Apoptin, a tumor-selective killer

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 8, 2009, Pages 1335-1342

  Los, Marek ^a,b   Panigrahi, Soumya ^c   Rashedi, Iran ^d   Mandal, Sanat ^e   Stetefeld, Joerg ^f   Essmann, Frank ^a   Schulze Osthoff, Klaus ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b BioApplications Enterprises Winnipeg   (Canada)

^c LERNER RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^f UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Apoptin; Apoptosis; CDK2; Nur77; Tumor

Indexed keywords

ANTINEOPLASTIC AGENT; APOPTIN; CYCLIN DEPENDENT KINASE 2; CYTOTOXIC FACTOR; DNA; DOCETAXEL; ETOPOSIDE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; HUMAN ALPHA LACTALBUMIN MADE LETHAL TO TUMOR CELLS PROTEIN; INTERLEUKIN 18; METHOTREXATE; NUCLEAR RECEPTOR NUR77; PACLITAXEL; PEPTIDYLPROLYL ISOMERASE; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN KINASE B; PROTEIN P53; RANPIRNASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANAPHASE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CANCER GENE THERAPY; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL KILLING; CELL NUCLEUS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CLINICAL TRIAL; CYTOPLASM; DRUG MECHANISM; HUMAN; LEWIS CARCINOMA; LIVER CELL CARCINOMA; MALIGNANT MESOTHELIOMA; MALIGNANT NEOPLASTIC DISEASE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SKIN PAPILLOMA; SQUAMOUS CELL CARCINOMA;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CAPSID PROTEINS; CHICKEN ANEMIA VIRUS; CHICKENS; CIRCOVIRIDAE INFECTIONS; GENES, VIRAL; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POULTRY DISEASES; SARCOMA, AVIAN;

CHICKEN ANEMIA VIRUS;

EID: 67651122925     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.04.002     Document Type: Review

References (77)

1. Noteborn M.H., de Boer G.F., van Roozelaar D.J., Karreman C., Kranenburg O., Vos J.G., Jeurissen S.H., Hoeben R.C., Zantema A., Koch G., et al. Characterization of cloned chicken anemia virus DNA that contains all elements for the infectious replication cycle. J. Virol. 65 (1991) 3131-3139
2. Natesan S., Kataria J.M., Dhama K., Bhardwaj N., and Sylvester A. Anti-neoplastic effect of chicken anemia virus VP3 protein (apoptin) in Rous sarcoma virus-induced tumours in chicken. J. Gen. Virol. 87 (2006) 2933-2940
3. Noteborn M.H., Verschueren C.A., Zantema A., Koch G., and van der Eb A.J. Identification of the promoter region of chicken anemia virus (CAV) containing a novel enhancer-like element. Gene 150 (1994) 313-318
4. Miller M.M., Jarosinski K.W., and Schat K.A. Positive and negative regulation of chicken anemia virus transcription. J. Virol. 79 (2005) 2859-2868
5. Noteborn M.H., Todd D., Verschueren C.A., de Gauw H.W., Curran W.L., Veldkamp S., Douglas A.J., McNulty M.S., van der E.A., and Koch G. A single chicken anemia virus protein induces apoptosis. J. Virol. 68 (1994) 346-351
6. Phenix K.V., Meehan B.M., Todd D., and McNulty M.S. Transcriptional analysis and genome expression of chicken anaemia virus. J. Gen. Virol. 75 (1994) 905-909
7. Maddika S., Mendoza F.J., Hauff K., Zamzow C.R., Paranjothy T., and Los M. Cancer-selective therapy of the future: apoptin and its mechanism of action. Cancer Biol. Ther. 5 (2006) 10-19
8. Noteborn M.H. Chicken anemia virus induced apoptosis: underlying molecular mechanisms. Vet. Microbiol. 98 (2004) 89-94
9. Heilman D.W., Teodoro J.G., and Green M.R. Apoptin nucleocytoplasmic shuttling is required for cell type-specific localization, apoptosis, and recruitment of the anaphase-promoting complex/cyclosome to PML bodies. J. Virol. 80 (2006) 7535-7545
10. Poon I.K.H., Oro C., Dias M.M., Zhang J., and Jans D.A. Apoptin nuclear accumulation is modulated by a CRM1-recognized nuclear export signal that is active in normal but not in tumor cells. Cancer Res. 65 (2005) 7059-7064
11. Kamada K., Kuroishi A., Kamahora T., Kabat P., Yamaguchi S., and Hino S. Spliced mRNAs detected during the life cycle of chicken anemia virus. J. Gen. Virol. 87 (2006) 2227-2233
12. Danen-Van Oorschot A.A., Zhang Y.H., Leliveld S.R., Rohn J.L., Seelen M.C., Bolk M.W., Van Zon A., Erkeland S.J., Abrahams J.P., Mumberg D., and Noteborn M.H. Importance of nuclear localization of apoptin for tumor-specific induction of apoptosis. J. Biol. Chem. 278 (2003) 27729-27736
13. Kuusisto H.V., Wagstaff K.M., Alvisi G., and Jans D.A. The C-terminus of apoptin represents a unique tumor cell-enhanced nuclear targeting module. Int. J. Cancer (2008) 2965-2969
14. Backendorf C., Visser A.E., de Boer A.G., Zimmerman R., Visser M., Voskamp P., Zhang Y.H., and Noteborn M. Apoptin: therapeutic potential of an early sensor of carcinogenic transformation. Annu. Rev. Pharmacol. Toxicol. 48 (2008) 143-169
15. Leliveld S.R., Zhang Y.H., Rohn J.L., Noteborn M.H., and Abrahams J.P. Apoptin induces tumor-specific apoptosis as a globular multimer. J. Biol. Chem. 278 (2003) 9042-9051
16. Leliveld S.R., Dame R.T., Mommaas M.A., Koerten H.K., Wyman C., Danen-van Oorschot A.A., Rohn J.L., Noteborn M.H., and Abrahams J.P. Apoptin protein multimers form distinct higher-order nucleoprotein complexes with DNA. Nucleic Acids Res. 31 (2003) 4805-4813
17. Tavassoli M., Guelen L., Luxon B.A., and Gäken J. Apoptin: specific killer of tumor cells?. Apoptosis 10 (2005) 717-724
18. Danen-Van Oorschot A.A., Fischer D.F., Grimbergen J.M., Klein B., Zhuang S., Falkenburg J.H., Backendorf C., Quax P.H., Van der Eb A.J., and Noteborn M.H. Apoptin induces apoptosis in human transformed and malignant cells but not in normal cells. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 5843-5847
19. Zhang Y.H., Abrahams P.J., van der Eb A.J., and Noteborn M.H. The viral protein Apoptin induces apoptosis in UV-C-irradiated cells from individuals with various hereditary cancer-prone syndromes. Cancer Res. 59 (1999) 3010-3015
20. Guelen L., Paterson H., Gaken J., Meyers M., Farzaneh F., and Tavassoli M. TAT-apoptin is efficiently delivered and induces apoptosis in cancer cells. Oncogene 23 (2004) 1153-1165
21. Pietersen A., Erkeland S.J., Rutjes S.A., Philipsen S., Medema J.P., and Noteborn M.H. Continuous apoptin expression in transgenic mice does not interfere with lymphocyte development and proliferation. J. Med. Mol. Biol. 2 (2005) 321-330
22. Pietersen A.M., van der Eb M.M., Rademaker H.J., van den Wollenberg D.J., Rabelink M.J., Kuppen P.J., van Dierendonck J.H., van Ormondt H., Masman D., van de Velde C.J., van der Eb A.J., Hoeben R.C., and Noteborn M.H. Specific tumor-cell killing with adenovirus vectors containing the apoptin gene. Gene Ther. 6 (1999) 882-892
23. Maddika S., Ande S.R., Wiechec E., Hansen L.L., Wesselborg S., and Los M. Akt-mediated phosphorylation of CDK2 regulates its dual role in cell cycle progression and apoptosis. J. Cell. Sci. 121 (2008) 979-988
24. Olijslagers S.J., Zhang Y.H., Backendorf C., and Noteborn M.H. Additive cytotoxic effect of apoptin and chemotherapeutic agents paclitaxel and etoposide on human tumour cells. Basic Clin. Pharmacol. Toxicol. 100 (2007) 127-131
25. Zhuang S.M., Shvarts A., van Ormondt H., Jochemsen A.G., van der Eb A.J., and Noteborn M.H. Apoptin, a protein derived from chicken anemia virus, induces p53-independent apoptosis in human osteosarcoma cells. Cancer Res. 55 (1995) 486-489
26. Los M., Wesselborg S., and Schulze-Osthoff K. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10 (1999) 629-639
27. Schwerk C., and Schulze-Osthoff K. Regulation of apoptosis by alternative pre-mRNA splicing. Mol. Cell 19 (2005) 1-13
28. Fischer U., Jänicke R.U., and Schulze-Osthoff K. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 10 (2003) 76-100
29. Danen-van Oorschot A.A., van Der Eb A.J., and Noteborn M.H. The chicken anemia virus-derived protein apoptin requires activation of caspases for induction of apoptosis in human tumor cells. J. Virol. 74 (2000) 7072-7078
30. Maddika S., Booy E.P., Johar D., Gibson S.B., Ghavami S., and Los M. Cancer-specific toxicity of apoptin is independent of death receptors but involves the loss of mitochondrial membrane potential and the release of mitochondrial cell-death mediators by a Nur77-dependent pathway. J. Cell. Sci. 118 (2005) 4485-4493
31. Burek M., Maddika S., Burek C.J., Daniel P.T., Schulze-Osthoff K., and Los M. Apoptin-induced cell death is modulated by Bcl-2 family members and is Apaf-1 dependent. Oncogene 25 (2005) 2213-2222
32. Danen-Van Oorschot A.A., van der Eb A.J., and Noteborn M.H. BCL-2 stimulates Apoptin-induced apoptosis. Adv. Exp. Med. Biol. 457 (1999) 245-249
33. Danen-Van Oorschot A.A., Zhang Y., Erkeland S.J., Fischer D.F., van der Eb A.J., and Noteborn M.H. The effect of Bcl-2 on Apoptin in 'normal' vs transformed human cells. Leukemia 13 Suppl 1 (1999) S75-S77
34. Liu X., Elojeimy S., El-Zawahry A.M., Holman D.H., Bielawska A., Bielawski J., Rubinchik S., Guo G.W., Dong J.Y., Keane T., Hannun Y.A., Tavassoli M., and Norris J.S. Modulation of ceramide metabolism enhances viral protein apoptin's cytotoxicity in prostate cancer. Molec. Ther. 14 (2006) 637-646
35. Lin B., Kolluri S.K., Lin F., Liu W., Han Y.H., Cao X., Dawson M.I., Reed J.C., and Zhang X.K. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116 (2004) 527-540
36. Huo D.H., Yi L.N., and Yang J. Interaction with Ppil3 leads to the cytoplasmic localization of Apoptin in tumor cells. Biochem. Biophys. Res. Commun. 372 (2008) 14-18
37. Cheng C.M., Huang S.P., Chang Y.F., Chung W.Y., and Yuo C.Y. The viral death protein Apoptin interacts with Hippi, the protein interactor of Huntingtin-interacting protein 1. Biochem. Biophys. Res. Commun. 305 (2003) 359-364
38. Sun G.J., Tong X., Dong Y., Mei Z.Z., and Sun Z.X. Identification of a protein interacting with apoptin from human leucocyte cDNA library by using yeast two-hybrid screening. ShengWu HuaXue Yu ShengWu WuLi XueBao (Shanghai) 34 (2002) 369-372
39. Teodoro J.G., Heilman D.W., Parker A.E., and Green M.R. The viral protein Apoptin associates with the anaphase-promoting complex to induce G2/M arrest and apoptosis in the absence of p53. Genes Dev. 18 (2004) 1952-1957
40. Danen-van Oorschot A.A., Voskamp P., Seelen M.C., van Miltenburg M.H., Bolk M.W., Tait S.W., Boesen-de Cock J.G., Rohn J.L., Borst J., and Noteborn M.H. Human death effector domain-associated factor interacts with the viral apoptosis agonist Apoptin and exerts tumor-preferential cell killing. Cell Death Differ. 11 (2004) 564-573
41. Janssen K., Hofmann T.G., Jans D.A., Hay R.T., Schulze-Osthoff K., and Fischer U. Apoptin is modified by SUMO conjugation and targeted to promyelocytic leukemia protein nuclear bodies. Oncogene 26 (2007) 1557-1566
42. Krieghoff-Henning E., and Hofmann T.G. Role of nuclear bodies in apoptosis signalling. Biochim. Biophys. Acta 1783 (2008) 2185-2194
43. Maddika S., Wiechec E., Ande S.R., Poon K., Fischer U., Wesselborg S., Jans D.A., Schulze-Osthoff K., and Los M. Interaction with PI3-kinase contributes to the cytotoxic activity of apoptin. Oncogene 27 (2008) 3060-3065
44. Maddika S., Bay G.H., Kroczak T.J., Ande S.R., Maddika S., Wiechec E., Gibson S.B., and Los M. Akt is transferred to the nucleus of cells treated with apoptin, and it participates in apoptin-induced cell death. Cell Prolif. 40 (2007) 835-848
45. Aki T., Yamaguchi K., Fujimiya T., and Mizukami Y. Phosphoinositide 3-kinase accelerates autophagic cell death during glucose deprivation in the rat cardiomyocyte-derived cell line H9c2. Oncogene 22 (2003) 8529-8535
46. Lu B., Wang L., Stehlik C., Medan D., Huang C., Hu S., Chen F., Shi X., and Rojanasakul Y. Phosphatidylinositol 3-kinase/Akt positively regulates Fas (CD95)-mediated apoptosis in epidermal Cl41 cells. J. Immunol. 176 (2006) 6785-6793
47. Nimbalkar D., Henry M.K., and Quelle F.W. Cytokine activation of phosphoinositide 3-kinase sensitizes hematopoietic cells to cisplatin-induced death. Cancer Res. 63 (2003) 1034-1039
48. Shack S., Wang X.T., Kokkonen G.C., Gorospe M., Longo D.L., and Holbrook N.J. Caveolin-induced activation of the phosphatidylinositol 3-kinase/Akt pathway increases arsenite cytotoxicity. Mol. Cell. Biol. 23 (2003) 2407-2414
49. Maddika S., Panigrahi S., Wiechec E., Wesselborg S., Fischer U., Schulze-Osthoff K., and Los M. Unscheduled Akt-triggered activation of CDK2 as a key effector mechanism of apoptin's anticancer toxicity. Mol. Cell. Biol. 29 (2009) 1235-1248
50. Lei H., Furlong P.J., Ra J.H., Mullins D., Cantor R., Fraker D.L., and Spitz F.R. AKT activation and response to interferon-beta in human cancer cells. Cancer Biol. Ther. 4 (2005) 709-715
51. Tang D., Okada H., Ruland J., Liu L., Stambolic V., Mak T.W., and Ingram A.J. Akt is activated in response to an apoptotic signal. J. Biol. Chem. 276 (2001) 30461-30466
52. van Gorp A.G., Pomeranz K.M., Birkenkamp K.U., Hui R.C., Lam E.W., Coffer P.J., and Chronic protein kinase B. (PKB/c-akt) activation leads to apoptosis induced by oxidative stress-mediated Foxo3a transcriptional up-regulation. Cancer Res. 66 (2006) 10760-10769
53. Nogueira V., Park Y., Chen C.C., Xu P.Z., Chen M.L., Tonic I., Unterman T., and Hay N. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 14 (2008) 458-470
54. Los M., Maddika S., Erb B., and Schulze-Osthoff K. Switching Akt: from survival signaling to deadly response. BioEssays 31 (2009) 492-495
55. Poon I.K., Oro C., Dias M.M., Zhang J.P., and Jans D.A. A tumor cell-specific nuclear targeting signal within chicken anemia virus VP3/Apoptin. J. Virol. 79 (2005) 1339-1341
56. Rohn J.L., and Noteborn M.H. The viral death effector Apoptin reveals tumor-specific processes. Apoptosis 9 (2004) 315-322
57. Rohn J.L., Zhang Y.-H., Aalbers R.I.J.M., Otto N., den Hertog J., Henriquez N.V., van de Velde C.J.H., Kuppen P.J.K., Mumberg D., Donner P., and Noteborn M.H.M. A tumor-specific kinase activity regulates the viral death protein apoptin. J. Biol. Chem. 277 (2002) 50820-50827
58. Lee Y.H., Cheng C.M., Chang Y.F., Wang T.Y., and Yuo C.Y. Apoptin T108 phosphorylation is not required for its tumor-specific nuclear localization but partially affects its apoptotic activity. Biochem. Biophys. Res. Commun. 354 (2007) 391-395
59. Leliveld S.R., Dame R.T., Rohn J.L., Noteborn M.H., and Abrahams J.P. Apoptin's functional N- and C-termini independently bind DNA. FEBS Lett. 557 (2004) 155-158
60. Nakayama S., Torikoshi Y., Takahashi T., Yoshida T., Sudo T., Matsushima T., Kawasaki Y., Katayama A., Gohda K., Hortobagyi G.N., Noguchi S., Sakai T., Ishihara H., and Ueno N.T. Prediction of paclitaxel sensitivity by CDK1 and CDK2 activity in human breast cancer cells. Breast Cancer Res. 11 (2009) R12
61. Gil-Gomez G., Berns A., and Brady H.J. A link between cell cycle and cell death: Bax and Bcl-2 modulate Cdk2 activation during thymocyte apoptosis. EMBO J. 17 (1998) 7209-7218
62. Liu Q., Fu H., Xing R., Tie Y., Zhu J., Sun Z., and Zheng X. Survivin knockdown combined with apoptin overexpression inhibits cell growth significantly. Cancer Biol. Ther. 7 (2008) 1053-1060
63. Panigrahi S., Klonisch T., and Los M. The art of killing: double stroke with apoptin and survivin as a novel approach in cancer therapy. Cancer Biol. Ther. 7 (2008) 1061-1062
64. Lian H., Jin N., Li X., Mi Z., Zhang J., Sun L., Li X., Zheng H., and Li P. Induction of an effective anti-tumor immune response and tumor regression by combined administration of IL-18 and Apoptin. Cancer Immunol. Immunother. 56 (2007) 181-192
65. Li X., Jin N., Mi Z., Lian H., Sun L., Li X., and Zheng H. Antitumor effects of a recombinant fowlpox virus expressing Apoptin in vivo and in vitro. Int. J. Cancer 119 (2006) 2948-2957
66. Peng D.J., Sun J., Wang J.Y.Z., Tian J., Zhang Y.H., Noteborn M.H., and Qu S. Inhibition of hepatocarcinoma by systemic delivery of Apoptin gene via the hepatic asialoglycoprotein receptor. Cancer Gene Ther. 14 (2007) 66-73
67. Schoop R.A., Baatenburg de Jong R.J., and Noteborn M.H. Apoptin induces apoptosis in an oral cancer mouse model. Cancer Biol. Ther. 7 (2008) 1368-1373
68. Held J., and Schulze-Osthoff K. Potential and caveats of TRAIL in cancer therapy. Drug Resist Updat. 4 (2001) 243-252
69. Johnstone R.W., Frew A.J., and Smyth M.J. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat. Rev., Cancer 8 (2008) 782-798
70. Shtrichman R., Sharf R., Barr H., Dobner T., and Kleinberger T. Induction of apoptosis by adenovirus E4orf4 protein is specific to transformed cells and requires an interaction with protein phosphatase 2A. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10080-10085
71. Champagne C., Landry M.C., Gingras M.C., and Lavoie J.N. Activation of adenovirus type 2 early region 4 ORF4 cytoplasmic death function by direct binding to Src kinase domain. J. Biol. Chem. 279 (2004) 25905-25915
72. de Smit M.H., and Noteborn M.H. Apoptosis-inducing proteins in chicken anemia virus and TT virus. Curr. Top. Microbiol. Immunol. 331 (2009) 131-149
73. Hino S., and Prasetyo A.A. Relationship of Torque teno virus to chicken anemia virus. Curr. Top. Microbiol. Immunol. 331 (2009) 117-130
74. zur Hausen H., and de Villiers E.M. TT viruses: oncogenic or tumor-suppressive properties?. Curr. Top. Microbiol. Immunol. 331 (2009) 109-116
75. Hallgren O., Aits S., Brest P., Gustafsson L., Mossberg A.K., Wullt B., and Svanborg C. Apoptosis and tumor cell death in response to HAMLET (human alpha-lactalbumin made lethal to tumor cells). Adv. Exp. Med. Biol. 606 (2008) 217-240
76. Gustafsson L., Leijonhufvud I., Aronsson A., Mossberg A.K., and Svanborg C. Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid. N. Engl. J. Med. 350 (2004) 2663-2672
77. Zhao H., Ardelt B., Ardelt W., Shogen K., and Darzynkiewicz Z. The cytotoxic ribonuclease onconase targets RNA interference (siRNA). Cell Cycle 7 (2008) 3258-3261