Tyrosine kinase receptor EGFR regulates the switch in cancer cells between cell survival and cell death induced by autophagy in hypoxia

Autophagy

Volumn 12, Issue 6, 2016, Pages 1029-1046

  Chen, Yongqiang ^a   Henson, Elizabeth S ^a,b   Xiao, Wenyan ^a   Huang, Daniel ^a   McMillan Ward, Eileen M ^a   Israels, Sara J ^a,b   Gibson, Spencer B ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Autophagy; autosis; CAV1 (caveolin 1); cell death; epidermal growth factor receptor (EGFR); hypoxia

Indexed keywords

AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 5; BECLIN 1; CAVEOLIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 BETA PROTEIN; UNCLASSIFIED DRUG; BECN1 PROTEIN, HUMAN; BENZYLOXYCARBONYL-VALYL-ALANYL-ASPARTIC ACID; CAV1 PROTEIN, HUMAN; OLIGOPEPTIDE; PROTEIN BCL 2; PROTEIN KINASE INHIBITOR;

A549 CELL LINE; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; AUTOPHOSPHORYLATION; CELL DEATH; CELL HYPOXIA; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; GENE SILENCING; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; LIPID RAFT; MITOCHONDRION; NON SMALL CELL LUNG CANCER; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; UPREGULATION; BIOLOGICAL MODEL; CELL SHAPE; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

AUTOPHAGY; BECLIN-1; CAVEOLIN 1; CELL HYPOXIA; CELL LINE, TUMOR; CELL SHAPE; CELL SURVIVAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MODELS, BIOLOGICAL; OLIGOPEPTIDES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84966702480     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1164357     Document Type: Article

References (76)

1. Y.Chen, D.J.Klionsky. The regulation of autophagy - unanswered questions. J Cell Sci 2011; 124:161-70; PMID:21187343; http://dx.doi.org/10.1242/jcs.064576
2. N.Mizushima, B.Levine, A.M.Cuervo, D.J.Klionsky. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
3. A.M.Choi, S.W.Ryter, B.Levine. Autophagy in human health and disease. N Engl J Med 2013; 368:651-62; PMID:23406030; http://dx.doi.org/10.1056/NEJMra1205406
4. J.L.Schneider, A.M.Cuervo. Autophagy and human disease: emerging themes. Curr Opin Genet Dev 2014; 26:16-23; PMID:24907664; http://dx.doi.org/10.1016/j.gde.2014.04.003
5. J.S.King. Autophagy across the eukaryotes: is S. cerevisiae the odd one out? Autophagy 2012; 8:1159-62; PMID:22722653; http://dx.doi.org/10.4161/auto.20527
6. P.M.Wong, C.Puente, I.G.Ganley, X.Jiang. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 2013; 9:124-37; PMID:23295650; http://dx.doi.org/10.4161/auto.23323
7. S.Sinha, B.Levine. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 2008; 27:S137-48; PMID:19641499; http://dx.doi.org/10.1038/onc.2009.51
8. F.Zhou, Y.Yang, D.Xing. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 2011; 278:403-13; PMID:21182587; http://dx.doi.org/10.1111/j.1742-4658.2010.07965.x
9. J.Cui, Y.F.Hu, X.M.Feng, T.Tian, Y.H.Guo, J.W.Ma, K.J.Nan, H.Y.Zhang. EGFR inhibitors and autophagy in cancer treatment. Tumour Biol 2014; 35:11701-9; PMID:25293518; http://dx.doi.org/10.1007/s13277-014-2660-z
10. B.Jutten, K.M.Rouschop. EGFR signaling and autophagy dependence for growth, survival, and therapy resistance. Cell Cycle 2014; 13:42-51; PMID:24335351; http://dx.doi.org/10.4161/cc.27518
11. X.Sui, N.Kong, M.Zhu, X.Wang, F.Lou, W.Han, H.Pan. Cotargeting EGFR and autophagy signaling: A novel therapeutic strategy for non-small-cell lung cancer. Mol Clin Oncol 2014; 2:8-12; PMID:24649300
12. Y.Wei, Z.Zou, N.Becker, M.Anderson, R.Sumpter, G.Xiao, L.Kinch, P.Koduru, C.S.Christudass, R.W.Veltri, et al. EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance. Cell 2013; 154:1269-84; PMID:24034250; http://dx.doi.org/10.1016/j.cell.2013.08.015
13. B.1.Jutten, T.G.Keulers, M.B.Schaaf, K.Savelkouls, J.Theys, P.N.Span, M.A.Vooijs, J.Bussink, K.M.Rouschop. EGFR overexpressing cells and tumors are dependent on autophagy for growth and survival. Radiother Oncol 2013; 108:479-83; PMID:23891088; http://dx.doi.org/10.1016/j.radonc.2013.06.033
14. C.Fung, X.Chen, J.R.Grandis, U.Duvvuri. EGFR tyrosine kinase inhibition induces autophagy in cancer cells. Cancer Biol Ther 2012; 13:1417-24; PMID:22954701; http://dx.doi.org/10.4161/cbt.22002
15. J.Baselga. Why the epidermal growth factor receptor? The rationale for cancer therapy. Oncologist 2002; 7:2-8; PMID:12202782; http://dx.doi.org/10.1634/theoncologist.7-suppl_4-2
16. R.Mathew, V.Karantza-Wadsworth, E.White. Role of autophagy in cancer. Nat Rev Cancer 2007; 7:961-7; PMID:17972889; http://dx.doi.org/10.1038/nrc2254
17. Y.1.Kondo, T.Kanzawa, R.Sawaya, S.Kondo. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726-34; PMID:16148885; http://dx.doi.org/10.1038/nrc1692
18. A.Thorburn, D.H.Thamm, D.L.Gustafson. Autophagy and cancer therapy. Mol Pharmacol 2014; 85:830-8; PMID:24574520; http://dx.doi.org/10.1124/mol.114.091850
19. E.White. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12:401-10; PMID:22534666; http://dx.doi.org/10.1038/nrc3262
20. C.M.Kenific, J.Debnath. Cellular and metabolic functions for autophagy in cancer cells. Trends Cell Biol 2015; 25:37-45; PMID:25278333; http://dx.doi.org/10.1016/j.tcb.2014.09.001
21. C.N.Coleman. Hypoxia in tumors: a paradigm for the approach to biochemical and physiologic heterogeneity. J Natl Cancer Inst 1998; 80:310-7; http://dx.doi.org/10.1093/jnci/80.5.310
22. P.1.Vaupel, F.Kallinowski, P.Okunieff. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989; 49:6449-65; PMID:2684393
23. 2 availability on human cancer. Nat Rev Cancer 2008; 8:967-75; PMID:18987634; http://dx.doi.org/10.1038/nrc2540
24. A.I.1.Minchinton, I.F.Tannock. Drug penetration in solid tumours. Nat Rev Cancer 2006; 6:583-92; PMID:16862189; http://dx.doi.org/10.1038/nrc1893
25. J.1.Zhou, T.Schmid, S.Schnitzer, B.Brüne. Tumor hypoxia and cancer progression. Cancer Lett 2006; 237:10-21; PMID:16002209; http://dx.doi.org/10.1016/j.canlet.2005.05.028
26. X.Cheng, H.Chen. Tumor heterogeneity and resistance to EGFR-targeted therapy in advanced nonsmall cell lung cancer: challenges and perspectives. Onco Targets Ther 2014; 7:1689-704; PMID:25285017; http://dx.doi.org/10.2147/OTT.S66502
27. G.Bellot, R.Garcia-Medina, P.Gounon, J.Chiche, D.Roux, J.Pouysségur, N.M.Mazure. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 2009; 29:2570-81; PMID:19273585; http://dx.doi.org/10.1128/MCB.00166-09
28. S.Carloni, G.Buonocore, W.Balduini. Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 2008; 32:329-39; PMID:18760364; http://dx.doi.org/10.1016/j.nbd.2008.07.022
29. H.Zhang, M.Bosch-Marce, L.A.Shimoda, Y.S.Tan, J.H.Baek, J.B.Wesley, F.J.Gonzalez, G.L.Semenza. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008; 283:10892-903; PMID:18281291; http://dx.doi.org/10.1074/jbc.M800102200
30. J.Song, Z.Qu, X.Guo, Q.Zhao, X.Zhao, L.Gao, K.Sun, F.Shen, M.Wu, L.Wei. Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells. Autophagy 2009; 5:1131-44; PMID:19786832; http://dx.doi.org/10.4161/auto.5.8.9996
31. A.Notte, N.Ninane, T.Arnould, C.Michiels. Hypoxia counteracts taxol-induced apoptosis in MDA-MB-231 breast cancer cells: role ofautophagy and JNK activation. Cell Death Dis 2013; 4:e638; PMID:23681233; http://dx.doi.org/10.1038/cddis.2013.167
32. M.B.Azad, Y.Chen, E.S.Henson, J.Cizeau, E.McMillan-Ward, S.J.Israels, S.B.Gibson. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 2008; 4:195-204; PMID:18059169; http://dx.doi.org/10.4161/auto.5278
33. M.B.Azad, S.B.Gibson. Role of BNIP3 in proliferation and hypoxia-induced autophagy: implications for personalized cancer therapies. Ann N Y Acad Sci 2010; 1210:8-16; PMID:20973794; http://dx.doi.org/10.1111/j.1749-6632.2010.05778.x
34. F.Adhami, G.Liao, Y.M.Morozov, A.Schloemer, V.J.Schmithorst, J.N.Lorenz, R.S.Dunn, C.V.Vorhees, M.Wills-Karp, J.L.Degen, et al. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006; 169:566-83; PMID:16877357; http://dx.doi.org/10.2353/ajpath.2006.051066
35. K.Tracy, B.C.Dibling, B.T.Spike, J.R.Knabb, P.Schumacker, K.F.Macleod. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol Cell Biol 2007; 27:6229-42; PMID:17576813; http://dx.doi.org/10.1128/MCB.02246-06
36. M.Koike, M.Shibata, M.Tadakoshi, K.Gotoh, M.Komatsu, S.Waguri, N.Kawahara, K.Kuida, S.Nagata, E.Kominami, et al. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008; 172:454-69; PMID:18187572; http://dx.doi.org/10.2353/ajpath.2008.070876
37. Y.Matsui, S.Kyoi, H.Takagi, C.P.Hsu, N.Hariharan, T.Ago, S.F.Vatner, J.Sadoshima. Molecular mechanisms and physiological significance of autophagy during myocardial ischemia and reperfusion. Autophagy 2008; 4:409-15; PMID:18227645; http://dx.doi.org/10.4161/auto.5638
38. I.Papandreou, A.L.Lim, K.Laderoute, N.C.Denko. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 2008; 15:1572-81; PMID:18551130; http://dx.doi.org/10.1038/cdd.2008.84
39. +-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. Proc Natl Acad Sci U S A 2013; 110:20364-71; PMID:24277826; http://dx.doi.org/10.1073/pnas.1319661110
40. Y.Liu, B.Levine. Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 2015; 22:367-76; PMID:25257169; http://dx.doi.org/10.1038/cdd.2014.143
41. A.Franovic, L.Gunaratnam, K.Smith, I.Robert, D.Patten, S.Lee. Translational up-regulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proc Natl Acad Sci U S A 2007; 104:13092-7; PMID:17670948; http://dx.doi.org/10.1073/pnas.0702387104
42. Y.Wang, O.Roche, C.Xu, E.H.Moriyama, P.Heir, J.Chung, F.C.Roos, Y.Chen, G.Finak, M.Milosevic, et al. Hypoxia promotes ligand-independent EGF receptor signaling via hypoxia-inducible factor-mediated upregulation of caveolin-1. Proc Natl Acad Sci U S A 2012; 109:4892-7; PMID:22411794; http://dx.doi.org/10.1073/pnas.1112129109
43. Z.H.Chen, J.F.Cao, J.S.Zhou, H.Liu, L.Q.Che, K.Mizumura, W.Li, A.M.Choi, H.H.Shen. Interaction of caveolin-1 with ATG12-ATG5 system suppresses autophagy in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2014; 306:L1016-25; PMID:24727585; http://dx.doi.org/10.1152/ajplung.00268.2013
44. Z.H.Chen, H.C.Lam, Y.Jin, H.P.Kim, J.Cao, S.J.Lee, E.Ifedigbo, H.Parameswaran, S.W.Ryter, A.M.Choi. Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 2010; 107:18880-5; PMID:20956295; http://dx.doi.org/10.1073/pnas.1005574107
45. A.Kuma, M.Hatano, M.Matsui, A.Yamamoto, H.Nakaya, T.Yoshimori, Y.Ohsumi, T.Tokuhisa, N.Mizushima. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6; PMID:15525940; http://dx.doi.org/10.1038/nature03029
46. M.Komatsu, S.Waguri, T.Ueno, J.Iwata, S.Murata, I.Tanida, J.Ezaki, N.Mizushima, Y.Ohsumi, Y.Uchiyama, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/jcb.200412022
47. T.Saitoh, N.Fujita, M.H.Jang, S.Uematsu, B.G.Yang, T.Satoh, H.Omori, T.Noda, N.Yamamoto, M.Komatsu, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature 2008; 456:264-8; PMID:18849965; http://dx.doi.org/10.1038/nature07383
48. T.Saitoh, N.Fujita, T.Hayashi, K.Takahara, T.Satoh, H.Lee, K.Matsunaga, S.Kageyama, H.Omori, T.Noda, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A 2009; 106:20842-6; PMID:19926846; http://dx.doi.org/10.1073/pnas.0911267106
49. Y.S.Sou, S.Waguri, J.Iwata, T.Ueno, T.Fujimura, T.Hara, N.Sawada, A.Yamada, N.Mizushima, Y.Uchiyama, et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell 2008; 19:4762–715; PMID:18768753; http://dx.doi.org/10.1091/mbc.E08-03-0309
50. E.H.Baehrecke. Autophagic programmed cell death in Drosophila. Cell Death Differ 2003; 10:940-5; PMID:12934068; http://dx.doi.org/10.1038/sj.cdd.4401280
51. H.Wang, Q.Lu, S.Cheng, X.Wang, H.Zhang. Autophagy activity contributes to programmed cell death in Caenorhabditis elegans. Autophagy 2013; 9:1975-82; PMID:24185352; http://dx.doi.org/10.4161/auto.26152
52. D.Hofius, T.Schultz-Larsen, J.Joensen, D.I.Tsitsigiannis, N.H.Petersen, O.Mattsson, L.B.Jörgensen, J.D.Jones, J.Mundy, M.Petersen. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 2009; 137:773-83; PMID:19450522; http://dx.doi.org/10.1016/j.cell.2009.02.036
53. C.Giusti, E.Tresse, M.F.Luciani, P.Golstein. Autophagic cell death: analysis in Dictyostelium. Biochim Biophys Acta 2009; 1793:1422-31; PMID:19133302; http://dx.doi.org/10.1016/j.bbamcr.2008.12.005
54. A.Abudugupur, K.Mitsui, S.Yokota, K.Tsurugi. ARL1 mutation affected autophagic cell death in yeast, causing a defect in central vacuole formation. Cell Death Differ 2002; 9:158-68; PMID:11840166; http://dx.doi.org/10.1038/sj.cdd.4400942
55. A.Misra, C.Pandey, S.K.Sze, T.Thanabalu. Hypoxia activated EGFR signaling induces epithelial to mesenchymal transition (EMT). PLoS One 2012; 7:e49766; PMID:23185433; http://dx.doi.org/10.1371/journal.pone.0049766
56. J.S.Carew, K.R.Kelly, S.T.Nawrocki. Autophagy as a target for cancer therapy: new developments. Cancer Manag Res 2012; 4:357-65; PMID:23091399
57. J.M.Farrow, J.C.Yang, C.P.Evans. Autophagy as a modulator and target in prostate cancer. Nat Rev Urol 2014; 11:508-16; PMID:25134829; http://dx.doi.org/10.1038/nrurol.2014.196
58. P.Maycotte, A.Thorburn. Targeting autophagy in breast cancer. World J Clin Oncol 2014; 5:224-40; PMID:25114840; http://dx.doi.org/10.5306/wjco.v5.i3.224
59. P.Jiang, N.Mizushima. Autophagy and human diseases. Cell Res 2014; 24:69-79; PMID:24323045; http://dx.doi.org/10.1038/cr.2013.161
60. A.L.Swampillai, P.Salomoni, S.C.Short. The role of autophagy in clinical practice. Clin Oncol (R Coll Radiol) 2012; 24:387-95; PMID:22032864; http://dx.doi.org/10.1016/j.clon.2011.09.010
61. Z.J.Yang, C.E.Chee, S.Huang, F.A.Sinicrope. The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 2011; 10:1533-41; PMID:21878654; http://dx.doi.org/10.1158/1535-7163.MCT-11-0047
62. E.White, R.S.DiPaola. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 2009; 15:5308-16; PMID:19706824; http://dx.doi.org/10.1158/1078-0432.CCR-07-5023
63. R.K.Amaravadi, D.Yu, J.J.Lum, T.Bui, M.A.Christophorou, G.I.Evan, A.Thomas-Tikhonenko, C.B.Thompson. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007; 117:326-36; PMID:17235397; http://dx.doi.org/10.1172/JCI28833
64. T.Kimura Y.Takabatake, A.Takahashi, Y.Isaka. Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res 2013; 73:3-7; PMID:23288916; http://dx.doi.org/10.1158/0008-5472.CAN-12-2464
65. J.Sotelo, E.Briceno, M.A.Lopez-Gonzalez. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med 2006; 144:337-43; PMID:16520474; http://dx.doi.org/10.7326/0003-4819-144-5-200603070-00008
66. R.Rangwala, Y.C.Chang, J.Hu, K.M.Algazy, T.L.Evans, L.A.Fecher, L.M.Schuchter, D.A.Torigian, J.T.Panosian, A.B.Troxel, et al. Combined MTOR and autophagy inhibition: phase I trial of hydroxychloroquine and temsirolimus in patients with advanced solid tumors and melanoma. Autophagy 2014; 10:1391-402; PMID:24991838; http://dx.doi.org/10.4161/auto.29119
67. X.Tan, N.Thapa, Y.Sun, R.A.Anderson. A kinase-independent role for EGF receptor in autophagy initiation. Cell 2015; 160:145-60; PMID:25594178; http://dx.doi.org/10.1016/j.cell.2014.12.006
68. R.I.Nicholson, J.M.Gee, M.E.Harper. EGFR and cancer prognosis. Eur J Cancer 2001; 37:S9-15; PMID:11597399; http://dx.doi.org/10.1016/S0959-8049(01)00231-3
69. Y.Chen, M.B.Azad, S.B.Gibson. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16:1040-52; PMID:19407826; http://dx.doi.org/10.1038/cdd.2009.49
70. S.Shetty, B.A.Graham, J.G.Brown, X.Hu, N.Vegh-Yarema, G.Harding, J.T.Paul, S.B.Gibson. Transcription factor NF-kappaB differentially regulates death receptor 5 expression involving histone deacetylase 1. Mol Cell Biol 2005; 25:5404-16; PMID:15964798; http://dx.doi.org/10.1128/MCB.25.13.5404-5416.2005
71. S.Kothari, J.Cizeau, E.McMillan-Ward, S.J.Israels, M.Bailes, K.Ens, L.A.Kirshenbaum, S.B.Gibson. BNIP3 plays a role in hypoxic cell death in human epithelial cells that is inhibited by growth factors EGF and IGF. Oncogene 2003; 22:4734-44; PMID:12879018; http://dx.doi.org/10.1038/sj.onc.1206666
72. Y.Chen, E.McMillan-Ward, J.Kong, S.J.Israels, S.B.Gibson. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008; 15:171-82; PMID:17917680; http://dx.doi.org/10.1038/sj.cdd.4402233
73. A.Hayer, M.Stoeber, C.Bissig, A.Helenius. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 2010; 11:361-82; PMID:20070607; http://dx.doi.org/10.1111/j.1600-0854.2009.01023.x
74. S.Kimura, T.Noda, T.Yoshimori. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452-60; PMID:17534139; http://dx.doi.org/10.4161/auto.4451
75. Y.Chen, H.Wei, F.Liu, J.L.Guan. Hyperactivation of mammalian target of rapamycin complex 1 (mTORC1) promotes breast cancer progression through enhancing glucose starvation-induced autophagy and Akt signaling. J Biol Chem 2014; 289:1164-73; PMID:24275666; http://dx.doi.org/10.1074/jbc.M113.526335
76. N.A.Franken, H.M.Rodermond, J.Stap, J.Haveman, C.van Bree. Clonogenic assay of cells in vitro. Nat Protoc 2006; 1:2315-9; PMID:17406473; http://dx.doi.org/10.1038/nprot.2006.339