Downregulation of voltage-dependent anion channel-1 expression by RNA interference prevents cancer cell growth in vivo

Cancer Biology and Therapy

Volumn 9, Issue 12, 2010, Pages 1046-1052

  Koren, Inbar ^a   Raviv, Ziv ^a   Shoshan Barmatz, Varda ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Cancer; shRNA; VDAC

Indexed keywords

ADENOSINE TRIPHOSPHATE; SHORT HAIRPIN RNA; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER MODEL; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENERGY BALANCE; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; NUDE MOUSE; OUTER MEMBRANE; PLASMID; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE;

ANIMALS; CELL PROLIFERATION; DOWN-REGULATION; DOXYCYCLINE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MICE; MICE, NUDE; MITOCHONDRIAL MEMBRANES; NEOPLASM TRANSPLANTATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 77954400635     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.9.12.11879     Document Type: Article

References (46)

1. Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003; 112:481-90. (Pubitemid 36263081)
2. Wallace DC. Mitochondrial diseases in man and mouse. Science 1999; 283:1482-8.
3. Bernardi P. Mitochondrial transport of cations: channels, exchangers and permeability transition. Physiol Rev 1999; 79:1127-55. (Pubitemid 29473313)
4. Rustin P. Mitochondria, from cell death to proliferation. Nat Genet 2002; 30:352-3.
5. The role of the mitochondria in human aging and disease: from gene to cell signaling. Proceedings of the second scientific meeting of the Asian Society for Mitochondrial Research and Medicine. April 1-2, 2004. Taipei, Taiwan. Ann N Y Acad Sci 2005; 1042:1-537.
6. Halestrap AP, Doran E, Gillespie JP, O'Toole A. Mitochondria and cell death. Biochem Soc Trans 2000; 28:170-7.
7. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004; 256:107-15. (Pubitemid 38181239)
8. Rostovtseva T, Colombini M. ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane. J Biol Chem 1996; 271:28006-8. (Pubitemid 26374603)
9. Hodge T, Colombini M. Regulation of metabolite flux through voltage-gating of VDAC channels. J Membr Biol 1997; 157:271-9. (Pubitemid 27276169)
10. Gincel D, Zaid H, Shoshan-Barmatz V. Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem J 2001; 358:147-55. (Pubitemid 32778108)
11. Tsujimoto Y, Shimizu S. The voltage-dependent anion channel: an essential player in apoptosis. Biochimie 2002; 84:187-93.
12. Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu S. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr Pharm Des 2006; 12:2249-70. (Pubitemid 43891398)
13. Lemasters JJ, Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim Biophys Acta 2006; 1762:181-90.
14. Zaid H, Abu-Hamad S, Israelson A, Nathan I, Shoshan-Barmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ 2005; 12:751-60. (Pubitemid 40945982)
15. Shoshan-Barmatz V, Arbel N, Arzoine l. VDAC, the voltage-dependent anion channel: function, regulation & mitochondrial signaling in cell life and death. Cell Science 2008; 4:74-118.
16. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70.
17. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001; 411:494-8. (Pubitemid 32494397)
18. Couzin J. Breakthrough of the year. Small RNAs make big splash. Science 2002; 298:2296-7.
19. Alexander HK, Booy EP, Xiao W, Ezzati P, Baust H, Los M. Selected technologies to control genes and their products for experimental and clinical purposes. Arch Immunol Ther Exp (Warsz) 2007; 55:139-49. (Pubitemid 46957404)
20. Cejka D, Losert D, Wacheck V. Short interfering RNA (siRNA): tool or therapeutic? Clin Sci (Lond) 2006; 110:47-58.
21. Abdelrahim M, Safe S, Baker C, Abudayyeh A. RNAi and cancer: Implications and applications. J RNAi Gene Silencing 2006; 2:136-45.
22. Mocellin S, Costa R, Nitti D. RNA interference: ready to silence cancer? J Mol Med 2006; 84:4-15.
23. Abu-Hamad S, Sivan S, Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc Natl Acad Sci USA 2006; 103:5787-92.
24. Simamura E, Shimada H, Hatta T, Hirai K. Mitochondrial voltage-dependent anion channels (VDACs) as novel pharmacological targets for anticancer agents. J Bioenerg Biomembr 2008; 40:213-7.
25. Deuschle U, Meyer WK, Thiesen HJ. Tetracycline-reversible silencing of eukaryotic promoters. Mol Cell Biol 1995; 15:1907-14.
26. Freundlieb S, Baron U, Bonin AL, Gossen M, Bujard H. Use of tetracycline-controlled gene expression systems to study mammalian cell cycle. Methods Enzymol 1997; 283:159-73.
27. Collins T, Stone JR, Williams AJ. All in the family: the BTB/POZ, KRAB and SCAN domains. Mol Cell Biol 2001; 21:3609-15.
28. Klopotowska D, Strzadala L, Matuszyk J. Inducibility of doxycycline-regulated gene in neural and neuroendocrine cells strongly depends on the appropriate choice of a tetracycline-responsive promoter. Neurochem Int 2008; 52:221-9.
29. Bustamante E, Pedersen PL. Mitochondrial hexokinase of rat hepatoma cells in culture: solubilization and kinetic properties. Biochemistry 1980; 19:4972-7. (Pubitemid 11205877)
30. Pedersen PL, Mathupala S, Rempel A, Geschwind JF, Ko YH. Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta 2002; 1555:14-20.
31. Rempel A, Bannasch P, Mayer D. Differences in expression and intracellular distribution of hexokinase isoenzymes in rat liver cells of different transformation stages. Biochim Biophys Acta 1994; 1219:660-8.
32. Arora KK, Pedersen PL. Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J Biol Chem 1988; 263:17422-8.
33. Pedersen PL. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 2007; 39:211-22.
34. Peng Q, Zhou Q, Zhou J, Zhong D, Pan F, Liang H. Stable RNA interference of hexokinase II gene inhibits human colon cancer LoVo cell growth in vitro and in vivo. Cancer Biol Ther 2008; 7:1128-35.
35. Tajeddine N, Galluzzi L, Kepp O, Hangen E, Morselli E, Senovilla L, et al. Hierarchical involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death. Oncogene 2008; 10:4221-32.
36. Yuan S, Fu Y, Wang X, Shi H, Huang Y, Song X, et al. Voltage-dependent anion channel 1 is involved in endostatin-induced endothelial cell apoptosis. Faseb J 2008; 22:2809-20.
37. Tomasello F, Messina A, Lartigue L, Schembri L, Medina C, Reina S, et al. Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis. Cell Res 2009.
38. Jones D. Teaming up to tackle RNAi delivery challenge. Nat Rev Drug Discov 2009; 8:525-6.
39. Spankuch B, Matthess Y, Knecht R, Zimmer B, Kaufmann M, Strebhardt K. Cancer inhibition in nude mice after systemic application of U6 promoter-driven short hairpin RNAs against PLK1. J Natl Cancer Inst 2004; 96:862-72.
40. Wang X, Wang M, Amarzguioui M, Liu F, Fodstad O, Prydz H. Downregulation of tissue factor by RNA interference in human melanoma LOX-L cells reduces pulmonary metastasis in nude mice. Int J Cancer 2004; 112:994-1002. (Pubitemid 39507005)
41. Gurzov EN, Izquierdo M. RNA interference against Hec1 inhibits tumor growth in vivo. Gene Ther 2006; 13:1-7. (Pubitemid 41823846)
42. Piva R, Chiarle R, Manazza AD, Taulli R, Simmons W, Ambrogio C, et al. Ablation of oncogenic ALK is a viable therapeutic approach for anaplastic large-cell lymphomas. Blood 2006; 107:689-97.
43. Shi YY, Small GW, Orlowski RZ. Proteasome inhibitors induce a p38 mitogen-activated protein kinase (MAPK)-dependent anti-apoptotic program involving MAPK phosphatase-1 and Akt in models of breast cancer. Breast Cancer Res Treat 2006; 100:33-47.
44. Ji J, Glaser A, Wernli M, Berke JM, Moradpour D, Erb P. Suppression of short interfering RNA-mediated gene silencing by the structural proteins of hepatitis C virus. J Gen Virol 2008; 89:2761-6.
45. Ben-Bassat H, Rosenbaum-Mitrani S, Hartzstark Z, Shlomai Z, Kleinberger-Doron N, Gazit A, et al. Inhibitors of epidermal growth factor receptor kinase and of cyclin-dependent kinase 2 activation induce growth arrest, differentiation and apoptosis of human papilloma virus 16-immortalized human keratinocytes. Cancer Res 1997; 57:3741-50.
46. Liu Y, Ludes-Meyers J, Zhang Y, Munoz-Medellin D, Kim HT, Lu C, et al. Inhibition of AP-1 transcription factor causes blockade of multiple signal transduction pathways and inhibits breast cancer growth. Oncogene 2002; 21:7680-9.