Cell death by autophagy: Emerging molecular mechanisms and implications for cancer therapy

Oncogene

Volumn 34, Issue 40, 2015, Pages 5105-5113

  Fulda, S ^a,b   Kogel D ^c  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 3 (1 NAPHTHOYL) 1 PROPYLINDOLE; ATG PROTEIN; BETULIC ACID; BH3 PROTEIN; CASPASE 10; CHLOROQUINE; DAPORINAD; DEXAMETHASONE; ENDOPHILIN; GOSSYPOL; HISTONE DEACETYLASE INHIBITOR; LAPATINIB; MICRORNA 101; OBATOCLAX; PROTEIN BCL 2; RESVERATROL; TEMOZOLOMIDE; TETRAHYDROCANNABINOL; UNCLASSIFIED DRUG; VORINOSTAT; ANTINEOPLASTIC AGENT;

AUTOPHAGY; B CELL LYMPHOMA; BREAST CARCINOMA; CANCER RESISTANCE; CANCER THERAPY; CELL DEATH; CELL SURVIVAL; CHONDROSARCOMA; CHRONIC MYELOID LEUKEMIA; COLON CARCINOMA; GLIOBLASTOMA; GLIOMA; LIVER CELL CARCINOMA; LYSOSOME MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROSTATE CARCINOMA; REVIEW; STRESS; UTERINE CERVIX CARCINOMA; ANIMAL; DRUG EFFECTS; HUMAN; NEOPLASMS; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; HUMANS; NEOPLASMS;

EID: 84943199868     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.458     Document Type: Review

References (76)

1. Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407: 770-776.
2. Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005; 11: 725-730.
3. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19: 107-120.
4. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta 2013; 1833: 3448-3459.
5. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-257.
6. Marino G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 2014; 15: 81-94.
7. Rami A, Kogel D. Apoptosis meets autophagy-like cell death in the ischemic penumbra: two sides of the same coin? Autophagy 2008; 4: 422-426.
8. Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005; 12: 1509-1518.
9. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93.
10. Frankel LB, Wen J, Lees M, Hoyer-Hansen M, Farkas T, Krogh A et al. microRNA-101 is a potent inhibitor of autophagy. EMBO J 2011; 30: 4628-4641.
11. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-5728.
12. Sinha S, Levine B. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 2008; 27: S137-S148.
13. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006; 8: 688-699.
14. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007; 9: 1142-1151.
15. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447: 1121-1125.
16. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004; 23: 2891-2906.
17. Munoz-Pinedo C, Martin SJ. Autosis: a new addition to the cell death tower of babel. Cell Death Dis 2014; 5: e1319.
18. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008; 15: 171-182.
19. Ginet V, Puyal J, Rummel C, Aubry D, Breton C, Cloux AJ et al. A critical role of autophagy in antileukemia/lymphoma effects of APO866, an inhibitor of NAD biosynthesis. Autophagy 2014; 10: 603-617.
20. Yu L, Wan F, Dutta S, Welsh S, Liu Z, Freundt E et al. Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci USA 2006; 103: 4952-4957.
21. Nihira K, Miki Y, Ono K, Suzuki T, Sasano H. An inhibition of p62/SQSTM1 caused autophagic cell death of several human carcinoma cells. Cancer Sci 2014; 105: 568-575.
22. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ et al. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 2008; 4: 195-204.
23. Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 2014; 22: 58-73.
24. Shen HM, Codogno P. Autophagic cell death: Loch Ness monster or endangered species? Autophagy 2011; 7: 457-465.
25. Berry DL, Baehrecke EH. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007; 131: 1137-1148.
26. Calvo-Garrido J, Carilla-Latorre S, Kubohara Y, Santos-Rodrigo N, Mesquita A, Soldati T et al. Autophagy in Dictyostelium: genes and pathways, cell death and infection. Autophagy 2010; 6: 686-701.
27. Samara C, Syntichaki P, Tavernarakis N. Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 2008; 15: 105-112.
28. Elgendy M, Sheridan C, Brumatti G, Martin SJ. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell 2011; 42: 23-35.
29. Liu Y, Shoji-Kawata S, Sumpter RM Jr., Wei Y, Ginet V, Zhang L et al. Autosis is a Na+,K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. Proc Natl Acad Sci USA 2013; 110: 20364-20371.
30. Zhaorigetu S, Wan G, Kaini R, Jiang Z, Hu CA. ApoL1 a BH3-only lipid-binding protein, induces autophagic cell death. Autophagy 2008; 4: 1079-1082.
31. Lamy L, Ngo VN, Emre NC, Shaffer AL 3rd, Yang Y, Tian E et al. Control of autophagic cell death by caspase-10 in multiple myeloma. Cancer Cell 2013; 23: 435-449.
32. Wang WJ, Wang Y, Chen HZ, Xing YZ, Li FW, Zhang Q et al. Orphan nuclear receptor TR3 acts in autophagic cell death via mitochondrial signaling pathway. Nat Chem Biol 2014; 10: 133-140.
33. Shen S, Kepp O, Michaud M, Martins I, Minoux H, Metivier D et al. Association and dissociation of autophagy, apoptosis and necrosis by systematic chemical study. Oncogene 2011; 30: 4544-4556.
34. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007; 26: 2527-2539.
35. Pattingre S, Levine B. Bcl-2 inhibition of autophagy: a new route to cancer? Cancer Res 2006; 66: 2885-2888.
36. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122: 927-939.
37. Hetschko H, Voss V, Senft C, Seifert V, Prehn JH, Kögel D. BH3 mimetics reactivate autophagic cell death in anoxia-resistant malignant glioma cells. Neoplasia 2008; 10: 873-885.
38. Friesen C, Glatting G, Koop B, Schwarz K, Morgenstern A, Apostolidis C et al. Breaking chemoresistance and radioresistance with [213Bi]anti-CD45 antibodies in leukemia cells. Cancer Res 2007; 67: 1950-1958.
39. Meng Y, Tang W, Dai Y, Wu X, Liu M, Ji Q et al. Natural BH3 mimetic (-)-gossypol chemosensitizes human prostate cancer via Bcl-xL inhibition accompanied by increase of Puma and Noxa. Mol Cancer Ther 2008; 7: 2192-2202.
40. Paoluzzi L, Gonen M, Gardner JR, Mastrella J, Yang D, Holmlund J et al. Targeting Bcl-2 family members with the BH3 mimetic AT-101 markedly enhances the therapeutic effects of chemotherapeutic agents in in vitro and in vivo models of B-cell lymphoma. Blood 2008; 111: 5350-5358.
41. Wolter KG, Wang SJ, Henson BS, Wang S, Griffith KA, Kumar B et al. (-)-gossypol inhibits growth and promotes apoptosis of human head and neck squamous cell carcinoma in vivo. Neoplasia 2006; 8: 163-172.
42. Balakrishnan K, Wierda WG, Keating MJ, Gandhi V. Gossypol a BH3 mimetic, induces apoptosis in chronic lymphocytic leukemia cells. Blood 2008; 112: 1971-1980.
43. Voss V, Senft C, Lang V, Ronellenfitsch MW, Steinbach JP, Seifert V et al. The panbcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol Cancer Res 2010; 8: 1002-1016.
44. Lian J, Wu X, He F, Karnak D, Tang W, Meng Y et al. A natural BH3 mimetic induces autophagy in apoptosis-resistant prostate cancer via modulating Bcl-2-Beclin1 interaction at endoplasmic reticulum. Cell Death Differ 2011; 18: 60-71.
45. Kaza N, Kohli L, Graham CD, Klocke BJ, Carroll SL, Roth KA. BNIP3 regulates AT101 [(-)-gossypol] induced death in malignant peripheral nerve sheath tumor cells. PLoS ONE 2014; 9: e96733.
46. Yuan Y, Tang AJ, Castoreno AB, Kuo SY, Wang Q, Kuballa P et al. Gossypol and an HMT G9a inhibitor act in synergy to induce cell death in pancreatic cancer cells. Cell Death Dis 2013; 4: e690.
47. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y, Kondo S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 2005; 24: 980-991.
48. Cheng P, Ni Z, Dai X, Wang B, Ding W, Rae Smith A et al. The novel BH-3 mimetic apogossypolone induces Beclin-1-and ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell Death Dis 2013; 4: e489.
49. Gao P, Bauvy C, Souquere S, Tonelli G, Liu L, Zhu Y et al. The Bcl-2 homology domain 3 mimetic gossypol induces both Beclin 1-dependent and Beclin 1-independent cytoprotective autophagy in cancer cells. J Biol Chem 2010; 285: 25570-25581.
50. Bonapace L, Bornhauser BC, Schmitz M, Cario G, Ziegler U, Niggli FK et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest 2010; 120: 1310-1323.
51. Basit F, Cristofanon S, Fulda S. Obatoclax (GX15-070) triggers necroptosis by promoting the assembly of the necrosome on autophagosomal membranes. Cell Death Differ 2013; 20: 1161-1173.
52. Heidari N, Hicks MA, Harada H. GX15-070 (obatoclax) overcomes glucocorticoid resistance in acute lymphoblastic leukemia through induction of apoptosis and autophagy. Cell Death Dis 2010; 1: e76.
53. Martin AP, Mitchell C, Rahmani M, Nephew KP, Grant S, Dent P. Inhibition of MCL-1 enhances lapatinib toxicity and overcomes lapatinib resistance via BAKdependent autophagy. Cancer Biol Ther 2009; 8: 2084-2096.
54. Chen YJ, Chi CW, Su WC, Huang HL. Lapatinib induces autophagic cell death and inhibits growth of human hepatocellular carcinoma. Oncotarget 2014; 5: 4845-4854.
55. Tang Y, Hamed HA, Poklepovic A, Dai Y, Grant S, Dent P. Poly(ADP-ribose) polymerase 1 modulates the lethality of CHK1 inhibitors in mammary tumors. Mol Pharmacol 2012; 82: 322-332.
56. Martin AP, Park MA, Mitchell C, Walker T, Rahmani M, Thorburn A et al. BCL-2 family inhibitors enhance histone deacetylase inhibitor and sorafenib lethality via autophagy and overcome blockade of the extrinsic pathway to facilitate killing. Mol Pharmacol 2009; 76: 327-341.
57. Wei Y, Kadia T, Tong W, Zhang M, Jia Y, Yang H et al. The combination of a histone deacetylase inhibitor with the Bcl-2 homology domain-3 mimetic GX15-070 has synergistic antileukemia activity by activating both apoptosis and autophagy. Clin Cancer Res 2010; 16: 3923-3932.
58. Brem EA, Thudium K, Khubchandani S, Tsai PC, Olejniczak SH, Bhat S et al. Distinct cellular and therapeutic effects of obatoclax in rituximab-sensitive and-resistant lymphomas. Br J Haematol 2011; 153: 599-611.
59. Pan J, Cheng C, Verstovsek S, Chen Q, Jin Y, Cao Q. The BH3-mimetic GX15-070 induces autophagy, potentiates the cytotoxicity of carboplatin and 5-fluorouracil in esophageal carcinoma cells. Cancer Lett 2010; 293: 167-174.
60. Schwartz-Roberts JL, Shajahan AN, Cook KL, Warri A, Abu-Asab M, Clarke R. GX15-070 (obatoclax) induces apoptosis and inhibits cathepsin D-and L-mediated autophagosomal lysis in antiestrogen-resistant breast cancer cells. Mol Cancer Ther 2013; 12: 448-459.
61. McCoy F, Hurwitz J, McTavish N, Paul I, Barnes C, O'Hagan B et al. Obatoclax induces Atg7-dependent autophagy independent of beclin-1 and BAX/BAK. Cell Death Dis 2010; 1: e108.
62. Fulda S, Kroemer G. Targeting mitochondrial apoptosis by betulinic acid in human cancers. Drug Discov Today 2009; 14: 885-890.
63. Gonzalez P, Mader I, Tchoghandjian A, Enzenmuller S, Cristofanon S, Basit F et al. Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ 2012; 19: 1337-1346.
64. Potze L, Mullauer FB, Colak S, Kessler JH, Medema JP. Betulinic acid-induced mitochondria-dependent cell death is counterbalanced by an autophagic salvage response. Cell Death Dis 2014; 5: e1169.
65. Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 2008; 15: 1318-1329.
66. Puissant A, Robert G, Fenouille N, Luciano F, Cassuto JP, Raynaud S et al. Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Res 2010; 70: 1042-1052.
67. Cea M, Cagnetta A, Fulciniti M, Tai YT, Hideshima T, Chauhan D et al. Targeting NAD+ salvage pathway induces autophagy in multiple myeloma cells via mTORC1 and extracellular signal-regulated kinase (ERK1/2) inhibition. Blood 2012; 120: 3519-3529.
68. Yamamoto S, Tanaka K, Sakimura R, Okada T, Nakamura T, Li Y et al. Suberoylanilide hydroxamic acid (SAHA) induces apoptosis or autophagy-associated cell death in chondrosarcoma cell lines. Anticancer Res 2008; 28: 1585-1591.
69. Cao Q, Yu C, Xue R, Hsueh W, Pan P, Chen Z et al. Autophagy induced by suberoylanilide hydroxamic acid in Hela S3 cells involves inhibition of protein kinase B and up-regulation of Beclin 1. Int J Biochem Cell Biol 2008; 40: 272-283.
70. Liu YL, Yang PM, Shun CT, Wu MS, Weng JR, Chen CC. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 2010; 6: 1057-1065.
71. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 2004; 11: 448-457.
72. Katayama M, Kawaguchi T, Berger MS, Pieper RO. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ 2007; 14: 548-558.
73. Knizhnik AV, Roos WP, Nikolova T, Quiros S, Tomaszowski KH, Christmann M et al. Survival and death strategies in glioma cells: autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage. PLoS One 2013; 8: e55665.
74. Salazar M, Carracedo A, Salanueva IJ, Hernandez-Tiedra S, Lorente M, Egia A et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest 2009; 119: 1359-1372.
75. Vara D, Salazar M, Olea-Herrero N, Guzman M, Velasco G, Diaz-Laviada I. Antitumoral action of cannabinoids on hepatocellular carcinoma: role of AMPKdependent activation of autophagy. Cell Death Differ 2011; 18: 1099-1111.
76. Lian J, Karnak D, Xu L. The Bcl-2-Beclin 1 interaction in (-)-gossypol-induced autophagy versus apoptosis in prostate cancer cells. Autophagy 2010; 6: 1201-1203.