Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways

Autophagy

Volumn 11, Issue 4, 2015, Pages 629-642

  Zhang, Jianbin ^a   Ng, Shukie ^a   Wang, Jigang ^c   Zhou, Jing ^d   Tan, Shi Hao ^a,b   Yang, Naidi ^a   Lin, Qingsong ^c   Xia, Dajing ^e   Shen, Han Ming ^a,b,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d Guangxi Scientific Experimental Center of Traditional Chinese Medicine   (China)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

Autophagy; Cancer; Cell death; FOXO1; Histone deacetylase inhibitors; MTOR

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; TRANSCRIPTION FACTOR FKHR; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; APOPTOSIS; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; AUTOPHAGY; CELL SURVIVAL; FORKHEAD BOX PROTEIN O1; FORKHEAD TRANSCRIPTION FACTORS; HISTONE DEACETYLASE INHIBITORS; HUMANS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84941218863     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1023981     Document Type: Article

References (66)

1. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10.1146/annurev-genet-102808-114910
2. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10(7):458-67; PMID:19491929; http://dx.doi.org/10.1038/nrm2708
3. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132(1):27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
4. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12(9):823-30; PMID:20811354; http://dx.doi.org/10.1038/ncb0910-823
5. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21(22):2861-2873; PMID:18006683; http://dx.doi.org/10.1101/gad.1599207
6. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20 (7):1981-91; PMID:19211835; http://dx.doi.org/10.1091/mbc.E08-12-1248
7. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 2010; 22 (2):132-9; PMID:20056399; http://dx.doi.org/10.1016/j.ceb.2009.12.004
8. Lee DF, Hung MC. All roads lead to mTOR: integrating inflammation and tumor angiogenesis. Cell Cycle 2007; 6(24):3011-4; PMID:18073529; http://dx.doi.org/10.4161/cc.6.24.5085
9. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and age- ing. Nat Rev Mol Cell Biol 2010; 12(1):21-35; PMID:21157483; http://dx.doi.org/10.1038/nrm3025
10. Jewell JL, Russell RC, Guan KL. Amino acid signalling upstream of mTOR. Nat Rev Mol Cell Biol 2013; 14 (3):133-9; PMID:23361334; http://dx.doi.org/10.1038/nrm3522
11. Wong PM, Puente C, Ganley IG, Jiang X. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 2013; 9(2):124-37; PMID:23295650; http://dx.doi.org/10.4161/auto.23323
12. Rosato RR, Almenara JA, Dai Y, Grant S. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2003; 2(12):1273-84; PMID:14707268
13. Emanuele S, Lauricella M, Tesoriere G. Histone deacetylase inhibitors: apoptotic effects and clinical implica- tions (Review). Int J Oncol 2008; 33(4):637-46; PMID:18813776
14. Yang Y, Zhao Y, Liao W, Yang J, Wu L, Zheng Z, Yu Y, Zhou W, Li L, Feng J, et al. Acetylation of FoxO1 acti- vates Bim expression to induce apoptosis in response to histone deacetylase inhibitor depsipeptide treatment. Neoplasia 2009; 11(4):313-24; PMID:19308286
15. Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, Chiao JH, Reilly JF, Ricker JL, Richon VM, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T- cell lymphoma (CTCL). Blood 2007; 109(1):31-9; PMID:16960145; http://dx.doi.org/10.1182/blood-2006-06-025999
16. Kim HJ, Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 2011; 3(2):166-79; PMID:21416059
17. Gillespie S, Borrow J, Zhang XD, Hersey P. Bim plays a crucial role in synergistic induction of apoptosis by the histone deacetylase inhibitor SBHA and TRAIL in melanoma cells. Apoptosis 2006; 11(12):2251-65; PMID:17051334; http://dx.doi.org/10.1007/s10495-006-0283-6
18. Inoue S, Riley J, Gant TW, Dyer MJ, Cohen GM. Apoptosis induced by histone deacetylase inhibitors in leukemic cells is mediated by Bim and Noxa. Leukemia 2007; 21(8):1773-82; PMID:17525724; http://dx.doi.org/10.1038/sj.leu.2404760
19. 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(8):1057-65; PMID:20962572; http://dx.doi.org/10.4161/auto.6.8.13365
20. Gammoh N, Lam D, Puente C, Ganley I, Marks PA, Jiang X. Role of autophagy in histone deacetylase inhibitor- induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci U S A 2012; 109(17):6561-5; PMID:22493;60; http://dx.doi.org/10.1073/pnas.1204429109
21. Yang PM, Chen CC. Life or death? Autophagy in anticancer therapies with statins and histone deacetylase inhibitors. Autophagy 2010; 7(1):107-8; PMID:21057221; http://dx.doi.org/10.4161/auto.7.1.13988
22. Hrzenjak A, Kremser ML, Strohmeier B, Moinfar F, Zatloukal K, Denk H. SAHA induces caspase-indepen- dent, autophagic cell death of endometrial stromal sarcoma cells by influencing the mTOR pathway. J Pathol 2008; 216(4):495-04; PMID:18850582; http://dx.doi.org/10.1002/path.2434
23. Carew JS, Medina EC, Esquivel JA, 2nd, Mahalingam D, Swords R, Kelly K, Zhang H, Huang P, Mita AC, Mita MM, et al. Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J Cell Mol Med 2009; 14(10):2448-59; PMID:19583815; http://dx.doi.org/10.1111/j.1582-4934.2009.00832.x
24. Lopez G, Torres K, Liu J, Hernandez B, Young E, Belousov R, Bolshakov S, Lazar AJ, Slopis JM, McCutcheon IE, et al. Autophagic survival in resistance to histone deacetylase inhibitors: novel strategies to treat malignant peripheral nerve sheath tumors. Cancer Res 2010; 71(1):185-96; PMID:21084276; http://dx. doi.org/10.1158/0008-5472.CAN-10-2799
25. Eijkelenboom A, Burgering BM. FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 2013; 14(2):83-97; PMID:23325358; http://dx.doi.org/10.1038/nrm3507
26. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Bur- gering BM. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002; 419(6904):316-21; PMID:12239572; http://dx.doi.org/10.1038/nature01036
27. Dijkers PF, Medema RH, Pals C, Banerji L, Thomas NS, Lam EW, Burgering BM, Raaijmakers JA, Lammers JW, Koenderman L, et al. Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27(KIP1). Mol Cell Biol 2000; 20(24):9138-48; PMID:11094066; http://dx.doi.org/10.1128/MCB.20.24.9138-9148.2000
28. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 2000; 10 (19):1201-4; PMID:11050388; http://dx.doi.org/10.1016/S0960-9822(00)00728-4
29. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120(Pt 15):2479-87; PMID:17646672; http://dx.doi.org/10.1242/jcs.001222
30. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96(6):857-68; PMID:10102273; http://dx.doi.org/10.1016/S0092-8674(00)80595-4
31. Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L, Zhu WG. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nature cell biology 2010; 12 (7):665-75; PMID:20543840; http://dx.doi.org/10.1038/ncb2069
32. Xiao D, Bommareddy A, Kim SH, Sehrawat A, Hahm ER, Singh SV. Benzyl isothiocyanate causes FoxO1- mediated autophagic death in human breast cancer cells. PLoS One 2012; 7(3): e32597; PMID:22457718
33. Han J, Pan XY, Xu Y, Xiao Y, An Y, Tie L, Pan Y, Li XJ. Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 2012; 8(5):812-25; PMID:22622204; http://dx.doi.org/10.4161/auto.19471
34. Michaelis M, Suhan T, Michaelis UR, Beek K, Rothweiler F, Tausch L, Werz O, Eikel D, Zornig M, Nau H, et al. Valproic acid induces extracellular signal-regulated kinase 1/2 activation and inhibits apoptosis in endothelial cells. Cell Death Differ 2006; 13(3):446-53; PMID:16167071; http://dx.doi.org/10.1038/sj.cdd.4401759
35. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995; 80(2):293-9; PMID:7834749; http://dx.doi.org/10.1016/0092-8674(95)90412-3
36. Tokino T, Nakamura Y. The role of p53-target genes in human cancer. Crit Rev Oncol Hematol 2000; 33 (1):1-6; PMID:10714958; http://dx.doi.org/10.1016/S1040-8428(99)00051-7
37. Shankar S, Chen Q, Srivastava RK. Inhibition of PI3K/ AKT and MEK/ERK pathways act synergistically to enhance antiangiogenic effects of EGCG through acti- vation of FOXO transcription factor. J Mol Signal 2008; 3:7; PMID:18355401; http://dx.doi.org/10.1186/1750-2187-3-7
38. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 2005; 24(50):7410-25; PMID:16288288; http://dx.doi.org/10.1038/sj.onc.1209086
39. Reagan-Shaw S, Ahmad N. The role of Forkhead-box Class O (FoxO) transcription factors in cancer: a target for the management of cancer. Toxicol Appl Pharmacol 2007; 224(3):360-8; PMID:17275054; http://dx.doi.org/10.1016/j.taap.2006.12.003
40. Nagashima T, Shigematsu N, Maruki R, Urano Y, Tanaka H, Shimaya A, Shimokawa T, Shibasaki M. Discovery of novel forkhead box O1 inhibitors for treating type 2 diabetes: improvement of fasting glycemia in diabetic db/db mice. Mol Pharmacol 2010; 78 (5):961-70; PMID:20736318; http://dx.doi.org/10.1124/mol.110.065714
41. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6(6):472-83; PMID:18054316; http://dx.doi.org/10.1016/j.cmet.2007.11.004
42. Kwiatkowski DJ. Rhebbing up mTOR: new insights on TSC1 and TSC2, and the pathogenesis of tuberous sclerosis. Cancer Biol Ther 2003; 2(5):471-6; PMID:14614311; http://dx.doi.org/10.4161/cbt.2.5.446
43. Chen CC, Jeon SM, Bhaskar PT, Nogueira V, Sundar- arajan D, Tonic I, Park Y, Hay N. FoxOs inhibit mTORC1 and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev Cell 2010; 18(4):592-604; PMID:20412774; http://dx.doi.org/10.1016/j.devcel.2010.03.008
44. Nogueira V, Park Y, Chen CC, Xu PZ, Chen ML, Tonic I, Unterman T, Hay N. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 2008; 14(6):458-70; PMID:19061837; http://dx.doi.org/10.1016/j.ccr.2008.11.003
45. Banreti A, Sass M, Graba Y. The emerging role of acetylation in the regulation of autophagy. Autophagy 2013; 9(6):819-29; PMID:23466676; http://dx.doi.org/10.4161/auto.23908
46. Marino G, Pietrocola F, Eisenberg T, Kong Y, Malik SA, Andryushkova A, Schroeder S, Pendl T, Harger A, Niso-Santano M, Zamzami N, et al. Regulation of autophagy by cytosolic acetyl-coenzyme A. Molecular cell 2014; 53(5):710-25; PMID:24560926; http://dx.doi.org/10.1016/j.molcel.2014.01.016
47. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW, Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A 2008; 105 (9):3374-9; PMID:18296641; http://dx.doi.org/10.1073/pnas.0712145105
48. Eisenberg T, Knauer H, Schauer A, Buttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, et al. Induction of autophagy by spermidine promotes longevity. Nature cell biology 2009; 11(11):1305-14; PMID:19801973; http://dx.doi.org/10.1038/ncb1975
49. Morselli E, Marino G, Bennetzen MV, Eisenberg T, Megalou E, Schroeder S, Cabrera S, Benit P, Rustin P, Criollo A, et al. Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol 2011; 192(4):615-29; PMID:21339330; http://dx.doi.org/10.1083/jcb.201008167
50. Yi C, Ma M, Ran L, Zheng J, Tong J, Zhu J, Ma C, Sun Y, Zhang S, Feng W, Zhu L, et al. Function and molecu- lar mechanism of acetylation in autophagy regulation. Science 2012; 336(6080):474-7; PMID:22539722; http://dx.doi.org/10.1126/science.1216990
51. Lin SY, Li TY, Liu Q, Zhang C, Li X, Chen Y, Zhang SM, Lian G, Liu Q, Ruan K, et al. GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science 2012; 336(6080):477-81; PMID:22539723; http://dx.doi.org/10.1126/science.1217032
52. Zhao Y, Li X, Cai MY, Ma K, Yang J, Zhou J, Fu W, Wei FZ, Wang L, Xie D, et al. XBP-1u suppresses autophagy by promoting the degradation of FoxO1 in cancer cells. Cell research 2013; 23(4):491-07; PMID:23277279; http://dx.doi.org/10.1038/cr.2013.2
53. Zhou J, Liao W, Yang J, Ma K, Li X, Wang Y, Wang D, Wang L, Zhang Y, Yin Y, et al. FOXO3 induces FOXO1-dependent autophagy by activating the AKT1 signaling pathway. Autophagy 2012; 8(12):1712-23; PMID:22931788; http://dx.doi.org/10.4161/auto.21830
54. Tan SH, Shui G, Zhou J, Li JJ, Bay BH, Wenk MR, Shen HM. Induction of autophagy by palmitic acid via protein kinase C-mediated signaling pathway independent of mTOR (mammalian target of rapamycin). J Biol Chem 2012; 287(18):14364-76; PMID:22408252; http://dx.doi.org/10.1074/jbc.M111.294157
55. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004; 303(5666):2011-15; PMID:14976264; http://dx.doi.org/10.1126/science.1094637
56. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W, Bultsma Y, McBurney M, Guarente L. Mammalian SIRT1 represses forkhead transcription factors. Cell 2004; 116(4):551-63; PMID:14980222; http://dx.doi.org/10.1016/S0092-8674(04)00126-6
57. Beharry AW, Sandesara PB, Roberts BM, Ferreira LF, Senf SM, Judge AR. HDAC1 activates FoxO and is both sufficient and required for skeletal muscle atrophy. J Cell Sci, 127(Pt 7):1441-53; PMID:24463822; http://dx.doi.org/10.1242/jcs.136390
58. Dansen TB, Burgering BM. Unravelling the tumorsuppressive functions of FOXO proteins. Trends Cell Biol 2008; 18(9):421-9; PMID:18715783; http://dx.doi.org/10.1016/j.tcb.2008.07.004
59. Nasrin N, Ogg S, Cahill CM, Biggs W, Nui S, Dore J, Calvo D, Shi Y, Ruvkun G, Alexander-Bridges MC. DAF-16 recruits the CREB-binding protein coactivator complex to the insulin-like growth factor binding protein 1 promoter in HepG2 cells. Proc Natl Acad Sci U S A 2000; 97(19):10412-7; PMID:10973497; http://dx.doi.org/10.1073/pnas.190326997
60. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 Plays an Essential Role in Mediating Starvation-Induced Autophagy in Cardiac Myocytes. Circ Res 2010; 107 (12):1470-82; PMID:20947830; http://dx.doi.org/10.1161/CIRCRESAHA.110.227371
61. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H, Barnett J, Leslie NR, Cheng S, Shepherd PR, et al. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J Cell Biol 2004; 166(2):213-23; PMID:15249583; http://dx.doi.org/10.1083/jcb.200403069
62. Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G, Ngo L, Holmgren A, Jiang X, Marks PA. Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci USA 2005;102(3):673-8;PMID:15637150;http://dx.doi.org/10.1073/pnas.0408732102
63. Ellis L, Bots M, Lindemann RK, Bolden JE, Newbold A, Cluse LA, Scott CL, Strasser A, Atadja P, Lowe SW, et al. The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood 2009; 114(2):380-93; PMID:19383971; http://dx.doi.org/10.1182/blood-2008-10-182758
64. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkanna- gari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P, et al. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther 2012; 11(4):973-83; PMID:22367781; http://dx.doi.org/10.1158/1535-7163.MCT-11-0979
65. Zhang H, Cicchetti G, Onda H, Koon HB, Asrican K, Bajraszewski N, Carpenter CL, Kwiatkowski DJ. Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR. J Clin Invest 2003; 112(8):1223-33; PMID:14561707; http://dx.doi.org/10.1172/JCI200317222
66. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004; 432(7020):1032-6; PMID:15525940; http://dx.doi.org/10.1038/nature 03029