDS)[J]. IOVS, 2012, 53(14): 6225.
28. Dix RD, Alston CI, Chien H. Pyroptosis and AIDS-related human cytomegalovirus (HCMV) retinitis: Caspase-1-dependent or caspase-1-independent interleukin-1β expression in response to HCMV infection is cell-type dependent[J]. IOVS, 2014, 55(13): 2818.
29. Dix RD, Alston CI, Chien H.Both canonical and non-canonical inflammasome systems may operate during development of murine cytomegalovirus (MCMV) retinitis in mice with retrovirus-induced immunodeficiency (MAIDS)[J]. IOVS, 2015, 56(7):1867.
30. Kataoka K, Matsumoto H, Kaneko H, et al. Macrophage-and RIP3-dependent inflammasome activation exacerbates retinal detachment-induced photoreceptor cell death[J]. Cell Death Dis, 2015, 6:1731. DOI: 10.1038/cddis.2015.73.
31. Mohr S, Yego EK, Trueblood-Doreian K, et al. Hyperglycemia leads to Müller cell death through induction of pyroptosis-like mechanisms[J]. IOVS, 2009, 50(13): 15.
32. Rao N, Saraswathy S. In the retinal mitochondrial oxidative stress NLRC4 inflammasome silencing attenuates photoreceptor pyroptosis[J]. IOVS, 2013, 54(15): 1806.

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