BIRC5/Survivin as a target for glycolysis inhibition in high-stage neuroblastoma

Oncogene

Volumn 35, Issue 16, 2016, Pages 2052-2061

  Hagenbuchner, J ^a   Kiechl Kohlendorfer, U ^a   Obexer, P ^a,b   Ausserlechner, M J ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b TYROLEAN CANCER RESEARCH INSTITUTE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; DEOXYGLUCOSE; PARKIN; SURVIVIN; BIRC5 PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL DEATH; CELL FUSION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METABOLIC INHIBITION; MITOCHONDRION; MOUSE; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; DRUG SCREENING; METABOLISM; OXIDATIVE PHOSPHORYLATION; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; AUTOPHAGY; CELL DEATH; CELL LINE, TUMOR; DEOXYGLUCOSE; FEMALE; GLYCOLYSIS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MICE; MICE, INBRED BALB C; NEUROBLASTOMA; OXIDATIVE PHOSPHORYLATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84935522603     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.264     Document Type: Article

References (67)

1. Islam A, Kageyama H, Takada N, Kawamoto T, Takayasu H, Isogai E et al. High expression of Survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 2000; 19: 617-623.
2. Verdecia MA, Huang Hk, Dutil E, Kaiser DA, Hunter T, Noel JP. Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat Struct Mol Biol 2000; 7: 602-608.
3. Morgillo F, Woo JK, Kim ES, Hong WK, Lee HY. Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib. Cancer Res 2006; 66: 10100-10111.
4. Tran J, Master Z, Yu JL, Rak J, Dumont DJ, Kerbel RS. A role for survivin in chemoresistance of endothelial cells mediated by VEGF. Proc Natl Acad Sci 2002; 99: 4349-4354.
5. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C et al. Analysis of human transcriptomes. Nat Genet 1999; 23: 387-388.
6. Kang BH, Altieri DC. Regulation of Survivin Stability by the Aryl Hydrocarbon Receptor-interacting Protein. J Biol Chem 2006; 281: 24721-24727.
7. Dohi T, Beltrami E, Wall NR, Plescia J, Altieri DC. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 2004; 114: 1117-1127.
8. Eckelman BPS. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006; 7: 988-994.
9. Obexer P, Hagenbuchner J, Unterkircher T, Sachsenmaier N, Seifarth C, Bock G et al. Repression of BIRC5/survivin by FOXO3/FKHRL1 sensitizes human neuroblastoma cells to DNA damage-induced apoptosis. Mol Biol Cell 2009; 20: 2041-2048.
10. Hagenbuchner J, Kuznetsov AV, Obexer P, Ausserlechner MJ. BIRC5/Survivin enhances aerobic glycolysis and drug resistance by altered regulation of the mitochondrial fusion/fission machinery. Oncogene 2013; 32: 4748-4757.
11. Zhou W, Yuan J. Necroptosis in health and diseases. Semin Cell Dev Biol 2014; 35: 14-23.
12. Debnath J, Baehrecke EH, Kroemer G. Does autophagy contribute to cell death? Autophagy 2005; 1: 66-74.
13. Denton D, Xu T, Kumar S. Autophagy as a pro-death pathway. Immunol Cell Biol 2014; 93: 35-42.
14. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306: 990-995.
15. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18: 571-580.
16. 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: 927-939.
17. Niu TK, Cheng Y, Ren X, Yang JM. Interaction of Beclin 1 with survivin regulates sensitivity of human glioma cells to TRAIL-induced apoptosis. FEBS Lett 2010; 584: 3519-3524.
18. Abe A, Kokuba H. Harmol induces autophagy and subsequent apoptosis in U251MG human glioma cells through the downregulation of survivin. Oncol Rep 2012; 29: 1333-1342.
19. Ganapathy-Kanniappan S, Geschwind JF. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol Cancer 2013; 12: 152.
20. Stern R, Shuster S, Neudecker BA, Formby B. Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res 2002; 276: 24-31.
21. Wang X, Perez E, Liu R, Yan LJ, Mallet RT, Yang SH. Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells. Brain Res 2007; 1132: 1-9.
22. De Lena M, Lorusso V, Latorre A, Fanizza G, Gargano G, Caporusso L et al. Paclitaxel, cisplatin and lonidamine in advanced ovarian cancer. A phase II study. Eur J Cancer 2001; 37: 364-368.
23. Maher J, Krishan A, Lampidis T. Greater cell cycle inhibition and cytotoxicity induced by 2-deoxy-d-glucose in tumor cells treated under hypoxic vs aerobic conditions. Cancer Chemother Pharmacol 2004; 53: 116-122.
24. Stein M, Lin H, Jeyamohan C, Dvorzhinski D, Gounder M, Bray K et al. Targeting tumor metabolism with 2-deoxyglucose in patients with castrate-resistant prostate cancer and advanced malignancies. Prostate 2010; 70: 1388-1394.
25. Sachita K, Yu HJ, Yun JW, Lee JS, Cho SD. YM155 induces apoptosis through downregulation of specificity protein 1 and myeloid cell leukemia-1 in human oral cancer cell lines. J Oral Pathol Med 2014; e-pub ahead of print 5 December 2014; doi:10.1111/jop.12299.
26. Cheng Y, Diao DM, Zhang H, Zhang HF, Song YC, Dang C-X et al. Proliferation enhanced by NGF-NTRK1 signaling makes pancreatic cancer cells more sensitive to 2DG-induced apoptosis. Int J Med Sci 2013; 10: 634-640.
27. Ramírez-Peinado S, Alcázar-Limones F, Lagares-Tena L, El Mjiyad N, Caro-Maldonado A, Tirado OM et al. 2-Deoxyglucose induces noxa-dependent apoptosis in alveolar rhabdomyosarcoma. Cancer Res 2011; 71: 6796-6806.
28. Ramírez-Peinado S, León-Annicchiarico CL, Galindo-Moreno J, Iurlaro R, Caro-Maldonado A, Prehn JH et al. Glucose-starved cells do not engage in prosurvival autophagy. J Biol Chem 2013; 288: 30387-30398.
29. Huang CY, Kuo WT, Huang YC, Lee TC, Yu LCH. Resistance to hypoxia-induced necroptosis is conferred by glycolytic pyruvate scavenging of mitochondrial superoxide in colorectal cancer cells. Cell Death Dis 2013; 4: e622.
30. Singh R, Cuervo A. Autophagy in the cellular energetic balance. Cell Metab 2011; 13: 495-504.
31. Sheen JH, Zoncu R, Kim D, Sabatini D. Defective regulation of autophagy upon leucine deprivation reveals a targetable liability of human melanoma cells in vitro and in vivo. Cancer Cell 2011; 19: 613-628.
32. Stock C, Bozsaky E, Watzinger F, Poetschger U, Orel L, Lion T et al. Genes proximal and distal to MYCN are highly expressed in human neuroblastoma as visualized by comparative expressed sequence hybridization. Am J Pathol 2008; 172: 203-214.
33. Saita S, Shirane M, Nakayama KI. Selective escape of proteins from the mitochondria during mitophagy. Nat Commun 2013; 4: 1410.
34. Novak I. Mitophagy: a complex mechanism of mitochondrial removal. Antioxid Redox Signal 2012; 17: 794-802.
35. Sandebring A, Thomas KJ, Beilina A, Beilina AF, van der Brug M, Cleland MM et al. Mitochondrial alterations in PINK1 deficient cells are influenced by calcineurindependent dephosphorylation of dynamin-related protein 1. PLos One 2009; 4: e5701.
36. Yamamoto A, Friedlein A, Imai Y, Takahashi R, Kahle PJ, Haass C. Parkin phosphorylation and modulation of its E3 ubiquitin ligase activity. J Biol Chem 2005; 280: 3390-3399.
37. Shutt D, O'Dorisio MS, Aykin-Burns N, Spitz D. 2-Deoxy-D-glucose induces oxidative stress and cell killing in human neuroblastoma cells. Cancer Biol Ther 2010; 9: 853-861.
38. Groner B, Weiss A. Targeting survivin in cancer: novel drug development approaches. BioDrugs 2014; 28: 27-39.
39. Park E, Gang EJ, Hsieh YT, Schaefer P, Chae S, Klemm L et al. Targeting survivin overcomes drug resistance in acute lymphoblastic leukemia. Blood 2011; 118: 2191-2199.
40. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004; 351: 2817-2826.
41. Zhang C, Lin M, Wu R, Wang X, Yang B, Levine AJ et al. Parkin, a p53 target gene, mediates the role of p53 in glucose metabolism and the Warburg effect. Proc Natl Acad Sci 2011; 108: 16259-16264.
42. Hoepken HH, Gispert S, Morales B, Wingerter O, Del Turco D, Mülsch A et al. Mitochondrial dysfunction, peroxidation damage and changes in glutathione metabolism in PARK6. Neurobiol Dis 2007; 25: 401-411.
43. Michiorri S, Gelmetti V, Giarda E, Lombardi F, Romano F, Marongiu R et al. The Parkinson-associated protein PINK1 interacts with Beclin1 and promotes autophagy. Cell Death Differ 2010; 17: 962-974.
44. Altieri DC. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 2003; 22: 8581-8589.
45. Caldas H, Holloway MP, Hall BM, Qualman SJ, Altura RA. Survivin-directed RNA interference cocktail is a potent suppressor of tumour growth in vivo. J Med Genet 2006; 43: 119-128.
46. Uchida H, Tanaka T, Sasaki K, Kato K, Dehari H, Ito Y et al. Adenovirus-mediated transfer of sirna against survivin induced apoptosis and attenuated tumor cell growth in vitro and in vivo. Mol Ther 2004; 10: 162-171.
47. Nakahara T, Takeuchi M, Kinoyama I, Minematsu T, Shirasuna K, Matsuhisa A et al. YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts. Cancer Res 2007; 67: 8014-8021.
48. Chang CC, Heller JD, Kuo J, Huang RC. Tetra-O-methyl nordihydroguaiaretic acid induces growth arrest and cellular apoptosis by inhibiting Cdc2 and survivin expression. Proc Natl Acad Sci USA 2004; 101: 13239-13244.
49. Rödel F, Frey B, Leitmann W, Capalbo G, Weiss C, Rödel C. Survivin antisense oligonucleotides effectively radiosensitize colorectal cancer cells in both tissue culture and murine xenograft models. Int J Radiat Oncol Biol Phys 2008; 71: 247-255.
50. Wobser M, Keikavoussi P, Kunzmann V, Weininger M, Andersen M, Becker J. Complete remission of liver metastasis of pancreatic cancer under vaccination with a HLA-A2 restricted peptide derived from the universal tumor antigen survivin. Cancer Immunol Immunother 2006; 55: 1294-1298.
51. Tolcher AW, Quinn DI, Ferrari A, Ahmann F, Giaccone G, Drake T et al. A phase II study of YM155, a novel small-molecule suppressor of survivin, in castrationresistant taxane-pretreated prostate cancer. Ann Oncol 2012; 23: 968-973.
52. Satoh T, Okamoto I, Miyazaki M, Morinaga R, Tsuya A, Hasegawa Y et al. Phase I study of YM155, a novel survivin suppressant, in patients with advanced solid tumors. Clin Cancer Res 2009; 15: 3872-3880.
53. Gurbuxani S, Xu Y, Keerthivasan G, Wickrema A, Crispino JD. Differential requirements for survivin in hematopoietic cell development. Proc Natl Acad Sci USA 2005; 102: 11480-11485.
54. Xing Z, Conway EM, Kang C, Winoto A. Essential role of survivin, an inhibitor of apoptosis protein, in T cell development, maturation, and homeostasis. J Exp Med 2004; 199: 69-80.
55. Mesri M, Morales-Ruiz M, Ackermann EJ, Bennett CF, Pober JS, Sessa WC et al. Suppression of vascular endothelial growth factor-mediated endothelial cell protection by survivin targeting. Am J Pathol 2001; 158: 1757-1765.
56. Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T, Altieri DC. Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Clin Cancer Res 2003; 9: 2683-2692.
57. Fortugno P, Beltrami E, Plescia J, Fontana J, Pradhan D, Marchisio PC et al. Regulation of survivin function by Hsp90. Proc Natl Acad Sci 2003; 100: 13791-13796.
58. Plescia J, Salz W, Xia F, Pennati M, Zaffaroni N, Daidone MG et al. Rational design of shepherdin, a novel anticancer agent. Cancer Cell 2005; 7: 457-468.
59. Fukuda SF. The antiapoptosis protein survivin is associated with cell cycle entry of normal cord blood CD34+ cells and modulates cell cycle and proliferation of mouse hematopoietic progenitor cells. Blood 2002; 100: 2463-2471.
60. Bean JF, Qiu YY, Yu S, Clark S, Chu F, Madonna MB. Glycolysis inhibition and its effect in doxorubicin resistance in neuroblastoma. J Pediatr Surg 2014; 49: 981-984.
61. Chuang JH, Chou MH, Tai MH, Lin TK, Liou CW, Chen T et al. 2-Deoxyglucose treatment complements the cisplatin- or BH3-only mimetic-induced suppression of neuroblastoma cell growth. Int J Biochem Cell Biol 2013; 45: 944-951.
62. Grignani F, Kinsella T, Mencarelli A, Valtieri M, Riganelli D, Grignani F et al. Highefficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res 1998; 58: 14-19.
63. Ausserlechner MJ, Obexer P, Deutschmann A, Geiger K, Kofler R. A retroviral expression system based on tetracycline-regulated tricistronic transactivator/repressor vectors for functional analyses of anti-proliferative and toxic genes. Mol Cancer Ther 2006; 5: 1927-1934.
64. Hagenbuchner J, Kuznetsov A, Hermann M, Hausott B, Obexer P, Ausserlechner MJ. FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J Cell Sci 2012; 125: 1191-1203.
65. Geiger K, Hagenbuchner J, Rupp M, Fiegl H, Sergi C, Meister B et al. FOXO3/FKHRL1 is activated by 5-aza-2-deoxycytidine and induces silenced caspase-8 in neuroblastoma. Mol Biol Cell 2012; 23: 2226-2234.
66. Hagenbuchner J, Ausserlechner MJ, Porto V, David R, Meister B, Bodner M et al. The anti-apoptotic protein BCL2L1/Bcl-xL is neutralized by pro-apoptotic PMAIP1/Noxa in neuroblastoma, thereby determining bortezomib sensitivity independent of prosurvival MCL1 expression. J Biol Chem 2010; 285: 6904-6912.
67. Hagenbuchner J, Kiechl-Kohlendorfer U, Obexer P, Ausserlechner MJ. A novel Mcl1 variant inhibits apoptosis via increased Bim sequestration. Oncotarget 2013; 4: 1241-1252.