Peptide-conjugated antisense oligonucleotides for targeted inhibition of a transcriptional regulator in vivo

Nature Biotechnology

Volumn 26, Issue 1, 2008, Pages 91-100

  Henke, Erik ^a   Perk, Jonathan ^a   Vider, Jelena ^a   De Candia, Paola ^a   Chin, Yvette ^a   Solit, David B ^a   Ponomarev, Vladimir ^a   Cartegni, Luca ^a   Manova, Katia ^a   Rosen, Neal ^a   Benezra, Robert ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METASTASIS; PEPTIDE-CONJUGATED ANTISENSE OLIGONUCLEOTIDES; PROTEIN-PROTEIN INTERACTIONS;

MEDICAL PROBLEMS; ONCOLOGY; PATIENT TREATMENT; PEPTIDES; TRANSCRIPTION; TUMORS;

OLIGONUCLEOTIDES;

ANTISENSE OLIGODEOXYNUCLEOTIDE; HEAT SHOCK PROTEIN 90 INHIBITOR; PEPTIDE DERIVATIVE; PROTEIN LD1; PROTEIN LD3; REGULATOR PROTEIN; TANESPIMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER INVASION; CANCER MODEL; CONTROLLED STUDY; DRUG CONJUGATION; DRUG STRUCTURE; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IN VIVO STUDY; KNOCKOUT MOUSE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR BLEEDING; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; GENE TARGETING; MICE; NEOPLASM PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDES; TRANSCRIPTION FACTORS;

MUS;

EID: 38049094661     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt1366     Document Type: Article

References (51)

1. Emanuel, B.S. et al. The 2p breakpoint of a 2;8 translocation in Burkitt lymphoma interrupts the V kappa locus. Proc. Natl. Acad. Sci. USA 81, 2444-2446 (1984).
2. Mushinski, J.F., Potter, M., Bauer, S.R. & Reddy, E.P. DNA rearrangement and altered RNA expression of the c-myb oncogene in mouse plasmacytoid lymphosarcomas. Science 220, 795-798 (1983).
3. Vogelstein, B. & Kinzler, K.W. Cancer genes and the pathways they control. Nat. Med. 10, 789-799 (2004).
4. Darnell, J.E., Jr. Transcription factors as targets for cancer therapy. Nat. Rev. Cancer 2, 740-749 (2002).
5. Wang, L.H., Yang, X.Y., Kirken, R.A., Resau, J.H. & Farrar, W.L. Targeted disruption of stat6 DNA binding activity by an oligonucleotide decoy blocks IL-4-driven T(H)2 cell response. Blood 95, 1249-1257 (2000).
6. Turkson, J. et al. Novel peptidomimetic inhibitors of signal transducer and activator of transcription 3 dimerization and biological activity. Mol. Cancer Ther. 3, 261-269 (2004).
7. Jing, N. et al. G-quartet oligonucleotides: a new class of signal transducer and activator of transcription 3 inhibitors that suppresses growth of prostate and breast tumors through induction of apoptosis. Cancer Res. 64, 6603-6609 (2004).
8. Mateo-Lozano, S. et al. Combined transcriptional and translational targeting of EWS/FLI-1 in Ewing's sarcoma. Clin. Cancer Res. 12, 6781-6790 (2006).
9. Sumida, T., Itahana, Y., Hamakawa, H. & Desprez, P.Y. Reduction of human metastatic breast cancer cell aggressiveness on introduction of either form a or B of the progesterone receptor and then treatment with progestins. Cancer Res. 64, 7886-7892 (2004).
10. Lee, K.T. et al. Overexpression of Id-1 is significantly associated with tumour angiogenesis in human pancreas cancers. Br. J. Cancer 90, 1198-1203 (2004).
11. Vandeputte, D.A. et al. Expression and distribution of id helix-loop-helix proteins in human astrocytic tumors. Glia 38, 329-338 (2002).
12. Minn, A.J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (2005).
13. Gupta, G.P. et al. ID genes mediate tumor re-initiation during breast cancer lung metastasis. Proc. Natl. Acad. Sci. USA (in the press).
14. Lyden, D. et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670-677 (1999).
15. de Candia, P. et al. Angiogenesis impairment in Id-deficient mice cooperates with an Hsp90 inhibitor to completely suppress HER2/neu-dependent breast tumors. Proc. Natl. Acad. Sci. USA 100, 12337-12342 (2003).
16. Ruzinova, M.B. et al. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 4, 277-289 (2003).
17. Li, H., Gerald, W.L. & Benezra, R. Utilization of bone marrow-derived endothelial cell precursors in spontaneous prostate tumors varies with tumor grade. Cancer Res. 64, 6137-6143 (2004).
18. Perk, J. et al. Reassessment of id1 protein expression in human mammary, prostate, and bladder cancers using a monospecific rabbit monoclonal anti-id1 antibody. Cancer Res. 66, 10870-10877 (2006).
19. Sakurai, D. et al. Crucial role of inhibitor of DNA binding/differentiation in the vascular endothelial growth factor-induced activation and angiogenic processes of human endothelial cells. J. Immunol. 173, 5801-5809 (2004).
20. Belletti, B. et al. Regulation of Id1 protein expression in mouse embryo fibroblasts by the type 1 insulin-like growth factor receptor. Exp. Cell Res. 277, 107-118 (2002).
21. Borlak, J., Meier, T., Halter, R., Spanel, R. & Spanel-Borowski, K. Epidermal growth factor-induced hepatocellular carcinoma: gene expression profiles in precursor lesions, early stage and solitary tumours. Oncogene 24, 1809-1819 (2005).
22. Viloria-Petit, A. et al. Acquired resistance to the antitumor effect of epidermal growth factor receptor-blocking antibodies in vivo: a role for altered tumor angiogenesis. Cancer Res. 61, 5090-5101 (2001).
23. Casanovas, O., Hicklin, D.J., Bergers, G. & Hanahan, D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8, 299-309 (2005).
24. Porkka, K., Laakkonen, P., Hoffman, J.A., Bernasconi, M. & Ruoslahti, E. A fragment of the HMGN2 protein homes to the nuclei of tumor cells and tumor endothelial cells in vivo. Proc. Natl. Acad. Sci. USA 99, 7444-7449 (2002).
25. Lyden, D. et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7, 1194-1201 (2001).
26. Ohtani, N. et al. Opposing effects of Ets and Id proteins on p16(INK4a) expression during cellular senescence. Nature 409, 1067-1070 (2001).
27. Fong, S. et al. Id-1 as a molecular target in therapy for breast cancer cell invasion and metastasis. Proc. Natl. Acad. Sci. USA 100, 13543-13548 (2003).
28. Christian, S. et al. Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J. Cell Biol. 163, 871-878 (2003).
29. Shi, H. et al. Nucleolin is a receptor that mediates antiangiogenic and anti-tumor activity of endostatin. Blood 110, 2899-2906 (2007).
30. Zhao, Q. et al. Cellular distribution of phosphorothioate oligonucleotide following intravenous administration in mice. Antisense Nucleic Acid Drug Dev. 8, 451-458 (1998).
31. Solit, D.B. et al. 17-Allylamino-17-demethoxygeldanamycin induces the degradation of androgen receptor and HER-2/neu and inhibits the growth of prostate cancer xenografts. Clin. Cancer Res. 8, 986-993 (2002).
32. Holmgren, L., O'Reilly, M.S. & Folkman, J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1, 149-153 (1995).
33. Doubrovin, M., Serganova, I., Mayer-Kuckuk, P., Ponomarev, V. & Blasberg, R.G. Multimodality in vivo molecular-genetic imaging. Bioconjug. Chem. 15, 1376-1388 (2004).
34. Ponomarev, V. et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur. J. Nucl. Med. Mol. Imaging 31, 740-751 (2004).
35. Perk, J., Iavarone, A. & Benezra, R. Id family of helix-loop-helix proteins in cancer. Nat. Rev. Cancer 5, 603-614 (2005).
36. Ruzinova, M.B. & Benezra, R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13, 410-418 (2003).
37. Akerman, M.E., Chan, W.C., Laakkonen, P., Bhatia, S.N. & Ruoslahti, E. Nanocrystal targeting in vivo. Proc. Natl. Acad. Sci. USA 99, 12617-12621 (2002).
38. Reddy, G.R. et al. Vascular targeted nanoparticles for imaging and treatment of brain tumors. Clin. Cancer Res. 12, 6677-6686 (2006).
39. Corey, D.R. 48000-fold Acceleration of hybridization by chemically modified oligonucleotides. J. Am. Chem. Soc. 117, 9373-9374 (1995).
40. Winkler, F. et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6, 553-563 (2004).
41. Shaked, Y. et al. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 313, 1785-1787 (2006).
42. Mabjeesh, N.J. et al. Geldanamycin induces degradation of hypoxia-inducible factor 1alpha protein via the proteosome pathway in prostate cancer cells. Cancer Res. 62, 2478-2482 (2002).
43. Petit, A.M. et al. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am. J. Pathol. 151, 1523-1530 (1997).
44. Henry, S.P., Grillone, L.R., Orr, J.L., Bruner, R.H. & Kornbrust, D.J. Comparison of the toxicity profiles of ISIS 1082 and ISIS 2105, phosphorothioate oligonucleotides, following subacute intradermal administration in Sprague-Dawley rats. Toxicology 116, 77-88 (1997).
45. Trepel, M., Arap, W. & Pasqualini, R. Modulation of the immune response by systemic targeting of antigens to lymph nodes. Cancer Res. 61, 8110-8112 (2001).
46. Arap, M.A. et al. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 6, 275-284 (2004).
47. Kolonin, M.G., Saha, P.K., Chan, L., Pasqualini, R. & Arap, W. Reversal of obesity by targeted ablation of adipose tissue. Nat. Med. 10, 625-632 (2004).
48. Ardelt, P.U. et al. Targeting urothelium: ex vivo assay standardization and selection of internalizing ligands. J. Urol. 169, 1535-1540 (2003).
49. Lee, L. et al. Identification of synovium-specific homing peptides by in vivo phage display selection. Arthritis Rheum. 46, 2109-2120 (2002).
50. Nowakowski, G.S. et al. A specific heptapeptide from a phage display peptide library homes to bone marrow and binds to primitive hematopoietic stem cells. Stem Cells 22, 1030-1038 (2004).
51. Harrison, J.G. & Balasubramanian, S. Synthesis and hybridization analysis of a small library of peptide-oligonucleotide conjugates. Nucleic Acids Res. 26, 3136-3145 (1998).