Beclin-1 and its role as a target for anticancer therapy

Journal of Physiology and Pharmacology

Volumn 65, Issue 4, 2014, Pages 459-467

  Toton, E ^a   Lisiak, N ^a   Sawicka, P ^a   Rybczynska, Maria ^a  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

Anticancer therapy; Autophagy; Beclin 1; Cancer; Signal transduction

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; MEMBRANE PROTEIN;

ANIMAL; AUTOPHAGY; CHEMISTRY; HUMAN; METABOLISM; NEOPLASMS;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; HUMANS; MEMBRANE PROTEINS; NEOPLASMS;

EID: 84906887552     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Review

References (94)

1. Kroemer G, Galluzzi L, Vandenabeele P, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16: 3-11.
2. Ouyang L, Shi Z, Zhao S, et al. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif 2012; 45: 487-498.
3. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8: 931-937.
4. Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 1992; 119: 301-311.
5. Mizushima N, Sugita H, Yoshimori T, Ohsumi Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 1998; 273: 33889-33892.
6. Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med 2003; 9: 65-76.
7. Rami A. Review: autophagy in neurodegeneration: firefighter and/or incendiarist? Neuropathol Appl Neurobiol 2009; 35: 449-461.
8. Carrera AC. TOR signaling in mammals. J Cell Sci 2004; 117: 4615-4616.
9. Mehrpour M, Esclatine A, Beau I, Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res 2010; 20: 748-762.
10. Chua CE, Gan BQ, Tang BL. Involvement of members of the Rab family and related small GTPases in autophagosome formation and maturation. Cell Mol Life Sci 2011; 68: 3349-3358.
11. Lynch-Day MA, Klionsky DJ. The Cvt pathway as a model for selective autophagy. FEBS Lett 2010; 584: 1359-1366.
12. Wirawan E, Vanden Berghe T, Lippens S, Agostinis P, Vandenabeele P. Autophagy: for better or for worse. Cell Res 2012; 22: 43-61.
13. Kaushik S, Cuervo AM. Chaperones in autophagy. Pharmacol Res 2012; 66: 484-493.
14. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
15. Cui J, Gong Z, Shen HM. The role of authophagy in liver cancer: molecular mechanism and potential therapeutic targets. Biochim Biophys Acta 2013; 1836: 15-26.
16. Zhang J. Autophagy and mitophagy in cellular damage control. Redox Biol 2013; 1: 19-23.
17. Hou W, Zhang Q, Yan Z, at al. Strange attractors: DAMPs and autophagy link tumor cell death and immunity. Cell Death Dis 2013; 4: e966.
18. Longatti A, Tooze SA. Vesicular trafficking and autophagosome formation. Cell Death Differ 2009; 16: 956-965.
19. Roy S, Debnath J. Autophagy and tumorigenesis. Semin Immunopathol 2010; 32: 383-396.
20. Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 2011; 80: 125-156.
21. Reggiori F, Shintani T, Nair U, Klionsky DJ. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 2005; 1: 101-109.
22. Suzuki K, Ohsumi Y. Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett 2007; 581: 2156-2161.
23. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 2010; 22: 132-139.
24. Li Z, Chen B, Wu Y, Jin F, Xia Y, Liu X. Genetic and epigenetic silencing of the beclin 1 gene in sporadic breast tumors. BMC Cancer 2010; 10: 98. doi: 10.1186/1471-2407- 10-98.
25. Li BX, Li CY, Peng RQ, et al. The expression of Beclin 1 is associated with favorable prognosis in stage IIIB colon cancers. Autophagy 2009; 5: 303-306.
26. Adi-Harel S, Erlich S, Schmukler E, et al. Beclin 1 selfassociation is independent of autophagy induction by amino acid deprivation and rapamycin treatment. J Cell Biochem 2010; 110: 1262-1271.
27. Noble CG, Dong JM, Manser E, Song H. Bcl-xL and UVRAG cause a monomer-dimer switch in Beclin 1. J Biol Chem 2008; 283: 26274-26282.
28. Shi CS, Kehrl JH. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci Signal 2010; 3: ra42.
29. Huang W, Choi W, Hu W, et al. Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein. Cell Res 2012; 22: 473-489.
30. Liang XH, Yu J, Brown K, Levine B. Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res 2001; 61: 3443-3449.
31. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
32. Shin JY, Park HJ, Kim HN, et al. Mesenchymal stem cells enhance autophagy and increase b-amyloid clearance in Alzheimer disease models. Autophagy 2014; 10: 1-13.
33. Pereira GJ, Tressoldi N, Hirata H, Bincoletto C, Smaili SS. Autophagy as a neuroprotective mechanism against 3- nitropropionic acid-induced murine astrocyte cell death. Neurochem Res 2013; 38: 2418-2426.
34. Geng QR, Xu DZ, He LJ, et al. Beclin-1 expression is a significant predictor of survival in patients with lymph nodepositive gastric cancer. PLoS One 2012; 7: e45968.
35. Shibata M, Lu T, Furuya T, et al. Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem 2006; 281: 14474-14485.
36. Hamacher-Brady A, Brady NR, Gottlieb RA. The interplay between pro-death and pro-survival signaling pathways in myocardial ischemia/reperfusion injury: apoptosis meets autophagy. Cardiovasc Drugs Ther 2006; 20: 445-462.
37. Peng W, Liu Y, Xu WJ, Xia QH. Role of Beclin 1-dependent autophagy in cardioprotection of ischemic preconditioning. J Huazhong Univ Sci Technolog Med Sci 2013; 33: 51-56.
38. Xu C, Liu J, Hsu LC, Luo Y, Xiang R, Chuang TH. Functional interaction of heat shock protein 90 and Beclin 1 modulates Toll-like receptor-mediated autophagy. FASEB J 2011; 25: 2700-2710.
39. Kang R, Zeh H, Lotze M, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18: 571-580.
40. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14: 1576-1582.
41. Matsunaga K, Saitoh T, Tabata K, et al. Two Beclin 1- binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biology. 2009; 11: 385-396.
42. Liu B, Cheng Y, Liu Q, Bao J, Yang JM. Autophagic pathways as new targets for cancer drug development. Acta Pharmacol Sin 2010; 31: 1154-1164.
43. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19: 5360-5372.
44. Takahashi Y, Coppola D, Matsushita N, et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007; 9: 1142-1151.
45. Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q. Identification of Barkor as a mammalian autophagyspecific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 2008; 105: 19211-19216.
46. Fan W, Nassiri A, Zhong Q. Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc Natl Acad Sci USA 2011, 108: 7769-7774.
47. Di Bartolomeo S, Corazzari M, Nazio F, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010; 191: 155-168.
48. He C, Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 2010; 22: 140-149.
49. Molejon MI, Ropolo A, Re AL, Boggio V, Vaccaro MI. The VMP1-Beclin 1 interaction regulates autophagy induction. Sci Rep 2013; 3: 1055. doi: 10.1038/srep01055.
50. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1- mediated phosphorylation of Bcl-2 regulates starvationinduced autophagy. Mol Cell 2008; 30: 678-688.
51. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122: 927-939.
52. Chang NC, Nguyen M, Germain M, Shore GC. Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1. EMBO J 2010; 29: 606-618.
53. Kang R, Livesey KM, Zeh HJ, Loze MT, Tang D. HMGB1: a novel Beclin 1-binding protein active in autophagy. Autophagy 2010; 6: 1209-1211.
54. Tang D, Kang R, Livesey KM, et al. Endogenous HMGB1 regulates autophagy. J Cell Biol 2010; 190: 881-892.
55. Zalckvar E, Berissi H, Mizrachy L, et al. DAP-kinasemediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep 2009; 10: 285-292.
56. Liang C, Jung JU. Autophagy genes as tumor supressors. Curr Opin Cell Biol 2010; 22: 226-233.
57. Liu B, Bao JK, Yang JM, Cheng Y. Targeting autophagic pathways for cancer drug discovery. Chin J Cancer 2013; 32: 113-120.
58. Cao Y, Klionsky D. Physiological functions of Atg6/Beclin 1: a unique autophagy- related protein. Cell Res 2007; 17: 839-849.
59. Sun Q, Fan W, Zhong Q. Regulation of Beclin 1 in autophagy. Autophagy. 2009; 5: 713-716.
60. Carew JS, Kelly KR, Nawrocki ST. Autophagy as a target for cancer therapy: new developments. Cancer Manag Res 2012; 4: 357-365.
61. Aita VM, Liang XH, Murty VV, et al. Cloning and genomic organization of Beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999; 59: 59-65.
62. Gajewska M, Sobolewska A, Kozlowski M, Motyl T. Role of autophagy in mammary gland development. J Physiol Pharmacol 2008; 59 (Suppl. 9): 237-249.
63. Miracco C, Cosci E, Oliveri G, et al. Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int J Oncol 2007; 30: 429-436.
64. Koukourakis M, Giatromanolaki A, Sivridis E, Pitiakoudis M, Gatter K, Harris A. Beclin 1 over- and underexpression in colorectal cancer: distinct patterns relate to prognosis and tumour hypoxia. Br J Cancer 2010; 103: 1209-1214.
65. Turcotte S, Giaccia AJ. Targeting cancer cells through autophagy for anticancer therapy. Curr Opin Cell Biol 2010; 22: 246-251.
66. Liang C, Feng P, Ku B, et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006; 8: 688-699.
67. Djavaheri-Mergny M, Maiuri MC, Kroemer G. Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene 2010; 29: 1717-1719.
68. Fu LL, Cheng Y, Liu B. Beclin-1: autophagic regulator and therapeutic target in cancer. Int J Biochem Cell Biol 2013; 45: 921-924.
69. Furuya D, Tsuji N, Yagihashi A, Watanabe N. Beclin 1 augmented cis diamminedichloroplatinum induced apoptosis via enhancing caspase-9 activity. Exp Cell Res 2005; 307: 26-40.
70. Daniel F, Legrand A, Pessayre D, Vadrot N, Descatoire V, Bernuau D. Partial Beclin 1 silencing aggravates doxorubicin- and Fas-induced apoptosis in HepG2 cells. World J Gastroenterol 2006; 12: 2895-2900.
71. Wirawan E, Vande Walle L, Kersse K, et al. Caspasemediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 2010; 1: e18.
72. Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: targeting autophagy signaling in cancer cells - trick or treats? FEBS J 2009; 276: 6084-6096.
73. Crighton D, Wilkinson S, Ryan KM. DRAM links autophagy to p53 and programmed cell death. Autophagy 2007; 3: 72-74.
74. Ertmer A, Huber V, Gilch S, et. al. The anticancer drug imatinib induces cellular autophagy. Leukemia 2007; 21: 936-942.
75. Tasdemir E, Maiuri MC, Galluzzi L, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 2008; 10: 676-687.
76. Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010; 6: 322-329.
77. Calgarotto AK, da Silva Pereira GJ, Bechara A, et al. Autophagy inhibited Ehrlich ascitic tumor cells apoptosis induced by the nitrostyrene derivative compounds: relationship with cytosolic calcium mobilization. Eur J Pharmacol 2012; 678: 6-14.
78. Kanzawa T, Kondo Y, Ito H, Kondo S, Germano I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res 2003; 63: 2103-2108.
79. Siedlecka-Kroplewska K, Jozwik A, Boguslawski W, et al. Pterostilbene induces accumulation of autophagic vacuoles followed by cell death in HL60 human leukemia cells. J Physiol Pharmacol 2013; 64: 545-556.
80. Hu H, Chai Y, Wang L, et al. Pentagalloylglucose induces autophagy and caspase-independent programmed deaths in human PC-3 and mouse TRAMP-C2 prostate cancer cells. Mol Cancer Ther 2009; 8: 2833-2843.
81. Samaddar JS, Gaddy VT, Duplantier J, et al. A role for macroautophagy in protection against 4-hydroxytamoxifeninduced cell death and the development of antiestrogen resistance. Mol Cancer Ther 2008; 7: 2977-2987.
82. Bursch W, Ellinger A, Kienzl H, et al. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 1996; 17: 1595-1607.
83. Hoyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jaattela M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 2005; 12: 1297-1309.
84. Siddiqui A, Dandawate P, Rub R, et al. Novel aza-resveratrol analogs: synthesis, characterization and anticancer activity against breast cancer cell lines. Bioorg Med Chem Lett 2013; 23: 635-640.
85. Crazzolara R, Bradstock KF, Bendall LJ. RAD001 (Everolimus) induces autophagy in acute lymphoblastic leukemia. Autophagy 2009; 5: 727-728.
86. Kumar D, Shankar S, Srivastava RK. Rottlerin induces autophagy and apoptosis in prostate cancer stem cells via PI3K/Akt/mTOR signaling pathway. Cancer Lett 2013; 343: 179-189.
87. Kaewpiboon C, Surapinit S, Malilas W, et al. Feroniellin Ainduced autophagy causes apoptosis in multidrug-resistant human A549 lung cancer cells. Int J Oncol 2014; 44: 1233-1242.
88. Yuan G, Yan SF, Xue H, Zhang P, Sun JT, Li G. Cucurbitacin I induces protective autophagy in glioblastoma in vitro and in vivo. J Biol Chem 2014; 289: 10607-10619.
89. Kim SY, Song X, Zhang L, Bartlett DL, Lee YJ. Role of BclxL/ Beclin-1 in interplay between apoptosis and autophagy in oxaliplatin and bortezomib-induced cell death. Biochem Pharmacol 2014; 88: 178-188.
90. Tsai CW, Lai FJ, Sheu HM, et al. WWOX suppresses autophagy for inducing apoptosis in methotrexate-treated human squamous cell carcinoma. Cell Death Dis 2013; 4: e792. doi: 10.1038/cddis.2013.308.
91. Shen J, Zheng H, Ruan J, et al. Autophagy inhibition induces enhanced proapoptotic effects of ZD6474 in glioblastoma. Br J Cancer 2013; 109: 164-171.
92. Li Z, Chen B, Wu Y, Jin F, Xia Y, Liu X. Genetic and epigenetic silencing of the Beclin 1 gene in sporadic breast tumors. BMC Cancer 2010; 10: 98. doi: 10.1186/1471-2407- 10-98.
93. Korbut E, Ptak-Belowska A, Brzozowski T. Mechanisms promoting physiological cells progression into tumorigenesis. J Physiol Pharmacol 2012; 63: 565-570.
94. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 2009; 15: 5308-5316.