Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer

Autophagy

Volumn 6, Issue 3, 2010, Pages 322-329

  Dalby, Kevin N ^a   Tekedereli, Ibrahim ^b   Lopez Berestein, Gabriel ^b   Ozpolat, Bulent ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Apoptosis; Autophagy; Bcl 2; Beclin 1; Cancer; Programmed cell death; siRNA; Small molecule inhibitors

Indexed keywords

BECLIN 1; CYTOPLASM PROTEIN; ELONGATION FACTOR 2 KINASE; GLYCOGEN SYNTHASE KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PROTEIN BCL 2; PROTEIN KINASE C GAMMA; SMALL INTERFERING RNA; TAMOXIFEN;

APOPTOSIS; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER RADIOTHERAPY; CANCER RESEARCH; CANCER THERAPY; CELL DEATH; CELL ORGANELLE; CELL STRESS; CELL SURVIVAL; DRUG TARGETING; ENVIRONMENTAL STRESS; GENE DELETION; GENE EXPRESSION; GENETIC SCREENING; HYPOXIA; MACROMOLECULE; NONHUMAN; NUTRITIONAL DEFICIENCY; ONCOGENE; OVARY CANCER; PANCREAS CANCER; PROTEIN TARGETING; REVIEW; TUMOR SUPPRESSOR GENE;

MUS;

EID: 77953699668     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.6.3.11625     Document Type: Review

References (85)

1. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21.
2. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6:463-77.
3. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726-34.
4. Qu X, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the Beclin 1 autophagy gene. J Clin Invest 2003; 112:1809-20.
5. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin1. Nature 1999; 402:672-76.
6. Aita VM, Liang XH. Cloning and genomic organization of beclin1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999; 59:59-65.
7. ShenY , Li D, Wang L, Deng R and Zhu XF. Decreased expression of autophagy-related proteins in malignant epithelial ovarian cancer. Autophagy 2008; 4:1067-8.
8. Koneri K, Goi T, Hirono Y. Beclin1 gene inhibits tumor growth in colon cancer cell lines. Anticancer Res 2007; 27:1453-7.
9. Miracco C, Cosci E. Protein and mRNA expression of autophagy gene Beclin1 in human brain tumours. Int J Oncol 2007; 30:429-36.
10. LmRNA expression in human hepatocellular carcinoma. Cancer Invest 2007; 25:226-31.
11. Wang ZH, Peng ZL, Duan ZL, et al. Expression and clinical significance of autophagy gene Beclin1 in cervical squamous cell carcinoma. Sichuan Da Xue Xue Bao Yi Xue Ban 200; 37:860-3.
12. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 2003; 100:15077-82.
13. Edinger AL, Thompson CB. Defective autophagy leads to cancer. Cancer Cell 2003; 4:422-4.
14. Ding ZB, Shi YH, Zhou J, Qiu SJ, Xu Y,Dai Z, Shi GM, Wang XY, Ke AW, Wu B, Fan J. Association of autophagy defect with a malignant phenotype and poor prognosis of hepatocellular carcinoma. Cancer Res 2008; 68:9167.
15. Rouschop KM, Wouters BG. Regulation of autophagy through multiple independent hypoxic signaling pathways. Curr Mol Med 2009; 9:417-24
16. Djavaheri-Mergny M, Botti J and Codogno P. Autophagy and Autophagic Cell Death. Apoptosis, Senescence, and Cancer (Editor: A.Gewirtz) 2007, 93-107.
17. Sotelo J, Briceno E, Lopez-Gonzalez MA. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med 2006; 144:337-343. (Pubitemid 46768188)
18. 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; 11:448-57.
19. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 2001; 61:439-44.
20. Boya P, Gonzalez-Polo R-A, Casares N, Perfettini J-L, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Pierron G, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025-40.
21. Qadir MA, Kwok B, Dragowska WH, To KH, Le D, Bally MB, Gorski SM. Macroautophagy inhibition sensitizes tamoxifen-resistant breast cancer cells and enhances mitochondrial depolarization. Breast Cancer Res Treat 2008; 112:389-403.
22. Carew JS, Nawrocki ST, Kahue CN, Zhang H, Yang C, Chung L, Houghton JA, Huang P, Giles FJ, Cleveland JL. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 2007; 110:313-22.
23. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007; 117:326-36.
24. Apel A, Herr I, Schwarz H, Rodemann HP, Mayer A. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 2008; 68:1485-94.
25. Abedin MJ, Wang D, McDonnell MA, Lehmann U, Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 2007; 14:500-10.
26. 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; 14:548-58.
27. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 1999; 147:435-46.
28. Moretti K, Attia, Kim Lu. Crosstalk between Bak/Bax and mTOR signaling regulates radiation-induced autophagy. Autophagy 2007; 3:142-4.
29. Akar U, Ozpolat B, Mehta K, Fok F, Lopez Berestein G. Tissue transglutaminase (TG2) inhibits autophagy in pancreatic cancer cells. Mol Cancer Res 2007; 5:241-9.
30. Xue L, Fletcher GC, Tolkovsky AM. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 1999; 14:180-98.
31. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 2004; 6:1221-8.
32. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y, Kondo S, Arun B, Lopez-Berestein G, Ozpolat B. Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 2008; 4:669-79.
33. 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; 122:927-39.
34. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nature Cell Biol 2006; 8:1124-32.
35. Lockshin RA, Zakeri Z. Cell death in health and disease. J Cell Mol Med 2007; 11:1214-24.
36. Ozpolat B, Akar U, Mehta K, Fok J, Kondo Y, Lopez-Berestein G. Mol Cancer Res 2007; 5:241-49.
37. PKCδ and tissue transglutaminase (TG2) are novel inhibitors of autophagy. Autophagy 2007; 3:480-3.
38. Verma A, Wang H, Manavathi B, Fok JY, Mann AP, Kumar R, Mehta K. Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res 2006; 66:10525-33.
39. Fesus L, Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 2005; 579:3297-302.
40. Mehta K, Fok J, Miller FR, Koul D, Sahin AA. Prognostic significance of tissue transglutaminase in drug resistant and metastatic breast cancer. Clin Cancer Res 2004; 10:8068-76.
41. Oliverio S, Amendola A, Di Sano F, Farrace MG, Fesus L, Nemes Z, et al. Tissue transglutaminase-dependent posttranslational modification of the retinoblastoma gene product in promonocytic cells undergoing apoptosis. Mol Cell Biol 1997; 17:6040-8.
42. Verma A, Guha S, Jansina F, et al. Therapeutic significance of elevated tissue transglutaminase expression in pancreatic cancer. Clin Cancer Res 2008; 14:2476.
43. Buchholz, T, Davis,D, McConkey, DJ, Symmans, F, Valero V, Tucker SL, Pusztai L, Cristofanilli M, Esteva FJ, Hortobagyi G, Sahin A. Chemotherapy-induced apoptosis and Bcl-2 levels correlate with breast cancer response to chemotherapy. Cancer J 2003; 9:33-41.
44. Bishop JM. Molecular themes in oncogenesis. Cell 1991; 64:235-48.
45. Reed JC. Bcl-2: prevention of apoptosis as a mechanism of drug resistance. Hematol Oncol Clin North Am 1995; 9:451-73.
46. Devarajan E, Sahin AA, Chen JS, Krishnamurthy RR, Aggarwal N, Brun AM, et al. Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene 2002; 21:8843-51.
47. Devarajan E, Chen J, Multani AS, Pathak S, Sahin AA, Mehta K. Human breast cancer MCF-7 cell line contains inherently drug-resistant subclones with distinct genotypic and phenotypic features. Int J Oncol 2002; 20:913-20.
48. Abedin MJ, Wang D, McDonnell MA, Lehmann U, Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 2007; 14:500-10.
49. Sotelo J, Briceño E, López-González MA. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med 2006; 144:337-43.
50. Bardeesy N, DePinho RA. Pancreatic cancer biology and genetics. Nat Rev Cancer 2002; 2:897-909.
51. Melnikova I. RNA-based therapies. Nat Rev Drug Dis 2007; 6:863-4.
52. Ovcharenko D, Jarvis R, Hunicke-Smith S, Kelnar K, Brown D. High-throughput RNAi screening in vitro: from cell lines to primary cells. RNA 2005; 11:985-93.
53. Chan EY, Kir S, Tooze SA. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 2007; 282:25464-74.
54. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-9.
55. Herrero-Martín G, Høyer-Hansen M, García- García C, Fumarola C, Farkas T, López-Rivas A, Jäättelä M. TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. EMBO J 2009; 28:677-85.
56. Meijer AJ, Codogno P. AMP-activated protein kinase and autophagy. Autophagy 2007; 3:238-40.
57. Harhaji-Trajkovic L, Vilimanovich U, Kravic-Stevovic T, Bumbasirevic V, Trajkovic V. AMPK-mediated autophagy inhibits apoptosis in cisplatin-treated tumor cells. J Cell Mol Med 2009; In press.
58. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, et al. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 2007; 9:218-24. (Pubitemid 46420865)
59. Zhang, Y., Wu, Y., Cheng, Y., Zhao, Z., Tashiro, S., Onodera, S., and Ikejima, T. (2008) Fas-mediated autophagy requires JNK activation in HeLa cells. Biochem Biophys Res Commun 2008; 377:1205-10.
60. Zhang Y, Wu Y, Cheng Y, Zhao Z, Tashiro S, Onodera S, Ikejima T. Involvement of PKC signal pathways in oridonin-induced autophagy in HeLa cells: a protective mechanism against apoptosis, Biochem Biophys Res Commun 378, 273-278.
61. Wu H, Zhu H, Liu DX, Niu TK, Ren X, Patel R, Hait WN, Yang JM. Silencing of elongation factor-2 kinase potentiates the effect of 2-deoxy-D-glucose against human glioma cells through blunting of autophagy. Cancer Res 2009; 69:2453-60.
62. Shinojima N, Yokoyama T, Kondo Y, Kondo S. Roles of the Akt/mTOR/p70S6K and ERK1/2 signaling pathways in curcumin-induced autophagy. Autophagy 2007; 3:635-7.
63. Sivaprasad U, Basu A. Inhibition of ERK attenuates autophagy and potentiates tumour necrosis factor-alpha-induced cell death in MCF-7 cells. J Cell Mol Med 2008; 12:1265-71.
64. Park MA, Zhang G, Norris J, Hylemon PB, Fisher PB, Grant S, Dent P. Regulation of autophagy by ceramide-CD95-PERK signaling, Autophagy 2008; 4:929-31.
65. Park MA, Curiel DT, Koumenis C, Graf M, Chen CS, Fisher PB, Grant S, Dent P. PERK-dependent regulation of HSP70 expression and the regulation of autophagy; Autophagy 2008; 4364-7.
66. Wang SH, Shih YL, Kuo TC, Ko WC, Shih CM. Cadmium toxicity toward autophagy through ROS-activated GSK-3beta in mesangial cells. Toxicol Sci 2009; 108:124-31.
67. Meijer AJ, Codogno P. Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol 2004; 36:2445-62.
68. Papandreou I, Lim AL, Laderoute K, Denko NC. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 2008; 15:1572-81.
69. Li DD, Wang LL, Deng R, Tang J, Shen Y, Guo JF, et al. The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agents-induced autophagy in cancer cells. Oncogene 2009; 28:886-98.
70. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, Jung JU. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006; 8:688-99.
71. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007; 9:1142-51.
72. Wei Y, Sinha S, Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 2008; 4:949-51.
73. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 2008; 30:678-88.
74. Hait WN, Wu H, Jin S, Yang JM. Elongation factor-2 kinase: its role in protein synthesis and autophagy. Autophagy 2006; 2:294-6.
75. Wu H, Yang JM, Jin S, Zhang H, Hait WN. Elongation factor-2 kinase regulates autophagy in human glioblastoma cells. Cancer Res 2006; 66:3015-23.
76. Gozuacik D, Kimchi A. DAPk protein family and cancer. Autophagy 2006; 2:74-9.
77. Hara T, Mizushima N. Role of ULK-FIP200 complex in mammalian autophagy: FIP200, a counterpart of yeast Atg17? Autophagy 2009; 5:85-87.
78. Ganley IG, Lam du H, Wang J, Ding X, Chen S, Jiang X. ULK1-ATG13-FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305.
79. L and induction of autophagy. EMBO Rep 2009; 10:285-92.
80. Chan EY, Longatti A, McKnight NC, Tooze SA. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol 2009; 29:157-71.
81. Congreve M, Carr R, Murray C, Jhoti H. A 'rule of three' for fragment-based lead discovery? Drug Discov Today 2003; 8:876-7.
82. Lukovic E, Gonzalez-Vera JA, Imperiali B. Recognition-domain focused chemosensors: versatile and efficient reporters of protein kinase activity. J Am Chem Soc 2008; 130:12821-7.
83. Shults MD, Carrico-Moniz D, Imperiali B. Optimal Sox-based fluorescent chemosensor design for serine/threonine protein kinases. Anal Biochem 2006; 352:198-207.
84. Rubinsztein D, Gestwicki JE, Klionsky D. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6:304-12.
85. Scott RC, Juhász G, Neufeld TP Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 2007; 17:1-11. (Pubitemid 46027564)