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

Oncogene volume 34, pages 5105–5113 (2015)Cite this article

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Abstract

Autophagy is a tightly-regulated catabolic process of cellular self-digestion by which cellular components are targeted to lysosomes for their degradation. Key functions of autophagy are to provide energy and metabolic precursors under conditions of starvation and to alleviate stress by removal of damaged proteins and organelles, which are deleterious for cell survival. Therefore, autophagy appears to serve as a pro-survival stress response in most settings. However, the role of autophagy in modulating cell death is highly dependent on the cellular context and its extent. There is an increasing evidence for cell death by autophagy, in particular in developmental cell death in lower organisms and in autophagic cancer cell death induced by novel cancer drugs. The death-promoting and -executing mechanisms involved in the different paradigms of autophagic cell death (ACD) are very diverse and complex, but a draft scenario of the key molecular targets involved in ACD is beginning to emerge. This review provides an up-to-date and comprehensive report on the molecular mechanisms of drug-induced autophagy-dependent cell death and highlights recent key findings in this exciting field of research.

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References

  1. Hengartner MO . The biochemistry of apoptosis. Nature 2000; 407: 770–776.

    CAS  PubMed  Google Scholar 

  2. Kroemer G, Martin SJ . Caspase-independent cell death. Nat Med 2005; 11: 725–730.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  4. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N . Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta 2013; 1833: 3448–3459.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  8. Codogno P, Meijer AJ . Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005; 12: 1509–1518.

    Article  CAS  PubMed  Google Scholar 

  9. He C, Klionsky DJ . Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sinha S, Levine B . The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 2008; 27: S137–S148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  16. Gozuacik D, Kimchi A . Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004; 23: 2891–2906.

    Article  CAS  PubMed  Google Scholar 

  17. Munoz-Pinedo C, Martin SJ . Autosis: a new addition to the cell death tower of babel. Cell Death Dis 2014; 5: e1319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Shen HM, Codogno P . Autophagic cell death: Loch Ness monster or endangered species? Autophagy 2011; 7: 457–465.

    Article  CAS  PubMed  Google Scholar 

  25. Berry DL, Baehrecke EH . Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007; 131: 1137–1148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  27. Samara C, Syntichaki P, Tavernarakis N . Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 2008; 15: 105–112.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Pattingre S, Levine B . Bcl-2 inhibition of autophagy: a new route to cancer? Cancer Res 2006; 66: 2885–2888.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Voss V, Senft C, Lang V, Ronellenfitsch MW, Steinbach JP, Seifert V et al. The pan-bcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol Cancer Res 2010; 8: 1002–1016.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 BAK-dependent autophagy. Cancer Biol Ther 2009; 8: 2084–2096.

    Article  CAS  PubMed  Google Scholar 

  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.

    PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fulda S, Kroemer G . Targeting mitochondrial apoptosis by betulinic acid in human cancers. Drug Discov Today 2009; 14: 885–890.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Vara D, Salazar M, Olea-Herrero N, Guzman M, Velasco G, Diaz-Laviada I . Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ 2011; 18: 1099–1111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The expert secretarial assistance of C Hugenberg is greatly appreciated. This work has been partly supported by a grant from the BMBF (to SF).

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Authors and Affiliations

  1. Institute for Experimental Cancer Research in Pediatrics, Goethe-University, Frankfurt, Germany

    S Fulda

  2. German Cancer Consortium (DKTK), Heidelberg, Germany

    S Fulda

  3. German Cancer Research Center (DKFZ), Heidelberg, Germany

    S Fulda

  4. Experimental Neurosurgery, Center for Neurology and Neurosurgery, Goethe-University Hospital, Frankfurt, Germany

    D Kögel

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Fulda, S., Kögel, D. Cell death by autophagy: emerging molecular mechanisms and implications for cancer therapy. Oncogene 34, 5105–5113 (2015). https://doi.org/10.1038/onc.2014.458

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