Regulated cell death and inflammation: An auto-amplification loop causes organ failure

Nature Reviews Immunology

Volumn 14, Issue 11, 2014, Pages 759-767

  Linkermann, Andreas ^a   Stockwell, Brent R ^b   Krautwald, Stefan ^a   Anders, Hans Joachim ^c  

^a UNIVERSITY OF KIEL   (Germany)

^b Howard Hughes Medical Institute   (United States)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; IMMUNOSUPPRESSIVE AGENT;

CELL DEATH; GENE AMPLIFICATION; HUMAN; INFLAMMATION; MULTIPLE ORGAN FAILURE; NEOPLASM; NONHUMAN; ORGAN TRANSPLANTATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; MITOCHONDRION; MOUSE; NECROSIS; NEOPLASMS;

ANIMALS; APOPTOSIS; HUMANS; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; IMMUNOTHERAPY; INFLAMMATION; MICE; MITOCHONDRIA; MULTIPLE ORGAN FAILURE; NECROSIS; NEOPLASMS;

EID: 84922394053     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3743     Document Type: Review

References (108)

1. Rock, K. L., Latz, E., Ontiveros, F. & Kono, H. The sterile inflammatory response. Annu. Rev. Immunol. 28, 321-342 (2010).
2. Galluzzi, L., Kepp, O., Krautwald, S., Kroemer, G. & Linkermann, A. Molecular mechanisms of regulated necrosis. Semin. Cell Dev. Biol. http://dx.doi. org/10.1016/j.semcdb.2014.02.006 (2014).
3. Galluzzi, L. et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death. Differ. 19, 107-120 (2012).
4. Panaretakis, T. et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 28, 578-590 (2009).
5. Kaiser, W. J. et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471, 368-372 (2011).
6. Oberst, A. et al. Catalytic activity of the caspase-8-FLIPL complex inhibits RIPK3-dependent necrosis. Nature 471, 363-367 (2011).
7. Gringhuis, S. I. et al. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a noncanonical caspase-8 inflammasome. Nature Immunol. 13, 246-254 (2012).
8. Kang, T. B., Yang, S. H., Toth, B., Kovalenko, A. & Wallach, D. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity. 38, 27-40 (2013).
9. Papatriantafyllou, M. Innate immunity: Caspase 8 prevents inflammasome activation. Nature Rev. Immunol. 13, 68-69 (2013).
10. Vince, J. E. et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity. 36, 215-227 (2012).
11. Monack, D. M., Raupach, B., Hromockyj, A. E. & Falkow, S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl Acad. Sci. USA 93, 9833-9838 (1996).
12. Bergsbaken, T., Fink, S. L. & Cookson, B. T. Pyroptosis: host cell death and inflammation. Nature Rev. Microbiol. 7, 99-109 (2009).
13. 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).
14. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H. & Vandenabeele, P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nature Rev. Mol. Cell. Biol. 15, 135-147 (2014).
15. Py, B. F. et al. Caspase-11 controls interleukin-1β release through degradation of TRPC1. Cell Rep. 6, 1122-1128 (2014).
16. Pilla, D. M. et al. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc. Natl Acad. Sci. USA 111, 6046-6051 (2014).
17. Lamkanfi, M. & Dixit, V. M. Mechanisms and functions of inflammasomes. Cell 157, 1013-1022 (2014).
18. Doitsh, G. et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505, 509-514 (2013).
19. Monroe, K. M. et al. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343, 428-432 (2014).
20. Zhang, D. W. et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325, 332-336 (2009).
21. He, S. et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137, 1100-1111 (2009).
22. Cho, Y. S. et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123 (2009).
23. Sun, L. et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213-227 (2012).
24. Zhao, J. et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl Acad. Sci. USA 109, 5322-5327 (2012).
25. Green, D. R. Pseudokiller, qu'est-ce que c'est? Immunity. 39, 421-422 (2013).
26. Murphy, J. M. et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity. 39, 443-453 (2013).
27. Dondelinger, Y. et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7, 971-981 (2014).
28. Wang, H. et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54, 133-146 (2014).
29. Linkermann, A. & Green, D. R. Necroptosis. N. Engl. J. Med. 370, 455-465 (2014).
30. Linkermann, A. et al. Regulated cell death in AKI. J. Am. Soc. Nephrol. http://dx.doi.org/10.1681/ASN.2014030262 (2014).
31. Wu, Z., Li, Y., Cai, Y., Yuan, J. & Yuan, C. A novel necroptosis inhibitor-necrostatin-21 and its SAR study. Bioorg. Med. Chem. Lett. 23, 4903-4906 (2013).
32. Xie, T. et al. Structural basis of RIP1 inhibition by necrostatins. Structure. 21, 493-499 (2013).
33. Degterev, A. et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nature Chem. Biol. 4, 313-321 (2008).
34. Tait, S. W. & Green, D. R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nature Rev. Mol. Cell. Biol. 11, 621-632 (2010).
35. Baines, C. P. et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662 (2005).
36. Basso, E. et al. Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J. Biol. Chem. 280, 18558-18561 (2005).
37. Schinzel, A. C. et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl Acad. Sci. USA 102, 12005-12010 (2005).
38. Nakagawa, T. et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658 (2005).
39. Linkermann, A. et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc. Natl Acad. Sci. USA 110, 12024-12029 (2013).
40. Yang, W. S. & Stockwell, B. R. Inhibition of casein kinase 1-epsilon induces cancer-cell-selective, PERIOD2-dependent growth arrest. Genome Biol. 9, R92 (2008).
41. Dolma, S., Lessnick, S. L., Hahn, W. C. & Stockwell, B. R. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3, 285-296 (2003).
42. Yagoda, N. et al. RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864-868 (2007).
43. Dixon, S. J. et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060-1072 (2012).
44. Dixon, S. J. & Stockwell, B. R. The role of iron and reactive oxygen species in cell death. Nature Chem. Biol. 10, 9-17 (2013).
45. Yang, W. S. et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 156, 317-331 (2014).
46. Brinkmann, V. et al. Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535 (2004).
47. Yipp, B. G. et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nature Med. 18, 1386-1393 (2012).
48. Tait, S. W. et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep. 5, 878-885 (2013).
49. Rickard, J. A. et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell 157, 1175-1188 (2014).
50. Linkermann, A. et al. Necroptosis in immunity and ischemia-reperfusion injury. Am. J. Transplant. 13, 2797-2804 (2013).
51. Welz, P. S. et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 447, 330-334 (2011).
52. Gunther, C. et al. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 477, 335-339 (2011).
53. Berger, S. B. et al. Cutting Edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J. Immunol. 192, 5476-5480 (2014).
54. Duprez, L. et al. RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity. 35, 908-918 (2011).
55. Linkermann, A. et al. Dichotomy between RIP1-and RIP3-mediated necroptosis in tumor necrosis factor-α-induced shock. Mol. Med. 18, 577-586 (2012).
56. Rieser, E., Cordier, S. M. & Walczak, H. Linear ubiquitination: a newly discovered regulator of cell signalling. Trends Biochem. Sci. 38, 94-102 (2013).
57. Gerlach, B. et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596 (2011).
58. Abdelkarim, G. E. et al. Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int. J. Mol. Med. 7, 255-260 (2001).
59. Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nature Chem. Biol. 1, 112-119 (2005).
60. Devalaraja-Narashimha, K., Diener, A. M. & Padanilam, B. J. Cyclophilin D gene ablation protects mice from ischemic renal injury. Am. J. Physiol. Renal Physiol. 297, F749-F759 (2009).
61. Ko, G. J. et al. Blocking Fas ligand on leukocytes attenuates kidney ischemia-reperfusion injury. J. Am. Soc. Nephrol. 22, 732-742 (2011).
62. Linkermann, A. et al. Rip1 (Receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Kidney Int. 81, 751-761 (2012).
63. McCullough, L. D., Zeng, Z., Blizzard, K. K., Debchoudhury, I. & Hurn, P. D. Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J. Cereb. Blood Flow Metab. 25, 502-512 (2005).
64. Smith, C. C. et al. Necrostatin: a potentially novel cardioprotective agent? Cardiovasc. Drugs Ther. 21, 227-233 (2007).
65. Szabo, G. et al. Poly(ADP-Ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ. Res. 90, 100-106 (2002).
66. Patel, V. A. et al. Recognition of apoptotic cells by epithelial cells: conserved versus tissue-specific signaling responses. J. Biol. Chem. 285, 1829-1840 (2010).
67. Amaravadi, R. & Thompson, C. B. The survival kinases Akt and Pim as potential pharmacological targets. J. Clin. Invest. 115, 2618-2624 (2005).
68. Williams, D. L., Ozment-Skelton, T. & Li, C. Modulation of the phosphoinositide 3-kinase signaling pathway alters host response to sepsis, inflammation, and ischemia/reperfusion injury. Shock 25, 432-439 (2006).
69. Abraham, E. Akt/protein kinase B. Crit. Care Med. 33, S420-S422 (2005).
70. Martin, S. J., Henry, C. M. & Cullen, S. P. A perspective on mammalian caspases as positive and negative regulators of inflammation. Mol. Cell 46, 387-397 (2012).
71. McDonald, B. et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362-366 (2010).
72. Oka, T. et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 485, 251-255 (2012).
73. Lau, A. et al. RIPK3-mediated necroptosis promotes donor kidney inflammatory injury and reduces allograft survival. Am. J. Transplant. 13, 2805-2818 (2013).
74. Pavlosky, A. et al. RIPK3-mediated necroptosis regulates cardiac allograft rejection. Am. J. Transplant. 14, 1778-1790 (2014).
75. Thapa, R. J. et al. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc. Natl Acad. Sci. USA 110, E3109-E3118 (2013).
76. Holler, N. et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nature Immunol. 1, 489-495 (2000).
77. Linkermann, A., Qian, J. & Janssen, O. Slowly getting a clue on CD95 ligand biology. Biochem. Pharmacol. 66, 1417-1426 (2003).
78. Obata, F. et al. Necrosis-driven systemic immune response alters SAM metabolism through the FOXO-GNMT axis. Cell Rep. 7, 821-833 (2014).
79. Takahashi, N. et al. Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models. Cell Death Dis. 3, e437 (2012).
80. Vanden Berghe, T. et al. Simultaneous targeting of IL-1 and IL-18 is required for protection against inflammatory and septic shock. Am. J. Respir. Crit. Care Med. 189, 282-291 (2014).
81. Kono, H., Chen, C. J., Ontiveros, F. & Rock, K. L. Uric acid promotes an acute inflammatory response to sterile cell death in mice. J. Clin. Invest. 120, 1939-1949 (2010).
82. Mulay, S. R., Evan, A. & Anders, H. J. Molecular mechanisms of crystal-related kidney inflammation and injury. Implications for cholesterol embolism, crystalline nephropathies and kidney stone disease. Nephrol. Dial. Transplant. 29, 507-514 (2014).
83. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A. & Tschopp, J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241 (2006).
84. Mulay, S. R. et al. Calcium oxalate crystals induce renal inflammation by NLRP3-mediated IL-1 β secretion. J. Clin. Invest. 123, 236-246 (2013).
85. Duewell, P. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361 (2010).
86. Jin, C. et al. NLRP3 inflammasome plays a critical role in the pathogenesis of hydroxyapatite-associated arthropathy. Proc. Natl Acad. Sci. USA 108, 14867-14872 (2011).
87. Halle, A. et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nature Immunol. 9, 857-865 (2008).
88. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nature Immunol. 9, 847-856 (2008).
89. Schorn, C. et al. Monosodium urate crystals induce extracellular DNA traps in neutrophils, eosinophils, and basophils but not in mononuclear cells. Front. Immunol. 3, 277 (2012).
90. Schorn, C. et al. Bonding the foe-NETting neutrophils immobilize the pro-inflammatory monosodium urate crystals. Front. Immunol. 3, 376 (2012).
91. Crittenden, D. B. & Pillinger, M. H. New therapies for gout. Annu. Rev. Med. 64, 325-337 (2013).
92. Schlesinger, N. Anti-interleukin-1 therapy in the management of gout. Curr. Rheumatol. Rep. 16, 398 (2014).
93. Schauer, C. et al. Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nature Med. 20, 511-517 (2014).
94. Linkermann, A., De, Z. F., Weinberg, J., Kunzendorf, U. & Krautwald, S. Programmed necrosis in acute kidney injury. Nephrol. Dial. Transplant. 27, 3412-3419 (2012).
95. Sogabe, K., Roeser, N. F., Venkatachalam, M. A. & Weinberg, J. M. Differential cytoprotection by glycine against oxidant damage to proximal tubule cells. Kidney Int. 50, 845-854 (1996).
96. Skouta, R. et al. Ferrostatins inhibit oxidative lipid damage and cell death in diverse disease models. J. Am. Chem. Soc. 136, 4551-4556 (2014).
97. Topalian, S. L. et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443-2454 (2012).
98. Zitvogel, L., Galluzzi, L., Smyth, M. J. & Kroemer, G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity. 39, 74-88 (2013).
99. Chen, L. et al. CD95 promotes tumour growth. Nature 465, 492-496 (2010).
100. Su, D., Stamatakis, L., Singer, E. A. & Srinivasan, R. Renal cell carcinoma: molecular biology and targeted therapy. Curr. Opin. Oncol. 26, 321-327 (2014).
101. Forbes, S. A. et al. The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr. Protoc. Hum. Genet. 57, 10.11.1-10.11.26 (2008).
102. Devalaraja-Narashimha, K., Singaravelu, K. & Padanilam, B. J. Poly(ADP-ribose) polymerase-mediated cell injury in acute renal failure. Pharmacol. Res. 52, 44-59 (2005).
103. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
104. Colbert, L. E. et al. Pronecrotic mixed lineage kinase domain-like protein expression is a prognostic biomarker in patients with early-stage resected pancreatic adenocarcinoma. Cancer 119, 3148-3155 (2013).
105. Dillon, C. P. et al. RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 157, 1189-1202 (2014).
106. Kaiser, W. J. et al. RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition. Proc. Natl Acad. Sci. USA 111, 7753-7758 (2014).
107. Takahashi, N. et al. RIPK1 ensures intestinal homeostasis by protecting the epithelium against apoptosis. Nature 513, 95-99 (2014).
108. Dannappel, M. et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 513, 90-94 (2014).