BIRC5/Survivin enhances aerobic glycolysis and drug resistance by altered regulation of the mitochondrial fusion/fission machinery

Oncogene

Volumn 32, Issue 40, 2013, Pages 4748-4757

  Hagenbuchner, J ^a,b   Kuznetsov, A V ^a   Obexer, P ^a,b   Ausserlechner, M J ^a,b  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b TYROLEAN CANCER RESEARCH INSTITUTE   (Austria)

Author keywords

chemotherapy; FOXO3; mitochondrial respiration; reactive oxygen species; Warburg effect

Indexed keywords

BIRC5 PROTEIN; REACTIVE OXYGEN METABOLITE; SURVIVIN; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; DNA DAMAGE; ENERGY YIELD; GLYCOLYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NEUROBLASTOMA; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL;

AEROBIOSIS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DRUG RESISTANCE; FORKHEAD TRANSCRIPTION FACTORS; GLYCOLYSIS; GTP PHOSPHOHYDROLASES; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 84885178346     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.500     Document Type: Article

References (40)

1. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 1984; 224: 1121-1124.
2. 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.
3. Opel D, Poremba C, Simon T, de batin KM, Fulda S. Activation of Akt predicts poor outcome in neuroblastoma. Cancer Res 2007; 67: 735-745.
4. Obexer P, Geiger K, Ambros PF, Meister B, Ausserlechner MJ. FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ 2007; 14: 534-547.
5. 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.
6. 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.
7. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006; 443: 658-662.
8. Sheridan C, de livani P, Cullen SP, Martin SJ. Bax-or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol Cell 2008; 31: 570-585.
9. Chen H, Chomyn A, Chan DC. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 2005; 280: 26185-26192.
10. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS. Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 2004; 279: 4127-4135.
11. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C et al. Electron transfer between cytochrome C and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005; 122: 221-233.
12. Connor KM, Subbaram S, Regan KJ, Nelson KK, Mazurkiewicz JE, Bartholomew PJ et al. Mitochondrial H2O2 regulates the angiogenic phenotype via PTEN oxidation. J Biol Chem 2005; 280: 16916-16924.
13. Chen K, Albano A, Ho A, Keaney Jr JF. Activation of p53 by oxidative stress involves platelet-derived growth factor-beta receptor-mediated ataxia telangiectasia mutated (ATM) kinase activation. J Biol Chem 2003; 278: 39527-39533.
14. Vazquez A, Liu J, Zhou Y, Oltvai ZN. Catabolic efficiency of aerobic glycolysis: The Warburg effect revisited. BMC Syst Biol 2010; 4: 58.
15. Heiden MGV, Cantley LC, Thompson CB. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
16. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006; 160: 1-40.
17. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 2007; 109: 3812-3819.
18. 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.
19. Simonnet H, Alazard N, Pfeiffer K, Gallou C, Beroud C, de mont J et al. Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis 2002; 23: 759-768.
20. Chen QR, Song YK, Yu LR, Wei JS, Chung JY, Hewitt SM et al. Global genomic and proteomic analysis identifies biological pathways related to high-risk neuroblastoma. J Proteome Res 2010; 9: 373-382.
21. Smith DJ, Cossins LR, Hatzinisiriou I, Haber M, Nagley P. Lack of correlation between MYCN expression and the Warburg effect in neuroblastoma cell lines. BMC Cancer 2008; 8: 259.
22. Geiger K, Hagenbuchner J, Rupp M, Fiegl H, Sergi EC, 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.
23. Dohi T, Xia F, Altieri DC. Compartmentalized phosphorylation of IAP by protein kinase A regulates cytoprotection. Mol Cell 2007; 27: 17-28.
24. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001; 1: 515-525.
25. Ausserlechner MJ, Obexer P, De utschmann 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.
26. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 2004; 64: 985-993.
27. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T et al. Mitochondrial bioenergetics and structural network organization. J Cell Sci 2007; 120: 838-848.
28. Guha M, Plescia J, Leav I, Li J, Languino LR, Altieri DC. Endogenous tumor suppression mediated by PTEN involves Survivin gene silencing. Cancer Res 2009; 69: 4954-4958.
29. Dohi T, Okada K, Xia F, Wilford CE, Samuel T, Welsh K et al. An IAP-IAP complex inhibits apoptosis. J Biol Chem 2004; 279: 34087-34090.
30. Kang BH, Xia F, Pop R, Dohi T, Socolovsky M, Altieri DC. Developmental control of apoptosis by the immunophilin aryl hydrocarbon receptor-interacting Protein (AIP) involves mitochondrial import of the Survivin protein. J Biol Chem 2011; 286: 16758-16767.
31. Wu S, Zhou F, Zhang Z. Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission/fusion proteins. FEBS J 2011; 278: 941-954.
32. Herrero-Mendez A, Almeida A, Fernandez E, Maestre C, Moncada S, Bolanos JP. The bioenergetic and antioxidant status of neurons is controlled by continuous de gradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol 2009; 11: 747-U105.
33. Almeida A, Bolanos JP, Moncada S. E3 ubiquitin ligase APC/C-Cdh1 accounts for the Warburg effect by linking glycolysis to cell proliferation. Proc Nat Acad Sci USA 2010; 107: 738-741.
34. Connell CM, Colnaghi R, Wheatley SP. Nuclear survivin has reduced stability and is not cytoprotective. J Biol Chem 2008; 283: 3289-3296.
35. 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.
36. Di Cosimo S, Ferretti G, Papaldo P, Carlini P, Fabi A, Cognetti F. Lonidamine: Efficacy and safety in clinical trials for the treatment of solid tumors. Drugs Today 2003; 39: 157-174.
37. Singh D, Banerji AK, Dwarakanath BS, Tripathi RP, Gupta JP, Mathew TL et al. Optimizing cancer radiotherapy with 2-deoxy-d-glucose dose escalation studies in patients with glioblastoma multiforme. Strahlenther Onkol 2005; 181: 507-514.
38. 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.
39. Hagenbuchner J, Ausserlechner MJ, Porto V, David R, Meister B, Bodner M et al. The antiapoptotic protein BCL2L1/BCL-XL is neutralized by proapoptotic PMAIP1/Noxa in neuroblastoma thereby de termining bortezomib-sensitivity independent of prosurvival MCL1 expression. J Biol Chem 2010; 285: 6904-6912.
40. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 2008; 3: 965-976.