The apoptosis-necrosis continuum: Insights from genetically altered mice

Veterinary Pathology

Volumn 40, Issue 5, 2003, Pages 481-495

  Zeiss, C J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Caspase; Knockout; Mice; Necrosis

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE; CATHEPSIN B;

APOPTOSIS; CELL DEATH; CELL STRUCTURE; CHEMICAL ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC CODE; KNOCKOUT MOUSE; NECROSIS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TRANSGENICS; ANIMAL; GENETICS; MITOCHONDRION; MOUSE; MOUSE MUTANT; PHYSIOLOGY;

ANIMALIA; MUS MUSCULUS;

ANIMALS; APOPTOSIS; CASPASES; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NECROSIS;

EID: 0642375240     PISSN: 03009858     EISSN: None     Source Type: Journal    
DOI: 10.1354/vp.40-5-481     Document Type: Review

References (98)

1. Belloc F, Belaud-Rotureau MA, Lavignolle V, Bascans E, Braz-Pereira E, Durrieu F, Lacombe F.: Flow cytometry detection of caspase-3 activation in pre-apoptotic leukemic cells. Cytometry 40(2):151-160, 2000
2. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JC, Hara H, Moskowitz MA, Li E, Greenburg A, Tilly JL, Yuan J.: Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 12(9):1304-1314, 1998
3. Blagosklonny MV: Cell death beyond apoptosis. Leukemia 14(8):1502-1508, 2000
4. Boot-Handford RP, Michaelidis TM, Hillarby MC, Zambelli A, Denton J, Hoyland JA, Freemont AJ, Grant ME, Wallis GA.: The bcl-2 knockout mouse exhibits marked changes in osteoblast phenotype and collagen deposition in bone as well as a mild growth plate phenotype. Int J Exp Pathol 79:329-335, 1998
5. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X: Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15:269-290, 1999
6. Bursch W: The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 8(6):569-581, 2001
7. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N, Kroemer G.: Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 84(2, 3):215-222, 2002
8. Chautan M, Chazal G, Cecconi F, Gruss P, Golstein P: Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 9(17):967-970, 1999
9. Chen G, Goeddel DV: TNFR I signaling: a beautiful pathway. Science 296(5573):1634-1635, 2002
10. Chen J, Flannery JG, LaVail MM, Steinberg RH, Xu J, Simon MI: Bcl-2 overexpression reduces apoptotic photoreceptor cell death in three different retinal degenerations. Proc Natl Acad Sci USA 93(14):7042-7047, 1996
11. Chung S, Gumienny TL, Hengartner MO, Driscoll M: A common set of engulfment genes mediates removal of both apoptotic and necrotic cell corpses in C. elegans. Nat Cell Biol 2(12):931-937, 2000
12. Clarke PG: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181(3):195-213, 1990
13. Conway EM, Pollefeyt S, Steiner-Mosonyi M, Luo W, Devriese A, Lupu F, Bono F, Leducq N, Dol F, Schaeffer P, Collen D, Herbert JM.: Deficiency of Survivin in transgenic mice exacerbates Fas-induced apoptosis via mitochondrial pathways. Gastroenterology 123(2):619-631, 2002
14. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, Yu SW, Dawson TM, Dawson VL, Park DS, Kroemer G, Slack RS.: Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 158(3):507-517, 2002
15. Denecker G, Vercammen D, Declercq W, Vandenabeele P: Apoptotic and necrotic cell death induced by death domain receptors. Cell Mol Life Sci 58(3):356-370, 2001
16. Dini L, Ruzittu MT, Falasca L: Recognition and phagocytosis of apoptotic cells. Scanning Microsc 10(1):239-251, 1996
17. Eguchi Y, Srinivasan A, Tomaselli KJ, Shimizu S, Tsujimoto Y: ATP-dependent steps in apoptotic signal transduction. Cancer Res 59(9):2174-2181, 1999
18. Erickson SL, de Sauvage FJ, Kikly K, Carver-Moore K, Pitts-Meek S, Gillett N, Sheehan KC, Schreiber RD, Goeddel DV, Moore MW.: Decreased sensitivity to tumour-necrosis factor but normal T-cell development in TNF receptor-2-deficient mice. Nature 372(6506):560-563, 1994
19. Esposti MD: The roles of Bid. Apoptosis 7(5):433-440, 2002
20. Eversole-Cire P, Concepcion FA, Simon MI, Takayama S, Reed JC, Chen J: Synergistic effect of Bcl-2 and BAG-1 on the prevention of photoreceptor cell death. Invest Ophthalmol Vis Sci 41(7):1953-1961, 2000
21. Fan H, Favero M, Vogel MW: Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells. J Comp Neurol 436:82-91, 2001
22. Flemming W: Uber die bildung von richtungsfiguren in saugthiereiern bein untergang graaf'scher follikel. Arch Anat Physiol 221-244, 1885
23. Gotz R: Regulation of neuronal cell death and differentiation by NGF and IAP family members. J Neural Transm 60(Suppl)60: 247-259, 2000
24. Guicciardi ME, Miyoshi H, Bronk SF, Gores GJ: Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am J Pathol 159(6):2045-2054, 2001
25. Harlin H, Reffey SB, Duckett CS, Lindsten T, Thompson CB: Characterization of X-Iap-deficient mice. Mol Cell Biol 10:3604-3608, 2001
26. Hengartner MO: The biochemistry of apoptosis. Nature 407(6805):770-776, 2000
27. Hirsch T, Marchetti P, Susin SA, Dallaporta B, Zamzami N, Marzo I, Geuskens M, Kroemer G.: The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15(13):1573-1581, 1997
28. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J.: Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1(6):489-495, 2000
29. Joza N, Kroemer G, Penninger JM: Genetic analysis of the mammalian cell death machinery. Trends Genet 18(3):142-149, 2002
30. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T: Bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation and distorted small intestine. Cancer Res 55:354-359, 1995
31. Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P: The death domain kinase RIP mediates the TNF-induced NF-kappa B signal. Immunity 8:297-303, 1998
32. Kerr JF: Shrinkage necrosis: a distinct mode of cellular death. J Pathol 105(1):13-20, 1971
33. Kerr JF, Wyllie AH, Currie AR: Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239-257, 1972
34. Kim GM, Xu J, Xu J, Song SK, Yan P, Ku G, Xu XM, Hsu CY.: Tumor necrosis factor receptor deletion reduces NF-kappa B activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J Neurosci 21(17):6617-6625, 2001
35. Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN, Bronson RT, Ackerman SL.: The harlequin mouse mutation down-regulates apoptosis-inducing factor. Nature 419(6905):367-374, 2002
36. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ: Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99, 1995
37. Kok YJ, Swe M, Sit KH: Necrosis has orderly DNA fragmentations. Biochem Biophys Res Commun 294(5): 934-999, 2002
38. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA.: Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase-9. Cell 94(3):325-337, 1998
39. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA.: Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267(5206):2000-2003, 1995
40. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA: Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384(6607):368-372, 1996
41. Laster SM, Wood JG, Gooding LR: Tumor necrosis factor can induce both apoptotic and necrotic forms of cell lysis. J Immunol 141(8):2629-2634, 1988
42. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P: Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185(8):1481-1486, 1997
43. Leonard JR, Klocke BJ, D'Sa C, Flavell RA, Roth KA: Strain-dependent neurodevelopmental abnormalities in caspase-3-deficient mice. J Neuropathol Exp Neurol 61(8):673-677, 2002
44. Li K, Li Y, Shelton JM, Richardson JA, Spencer E, Chen ZJ, Wang X, Williams RS.: Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 101(4):389-399, 2000
45. Locksley RM, Killeen N, Lenardo MJ: The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104(4):487-501, 2001
46. Majno G, Joris I: Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146(1):3-15, 1995
47. Matsumura H, Shimizu Y, Ohsawa Y, Kawahara A, Uchiyama Y, Nagata S: Necrotic death pathway in Fas receptor signaling. J Cell Biol 151(6):1247-1256, 2000
48. McCurrach ME, Shu HB, Elia AJ, Yeh WC, Pompa JL: FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954-1958, 1998
49. Michaelidis TM, Sendtner M, Cooper JD, Airaksinen MS, Holtmann B: Inactivation of Bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 17:75-89, 1996
50. Mosinger Ogilvie J, Deckwerth TL, Knudson CM, Korsmeyer SJ.: Suppression of developmental retinal cell death but not of photoreceptor degeneration in Bax-deficient mice. Invest Ophthalmol Vis Sci 39:1713-1721, 1998
51. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, Loh DY.: Massive cell death of immature hematopoietic cells and neurons in Bcl-X-deficient mice. Science 267:1506-1510, 1995
52. Naito A, Azuma S, Tanaka S, Miyazaki T, Takaki S, Takatsu K, Nakao K, Nakamura K, Katsuki M, Yamamoto T, Inoue J.: Severe osteopetrosis, defective interleukin-1 signaling and lymph node organogenesis in Traf-6-deficient mice. Genes Cells Jun 4:353-362, 1999
53. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J.: Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403(6765):98-103, 2000
54. Nakano H, Sakon S, Koseki H, Takemori T, Tada K, Matsumoto M, Munechika E, Sakai T, Shirasawa T, Akiba H, Kobata T, Santee SM, Ware CF, Rennert PD, Taniguchi M, Yagita H, Okumura K.: Targeted disruption of Traf-5 gene causes defects in CD40-and CD27-mediated lymphocyte activation. Proc Natl Acad Sci USA 96: 9803-9808, 1999.
55. Nakayama K, Nakayama K, Negishi I, Kuida K, Sawa H: Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci USA 91:3700-3704, 1994
56. Nambu H, Yuge K, Shikata N, Tsubura A, Matsuzawa A: Fas-independent apoptosis of photoreceptor cells in C3H mice. Exp Anim 45(4):309-315, 1996
57. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju AM, Smulson ME, Yamin T-T, Yu VL, Miller DK.: Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376(6535):37-43, 1995
58. Nicotera P: Apoptosis and age-related disorders: role of caspase-dependent and caspase-independent pathways. Toxicol Lett 127(1-3):189-195, 2002
59. Nicotera P, Leist M, Ferrando-May E: Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett 102, 103:139-142, 1998
60. Okada H, Suh WK, Jin J, Woo M, Du C, Elia A, Duncan GS, Wakeham A, Itie A, Lowe SW, Wang X, Mak TW.: Generation and characterization of Smac/DIABLO-deficient mice. Mol Cell Biol 22(10):3509-3517, 2002
61. Oppenheim RW, Flavell RA, Vinsant S, Prevette D, Kuan CY, Rakic P: Programmed cell death of developing mammalian neurons after genetic deletion of caspases. J Neurosci 21(13):4752-4760, 2001
62. Paweletz N, Walther Flemming: pioneer of mitosis research. Nat Rev Mol Cell Biol 2(1):72-75, 2001
63. Pepper C, Thomas A, Tucker H, Hoy T, Bentley P. Flow cytometric assessment of three different methods for the measurement of in vitro apoptosis. Leuk Res 22(5):439-444, 1998
64. Portera-Cailliau C, Price DL, Martin LJ: Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 378(1):70-87, 1997
65. Raffray M, Cohen GM: Apoptosis and necrosis in toxicology: a continuum or distinct modes of cell death? Pharmacol Ther 75(3):153-177, 1997
66. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM.: Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 277(24):21836-21842, 2002
67. Reed JC: The Survivin saga goes in vivo. J Clin Invest 108(7):965-999, 2001
68. Rosenfeld ME, Prichard L, Shiojiri N, Fausto N: Prevention of hepatic apoptosis and embryonic lethality in RelA/TNFR I double knockout mice. Am J Pathol 156(3):997-1007, 2000
69. Rothe J, Lesslauer W, Lotscher H, Lang Y, Koebel P, Kontgen F, Althage A, Zinkernagel R, Steinmetz M, Bluethmann H.: Mice lacking the tumour necrosis factor receptor I are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364:798-802, 1993
70. Roy M, Sapolsky R: Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? Trends Neurosci 22(10):419-422, 1999
71. Rudolph D, Yeh WC, Wakeham A, Rudolph B, Nallainathan D, Potter J, Elia AJ, Mak TW.: Severe liver degeneration and lack of NF-kappaB activation in NEMO/ IKKgamma-deficient mice. Genes Dev 14(7):854-862, 2000
72. Saraste A, Pulkki K: Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45(3):528-537, 2000
73. Schmidt-Supprian M, Bloch W, Courtois G, Addicks K, Israel A, Rajewsky K, Pasparakis M.: Nemo/IKK gamma-deficient mice model incontinentia pigmenti. Mol Cell 5(6):981-992, 2000
74. Schreyer SA, Peschon JJ, LeBoeuf RC: Accelerated atherosclerosis in mice lacking tumor necrosis factor receptor p55. J Biol Chem 271:26174-26178, 1996
75. Shiels H, Li X, Schumacker PT, Maltepe E, Padrid PA, Sperling A, Thompson CB, Lindsten T.: Traf-4 deficiency leads to tracheal malformation with resulting alterations in air flow to the lungs. Am J Pathol 157:679-688, 2000
76. Shindler KS, Latham CB, Roth KA: Bax deficiency prevents the increased cell death of immature neurons in Bcl-X-deficient mice. J Neurosci 17:3112-3119, 1997
77. Slee EA, Harte MT, Kluck RM, Wolfe BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ.: Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144(2):281-292, 1999
78. Sperandio S, de Belle I, Bredesen DE: An alternative, non-apoptotic form of programmed cell death. Proc Natl Acad Sci USA 97(26):14376-14381, 2000
79. Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 281(5381):1312-1316, 1998
80. Tsitsikov EN, Laouini D, Dunn IF, Sannikova TY, Davidson L, Alt FW, Geha RS.: TRAF1 is a negative regulator of TNF signaling. Enhanced TNF signaling in Traf-1-deficient mice. Immunity 15(4):647-657, 2001
81. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Arraham KB, Goncharov T, Holtmann H, Lonai P, Wallach D.: Targeted disruption of the mouse caspase-8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9(2):267-276, 1998
82. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P.: Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187(9):1477-1485, 1998
83. Wajant H: The Fas signaling pathway: more than a paradigm. Science 296(5573):1635-1636, 2002
84. Wang J, Lenardo MJ. Roles of caspases in apoptosis, development, and cytokine maturation revealed by homozygous gene deficiencies. J Cell Sci 113(Pt 5):753-757, 2000
85. Wang S, Miura M, Jung YK, Zhu H, Li E, Yuan J: Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92(4):501-509, 1998
86. Watanabe D, Suda T, Hashimoto H, Nagata S: Constitutive activation of the Fas ligand gene in mouse lymphoproliferative disorders. EMBO J 14:12-18, 1995
87. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S: Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356:314-317, 1992
88. Woo M, Hakem R, Mak TW: Executionary pathway for apoptosis: lessons from mutant mice. Cell Res 10(4): 267-278, 2000
89. Xiang J, Chao DT, Korsmeyer SJ: BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc Natl Acad Sci USA 93(25): 14559-14563, 1996
90. Xu Y, Cheng G, Baltimore D: Targeted disruption of TRAF3 leads to postnatal lethality and defective T-dependent immune responses. Immunity 5:407-415, 1996
91. Yeh WC, Hakem R, Woo M, Mak TW: Gene targeting in the analysis of mammalian apoptosis and TNF receptor superfamily signaling. Immunol Rev 169:283-302, 1999
92. Yeh W-C, Itie A, Elia AJ, Ng M, Shu H-B: Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12:633-642, 2000
93. Yeh WC, Shahinian A, Speiser D, Kraunus J, Billia F, Wakeham A, de la Pompa JL, Ferrick D, Hum B, Iscove N, Ohashi P, Rothe M, Goeddel DV, Mak TW.: Early lethality, functional NF-kappa B activation, and increased sensitivity to TNF-induced cell death in Traf-2-deficient mice. Immunity 7:715-725, 1997
94. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B, Roth KA, Korsmeyer SJ.: Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400:886-891, 1999
95. Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, Mak TW.: Apaf-1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750, 1998
96. Zamzami N, Hirsch T, Dallaporta B, Petit PX, Kroemer G: Mitochondrial implication in accidental and programmed cell death: apoptosis and necrosis. J Bioenerg Biomembr 29(2):185-193, 1997
97. Zheng TS, Flavell RA: Divinations and surprises: genetic analysis of caspase function in mice. Exp Cell Res 256(1):67-73, 2000
98. Zheng TS, Hunot S, Kuida K, Flavell RA: Caspase knockouts: matters of life and death. Cell Death Differ 6(11):1043-1053, 1999