Histone deacetylase 10 promotes autophagy-mediated cell survival

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 28, 2013, Pages

  Oehme, Ina ^a   Linke, Jan Peter ^a   Böck, Barbara C ^b,c   Milde, Till ^a,b   Lodrini, Marco ^a   Hartenstein, Bettina ^a   Wiegand, Inga ^a   Eckert, Christian ^d   Roth, Wilfried ^a   Kool, Marcel ^a   Kaden, Sylvia ^a   Gröne, Hermann Josef ^a   Schulte, Johannes H ^a,e,f   Lindner, Sven ^e   Hamacher Brady, Anne ^a   Brady, Nathan R ^a   Deubzer, Hedwig E ^a,b   Witt, Olaf ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c Centre for Biomedicine and Medical Technology   (Germany)

^d Tech Evotec (Munich) GmbH   (Germany)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

^f UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Childhood tumors; Drug resistance; Hdac inhibitor

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 10; PROTEIN P62; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL SURVIVAL; CHEMOSENSITIZATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEACETYLATION; ENZYME DEGRADATION; ENZYME INHIBITION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LYSOSOME; NEUROBLASTOMA; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; TREATMENT OUTCOME;

CHILDHOOD TUMORS; DRUG RESISTANCE; HDAC INHIBITOR;

AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NEUROBLASTOMA; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84879919205     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300113110     Document Type: Article

References (59)

1. Pan Y, et al. (2011) Targeting autophagy augments in vitro and in vivo antimyeloma activity of DNA-damaging chemotherapy. Clin Cancer Res 17(10):3248-3258.
2. Klionsky DJ, Cuervo AM, Seglen PO (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3(3):181-206. (Pubitemid 46752679)
3. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290(5497):1717-1721. (Pubitemid 32004796)
4. Dice JF (2007) Chaperone-mediated autophagy. Autophagy 3(4):295-299.
5. Agarraberes FA, Dice JF (2001) A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 114(Pt 13):2491-2499. (Pubitemid 32684803)
6. Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM (2008) The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell Biol 28(18):5747-5763.
7. Bolden JE, Peart MJ, Johnstone RW (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5(9):769-784. (Pubitemid 44348499)
8. Witt O, Deubzer HE, Milde T, Oehme I (2009) HDAC family: What are the cancer relevant targets? Cancer Lett 277(1):8-21.
9. Glaser KB (2007) HDAC inhibitors: Clinical update and mechanism-based potential. Biochem Pharmacol 74(5):659-671.
10. Shao Y, Gao Z, Marks PA, Jiang X (2004) Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 101(52):18030-18035. (Pubitemid 40054069)
11. Cao Q, et al. (2008) 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 40(2):272-283. (Pubitemid 350137879)
12. Thomas S, Thurn KT, Biçaku E, Marchion DC, Münster PN (2011) Addition of a histone deacetylase inhibitor redirects tamoxifen-treated breast cancer cells into apoptosis, which is opposed by the induction of autophagy. Breast Cancer Res Treat 130(2):437-447.
13. Lopez G, Torres K, Lev D (2011) Autophagy blockade enhances HDAC inhibitors' proapoptotic effects: Potential implications for the treatment of a therapeutic-resistant malignancy. Autophagy 7(4):440-441.
14. Liu YL, et al. (2010) Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 6(8):1057-1065.
15. Carew JS, et al. (2010) Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J Cell Mol Med 14(10):2448-2459.
16. Yamamoto S, et al. (2008) Suberoylanilide hydroxamic acid (SAHA) induces apoptosis or autophagy-associated cell death in chondrosarcoma cell lines. Anticancer Res 28(3A):1585-1591. (Pubitemid 351892934)
17. Carew JS, et al. (2007) Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 110(1):313-322. (Pubitemid 47026849)
18. Choudhary C, et al. (2009) Lysine acetylation targets protein complexes and coregulates major cellular functions. Science 325(5942):834-840.
19. Gu W, Roeder RG (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90(4):595-606. (Pubitemid 27357952)
20. Hubbert C, et al. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417(6887):455-458. (Pubitemid 34563539)
21. Bali P, et al. (2005) Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: A novel basis for antileukemia activity of histone deacetylase inhibitors. J Biol Chem 280(29):26729-26734. (Pubitemid 41040705)
22. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB (2003) Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J 370(Pt 3):737-749. (Pubitemid 36399066)
23. Gao L, Cueto MA, Asselbergs F, Atadja P (2002) Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J Biol Chem 277(28):25748-25755. (Pubitemid 34951896)
24. Rodriguez-Gonzalez A, et al. (2008) Role of the aggresome pathway in cancer: Targeting histone deacetylase 6-dependent protein degradation. Cancer Res 68(8):2557-2560. (Pubitemid 351556250)
25. Guardiola AR, Yao TP (2002) Molecular cloning and characterization of a novel histone deacetylase HDAC10. J Biol Chem 277(5):3350-3356. (Pubitemid 34953202)
26. Brodeur GM (2003) Neuroblastoma: Biological insights into a clinical enigma. Nat Rev Cancer 3(3):203-216.
27. Berthold F, et al. (2005) Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: A randomised controlled trial. Lancet Oncol 6(9):649-658. (Pubitemid 41222755)
28. Milde T, et al. (2010) HDAC5 and HDAC9 in medulloblastoma: Novel markers for risk stratification and role in tumor cell growth. Clin Cancer Res 16(12):3240-3252.
29. Oehme I, et al. (2009) Histone deacetylase 8 in neuroblastoma tumorigenesis. Clin Cancer Res 15(1):91-99.
30. Oehme I, Deubzer HE, Lodrini M, Milde T, Witt O (2009) Targeting of HDAC8 and investigational inhibitors in neuroblastoma. Expert Opin Investig Drugs 18(11):1605-1617.
31. Molenaar JJ, et al. (2012) Copy number defects of G1-cell cycle genes in neuroblastoma are frequent and correlate with high expression of E2F target genes and a poor prognosis. Genes Chromosomes Cancer 51(1):10-19.
32. Chen QR, et al. (2008) An integrated cross-platform prognosis study on neuroblastoma patients. Genomics 92(4):195-203.
33. Remke M, et al. (2011) FSTL5 is a marker of poor prognosis in non-WNT/non-SHH medulloblastoma. J Clin Oncol 29(29):3852-3861.
34. Bjørkøy G, et al. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171(4):603-614. (Pubitemid 41668720)
35. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140(3):313-326.
36. Bantscheff M, et al. (2011) Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat Biotechnol 29(3):255-265.
37. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL (2003) Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci USA 100(8):4389-4394. (Pubitemid 36457739)
38. Molenaar JJ, et al. (2012) LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat Genet 44(11):1199-1206.
39. Chen N, Karantza V (2011) Autophagy as a therapeutic target in cancer. Cancer Biol Ther 11(2):157-168.
40. Hundeshagen P, Hamacher-Brady A, Eils R, Brady NR (2011) Concurrent detection of autolysosome formation and lysosomal degradation by flow cytometry in a high-content screen for inducers of autophagy. BMC Biol 9:38.
41. Gogolin S, et al. (2010) MYCN/MYC-mediated drug resistance mechanisms in neuroblastoma. Int J Clin Pharmacol Ther 48(7):489-491.
42. Nylandsted J, et al. (2004) Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 200(4):425-435. (Pubitemid 39121900)
43. Doulias PT, et al. (2007) Involvement of heat shock protein-70 in the mechanism of hydrogen peroxide-induced DNA damage: The role of lysosomes and iron. Free Radic Biol Med 42(4):567-577.
44. Kirkegaard T, et al. (2010) Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463(7280):549-553.
45. Leu JI, Pimkina J, Pandey P, Murphy ME, George DL (2011) HSP70 inhibition by the small-molecule 2-phenylethynesulfonamide impairs protein clearance pathways in tumor cells. Mol Cancer Res 9(7):936-947.
46. Leu JI, Pimkina J, Frank A, Murphy ME, George DL (2009) A small molecule inhibitor of inducible heat shock protein 70. Mol Cell 36(1):15-27.
47. Lai IL, et al. (2010) Histone deacetylase 10 relieves repression on the melanogenic program by maintaining the deacetylation status of repressors. J Biol Chem 285(10):7187-7196.
48. Witt O, Deubzer HE, Lodrini M, Milde T, Oehme I (2009) Targeting histone deacetylases in neuroblastoma. Curr Pharm Des 15(4):436-447.
49. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280(48):40282-40292. (Pubitemid 41779165)
50. Kawaguchi Y, et al. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115(6):727-738. (Pubitemid 38030301)
51. Pandey UB, Batlevi Y, Baehrecke EH, Taylor JP (2007) HDAC6 at the intersection of autophagy, the ubiquitin-proteasome system and neurodegeneration. Autophagy 3(6):643-645. (Pubitemid 350064219)
52. Lee JY, et al. (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29(5):969-980.
53. Lee JH, et al. (2010) Inhibition of histone deacetylase 10 induces thioredoxin-interacting protein and causes accumulation of reactive oxygen species in SNU-620 human gastric cancer cells. Mol Cells 30(2):107-112.
54. Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581(19):3702-3710. (Pubitemid 47081009)
55. Mariño G, et al. (2003) Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem 278(6):3671-3678. (Pubitemid 36801091)
56. Sharma K, et al. (2009) Proteomics strategy for quantitative protein interaction profiling in cell extracts. Nat Methods 6(10):741-744.
57. Oehme I, Bösser S, Zörnig M (2006) Agonists of an ecdysone-inducible mammalian expression system inhibit Fas Ligand- and TRAIL-induced apoptosis in the human colon carcinoma cell line RKO. Cell Death Differ 13(2):189-201. (Pubitemid 43102203)
58. Moriyama Y, Takano T, Ohkuma S (1982) Acridine orange as a fluorescent probe for lysosomal proton pump. J Biochem 92(4):1333-1336.
59. Shvets E, Fass E, Elazar Z (2008) Utilizing flow cytometry to monitor autophagy in living mammalian cells. Autophagy 4(5):621-628.