Novel delivery system for T-oligo using a nanocomplex formed with an alpha helical peptide for melanoma therapy

International Journal of Nanomedicine

Volumn 9, Issue 1, 2013, Pages 43-53

  Uppada, Srijayaprakash B ^a   Erickson, Terrianne ^a   Wojdyla, Luke ^a   Moravec, David N ^a   Song, Ziyuan ^b   Cheng, Jianjun ^b   Puri, Neelu ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

Angiogenesis; Apoptosis; Melanoma; Senescence; T oligo

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE; CASPASE 3; MELAN A; MOLECULAR THERAPY AGENT; PROCASPASE 3; PROCASPASE 7; PROTEIN P73; TELOMERE OVERHANG OLIGONUCLEOTIDE; TELOMERE OVERHANG OLIGONUCLEOTIDE PVBLG 8 PEPTIDE NANOCOMPLEX; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MALE; MELANOMA; MOUSE; NONHUMAN; PARTICLE SIZE; PROTEIN EXPRESSION; TUMOR VOLUME; ZETA POTENTIAL;

ANGIOGENESIS; APOPTOSIS; MELANOMA; SENESCENCE; T-OLIGO;

ANIMALS; CELL LINE, TUMOR; DRUG COMBINATIONS; MALE; MELANOMA; MICE; MICE, NUDE; NANOCAPSULES; OLIGONUCLEOTIDES; PARTICLE SIZE; PEPTIDES; TREATMENT OUTCOME;

EID: 84890535187     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S55133     Document Type: Article

References (64)

1. Khan KH, Goody RB, Hameed H, Jalil A, Coyle VM, McAleer JJ. Metastatic melanoma: a regional review and future directions. Tumori. 2012;98:575-580.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11-30.
3. Viola JR, Rafael DF, Wagner E, Besch R, Ogris M. Gene therapy for advanced melanoma: selective targeting and therapeutic nucleic acids. J Drug Deliv. 2013;2013:897348.
4. Haluska FG, Tsao H, Wu H, Haluska FS, Lazar A, Goel V. Genetic alterations in signaling pathways in melanoma. Clin Cancer Res. 2006;12: 2301s-2307s.
5. Chapman PB, Hauschild A, Robert C, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364:2507-2516.
6. Lu H, Wang J, Bai Y, et al. Ionic polypeptides with unusual helical stability. Nat Commun. 2011;2:206.
7. Li GZ, Eller MS, Firoozabadi R, Gilchrest BA. Evidence that exposure of the telomere 3′ overhang sequence induces senescence. Proc Natl Acad Sci U S A. 2003;100:527-531.
8. Puri N, Eller MS, Byers HR, Dykstra S, Kubera J, Gilchrest BA. Telomere-based DNA damage responses: a new approach to melanoma. FASEB J. 2004;18:1373-1381.
9. Rankin AM, Sarkar S, Faller DV. Mechanism of T-oligo-induced cell cycle arrest in Mia-PaCa pancreatic cancer cells. J Cell Physiol. 2012;227:2586-2594.
10. Li GZ, Eller MS, Hanna K, Gilchrest BA. Signaling pathway requirements for induction of senescence by telomere homolog oligonucleotides. Exp Cell Res. 2004;301:189-200.
11. Yaar M, Eller MS, Panova I, et al. Telomeric DNA induces apoptosis and senescence of human breast carcinoma cells. Breast Cancer Res. 2007;9:R13.
12. Pitman RT, Wojdyla L, Puri N. Mechanism of DNA damage responses induced by exposure to an oligonucleotide homologous to the telomere overhang in melanoma. Oncotarget. 2013;4:761-771.
13. Gnanasekar M, Thirugnanam S, Zheng G, Chen A, Ramaswamy K. T-oligo induces apoptosis in advanced prostate cancer cells. Oligonucleotides. 2009;19:287-292.
14. Sarkar S, Faller D V. T-oligos inhibit growth and induce apoptosis in human ovarian cancer cells. Oligonucleotides. 2011;21:47-53.
15. Puri N, Pitman RT, Mulnix RE, et al. Non-small cell lung cancer is susceptible to induction of DNA damage responses and inhibition of angiogenesis by telomere overhang oligonucleotides. Cancer Lett. September 4, 2013. [Epub ahead of print.]
16. Wickstrom E. Oligodeoxynucleotide stability in subcellular extracts and culture media. J Biochem Biophys Methods. 1986;13:97-102.
17. Gabrielson N P, Lu H, Yin L, Kim KH, Cheng J. A cell-penetrating helical polymer for siRNA delivery to mammalian cells. Mol Ther. 2012;20:1599-1609.
18. Lu H, Bai Y, Wang J, et al. Ring-opening polymerization of gamma-(4-vinylbenzyl)-(L)-glutamate N-carboxyanhydride for the synthesis of functional polypeptides. Macromolecules. 2011;44:6237-6240.
19. Eller MS, Puri N, Hadshiew IM, Venna SS, Gilchrest BA. Induction of apoptosis by telomere 3′ overhang-specifc DNA. Exp Cell Res. 2002;276:185-193.
20. Puri N, Salgia R. Synergism of EGFR and c-Met pathways, cross-talk and inhibition, in non-small cell lung cancer. J Carcinog. 2008;7:9.
21. Kang T W, Yevsa T, Woller N, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature. 2011;479:547-551.
22. Butterfeld LH, Comin-Anduix B, Vujanovic L, et al. Adenovirus MART-1-engineered autologous dendritic cell vaccine for metastatic melanoma. J Immunother. 2008;31:294-309.
23. Cavallaro U, Christofori G. Molecular mechanisms of tumor angiogenesis and tumor progression. J Neurooncol. 2000;50: 63-70.
24. Kaur S, Martin-Manso G, Pendrak ML, Garfeld SH, Isenberg JS, Roberts DD. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J Biol Chem. 2010;285: 38923-38932.
25. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neo-vascularization by thrombospondin-1. Nat Med. 2000;6:41-48.
26. Fleitas T, Martinez-Sales V, Vila V, et al. VEGF and TSP1 levels correlate with prognosis in advanced non-small cell lung cancer. Clin Transl Oncol. 2013;15:897-902.
27. Parkinson EK, Minty F. Anticancer therapy targeting telomeres and telomerase: current status. BioDrugs. 2007;21:375-385.
28. Eder PS, DeVine RJ, Dagle JM, Walder JA. Substrate specificity and kinetics of degradation of antisense oligonucleotides by a 3′ exonuclease in plasma. Antisense Res Dev. 1991;1:141-151.
29. Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov. 2008;7: 771-782.
30. Ali HM, Urbinati G, Raouane M, Massaad-Massade L. Signifcance and applications of nanoparticles in siRNA delivery for cancer therapy. Expert Rev Clin Pharmacol. 2012;5:403-412.
31. Chen Y, Bathula SR, Yang Q, Huang L. Targeted nanoparticles deliver siRNA to melanoma. J Invest Dermatol. 2010;130:2790-2798.
32. Nguyen LT, Atobe K, Barichello JM, Ishida T, Kiwada H. Complex formation with plasmid DNA increases the cytotoxicity of cationic liposomes. Biol Pharm Bull. 2007;30:751-757.
33. Yin L, Song Z, Qu Q, et al. Supramolecular self-assembled nanoparticles mediate oral delivery of therapeutic TNF-alpha siRNA against systemic infammation. Angew Chem Int Ed Engl. 2013;52:5757-5761.
34. Yin L, Song Z, Kim KH, Zheng N, Gabrielson N P, Cheng J. Non-viral gene delivery via membrane-penetrating, mannose-targeting supramolec-ular self-assembled nanocomplexes. Adv Mater. 2013;25:3063-3070.
35. Rankin AM, Forman L, Sarkar S, Faller DV. Enhanced cytotoxicity from deoxyguanosine-enriched T-oligo in prostate cancer cells. Nucleic Acid Ther. 2013;23:311-321.
36. Terrinoni A, Ranalli M, Cadot B, et al. p73-alpha is capable of inducing scotin and ER stress. Oncogene. 2004;23:3721-3725.
37. Ramadan S, Terrinoni A, Catani M V, et al. p73 induces apoptosis by different mechanisms. Biochem Biophys Res Commun. 2005;331:713-717.
38. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol. 2004;5:897-907.
39. Dias N, Stein CA. Antisense oligonucleotides: basic concepts and mechanisms. Mol Cancer Ther. 2002;1:347-355.
40. Wojcik M, Cieslak M, Stec WJ, Goding J W, Koziolkiewicz M. Nucleotide pyrophosphatase/phosphodiesterase 1 is responsible for degradation of antisense phosphorothioate oligonucleotides. Oligonucleotides. 2007;17:134-145.
41. Brown DA, Kang SH, Gryaznov SM, et al. Effect of phosphoro-thioate modifcation of oligodeoxynucleotides on specifc protein binding. J Biol Chem. 1994;269:26801-26805.
42. Levin AA. A review of the issues in the pharmacokinetics and toxicology of phosphorothioate antisense oligonucleotides. Biochim Biophys Acta. 1999;1489:69-84.
43. Elsabahy M, Nazarali A, Foldvari M. Non-viral nucleic acid delivery: key challenges and future directions. Curr Drug Deliv. 2011;8:235-244.
44. Yen J, Zhang Y, Gabrielson N P, et al. Cationic, helical polypeptide-based gene delivery for IMR-90 fbroblasts and human embryonic stem cells. Biomater Sci. 2013;1:719-727.
45. Lawler J. Thrombospondin-1 as an endogenous inhibitor of angio-genesis and tumor growth. J Cell Mol Med. 2002;6:1-12.
46. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev. 2004;56:549-580.
47. Nakagawa T, Li JH, Garcia G, et al. TGF-beta induces proangio-genic and antiangiogenic factors via parallel but distinct Smad pathways. Kidney Int. 2004;66:605-613.
48. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3:401-410.
49. Kieran M W, Kalluri R, Cho YJ. The VEGF pathway in cancer and disease: responses, resistance, and the path forward. Cold Spring Harb Perspect Med. 2012;2:a006593.
50. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23:1011-1027.
51. Ugurel S, Rappl G, Tilgen W, Reinhold U. Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol. 2001;19:577-583.
52. Rajabi P, Neshat A, Mokhtari M, Rajabi MA, Eftekhari M, Tavakoli P. The role of VEGF in melanoma progression. J Res Med Sci. 2012;17:534-539.
53. Dvorak HF. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol. 2002;20:4368-4380.
54. Willett CG, Boucher Y, Di Tomaso E, et al. Direct evidence that the VEGF-specifc antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med. 2004;10:145-147.
55. Chekhonin V P, Shein SA, Korchagina AA, Gurina OI. VEGF in tumor progression and targeted therapy. Curr Cancer Drug Targets. 2013;13:423-443.
56. Planchard D. Bevacizumab in non-small-cell lung cancer: a review. Expert Rev Anticancer Ther. 2011;11:1163-1179.
57. Shih T, Lindley C. Bevacizumab: an angiogenesis inhibitor for the treatment of solid malignancies. Clin Ther. 2006;28:1779-1802.
58. Ferrara N, Hillan KJ, Gerber H P, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov. 2004;3:391-400.
59. Adams JC, Lawler J. The thrombospondins. Cold Spring Harb Perspect Biol. 2011;3:a009712.
60. Jin RJ, Kwak C, Lee SG, et al. The application of an anti-angiogenic gene (thrombospondin-1) in the treatment of human prostate cancer xenografts. Cancer Gene Ther. 2000;7:1537-1542.
61. Lee YJ, Koch M, Karl D, et al. Variable inhibition of thrombospondin 1 against liver and lung metastases through differential activation of metalloproteinase ADAMTS1. Cancer Res. 2010;70:948-956.
62. Bornstein P. Thrombospondins as matricellular modulators of cell function. J Clin Invest. 2001;107:929-934.
63. Rofstad EK, Henriksen K, Galappathi K, Mathiesen B. Antiangiogenic treatment with thrombospondin-1 enhances primary tumor radiation response and prevents growth of dormant pulmonary micrometastases after curative radiation therapy in human melanoma xenografts. Cancer Res. 2003;63:4055-4061.
64. Horiguchi H, Yamagata S, Rong Qian Z, Kagawa S, Sakashita N. Thrombospondin-1 is highly expressed in desmoplastic components of invasive ductal carcinoma of the breast and associated with lymph node metastasis. J Med Invest. 2013;60:91-96.