1932

Abstract

Programmed cell death (self-induced) is intrinsic to all cellular life forms, including unicellular organisms. However, cell death research has focused on animal models to understand cancer, degenerative disorders, and developmental processes. Recently delineated suicidal death mechanisms in bacteria and fungi have revealed ancient origins of animal cell death that are intertwined with immune mechanisms, allaying earlier doubts that self-inflicted cell death pathways exist in microorganisms. Approximately 20 mammalian death pathways have been partially characterized over the last 35 years. By contrast, more than 100 death mechanisms have been identified in bacteria and a few fungi in recent years. However, cell death is nearly unstudied in most human pathogenic microbes that cause major public health burdens. Here, we consider how the current understanding of programmed cell death arose through animal studies and how recently uncovered microbial cell death mechanisms in fungi and bacteria resemble and differ from mechanisms of mammalian cell death.

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2023-11-27
2024-04-15
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Literature Cited

  1. 1.
    Aguilera A, Berdun F, Bartoli C, Steelheart C, Alegre M et al. 2021. C-ferroptosis is an iron-dependent form of regulated cell death in cyanobacteria. J. Cell Biol. 221:2e201911005
    [Google Scholar]
  2. 2.
    Aouacheria A, Cunningham KW, Hardwick JM, Palková Z, Powers T et al. 2018. Comment on “Sterilizing immunity in the lung relies on targeting fungal apoptosis-like programmed cell death. .” Science 360:6395eaar6910
    [Google Scholar]
  3. 3.
    Aouacheria A, Le Goff E, Godefroy N, Baghdiguian S. 2016. Evolution of the BCL-2-regulated apoptotic pathway. Evolutionary Biology: Convergent Evolution, Evolution of Complex Traits, Concepts and Methods P Pontarotti 137–56. Cham, Switz.: Springer
    [Google Scholar]
  4. 4.
    Aouacheria A, Rech de Laval V, Combet C, Hardwick JM. 2013. Evolution of Bcl-2 homology motifs: homology versus homoplasy. Trends Cell Biol. 23:3103–11
    [Google Scholar]
  5. 5.
    Arama E, Agapite J, Steller H. 2003. Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev. Cell 4:5687–97
    [Google Scholar]
  6. 6.
    Aravind L, Iyer LM, Burroughs AM. 2022. Discovering biological conflict systems through genome analysis: evolutionary principles and biochemical novelty. Annu. Rev. Biomed. Data Sci. 5:367–91
    [Google Scholar]
  7. 7.
    Athukoralage JS, White MF. 2022. Cyclic nucleotide signaling in phage defense and counter-defense. Annu. Rev. Virol. 9:451–68
    [Google Scholar]
  8. 8.
    Barragan CA, Wu R, Kim S-T, Xi W, Habring A et al. 2019. RPW8/HR repeats control NLR activation in Arabidopsis thaliana. PLOS Genet. 15:7e1008313
    [Google Scholar]
  9. 9.
    Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:58191709–12
    [Google Scholar]
  10. 10.
    Bedoui S, Herold MJ, Strasser A. 2020. Emerging connectivity of programmed cell death pathways and its physiological implications. Nat. Rev. Mol. Cell Biol. 21:11678–95
    [Google Scholar]
  11. 11.
    Bock FJ, Tait SWG. 2020. Mitochondria as multifaceted regulators of cell death. Nat. Rev. Mol. Cell Biol. 21:285–100
    [Google Scholar]
  12. 12.
    Bogacz M, Krauth-Siegel RL. 2018. Tryparedoxin peroxidase-deficiency commits trypanosomes to ferroptosis-type cell death. eLife 7:e37503
    [Google Scholar]
  13. 13.
    Bogner C, Kale J, Pogmore J, Chi X, Shamas-Din A et al. 2020. Allosteric regulation of BH3 proteins in Bcl-xL complexes enables switch-like activation of Bax. Mol. Cell 77:4901–12.e9
    [Google Scholar]
  14. 14.
    Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:5891960–64
    [Google Scholar]
  15. 15.
    Broz P, Pelegrín P, Shao F. 2020. The gasdermins, a protein family executing cell death and inflammation. Nat. Rev. Immunol. 20:3143–57
    [Google Scholar]
  16. 16.
    Čáp M, Štěpánek L, Harant K, Váchová L, Palková Z. 2012. Cell differentiation within a yeast colony: metabolic and regulatory parallels with a tumor-affected organism. Mol. Cell 46:4436–48
    [Google Scholar]
  17. 17.
    Chau BN, Pan CW, Wang JYJ. 2006. Separation of anti-proliferation and anti-apoptotic functions of retinoblastoma protein through targeted mutations of its A/B domain. PLOS ONE 1:1e82
    [Google Scholar]
  18. 18.
    Chen Y-B, Aon MA, Hsu Y-T, Soane L, Teng X et al. 2011. Bcl-xL regulates mitochondrial energetics by stabilizing the inner membrane potential. J. Cell Biol. 195:2263–76
    [Google Scholar]
  19. 19.
    Cheng W-C, Teng X, Park HK, Tucker CM, Dunham MJ, Hardwick JM. 2008. Fis1 deficiency selects for compensatory mutations responsible for cell death and growth control defects. Cell Death Differ. 15:121838–46
    [Google Scholar]
  20. 20.
    Cho YS, Challa S, Moquin D, Genga R, Ray TD et al. 2009. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:61112–23
    [Google Scholar]
  21. 21.
    Clarke PGH, Clarke S. 1996. Nineteenth century research on naturally occurring cell death and related phenomena. Anat. Embryol. 193:281–99
    [Google Scholar]
  22. 22.
    Clavé C, Dyrka W, Turcotte EA, Granger-Farbos A, Ibarlosa L et al. 2022. Fungal gasdermin-like proteins are controlled by proteolytic cleavage. PNAS 119:7e2109418119
    [Google Scholar]
  23. 23.
    Cohen D, Melamed S, Millman A, Shulman G, Oppenheimer-Shaanan Y et al. 2019. Cyclic GMP-AMP signalling protects bacteria against viral infection. Nature 574:7780691–95
    [Google Scholar]
  24. 24.
    Conlon M, Poltorack CD, Forcina GC, Armenta DA, Mallais M et al. 2021. A compendium of kinetic modulatory profiles identifies ferroptosis regulators. Nat. Chem. Biol. 17:6665–74
    [Google Scholar]
  25. 25.
    Conradt B, Horvitz HR. 1998. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93:4519–29
    [Google Scholar]
  26. 26.
    Cookson BT, Brennan MA. 2001. Pro-inflammatory programmed cell death. Trends Microbiol. 9:3113–14
    [Google Scholar]
  27. 27.
    Cowan WM. 2001. Viktor Hamburger and Rita Levi-Montalcini: the path to the discovery of nerve growth factor. Annu. Rev. Neurosci. 24:551–600
    [Google Scholar]
  28. 28.
    Czabotar PE, Lessene G, Strasser A, Adams JM. 2014. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15:149–63
    [Google Scholar]
  29. 29.
    Dangol S, Chen Y, Hwang BK, Jwa N-S. 2019. Iron- and reactive oxygen species–dependent ferroptotic cell death in rice–Magnaporthe oryzae interactions. Plant Cell 31:1189–209
    [Google Scholar]
  30. 30.
    Daskalov A, Gladieux P, Heller J, Glass NL. 2019. Programmed cell death in Neurospora crassa is controlled by the allorecognition determinant rcd-1. Genetics 213:41387–400
    [Google Scholar]
  31. 31.
    Daskalov A, Glass NL. 2022. Gasdermin and gasdermin-like pore-forming proteins in invertebrates, fungi and bacteria. J. Mol. Biol. 434:4167273
    [Google Scholar]
  32. 32.
    Daskalov A, Habenstein B, Sabaté R, Berbon M, Martinez D et al. 2016. Identification of a novel cell death–inducing domain reveals that fungal amyloid-controlled programmed cell death is related to necroptosis. PNAS 113:102720–25
    [Google Scholar]
  33. 33.
    Daskalov A, Heller J, Herzog S, Fleißner A, Glass NL. 2017. Molecular mechanisms regulating cell fusion and heterokaryon formation in filamentous fungi. Microbiol. Spectr. 5:2 https://doi.org/10.1128/microbiolspec.funk-0015-2016
    [Google Scholar]
  34. 34.
    Daskalov A, Mitchell PS, Sandstrom A, Vance RE, Glass NL. 2020. Molecular characterization of a fungal gasdermin-like protein. PNAS 117:3118600–607
    [Google Scholar]
  35. 35.
    Degterev A, Ofengeim D, Yuan J. 2019. Targeting RIPK1 for the treatment of human diseases. PNAS 116:209714–22
    [Google Scholar]
  36. 36.
    Distéfano AM, Martin MV, Córdoba JP, Bellido AM, D'Ippólito S et al. 2017. Heat stress induces ferroptosis-like cell death in plants. J. Cell Biol. 216:2463–76
    [Google Scholar]
  37. 37.
    Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM et al. 2012. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149:51060–72
    [Google Scholar]
  38. 38.
    Duncan-Lowey B, McNamara-Bordewick NK, Tal N, Sorek R, Kranzusch PJ. 2021. Effector-mediated membrane disruption controls cell death in CBASS antiphage defense. Mol. Cell 81:245039–51.e5
    [Google Scholar]
  39. 39.
    Duncan-Lowey B, Tal N, Johnson AG, Rawson S, Mayer ML et al. 2023. Cryo-EM structure of the RADAR supramolecular anti-phage defense complex. Cell 186:5987–98.e15
    [Google Scholar]
  40. 40.
    Eastwood MD, Cheung SWT, Lee KY, Moffat J, Meneghini MD. 2012. Developmentally programmed nuclear destruction during yeast gametogenesis. Dev. Cell 23:135–44
    [Google Scholar]
  41. 41.
    Eastwood MD, Cheung SWT, Meneghini MD. 2013. Programmed nuclear destruction in yeast. Autophagy 9:2263–65
    [Google Scholar]
  42. 42.
    Elmore S. 2007. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35:4495–516
    [Google Scholar]
  43. 43.
    Essuman K, Milbrandt J, Dangl JL, Nishimura MT. 2022. Shared TIR enzymatic functions regulate cell death and immunity across the tree of life. Science 377:6605eabo0001
    [Google Scholar]
  44. 44.
    Fabrizio P, Battistella L, Vardavas R, Gattazzo C, Liou L-L et al. 2004. Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J. Cell Biol. 166:71055–67
    [Google Scholar]
  45. 45.
    Fannjiang Y, Cheng W-C, Lee SJ, Qi B, Pevsner J et al. 2004. Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev. 18:222785–97
    [Google Scholar]
  46. 46.
    Flores-Romero H, Ros U, Garcia-Saez AJ. 2020. Pore formation in regulated cell death. EMBO J. 39:23e105753
    [Google Scholar]
  47. 47.
    Frampton RA, Taylor C, Holguín Moreno AV, Visnovsky SB, Petty NK et al. 2014. Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Appl. Environ. Microbiol. 80:72216–28
    [Google Scholar]
  48. 48.
    Fries BC, Goldman DL, Cherniak R, Ju R, Casadevall A. 1999. Phenotypic switching in Cryptococcus neoformans results in changes in cellular morphology and glucuronoxylomannan structure. Infect. Immun. 67:116076–83
    [Google Scholar]
  49. 49.
    Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM et al. 2015. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 22:158–73
    [Google Scholar]
  50. 50.
    Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D et al. 2018. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 25:3486–541
    [Google Scholar]
  51. 51.
    Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH et al. 2012. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19:1107–20
    [Google Scholar]
  52. 52.
    Gebreegziabher Amare M, Westrick NM, Keller NP, Kabbage M. 2022. The conservation of IAP-like proteins in fungi, and their potential role in fungal programmed cell death. Fungal Genet. Biol. 162:103730
    [Google Scholar]
  53. 53.
    Gonçalves AP, Heller J, Daskalov A, Videira A, Glass NL. 2017. Regulated forms of cell death in fungi. Front. Microbiol. 8:1837
    [Google Scholar]
  54. 54.
    Gong Y-N, Guy C, Olauson H, Becker JU, Yang M et al. 2017. ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell 169:2286–300.e16
    [Google Scholar]
  55. 55.
    González-Cofrade L, Green JP, Cuadrado I, Amesty Á, Oramas-Royo S et al. 2023. Phenolic and quinone methide nor-triterpenes as selective NLRP3 inflammasome inhibitors. Bioorgan. Chem. 132:106362
    [Google Scholar]
  56. 56.
    Griffin DE, Hardwick JM. 1999. Perspective: virus infections and the death of neurons. Trends Microbiol. 7:4155–60
    [Google Scholar]
  57. 57.
    Grootjans S, Vanden Berghe T, Vandenabeele P. 2017. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ. 24:71184–95
    [Google Scholar]
  58. 58.
    Grootveld AK, Kyaw W, Panova V, Lau AWY, Ashwin E et al. 2023. Apoptotic cell fragments locally activate tingible body macrophages in the germinal center. Cell 186:61144–61.e18
    [Google Scholar]
  59. 59.
    Hardwick JM. 2018. Do fungi undergo apoptosis-like programmed cell death?. mBio 9:4e00948
    [Google Scholar]
  60. 60.
    Hazan R, Engelberg-Kulka H. 2004. Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol. Genet. Genom. 272:2227–34
    [Google Scholar]
  61. 61.
    Hengartner MO, Ellis R, Horvitz R. 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356:6369494–99
    [Google Scholar]
  62. 62.
    Hong Z, Mei J, Li C, Bai G, Maimaiti M et al. 2021. STING inhibitors target the cyclic dinucleotide binding pocket. PNAS 118:24e2105465118
    [Google Scholar]
  63. 63.
    Hu JJ, Liu X, Xia S, Zhang Z, Zhang Y et al. 2020. FDA-approved disulfiram inhibits pyroptosis by blocking gasdermin D pore formation. Nat. Immunol. 21:7736–45
    [Google Scholar]
  64. 64.
    Huska JD, Lamb HM, Hardwick JM. 2019. Overview of BCL-2 family proteins and therapeutic potentials. Methods Mol. Biol. 1877:1–21
    [Google Scholar]
  65. 65.
    Ikegawa Y, Combet C, Groussin M, Navratil V, Safar-Remali S et al. 2023. Evidence for existence of an apoptosis-inducing BH3-only protein, sayonara, in Drosophila. EMBO J. 42:e110454
    [Google Scholar]
  66. 66.
    Ivanovska I, Hardwick JM. 2005. Viruses activate a genetically conserved cell death pathway in a unicellular organism. J. Cell Biol. 170:3391–99
    [Google Scholar]
  67. 67.
    Johnson AG, Kranzusch PJ. 2022. What bacterial cell death teaches us about life. PLOS Pathog. 18:10e1010879
    [Google Scholar]
  68. 68.
    Johnson AG, Wein T, Mayer ML, Duncan-Lowey B, Yirmiya E et al. 2022. Bacterial gasdermins reveal an ancient mechanism of cell death. Science 375:6577221–25
    [Google Scholar]
  69. 69.
    Junqueira C, Crespo Â, Ranjbar S, de Lacerda LB, Lewandrowski M et al. 2022. FcγR-mediated SARS-CoV-2 infection of monocytes activates inflammation. Nature 606:7914576–84
    [Google Scholar]
  70. 70.
    Kang S-J, Wang S, Hara H, Peterson EP, Namura S et al. 2000. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 149:3613–22
    [Google Scholar]
  71. 71.
    Kayagaki N, Kornfeld OS, Lee BL, Stowe IB, O'Rourke K et al. 2021. NINJ1 mediates plasma membrane rupture during lytic cell death. Nature 591:7848131–36
    [Google Scholar]
  72. 72.
    Kerr JFR, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:4239–57
    [Google Scholar]
  73. 73.
    Kershaw MJ, Talbot NJ. 2009. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. PNAS 106:3715967–72
    [Google Scholar]
  74. 74.
    Kim A, Cunningham KW. 2015. A LAPF/phafin1-like protein regulates TORC1 and lysosomal membrane permeabilization in response to endoplasmic reticulum membrane stress. Mol. Biol. Cell 26:254631–45
    [Google Scholar]
  75. 75.
    Kim H, Kim A, Cunningham KW. 2012. Vacuolar H+-ATPase (V-ATPase) promotes vacuolar membrane permeabilization and nonapoptotic death in stressed yeast. J. Biol. Chem. 287:2319029–39
    [Google Scholar]
  76. 76.
    Kortright KE, Chan BK, Koff JL, Turner PE. 2019. Phage therapy: a renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 25:2219–32
    [Google Scholar]
  77. 77.
    Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D et al. 2005. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 12:21463–67
    [Google Scholar]
  78. 78.
    Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES et al. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16:13–11
    [Google Scholar]
  79. 79.
    Kuida K, Haydar TF, Kuan C-Y, Gu Y, Taya C et al. 1998. Reduced apoptosis and cytochrome c–mediated caspase activation in mice lacking caspase 9. Cell 94:3325–37
    [Google Scholar]
  80. 80.
    Kulkarni M, Stolp ZD, Hardwick JM. 2019. Targeting intrinsic cell death pathways to control fungal pathogens. Biochem. Pharmacol. 162:71–78
    [Google Scholar]
  81. 81.
    Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M et al. 2002. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:3331–42
    [Google Scholar]
  82. 82.
    Leavitt A, Yirmiya E, Amitai G, Lu A, Garb J et al. 2022. Viruses inhibit TIR gcADPR signalling to overcome bacterial defence. Nature 611:7935326–31
    [Google Scholar]
  83. 83.
    Legrand AJ, Konstantinou M, Goode EF, Meier P. 2019. The diversification of cell death and immunity: memento mori. Mol. Cell 76:2232–42
    [Google Scholar]
  84. 84.
    Leiter É, Csernoch L, Pócsi I. 2018. Programmed cell death in human pathogenic fungi—a possible therapeutic target. Expert Opin. Ther. Targets 22:121039–48
    [Google Scholar]
  85. 85.
    Levine B, Griffin DE. 1992. Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis. J. Virol. 66:116429–35
    [Google Scholar]
  86. 86.
    Levine B, Huang Q, Isaacs JT, Reed JC, Griffin DE, Hardwick JM. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:6414739–42
    [Google Scholar]
  87. 87.
    Lewis J, Oyler GA, Ueno K, Fannjiang Y-R, Chau BN et al. 1999. Inhibition of virus-induced neuronal apoptosis by Bax. Nat. Med. 5:7832–35
    [Google Scholar]
  88. 88.
    Liang M, Ye H, Shen Q, Jiang X, Cui G et al. 2021. Tangeretin inhibits fungal ferroptosis to suppress rice blast. J. Integr. Plant Biol. 63:122136–49
    [Google Scholar]
  89. 89.
    Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG et al. 2016. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535:7610153–58
    [Google Scholar]
  90. 90.
    Lockshin RA. 2016. Programmed cell death 50 (and beyond). Cell Death Differ. 23:110–17
    [Google Scholar]
  91. 91.
    Lockshin RA, Williams CM. 1965. Programmed cell death—I. Cytology of degeneration in the intersegmental muscles of the Pernyi silkmoth. J. Insect Physiol. 11:2123–33
    [Google Scholar]
  92. 92.
    Lopatina A, Tal N, Sorek R. 2020. Abortive infection: bacterial suicide as an antiviral immune strategy. Annu. Rev. Virol. 7:371–84
    [Google Scholar]
  93. 93.
    Lopes Fischer N, Naseer N, Shin S, Brodsky IE. 2020. Effector-triggered immunity and pathogen sensing in metazoans. Nat. Microbiol. 5:114–26
    [Google Scholar]
  94. 94.
    Ludovico P, Rodrigues F, Almeida A, Silva MT, Barrientos A, Côrte-Real M. 2002. Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell 13:82598–606
    [Google Scholar]
  95. 95.
    Maekawa T, Kashkar H, Coll NS. 2023. Dying in self-defence: a comparative overview of immunogenic cell death signalling in animals and plants. Cell Death Differ. 30:2258–68
    [Google Scholar]
  96. 96.
    Magtanong L, Mueller GD, Williams KJ, Billmann M, Chan K et al. 2022. Context-dependent regulation of ferroptosis sensitivity. Cell Chem. Biol. 29:101409–18.e6
    [Google Scholar]
  97. 97.
    Mahdi LK, Huang M, Zhang X, Nakano RT, Kopp LB et al. 2020. Discovery of a family of mixed lineage kinase domain–like proteins in plants and their role in innate immune signaling. Cell Host Microbe 28:6813–24.e6
    [Google Scholar]
  98. 98.
    Manon S. 2022. Yeast as a tool to decipher the molecular mechanisms underlying the functions of Bcl-2 family. Explor. Target. Antitumor Ther. 3:2128–48
    [Google Scholar]
  99. 99.
    Martinon F, Burns K, Tschopp J. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell 10:2417–26
    [Google Scholar]
  100. 100.
    Martin-Urdiroz M, Oses-Ruiz M, Ryder LS, Talbot NJ. 2016. Investigating the biology of plant infection by the rice blast fungus Magnaporthe oryzae. Fungal Genet. Biol. 90:61–68
    [Google Scholar]
  101. 101.
    Maruta N, Burdett H, Lim BYJ, Hu X, Desa S et al. 2022. Structural basis of NLR activation and innate immune signalling in plants. Immunogenetics 74:15–26
    [Google Scholar]
  102. 102.
    Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M et al. 2010. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11:121136–42
    [Google Scholar]
  103. 103.
    Mifflin L, Ofengeim D, Yuan J. 2020. Receptor-interacting protein kinase 1 (RIPK1) as a therapeutic target. Nat. Rev. Drug Discov. 19:8553–71
    [Google Scholar]
  104. 104.
    Minina EA, Staal J, Alvarez VE, Berges JA, Berman-Frank I et al. 2020. Classification and nomenclature of metacaspases and paracaspases: no more confusion with caspases. Mol. Cell 77:5927–29
    [Google Scholar]
  105. 105.
    Nagata S. 2018. Apoptosis and clearance of apoptotic cells. Annu. Rev. Immunol. 36:489–517
    [Google Scholar]
  106. 106.
    Nassour J, Radford R, Correia A, Fusté JM, Schoell B et al. 2019. Autophagic cell death restricts chromosomal instability during replicative crisis. Nature 565:7741659–63
    [Google Scholar]
  107. 107.
    Nguyen PV, Hlaváček O, Maršíková J, Váchová L, Palková Z. 2018. Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms. PLOS Genet. 14:7e1007495
    [Google Scholar]
  108. 108.
    Nozaki K, Maltez VI, Rayamajhi M, Tubbs AL, Mitchell JE et al. 2022. Caspase-7 activates ASM to repair gasdermin and perforin pores. Nature 606:7916960–67
    [Google Scholar]
  109. 109.
    Nozaki K, Miao EA. 2023. Bucket lists must be completed during cell death. Trends Cell Biol. 33:9P803–15
    [Google Scholar]
  110. 110.
    Ofengeim D, Chen Y-B, Miyawaki T, Li H, Sacchetti S et al. 2012. N-terminally cleaved Bcl-xL mediates ischemia-induced neuronal death. Nat. Neurosci. 15:4574–80
    [Google Scholar]
  111. 111.
    Ofir G, Herbst E, Baroz M, Cohen D, Millman A et al. 2021. Antiviral activity of bacterial TIR domains via immune signalling molecules. Nature 600:7887116–20
    [Google Scholar]
  112. 112.
    Pattingre S, Tassa A, Qu X, Garuti R, Liang XH et al. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1–dependent autophagy. Cell 122:6927–39
    [Google Scholar]
  113. 113.
    Peltzer N, Walczak H. 2019. Cell death and inflammation—a vital but dangerous liaison. Trends Immunol. 40:5387–402
    [Google Scholar]
  114. 114.
    Pihán P, Lisbona F, Borgonovo J, Edwards-Jorquera S, Nunes-Hasler P et al. 2021. Control of lysosomal-mediated cell death by the pH-dependent calcium channel RECS1. Sci. Adv. 7:46eabe5469
    [Google Scholar]
  115. 115.
    Qi W, Yuan J. 2022. RIPK1 and RIPK3 form mosaic necrosomes. Nat. Cell Biol. 24:4406–7
    [Google Scholar]
  116. 116.
    Randow F, MacMicking JD, James LC. 2013. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340:6133701–6
    [Google Scholar]
  117. 117.
    Ratan RR. 2020. The chemical biology of ferroptosis in the central nervous system. Cell Chem. Biol. 27:5479–98
    [Google Scholar]
  118. 118.
    Rico-Ramírez AM, Gonçalves AP, Glass NL. 2022. Fungal cell death: the beginning of the end. Fungal Genet. Biol. 159:103671
    [Google Scholar]
  119. 119.
    Roberts AW, Davids MS, Pagel JM, Kahl BS, Puvvada SD et al. 2016. Targeting BCL2 with Venetoclax in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 374:4311–22
    [Google Scholar]
  120. 120.
    Sberro H, Leavitt A, Kiro R, Koh E, Peleg Y et al. 2013. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol. Cell 50:1136–48
    [Google Scholar]
  121. 121.
    Seuring C, Greenwald J, Wasmer C, Wepf R, Saupe SJ et al. 2012. The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLOS Biol. 10:12e1001451
    [Google Scholar]
  122. 122.
    Shan B, Pan H, Najafov A, Yuan J. 2018. Necroptosis in development and diseases. Genes Dev. 32:5–6327–40
    [Google Scholar]
  123. 123.
    Shen Q, Liang M, Yang F, Deng YZ, Naqvi NI. 2020. Ferroptosis contributes to developmental cell death in rice blast. New Phytol. 227:61831–46
    [Google Scholar]
  124. 124.
    Skouta R, Dixon SJ, Wang J, Dunn DE, Orman M et al. 2014. Ferrostatins inhibit oxidative lipid damage and cell death in diverse disease models. J. Am. Chem. Soc. 136:124551–56
    [Google Scholar]
  125. 125.
    Soll DR. 2014. The role of phenotypic switching in the basic biology and pathogenesis of Candida albicans. J. Oral Microbiol. 6:122993
    [Google Scholar]
  126. 126.
    Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND et al. 2013. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 19:2202–8
    [Google Scholar]
  127. 127.
    Stolp ZD, Kulkarni M, Liu Y, Zhu C, Jalisi A et al. 2022. Yeast cell death pathway requiring AP-3 vesicle trafficking leads to vacuole/lysosome membrane permeabilization. Cell Rep. 39:2110647
    [Google Scholar]
  128. 128.
    Tal N, Morehouse BR, Millman A, Stokar-Avihail A, Avraham C et al. 2021. Cyclic CMP and cyclic UMP mediate bacterial immunity against phages. Cell 184:235728–39.e16
    [Google Scholar]
  129. 129.
    Teng X, Cheng W-C, Qi B, Yu T-X, Ramachandran K et al. 2011. Gene-dependent cell death in yeast. Cell Death Dis. 2:8e188
    [Google Scholar]
  130. 130.
    Teng X, Dayhoff-Brannigan M, Cheng W-C, Gilbert CE, Sing CN et al. 2013. Genome-wide consequences of deleting any single gene. Mol. Cell 52:4485–94
    [Google Scholar]
  131. 131.
    Terrones O, Antonsson B, Yamaguchi H, Wang H-G, Liu J et al. 2004. Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J. Biol. Chem. 279:2930081–91
    [Google Scholar]
  132. 132.
    Tsvetkov P, Coy S, Petrova B, Dreishpoon M, Verma A et al. 2022. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science 375:65861254–61
    [Google Scholar]
  133. 133.
    Unterholzner SJ, Poppenberger B, Rozhon W. 2013. Toxin–antitoxin systems. Mob. Genet. Elem. 3:5e26219
    [Google Scholar]
  134. 134.
    Uren AG, O'Rourke K, Aravind L, Pisabarro MT, Seshagiri S et al. 2000. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6:4961–67
    [Google Scholar]
  135. 135.
    Váchová L, Palková Z. 2018. How structured yeast multicellular communities live, age and die?. FEMS Yeast Res. 18:4foy033
    [Google Scholar]
  136. 136.
    Valent B. 2021. The impact of blast disease: past, present, and future. Methods Mol. Biol. 2356:1–18
    [Google Scholar]
  137. 137.
    Vaux DL, Cory S, Adams JM. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:6189440–42
    [Google Scholar]
  138. 138.
    Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ. 2006. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:5773580–83
    [Google Scholar]
  139. 139.
    Vitale I, Pietrocola F, Guilbaud E, Aaronson SA, Abrams JM et al. 2023. Apoptotic cell death in disease—current understanding of the NCCD 2023. Cell Death Differ. 30:51097–154
    [Google Scholar]
  140. 140.
    Wang JQ, Jeelall YS, Ferguson LL, Horikawa K. 2014. Toll-like receptors and cancer: MYD88 mutation and inflammation. Front. Immunol. 5:367
    [Google Scholar]
  141. 141.
    Wang S, Miura M, Jung Y-k, Zhu H, Li E, Yuan J 1998. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92:4501–9
    [Google Scholar]
  142. 142.
    Wein T, Sorek R. 2022. Bacterial origins of human cell-autonomous innate immune mechanisms. Nat. Rev. Immunol. 22:10629–38
    [Google Scholar]
  143. 143.
    Westphal D, Kluck RM, Dewson G. 2014. Building blocks of the apoptotic pore: how Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ. 21:2196–205
    [Google Scholar]
  144. 144.
    White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H. 1994. Genetic control of programmed cell death in Drosophila. Science 264:5159677–83
    [Google Scholar]
  145. 145.
    Wiernicki B, Dubois H, Tyurina YY, Hassannia B, Bayir H et al. 2020. Excessive phospholipid peroxidation distinguishes ferroptosis from other cell death modes including pyroptosis. Cell Death Dis. 11:10922
    [Google Scholar]
  146. 146.
    Wilkinson D, Maršíková J, Hlaváček O, Gilfillan GD, Ježková E et al. 2018. Transcriptome remodeling of differentiated cells during chronological ageing of yeast colonies: new insights into metabolic differentiation. Oxid. Med. Cell. Longev. 2018:e4932905
    [Google Scholar]
  147. 147.
    Wissing S, Ludovico P, Herker E, Büttner S, Engelhardt SM et al. 2004. An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 166:7969–74
    [Google Scholar]
  148. 148.
    Wojciechowski JW, Tekoglu E, Gąsior-Głogowska M, Coustou V, Szulc N et al. 2022. Exploring a diverse world of effector domains and amyloid signaling motifs in fungal NLR proteins. PLOS Comput. Biol. 18:12e1010787
    [Google Scholar]
  149. 149.
    Xia S, Zhang Z, Magupalli VG, Pablo JL, Dong Y et al. 2021. Gasdermin D pore structure reveals preferential release of mature interleukin-1. Nature 593:7860607–11
    [Google Scholar]
  150. 150.
    Xu D, Zou C, Yuan J. 2021. Genetic regulation of RIPK1 and necroptosis. Annu. Rev. Genet. 55:235–63
    [Google Scholar]
  151. 151.
    Xu H-D, Qin Z-H. 2019. Beclin 1, Bcl-2 and autophagy. Adv. Exp. Med. Biol. 1206:109–26
    [Google Scholar]
  152. 152.
    Yoon S, Bogdanov K, Kovalenko A, Wallach D. 2016. Necroptosis is preceded by nuclear translocation of the signaling proteins that induce it. Cell Death Differ. 23:2253–60
    [Google Scholar]
  153. 153.
    Yoon S, Kovalenko A, Bogdanov K, Wallach D. 2017. MLKL, the protein that mediates necroptosis, also regulates endosomal trafficking and extracellular vesicle generation. Immunity 47:151–65.e7
    [Google Scholar]
  154. 154.
    Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75:4641–52
    [Google Scholar]
  155. 155.
    Zhou Z, He H, Wang K, Shi X, Wang Y et al. 2020. Granzyme A from cytotoxic lymphocytes cleaves GSDMB to trigger pyroptosis in target cells. Science 368:6494eaaz7548
    [Google Scholar]
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