Switch between apoptosis and autophagy: Radiation-induced endoplasmic reticulum stress?

Cell Cycle

Volumn 6, Issue 7, 2007, Pages 793-798

  Moretti, Luigi ^a   Cha, Yong I ^a   Niermann, Kenneth John ^a   Lu, Bo ^a,b  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Apoptosis; Autophagy; Cancer cell death; ER stress; mTOR; Radiation

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

APOPTOSIS; AUTOPHAGY; CANCER RADIOTHERAPY; CELL ACTIVATION; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; HUMAN; PHAGOSOME; REVIEW;

EID: 34147141497     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.7.4036     Document Type: Review

References (87)

1. Sellins KS, Cohen JJ. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J Immun 1987; 139:3199-206.
2. Ameisen JC. On the origin, evolution, and nature of programmed cell death: A timeline of four billion years. Cell Death Differ 2002; 9:367-93.
3. Baehrecke EH. How death shapes life during development. Nat Rev Mol Cell Biol 2002; 3:779-87.
4. Reggiori F, Klionsky DJ. Autophagosomes: Biogenesis from scratch? Curr Opin Cell Biol 2005; 17:415-22.
5. Edinger AL, Thompson CB. Death by design: Apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004; 16:663-9.
6. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 1993; 362:847-849.
7. Held KD. Radiation-induced apoptosis and its relationship to loss of clonogenic survival. Apoptosis 1997; 2:265-82.
8. Rudner J, Belka C, Marini P, Wagner RJ, Faltin H, Lepple-Wienhues A, Bamberg M, Budach W. Radiation sensitivity and apoptosis in human lymphoma cells. Int J Radiat Biol 2001; 77:1-11.
9. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, Hooper ML, Wyllie AH. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 1993; 362:849-852.
10. Brown JM, Wouters BG. Apoptosis, p53, and tumor cell sensitivity to anticancer agents. Cancer Res 1999; 59:1391-99.
11. Sartorius U, Schmitz I, Krammer PH. Molecular mechanisms of death-receptor-mediated apoptosis. Chembiochem 2001; 2:20-29.
12. Denault JB, Salvesen GS. Caspases: Keys in the ignition of cell death. Chem Rev 2002; 102:4489-500.
13. Baker SJ, Reddy EP. Modulation of life and death by the TNF receptor superfamily. Oncogene 1998; 17:3261-270.
14. Tartaglia LA, Rothe M, Hu YF, Goeddel DV. Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor. Cell 1993; 73:213-216.
15. Baud V, Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001; 11:372-7.
16. Verheij M, Bartelink H. Radiation-induced apoptosis. Cell Tissue Res 2000; 301:133-142.
17. Kim KW, Mutter RW, Cao C, Albert JM, Freeman M, Hallahan DE, Lu B. Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J Biol Chem 2006; 281:36883-90.
18. Nicholson KM, Anderson NG. The protein kinase B/Akt signaling pathway in human malignancy. Cell Signal 2002; 14:381-95.
19. Majumder P, Sellers W. Akt-regulated pathways in prostate cancer. Oncogene 2005; 24:7465-74.
20. McMenamin ME, Soung P, Perera S, Kaplan I, Loda M, Sellers WR. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res 1999; 59:4291-6.
21. Rasheed BK, Stenzel TT, McLendon RE, Parsons R, Friedman AH, Friedman HS, Bigner DD, Bigner SH. PTEN gene mutations are seen in high-grade but not in low-grade gliomas. Cancer Res 1997; 57:4187-90.
22. Shinohara ET, Cao C, Niermann K, Mu Y, Zeng F, Hallahan DE, Lu B. Nhanced radiation damage of tumor vasculature by mTOR inhibitors. Oncogene 2005; 24:5414-22.
23. Cao C, Subhawong T, Albert JM, Kim KW, Geng L, Sekhar KR, Gi YJ, Lu B. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 2006; 66:10040-47.
24. Harding HP, Calfon M, Urano F, Novoa I, Ron D. Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol 2002; 18:575-599.
25. Sidrauski C, Chapman R, Walter P. The unfolded protein response: An intracellular signaling pathway with many surprising features. Trends Cell Biol 1998; 8:245-249.
26. Rutkowski DT, Kaufman RJ. A trip to the ER: Coping with stress. Trends Cell Biol 2004; 14:20-28.
27. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 2006; 281:30299-304.
28. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem 2000; 69:217-245.
29. Ferrari D, Pinton P, Szabadkai G, Chami M, Campanella M, Pozzan T, Rizzuto R. Endoplasmic reticulum, Bcl-2 and Ca2+ handling in apoptosis. Cell Calcium 2002; 32:413-420.
30. Green DR, Evan GI. A matter of life and death. Cancer Cell 2002; 1:19-30.
31. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003; 22:8608-618.
32. Hajnoczky G, Davies E, Madesh M. Calcium signaling and apoptosis. Biochem Biophys Res Commun 2003; 304:445-54.
33. Ferri KF, Kroemer G. Organelle-specific initiation of cell death pathways. Nat Cell Biol 2001; 3:E255-263.
34. Danial NN, Korsmeyer SJ. Cell death: Critical control points. Cell 2004; 116:205-19.
35. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000; 5:897-904.
36. Liu CY, Schroder M, Kaufman RJ. Ligand-dependent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 2000; 275:24881-885.
37. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998; 12:982-95.
38. Matsumoto M, Minami M, Takeda K, Sakao Y, Akira S. Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett 1996; 395:143-147.
39. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bc12 and perturbing the cellular redox state. Mol Cell Biol 2001; 21:1249-59.
40. Cnop M, Ladriere L, Hekerman P, Ortis F, Cardozo AK, Dogusan Z, Flamez D, Boyce M, Yuan J, Eizirik DL. Selective inhibition of eukaryotic translation initiation factor 2α dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic β-cell dysfunction and apoptosis. J Biol Chem 2007; 282:3989-97.
41. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J Cell Biol 2001; 153:1011-22.
42. Brush MH, Weiser DC, Shenolikar S. Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Mol Cell Biol 2003; 23:1292-1303.
43. Adler HT, Chinery R, Wu DY, Kussick Jr S, Payne JM, Fornace Jr AJ, Tkachuk DC. Leukemic HX fusion proteins inhibit GADD34-induced apoptosis and associate with the GADD34 and hNF5/INI1 proteins. Mol Cell Biol 1999; 19:7050-7060.
44. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 2004; 18:3066-77.
45. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 2005; 307:935-939.
46. Boya P, Cohen I, Zamzami N, Vieira HL, Kroemer G. Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ 2002; 9:465-7.
47. Hacki J, Egger L, Monney L, Conus S, Rosse T, Fellay I, Borner C. Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 2000; 19:2286-95.
48. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003; 162:59-69.
49. Scheuner D, Patel R, Wang F, Lee K, Kumar K, Wu J, Nilsson A, Karin M, Kaufman RJ. Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 2006; 281:21458-68.
50. 2+ fluxes to inhibit apoptosis in thapsigargin- and glucocorticoid-treated mouse lymphoma cells. Cell Calcium 1996; 19:473-483.
51. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 2001; 292:727-730.
52. Boyce M, Yuan J. Cellular response to endoplasmic reticulum stress: A matter of life or death. Cell Death Differ 2006; 13:363-73.
53. Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 1998; 17:5708-5717.
54. Kharbanda S, Ren R, Pandey P, Shafman TD, Feller SM, Weichselbaum RR, Kufe DW. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 1995; 376:785-788.
55. Chen YR, Meyer CF, Tan TH. Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in gamma radiation-induced apoptosis. J Biol Chem 1996; 271:631-34.
56. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000; 287:664-666.
57. Nishitoh H, Saitoh M, Mochida Y, Takeda K, Nakano H, Rothe M, Miyazono K, Ichijo H. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 1998; 2:389-395.
58. Hatai T, Matsuzawa A, Inoshita S, Mochida Y, Kuroda T, Sakamaki K, Kuida K, Yonehara S, Ichijo H, Takeda K. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J Biol Chem 2000; 275:26576-581.
59. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002; 16:1345-55.
60. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000; 103:239-252.
61. Morishima N, Nakanishi K, Tsuchiya K, Shibata T, Seiwa E. Translocation of Bim to the ER mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J Biol Chem 2004; 279:50375-381.
62. Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 2003; 100:2432-2437.
63. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1α. Science 2006; 312:572-576.
64. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001; 276:13935-40.
65. Mori K, Kawahara T, Yoshida H, Yanagi H, Yura T. Signaling from endoplasmic reticulum to nucleus: Transcription factor with a basic-leucine zipper motif is required for unfolded protein-response pathway. Genes Cells 1996; 1:803-17.
66. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739-789.
67. Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 1998; 17:5708-17.
68. McCullough KD, Martindale JK, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21:1249-59.
69. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M, Mori K. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 2000; 20:6755-6767.
70. Nakanishi K, Sudo T, Morishima N. Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. J Cell Biol 2005; 169:555-60.
71. 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 2000; 403:98-103.
72. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families: Activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000; 150:887-94.
73. Momoi T. Caspases involved in ER stress-mediated cell death. J Chem Neuroanat 2004; 28:101-105.
74. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An ER stress-specific caspase cascade in apoptosis: Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002; 277:34287-94.
75. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM. Coupling ER stress to the cell death program: An Apaf-1-independent intrinsic pathway. J Biol Chem 2002; 277:21836-42.
76. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplasmic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001; 276:13935-940.
77. Strasser A, Puthalakath H, Bouillet P, Huang DC, O'Connor L, O'Reilly LA, Cullen L, Cory S, Adams JM. The role of bim, a proapoptotic BH3-only member of the Bcl-2 family in cell-death control. Ann N Y Acad Sci 2000; 917:541-8.
78. Zong WA, Li C, Hatzivassilion G, Lmdrtem T, Yu QC, Yuan I, Thompson CB. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003; 162:59-69.
79. Annis MG, Yethon JA, Leber B, Andrews DW. There is more to life and death than mitochondria: Bcl-2 proteins at the endoplasmic reticulum. Biochim Biophys Acta 2004; 1644:115-23.
80. Wood DE, Thomas A, Devi LA, Berman Y, Beavis RC, Reed JC, Newcomb EW. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 1998; 17:1069-78.
81. Choi WS, Lee EH, Chung CW, Jung YK, Jin BK, Kim SU, Oh TH, Saido TC, Oh YJ. Cleavage of Bax is mediated by caspase-dependent or -independent calpain activation in dopaminergic neuronal cells: Protective role of Bcl-2. J Neurochem 2001; 77:1531-41.
82. Groenendyk J, Michalak M. Endoplasmic reticulum quality control and apoptosis. Acta Biochim Pol 2005; 52:381-95.
83. Novikoff A, Shin WY. Endoplasmic reticulum and autophagy in rat hepatocytes. Proc Natl Acad Sci USA 1978; 75:5039-5502.
84. Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct 2002; 27:421-429.
85. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T. ER stress (PERK/eIF2αlpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007; 14:230-9.
86. Talloczy Z, Jiang W, Virgin IVth HW, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B. Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway. Proc Natl Acad Sci USA 2002; 99:190-5.
87. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26:9220-31.