Preclinical characterization of AEG35156/GEM 640, a second-generation antisense oligonucleotide targeting X-linked inhibitor of apoptosis

Clinical Cancer Research

Volumn 12, Issue 17, 2006, Pages 5231-5241

  LaCasse, Eric C ^a   Cherton Horvat, Gabriele G ^a   Hewitt, Kimberley E ^a   Jerome, Lori J ^a   Morris, Stephen J ^a   Kandimalla, Ekambar R ^b   Yu, Dong ^b   Wang, Hui ^c   Wang, Wei ^c   Zhang, Ruiwen ^c   Agrawal, Sudhir ^b   Gillard, John W ^a   Durkin, Jon P ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b HYBRIDON INC   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEG 35156; AEG 35157; AEG 35185; AEG 35187; AEG 35191; ANTISENSE OLIGONUCLEOTIDE; CARBOPLATIN; CISPLATIN; DOCETAXEL; MESSENGER RNA; TAXANE DERIVATIVE; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BODY WEIGHT; BREAST CANCER; CANCER CELL CULTURE; CELL DEATH; COLON CANCER; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG SENSITIZATION; FEMALE; GENE THERAPY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SPLENOMEGALY; TUMOR REGRESSION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; GENE EXPRESSION PROFILING; HUMANS; MICE; MICE, NUDE; NEOPLASMS; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; OLIGONUCLEOTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP; TAXOIDS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSPLANTATION, HETEROLOGOUS; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33748990325     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-06-0608     Document Type: Article

References (57)

1. LaCasse EC, Holcik M, Korneluk RG, MacKenzie AE. Apoptosis in health, disease, and therapy: overview and methodology. In: Holcik M, LaCasse E, MacKenzie A, Korneluk R, editors. Apoptosis in health and disease: clinical and therapeutic aspects. Cambridge: Cambridge University Press; 2005. p. 1-48.
2. Schimmer AD, Dalili S, Batey RA, Riedl SJ. Targeting XIAP for the treatment of malignancy. Cell Death Differ 2006;13:179-88.
3. Wright CW, Duckett CS. Reawakening the cellular death program in neoplasia through the therapeutic blockade of IAP function. J Clin Invest 2005;115:2673-8.
4. Kaufmann SH, Vaux DL. Alterations in the apoptotic machinery and their potential role in anticancer drug resistance. Oncogene 2003;22:7414-30.
5. Wrzesien-Kus A, Smolewski P, Sobczak-Pluta A, Wierzbowska A, Robak T. The inhibitor of apoptosis protein family and its antagonists in acute leukemias. Apoptosis 2004;9:705-15.
6. LaCasse EC, Baird S, Korneluk RG, MacKenzie AE. The inhibitors of apoptosis (IAPs) and their emerging role in cancer. Oncogene 1998;17:3247-59.
7. Lewis J, Burstein E, Reffey SB, Bratton SB, Roberts AB, Duckett CS. Uncoupling of the signaling and caspase-inhibitory properties of X-linked inhibitor of apoptosis. J Biol Chem 2004;279:9023-9.
8. Fong WG, Liston P, Rajcan-Separovic E, St Jean M, Craig C, Korneluk RG. Expression and genetic analysis of XIAP-associated factor 1 (XAF1) in cancer cell lines. Genomics 2000;70:113-22.
9. Tamm I, Kornblau SM, Sepall H, et al. Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin Cancer Res 2000;6:1796-803.
10. Takeuchi H, Kim J, Fujimoto A, et al. X-linked inhibitor of apoptosis protein expression level in colorectal cancer is regulated by hepatocyte growth factor/C-met pathway via Akt signaling. Clin Cancer Res 2005;11:7621-8.
11. Wu M, Yuan S, Szporn AH, Gan L, Shtilbans V, Burstein DE. Immunocytochemical detection of XIAP in body cavity effusions and washes. Mod Pathol 2005;18:1618-22.
12. Tamm I, Richter S, Oltersdorf D, et al. High expression levels of X-linked inhibitor of apoptosis protein and survivin correlate with poor overall survival in childhood de novo acute myeloid leukemia. Clin Cancer Res 2004;10:3737-44.
13. Nakagawa Y, Hasegawa M, Kurata M, et al. Expression of IAP-family proteins in adult acute mixed lineage leukemia (AMLL). Am J Hematol 2005;78:173-80.
14. Yamamoto K, Abe S, Nakagawa Y, et al. Expression of IAP family proteins in myelodysplastic syndromes transforming to overt leukemia. Leuk Res 2004;28:1203-11.
15. Ramaswamy S, Tamayo P, Rifkin R, et al. Multiclass cancer diagnosis using tumor gene expression signatures. Proc Natl Acad Sci U S A 2001;98:15149-54.
16. Ramp U, Krieg T, Caliskan E, et al. XIAP expression is an independent prognostic marker in clear-cell renal carcinomas. Hum Pathol 2004;35:1022-8.
17. Yan Y, Mahotka C, Heikaus S, et al. Disturbed balance of expression between XIAP and Smac/DIABLO during tumor progression in renal cell carcinomas. Br J Cancer 2004;91:1349-57.
18. Agrawal S, Kandimalla ER. Role of Toll-like receptors in antisense and siRNA. Nat Biotechnol 2004;22:1533-7.
19. Agrawal S, Jiang Z, Zhao Q, et al. Mixed-backbone oligonucleotides as second generation antisense oligonucleotides: in vitro and in vivo studies. Proc Natl Acad Sci U S A 1997;94:2620-5.
20. Wang H, Cai Q, Zeng X, Yu D, Agrawal S, Zhang R. Anti-tumor activity and pharmacokinetics of a mixed-backbone antisense oligonucleotide targeted to RIα subunit of protein kinase A after oral administration. Proc Natl Acad Sci U S A 1999;96:13989-94.
21. Wang H, Nan L, Yu D, Lindsey JR, Agrawal S, Zhang R. Anti-tumor efficacy of a novel antisense anti-mdm2 mixed-backbone oligonucleotide in human colon cancer models: p53-dependent and p53-independent mechanisms. Mol Med 2002;8:185-99.
22. Wang H, Yu D, Agrawal S, Zhang R. Experimental therapy of human prostate cancer by inhibiting MDM2 expression with novel mixed-backbone antisense oligonucleotides: in vitro and in vivo activities and mechanisms. Prostate 2003;54:194-205.
23. Zhang Z, Li M, Wang H, Agrawal S, Zhang R. Antisense therapy targeting MDM2 oncogene in prostate cancer: effects on proliferation, apoptosis, multiple gene expression, and chemotherapy. Proc Natl Acad Sci U S A 2003;100:11636-41.
24. Cummings J, Ward TH, LaCasse E, et al. Validation of pharmacodynamic assays to evaluate the clinical efficacy of an antisense compound (AEG 35156) targeted to the X-linked inhibitor of apoptosis protein XIAP. Br J Cancer 2005;92:532-8.
25. Kandimalla ER, Bhagat L, Wang D, et al. Divergent synthetic nucleotide motif recognition pattern: design and development of potent immunomodulatory oligodeoxyribonucleotide agents with distinct cytokine induction profiles. Nucleic Acids Res 2003;31:2393-400.
26. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002;8:808-15.
27. Ng CP, Bonavida B. X-linked inhibitor of apoptosis (XIAP) blocks Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis of prostate cancer cells in the presence of mitochondrial activation: sensitization by overexpression of second mitochondria-derived activator of caspase/ direct IAP-binding protein with low pl (Smac/DIABLO). Mol Cancer Ther 2002;1:1051-8.
28. Guo F, Nimmanapalli R, Paranawithana S, et al. Ectopic overexpression of second mitochondria-derived activator of caspases (Smac/DIABLO) or cotreatment with N-terminus of Smac/DIABLO peptide potentiates epothilone B derivative- (BMS 247550) and Apo-2L/TRAIL-induced apoptosis. Blood 2002;99:3419-26.
29. Leaman DW, Chawla-Sarkar M, Vyas K, et al. Identification of X-linked inhibitor of apoptosis-associated factor-1 as an interferon-stimulated gene that augments TRAIL Apo2L-induced apoptosis. J Biol Chem 2002;277:28504-11.
30. McManus DC, Lefebvre CA, Cherton-Horvat G, et al. Loss of XIAP protein expression by RNAi and antisense approaches sensitizes cancer cells to functionally diverse chemotherapeutics. Oncogene 2004;23:8105-17.
31. Cummins JM, Kohli M, Rago C, Kinzler KW, Vogelstein B, Bunz F. X-linked inhibitor of apoptosis protein (XIAP) is a nonredundant modulator of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis in human cancer cells. Cancer Res 2004;64:3006-8.
32. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG. A small molecule Smac mimic potentiates TRAIL- and TNFα-mediated cell death. Science 2004;305:1471-4.
33. Yamaguchi Y, Shiraki K, Fuke H, et al. Targeting of X-linked inhibitor of apoptosis protein or survivin by short interfering RNAs sensitize hepatoma cells to TNF-related apoptosis-inducing ligand- and chemotherapeutic agent-induced cell death. Oncol Rep 2005;14:1311-6.
34. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature 2004;432:307-15.
35. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2002;2:277-88.
36. Tong QS, Zheng LD, Wang L, et al. Downregulation of XIAP expression induces apoptosis and enhances chemotherapeutic sensitivity in human gastric cancer cells. Cancer Gene Ther 2005;12:509-14.
37. Yang X, Xing H, Gao Q, et al. Regulation of HtrA2/Omi by X-linked inhibitor of apoptosis protein in chemoresistance in human ovarian cancer cells. Gynecol Oncol 2005;97:413-21.
38. Hu P, Han Z, Couvillon AD, Exton JH. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 2004;279:49420-9.
39. Pardo OE, Lesay A, Arcaro A, et al. Fibroblast growth factor 2-mediated translational control of IAPs blocks mitochondrial release of Smac/DIABLO and apoptosis in small cell lung cancer cells. Mol Cell Biol 2003;23:7600-10.
40. Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004;30:1-9.
41. Berezovskaya O, Schimmer AD, Glinskii AB, et al. Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells. Cancer Res 2005;65:2378-86.
42. Kaur S, Wang F, Venkatraman M, Arsura M. X-linked inhibitor of apoptosis (XIAP) inhibits c-Jun N-terminal kinase 1 (JNK1) activation by transforming growth factor β1 (TGF-β1) through ubiquitin-mediated proteosomal degradation of the TGF-β1-activated kinase 1 (TAK1). J Biol Chem 2005;280:38599-608.
43. Lima RT, Martins LM, Guimaraes JE, Sambade C, Vasconcelos MH. Specific downregulation of bcl-2 and xIAP by RNAi enhances the effects of chemotherapeutic agents in MCF-7 human breast cancer cells. Cancer GeneTher 2004;11:309-16.
44. Liu Z, Li H, Derouet M, et al. ras oncogene triggers up-regulation of cIAP2 and XIAP in intestinal epithelial cells: epidermal growth factor receptor-dependent and -independent mechanisms of ras-induced transformation. J Biol Chem 2005;280:37383-92.
45. Hatano M, Mizuno M, Yoshida J. Enhancement of C2-ceramide antitumor activity by small interfering RNA on X chromosome-linked inhibitor of apoptosis protein in resistant human glioma cells. J Neurosurg 2004;101:119-27.
46. Marienfeld C, Yamagiwa Y, Ueno Y, et al. Translational regulation of XIAP expression and cell survival during hypoxia in human cholangiocarcinoma. Gastroenterology 2004;127:1787-97.
47. Mohapatra S, Chu B, Zhao X, Pledger WJ. Accumulation of p53 and reductions in XIAP abundance promote the apoptosis of prostate cancer cells. Cancer Res 2005;65:7717-23.
48. Cao C, Mu Y, Hallahan DE, Lu B. XIAP and survivin as therapeutic targets for radiation sensitization in preclinical models of lung cancer. Oncogene 2004;23:7047-52.
49. Carter BZ, Milella M, Tsao T, et al. Regulation and targeting of antiapoptotic XIAP in acute myeloid leukemia. Leukemia 2003;17:2081-9.
50. Miranda MB, Dyer KF, Grandis JR, Johnson DE. Differential activation of apoptosis regulatory pathways during monocytic vs granulocytic differentiation: a requirement for Bcl-X(L) and XIAP in the prolonged survival of monocytic cells. Leukemia 2003;17:390-400.
51. Hu Y, Cherton-Horvat G, Dragowska V, et al. Antisense oligonucleotides targeting XIAP induce apoptosis and enhance therapeutic activity against human lung cancer cells when combined with anticancer drug in vitro and in vivo. Clin Cancer Res 2003;9:2826-36.
52. Trauzold A, Schmiedel S, Roder C, et al. Multiple and synergistic deregulations of apoptosis-controlling genes in pancreatic carcinoma cells. Br J Cancer 2003;89:1714-21.
53. Roa WH, Chen H, Fulton D, et al. X-linked inhibitor regulating TRAIL-induced apoptosis in chemoresistant human primary glioblastoma cells. Clin Invest Med 2003;26:231-42.
54. Ravi R, Fuchs EJ, Jain A, et al. Resistance of cancers to immunologic cytotoxicity and adoptive immunotherapy via X-linked inhibitor of apoptosis protein expression and coexisting defects in mitochondrial death signaling. Cancer Res 2006;66:1730-9.
55. Park SJ, Wu CH, Gordon JD, Zhong X, Emami A, Safa AR. Taxol induces caspase-10-dependent apoptosis. J Biol Chem 2004;279:51057-67.
56. Nicklin PL, Bayley D, Giddings J, et al. Pulmonary bioavailability of a phosphorothioate oligonucleotide (CGP 64128A): comparison with other delivery routes. Pharm Res 1998;15:583-91.
57. Vidal L, Blagden S, Attard G, de Bono J. Making sense of antisense. Eur J Cancer 2005;41:2812-8.