1932

Abstract

Balancing cell death and survival is essential for normal development and homeostasis and for preventing diseases, especially cancer. Conventional cell death pathways include apoptosis, a form of programmed cell death controlled by a well-defined biochemical pathway, and necrosis, the lysis of acutely injured cells. New types of regulated cell death include necroptosis, pyroptosis, ferroptosis, phagoptosis, and entosis. Autophagy can promote survival or can cause death. Newly described processes of anastasis and resuscitation show that, remarkably, cells can recover from the brink of apoptosis or necroptosis. Important new work shows that epithelia achieve homeostasis by extruding excess cells, which then die by anoikis due to loss of survival signals. This mechanically regulated process both maintains barrier function as cells die and matches rates of proliferation and death. In this review, we describe these unconventional ways in which cells have evolved to die or survive, as well as the contributions that these processes make to homeostasis and cancer.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100616-060748
2018-10-06
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/34/1/annurev-cellbio-100616-060748.html?itemId=/content/journals/10.1146/annurev-cellbio-100616-060748&mimeType=html&fmt=ahah

Literature Cited

  1. Abdelwahid E, Pelliniemi LJ, Jokinen E 2002. Cell death and differentiation in the development of the endocardial cushion of the embryonic heart. Microsc. Res. Tech. 58:5395–403
    [Google Scholar]
  2. Abraham MC, Lu Y, Shaham S 2007. A morphologically conserved nonapoptotic program promotes linker cell death in Caenorhabditis elegans. Dev. . Cell 12:173–86
    [Google Scholar]
  3. Andrade D, Rosenblatt J 2011. Apoptotic regulation of epithelial cellular extrusion. Apoptosis Int. J. Program. Cell Death 16:5491–501
    [Google Scholar]
  4. Araki K, Shimura T, Suzuki H, Tsutsumi S, Wada W et al. 2011. E/N-cadherin switch mediates cancer progression via TGF-β-induced epithelial-to-mesenchymal transition in extrahepatic cholangiocarcinoma. Br. J. Cancer 105:121885–93
    [Google Scholar]
  5. Ashkenazi A, Salvesen G 2014. Regulated cell death: signaling and mechanisms. Annu. Rev. Cell Dev. Biol. 30:337–56
    [Google Scholar]
  6. Attwell S, Roskelley C, Dedhar S 2000. The integrin-linked kinase (ILK) suppresses anoikis. Oncogene 19:333811–15
    [Google Scholar]
  7. Bergsbaken T, Fink SL, Cookson BT 2009. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7:299–109
    [Google Scholar]
  8. Berry DL, Baehrecke EH 2008. Autophagy functions in programmed cell death. Autophagy 4:3359–60
    [Google Scholar]
  9. Boisvert-Adamo K, Aplin AE 2006. B-RAF and PI-3 kinase signaling protect melanoma cells from anoikis. Oncogene 25:354848–56
    [Google Scholar]
  10. Brown GC, Neher JJ 2012. Eaten alive! Cell death by primary phagocytosis: “phagoptosis. .” Trends Biochem. Sci. 37:8325–32
    [Google Scholar]
  11. Bursch W 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 8:6569–81
    [Google Scholar]
  12. Cai Z, Jitkaew S, Zhao J, Chiang H-C, Choksi S et al. 2013. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16:155–65
    [Google Scholar]
  13. Cartwright IM, Liu X, Zhou M, Li F, Li C-Y 2017. Essential roles of Caspase-3 in facilitating Myc-induced genetic instability and carcinogenesis. eLife 6:e26371
    [Google Scholar]
  14. Castellano E, Downward J 2011. RAS interaction with PI3K: more than just another effector pathway. Genes Cancer 2:3261–74
    [Google Scholar]
  15. Chen HX, Sharon E 2013. IGF-1R as an anti-cancer target—trials and tribulations. Chin. J. Cancer 32:5242–52
    [Google Scholar]
  16. Chen Y, Wang S, He M, Wang Y, Zhao H et al. 2013. Prevalence of heterotypic tumor/immune cell-in-cell structure in vitro and in vivo leading to formation of aneuploidy. PLOS ONE 8:3e59418
    [Google Scholar]
  17. Cho Y, 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]
  18. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF 2001. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3:4339–45
    [Google Scholar]
  19. Cookson BT, Brennan MA 2001. Pro-inflammatory programmed cell death. Trends Microbiol 9:3113–14
    [Google Scholar]
  20. de Calignon A, Fox LM, Pitstick R, Carlson GA, Bacskai BJ et al. 2010. Caspase activation precedes and leads to tangles. Nature 464:72921201–4
    [Google Scholar]
  21. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS 2002. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111:129–40
    [Google Scholar]
  22. Dekkers MPJ, Nikoletopoulou V, Barde Y-A 2013. Death of developing neurons: new insights and implications for connectivity. J. Cell Biol 203:3385–93
    [Google Scholar]
  23. Denton D, Nicolson S, Kumar S 2012. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 19:187–95
    [Google Scholar]
  24. Denton D, Shravage B, Simin R, Mills K, Berry DL et al. 2009. Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. . Biol 19:201741–46
    [Google Scholar]
  25. Derksen PWB, Liu X, Saridin F, van der Gulden H, Zevenhoven J et al. 2006. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:5437–49
    [Google Scholar]
  26. Diamond ME, Sun L, Ottaviano AJ, Joseph MJ, Munshi HG 2008. Differential growth factor regulation of N-cadherin expression and motility in normal and malignant oral epithelium. J. Cell Sci. 121:Pt 132197–207
    [Google Scholar]
  27. Ding AX, Sun G, Argaw YG, Wong JO, Easwaran S, Montell DJ 2016. CasExpress reveals widespread and diverse patterns of cell survival of caspase-3 activation during development in vivo. eLife 5:e10936
    [Google Scholar]
  28. 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]
  29. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8:8793–800
    [Google Scholar]
  30. Dunn SE, Ehrlich M, Sharp NJ, Reiss K, Solomon G et al. 1998. A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer. Cancer Res 58:153353–61
    [Google Scholar]
  31. Durgan J, Tseng Y-Y, Hamann JC, Domart M-C, Collinson L et al. 2017. Mitosis can drive cell cannibalism through entosis. eLife 6:e27134
    [Google Scholar]
  32. Eckhart L, Lippens S, Tschachler E, Declercq W 2013. Cell death by cornification. Biochim. Biophys. Acta Mol. Cell Res. 1833:123471–80
    [Google Scholar]
  33. Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien C-B et al. 2012. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484:7395546–49
    [Google Scholar]
  34. Elgendy M, Sheridan C, Brumatti G, Martin SJ 2011. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol. Cell 42:123–35
    [Google Scholar]
  35. Elmore S 2007. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35:4495–516
    [Google Scholar]
  36. Ertao Z, Jianhui C, Kang W, Zhijun Y, Hui W et al. 2016. Prognostic value of mixed lineage kinase domain–like protein expression in the survival of patients with gastric cancer. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 37:1013679–85
    [Google Scholar]
  37. Ezaki J, Matsumoto N, Takeda-Ezaki M, Komatsu M, Takahashi K et al. 2011. Liver autophagy contributes to the maintenance of blood glucose and amino acid levels. Autophagy 7:7727–36
    [Google Scholar]
  38. Feig C, Peter ME 2007. How apoptosis got the immune system in shape. Eur. J. Immunol. 37:Suppl. 161–70
    [Google Scholar]
  39. Finn PF, Dice JF 2006. Proteolytic and lipolytic responses to starvation. Nutrition 22:7–8830–44
    [Google Scholar]
  40. Fisher SA, Langille BL, Srivastava D 2000. Apoptosis during cardiovascular development. Circ. Res. 87:10856–64
    [Google Scholar]
  41. Florey O, Kim SE, Sandoval CP, Haynes CM, Overholtzer M 2011. Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat. Cell Biol. 13:111335–43
    [Google Scholar]
  42. Frisch SM, Francis H 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:4619–26
    [Google Scholar]
  43. Frisch SM, Schaller M, Cieply B 2013. Mechanisms that link the oncogenic epithelial-mesenchymal transition to suppression of anoikis. J. Cell Sci. 126:Pt 121–29
    [Google Scholar]
  44. Fuchs Y, Steller H 2011. Programmed cell death in animal development and disease. Cell 147:4742–58
    [Google Scholar]
  45. Fuchslocher Chico J, Saggau C, Adam D 2017. Proteolytic control of regulated necrosis. Biochim. Biophys. Acta Mol. Cell Res. 1864:11, Part B2147–61
    [Google Scholar]
  46. Fung C, Lock R, Gao S, Salas E, Debnath J 2008. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol. Biol. Cell 19:3797–806
    [Google Scholar]
  47. 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]
  48. Giusti C, Tresse E, Luciani M-F, Golstein P 2009. Autophagic cell death: Analysis in Dictyostelium. Biochim. Biophys. . Acta 1793:91422–31
    [Google Scholar]
  49. Gong Y-N, Guy C, Crawford JC, Green DR 2017.a Biological events and molecular signaling following MLKL activation during necroptosis. Cell Cycle 16:191748–60
    [Google Scholar]
  50. Gong Y-N, Guy C, Olauson H, Becker JU, Yang M et al. 2017.b ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell 169:2286–300.e16
    [Google Scholar]
  51. Goundiam O, Nagel M-D, Vayssade M 2012. Akt and RhoA inhibition promotes anoikis of aggregated B16F10 melanoma cells. Cell Biol. Int. 36:3311–19
    [Google Scholar]
  52. Grassian AR, Schafer ZT, Brugge JS 2011. ErbB2 stabilizes epidermal growth factor receptor (EGFR) expression via Erk and Sprouty2 in extracellular matrix–detached cells. J. Biol. Chem. 286:179–90
    [Google Scholar]
  53. Green D, Kroemer G 1998. The central executioners of apoptosis: caspases or mitochondria. ? Trends Cell Biol 8:7267–71
    [Google Scholar]
  54. Grootjans S, Vanden Berghe T, Vandenabeele P 2017. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ 24:71184–95
    [Google Scholar]
  55. Gschwind A, Fischer OM, Ullrich A 2004. The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat. Rev. Cancer 4:5361–70
    [Google Scholar]
  56. Gu Y, Forostyan T, Sabbadini R, Rosenblatt J 2011. Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway. J. Cell Biol. 193:4667–76
    [Google Scholar]
  57. Gu Y, Shea J, Slattum G, Firpo MA, Alexander M et al. 2015. Defective apical extrusion signaling contributes to aggressive tumor hallmarks. eLife 4:e04069
    [Google Scholar]
  58. Guo JY, Chen H-Y, Mathew R, Fan J, Strohecker AM et al. 2011. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 25:5460–70
    [Google Scholar]
  59. Guo JY, Karsli-Uzunbas G, Mathew R, Aisner SC, Kamphorst JJ et al. 2013. Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis. Genes Dev 27:131447–61
    [Google Scholar]
  60. Haenssen KK, Caldwell SA, Shahriari KS, Jackson SR, Whelan KA et al. 2010. ErbB2 requires integrin α5 for anoikis resistance via Src regulation of receptor activity in human mammary epithelial cells. J. Cell Sci. 123:81373–82
    [Google Scholar]
  61. Hanahan D, Weinberg RA 2011. Hallmarks of cancer: the next generation. Cell 144:5646–74
    [Google Scholar]
  62. He W, Wan H, Hu L, Chen P, Wang X et al. 2015. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res 25:121285–98
    [Google Scholar]
  63. Hendley AM, Wang YJ, Polireddy K, Alsina J, Ahmed I et al. 2016. p120 catenin suppresses basal epithelial cell extrusion in invasive pancreatic neoplasia. Cancer Res 76:113351–63
    [Google Scholar]
  64. Ichim G, Lopez J, Ahmed SU, Muthalagu N, Giampazolias E et al. 2015. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol. Cell 57:5860–72
    [Google Scholar]
  65. Jorgensen I, Rayamajhi M, Miao EA 2017. Programmed cell death as a defence against infection. Nat. Rev. Immunol. 17:3151–64
    [Google Scholar]
  66. Kaczmarek A, Vandenabeele P, Krysko DV 2013. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38:2209–23
    [Google Scholar]
  67. Kaiser WJ, Upton JW, Mocarski ES 2013. Viral modulation of programmed necrosis. Curr. Opin. Virol. 3:3296–306
    [Google Scholar]
  68. Kaur J, Debnath J 2015. Autophagy at the crossroads of catabolism and anabolism. Nat. Rev. Mol. Cell Biol. 16:8461–72
    [Google Scholar]
  69. Kay RR 1987. Cell differentiation in monolayers and the investigation of slime mold morphogens. Methods Cell Biol 28:433–48
    [Google Scholar]
  70. Kenis H, Zandbergen HR, Hofstra L, Petrov AD, Dumont EA et al. 2010. Annexin A5 uptake in ischemic myocardium: demonstration of reversible phosphatidylserine externalization and feasibility of radionuclide imaging. J. Nucl. Med. 51:2259–67
    [Google Scholar]
  71. Kerr JF, 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]
  72. Kheloufi M, Boulanger CM, Codogno P, Rautou P-E 2015. Autosis occurs in the liver of patients with severe anorexia nervosa. Hepatology 62:2657–58
    [Google Scholar]
  73. Kim YK, Mbonye U, Hokello J, Karn J 2011. T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J. Mol. Biol. 410:5896–916
    [Google Scholar]
  74. Kim Y-N, Koo KH, Sung JY, Yun U-J, Kim H 2012. Anoikis resistance: an essential prerequisite for tumor metastasis. Int. J. Cell Biol. 2012:306879
    [Google Scholar]
  75. Kolb R, Liu G-H, Janowski AM, Sutterwala FS, Zhang W 2014. Inflammasomes in cancer: a double-edged sword. Protein Cell 5:112–20
    [Google Scholar]
  76. Kraft C, Peter M, Hofmann K 2010. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12:9836–41
    [Google Scholar]
  77. Krajcovic M, Johnson NB, Sun Q, Normand G, Hoover N et al. 2011. A non-genetic route to aneuploidy in human cancers. Nat. Cell Biol. 13:3324–30
    [Google Scholar]
  78. Kroemer G, Mariño G, Levine B 2010. Autophagy and the integrated stress response. Mol. Cell 40:2280–93
    [Google Scholar]
  79. Kroemer G, Perfettini J-L 2014. Entosis, a key player in cancer cell competition. Cell Res 24:111280–81
    [Google Scholar]
  80. Lakhani SA 2006. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311:5762847–51
    [Google Scholar]
  81. Lamouille S, Xu J, Derynck R 2014. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15:3178–96
    [Google Scholar]
  82. Lamy L, Ngo VN, Emre NCT, Shaffer AL, Yang Y et al. 2013. Control of autophagic cell death by caspase-10 in multiple myeloma. Cancer Cell 23:4435–49
    [Google Scholar]
  83. Levayer R, Dupont C, Moreno E 2016. Tissue crowding induces caspase-dependent competition for space. Curr. Biol. 26:5670–77
    [Google Scholar]
  84. Li Y, Sun X, Dey SK 2015. Entosis allows timely elimination of the luminal epithelial barrier for embryo implantation. Cell Rep 11:3358–65
    [Google Scholar]
  85. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC et al. 2000. The combined functions of proapoptotic Bcl-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol. Cell 6:61389–99
    [Google Scholar]
  86. Liu X, He Y, Li F, Huang Q, Kato TA et al. 2015. Caspase-3 promotes genetic instability and carcinogenesis. Mol. Cell 58:2284–96
    [Google Scholar]
  87. 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]
  88. Liu Y, Levine B 2015. Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 22:3367–76
    [Google Scholar]
  89. Liu Y, Shoji-Kawata S, Sumpter RM, Wei Y, Ginet V et al. 2013. Autosis is a Na+,K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. PNAS 110:5120364–71
    [Google Scholar]
  90. Lock R, Kenific CM, Leidal AM, Salas E, Debnath J 2014. Autophagy-dependent production of secreted factors facilitates oncogenic RAS-driven invasion. Cancer Discov 4:4466–79
    [Google Scholar]
  91. Lüthi AU, Martin SJ 2007. The CASBAH: a searchable database of caspase substrates. Cell Death Differ 14:4641–50
    [Google Scholar]
  92. Ma S, Henson ES, Chen Y, Gibson SB 2016. Ferroptosis is induced following siramesine and lapatinib treatment of breast cancer cells. Cell Death Dis 7:7e2307
    [Google Scholar]
  93. Ma Z, Myers DP, Wu RF, Nwariaku FE, Terada LS 2007. p66Shc mediates anoikis through RhoA. J. Cell Biol. 179:123–31
    [Google Scholar]
  94. Malin JA, Kinet MJ, Abraham MC, Blum ES, Shaham S 2016. Transcriptional control of non-apoptotic developmental cell death in C. elegans. . Cell Death Differ 23:121985–94
    [Google Scholar]
  95. Man SM, Karki R, Kanneganti T-D 2017. Molecular mechanisms and functions of pyroptosis, inflammatory caspases and inflammasomes in infectious diseases. Immunol. Rev 277:161–75
    [Google Scholar]
  96. Manic G, Obrist F, Kroemer G, Vitale I, Galluzzi L 2014. Chloroquine and hydroxychloroquine for cancer therapy. Mol. Cell. Oncol. 1:1e29911
    [Google Scholar]
  97. Marshall TW, Lloyd IE, Delalande JM, Näthke I, Rosenblatt J 2011. The tumor suppressor adenomatous polyposis coli controls the direction in which a cell extrudes from an epithelium. Mol. Biol. Cell 22:213962–70
    [Google Scholar]
  98. Martin SJ, Green DR 1995. Protease activation during apoptosis: death by a thousand cuts?. Cell 82:3349–52
    [Google Scholar]
  99. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC et al. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:51545–56
    [Google Scholar]
  100. Mazure NM, Pouysségur J 2009. Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy 5:6868–69
    [Google Scholar]
  101. Meghana C, Ramdas N, Hameed FM, Rao M, Shivashankar GV, Narasimha M 2011. Integrin adhesion drives the emergent polarization of active cytoskeletal stresses to pattern cell delamination. PNAS 108:229107–12
    [Google Scholar]
  102. Morris HR, Taylor GW, Masento MS, Jermyn KA, Kay RR 1987. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. . Nature 328:6133811–14
    [Google Scholar]
  103. Muller PAJ, Vousden KH 2013. p53 mutations in cancer. Nat. Cell Biol. 15:12–8
    [Google Scholar]
  104. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y 2009. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10:7458–67
    [Google Scholar]
  105. Neher JJ, Neniskyte U, Brown GC 2012. Primary phagocytosis of neurons by inflamed microglia: potential roles in neurodegeneration. Front. Pharmacol. 3:27
    [Google Scholar]
  106. Overholtzer M, Mailleux AA, Mouneimne G, Normand G, Schnitt SJ et al. 2007. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 131:5966–79
    [Google Scholar]
  107. Pérez E, Lindblad JL, Bergmann A 2017. Tumor-promoting function of apoptotic caspases by an amplification loop involving ROS, macrophages and JNK in Drosophila. . eLife 6:e26747
    [Google Scholar]
  108. Peterson JS, Timmons AK, Mondragon AA, McCall K 2015. The end of the beginning. Curr. Top. Dev. Biol 114:93–119
    [Google Scholar]
  109. Rabinowitz JD, White E 2010. Autophagy and metabolism. Science 330:60091344–48
    [Google Scholar]
  110. Reginato MJ, Mills KR, Becker EBE, Lynch DK, Bonni A et al. 2005. Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol. Cell. Biol. 25:114591–601
    [Google Scholar]
  111. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T 2011. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ 18:4581–88
    [Google Scholar]
  112. Resnicoff M, Coppola D, Sell C, Rubin R, Ferrone S, Baserga R 1994. Growth inhibition of human melanoma cells in nude mice by antisense strategies to the type 1 insulin-like growth factor receptor. Cancer Res 54:184848–50
    [Google Scholar]
  113. Rogers C, Fernandes-Alnemri T, Mayes L, Alnemri D, Cingolani G, Alnemri ES 2017. Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death. Nat. Commun. 8:14128
    [Google Scholar]
  114. Roos WP, Thomas AD, Kaina B 2015. DNA damage and the balance between survival and death in cancer biology. Nat. Rev. Cancer 16:120–33
    [Google Scholar]
  115. Rosen K, Rak J, Leung T, Dean NM, Kerbel RS, Filmus J 2000. Activated ras prevents downregulation of Bcl-XL triggered by detachment from the extracellular matrix: a mechanism of ras-induced resistance to anoikis in intestinal epithelial cells. J. Cell Biol. 149:2447–56
    [Google Scholar]
  116. Rosenblatt J, Raff MC, Cramer LP 2001. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr. Biol. 11:231847–57
    [Google Scholar]
  117. Ruan J, Mei L, Zhu Q, Shi G, Wang H 2015. Mixed lineage kinase domain–like protein is a prognostic biomarker for cervical squamous cell cancer. Int. J. Clin. Exp. Pathol. 8:1115035–38
    [Google Scholar]
  118. Sahai E, Marshall CJ 2002. RHO-GTPases and cancer. Nat. Rev. Cancer 2:2133–42
    [Google Scholar]
  119. Salvesen GS, Ashkenazi A 2011. Snapshot: caspases. Cell 147:2476.e1
    [Google Scholar]
  120. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S et al. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6:121221–28
    [Google Scholar]
  121. Silva MT, do Vale A, dos Santos NMN 2008. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis Int. J. Program. Cell Death 13:4463–82
    [Google Scholar]
  122. Simpson CD, Anyiwe K, Schimmer AD 2008. Anoikis resistance and tumor metastasis. Cancer Lett 272:2177–85
    [Google Scholar]
  123. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I et al. 2009. Autophagy regulates lipid metabolism. Nature 458:72421131–35
    [Google Scholar]
  124. Slattum G, Gu Y, Sabbadini R, Rosenblatt J 2014. Autophagy in oncogenic K-Ras promotes basal extrusion of epithelial cells by degrading S1P. Curr. Biol. 24:119–28
    [Google Scholar]
  125. Slattum G, McGee KM, Rosenblatt J 2009. P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J. Cell Biol. 186:5693–702
    [Google Scholar]
  126. Slattum GM, Rosenblatt J 2014. Tumour cell invasion: an emerging role for basal epithelial cell extrusion. Nat. Rev. Cancer 14:7495–501
    [Google Scholar]
  127. Strilic B, Yang L, Albarrán-Juárez J, Wachsmuth L, Han K et al. 2016. Tumour-cell-induced endothelial cell necroptosis via death receptor 6 promotes metastasis. Nature 536:7615215–18
    [Google Scholar]
  128. Sun G, Guzman E, Balasanyan V, Conner CM, Wong K et al. 2017. A molecular signature for anastasis, recovery from the brink of apoptotic cell death. J. Cell Biol. 216:103355–68
    [Google Scholar]
  129. Sun G, Montell DJ 2017. Q&A: Cellular near death experiences—what is anastasis. ? BMC Biol 15:192
    [Google Scholar]
  130. Sun L, Wang H, Wang Z, He S, Chen S et al. 2012. Mixed lineage kinase domain–like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148:1–2213–27
    [Google Scholar]
  131. Sun Q, Cibas ES, Huang H, Hodgson L, Overholtzer M 2014. Induction of entosis by epithelial cadherin expression. Cell Res 24:111288–98
    [Google Scholar]
  132. Tait SWG, Green DR 2008. Caspase-independent cell death: leaving the set without the final cut. Oncogene 27:506452–61
    [Google Scholar]
  133. Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y 1992. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119:2301–11
    [Google Scholar]
  134. Tang HL, Tang HM, Mak KH, Hu S, Wang SS et al. 2012. Cell survival, DNA damage, and oncogenic transformation after a transient and reversible apoptotic response. Mol. Biol. Cell 23:122240–52
    [Google Scholar]
  135. Taylor RC, Cullen SP, Martin SJ 2008. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9:3231–41
    [Google Scholar]
  136. Thi HTH, Hong S 2017. Inflammasome as a therapeutic target for cancer prevention and treatment. J. Cancer Prev. 22:262–73
    [Google Scholar]
  137. Tracy K, Baehrecke EH 2013. The role of autophagy in Drosophila metamorphosis. Curr. Top. Dev. Biol. 103:101–25
    [Google Scholar]
  138. Vanlangenakker N, Vanden Berghe T, Vandenabeele P 2012. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 19:175–86
    [Google Scholar]
  139. Vaux DL 2002. Apoptosis timeline. Cell Death Differ 9:4349–54
    [Google Scholar]
  140. Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J et al. 2015. Immune evasion in cancer: mechanistic basis and therapeutic strategies. Semin. Cancer Biol. 35:S185–98
    [Google Scholar]
  141. Wang H, Sun L, Su L, Rizo J, Liu L et al. 2014. Mixed lineage kinase domain–like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54:1133–46
    [Google Scholar]
  142. Weigel KJ, Jakimenko A, Conti BA, Chapman SE, Kaliney WJ et al. 2014. CAF-secreted IGFBPs regulate breast cancer cell anoikis. Mol. Cancer Res. 12:6855–66
    [Google Scholar]
  143. Weinlich R, Oberst A, Beere HM, Green DR 2017. Necroptosis in development, inflammation and disease. Nat. Rev. Mol. Cell Biol. 18:2127–36
    [Google Scholar]
  144. Whelan KA, Schwab LP, Karakashev SV, Franchetti L, Johannes GJ et al. 2013. The oncogene HER2/neu (ERBB2) requires the hypoxia-inducible factor HIF-1 for mammary tumor growth and anoikis resistance. J. Biol. Chem. 288:2215865–77
    [Google Scholar]
  145. White E 2012. Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer 12:6401–10
    [Google Scholar]
  146. Willingham SB, Volkmer J-P, Gentles AJ, Sahoo D, Dalerba P et al. 2012. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. PNAS 109:176662–67
    [Google Scholar]
  147. Xie C, Ginet V, Sun Y, Koike M, Zhou K et al. 2016. Neuroprotection by selective neuronal deletion of Atg7 in neonatal brain injury. Autophagy 12:2410–23
    [Google Scholar]
  148. Xie Y, Hou W, Song X, Yu Y, Huang J et al. 2016. Ferroptosis: process and function. Cell Death Differ 23:3369–79
    [Google Scholar]
  149. Yamaki N, Negishi M, Katoh H 2007. RhoG regulates anoikis through a phosphatidylinositol 3-kinase-dependent mechanism. Exp. Cell Res. 313:132821–32
    [Google Scholar]
  150. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA et al. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:7927–39
    [Google Scholar]
  151. Yang S, Wang X, Contino G, Liesa M, Sahin E et al. 2011. Pancreatic cancers require autophagy for tumor growth. Genes Dev 25:7717–29
    [Google Scholar]
  152. Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R et al. 2014. Regulation of ferroptotic cancer cell death by GPX4. Cell 156:1–2317–31
    [Google Scholar]
  153. Yip KW, Reed JC 2008. Bcl-2 family proteins and cancer. Oncogene 27:506398–406
    [Google Scholar]
  154. Yoo BH, Wang Y, Erdogan M, Sasazuki T, Shirasawa S et al. 2011. Oncogenic ras-induced down-regulation of pro-apoptotic protease caspase-2 is required for malignant transformation of intestinal epithelial cells. J. Biol. Chem. 286:4538894–903
    [Google Scholar]
  155. 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]
  156. Yu M, Ting DT, Stott SL, Wittner BS, Ozsolak F et al. 2012. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 487:7408510–13
    [Google Scholar]
  157. Zargarian S, Shlomovitz I, Erlich Z, Hourizadeh A, Ofir-Birin Y et al. 2017. Phosphatidylserine externalization, “necroptotic bodies” release, and phagocytosis during necroptosis. PLOS Biol 15:6e2002711
    [Google Scholar]
  158. Zhang J, Yang Y, He W, Sun L 2016. Necrosome core machinery: MLKL. Cell. Mol. Life Sci. 73:11–122153–63
    [Google Scholar]
  159. Zhu S, Zhang Q, Sun X, Zeh HJ, Lotze MT et al. 2017. HSPA5 regulates ferroptotic cell death in cancer cells. Cancer Res 77:82064–77
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100616-060748
Loading
/content/journals/10.1146/annurev-cellbio-100616-060748
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error