Targeted nanoparticle delivery overcomes off-target immunostimulatory effects of oligonucleotides and improves therapeutic efficacy in chronic lymphocytic leukemia

Blood

Volumn 121, Issue 1, 2013, Pages 136-147

  Yu, Bo ^a,b   Mao, Yicheng ^b   Bai, Li Yuan ^c   Herman, Sarah E M ^d   Wang, Xinmei ^b   Ramanunni, Asha ^d   Jin, Yan ^b   Mo, Xiaokui ^b   Cheney, Carolyn ^d   Chan, Kenneth K ^b,d   Jarjoura, David ^b   Marcucci, Guido ^b,d   Lee, Robert J ^a,b   Byrd, John C ^c,d   Lee, L James ^a,b   Muthusamy, Natarajan ^d,e  

^a The Ohio State University   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^e OSUCCC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUDARABINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOLIPOSOME; NANOPARTICLE; OBLIMERSEN; PROTEIN BCL 2; RITUXIMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CHEMOSENSITIVITY; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG CONJUGATION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; ENDOSOME; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VIVO STUDY; LIPOSOMAL DELIVERY; MOUSE; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; TARGET CELL; TUMOR XENOGRAFT;

EID: 84872093800     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-01-407742     Document Type: Article

References (43)

1. Rayburn ER, Zhang R. Antisense, RNAi, and gene silencing strategies for therapy: mission possible or impossible? Drug Discov Today. 2008;13(11-12):513- 521.
2. Yu B, Zhao X, Lee LJ, et al. Targeted delivery systems for oligonucleotide therapeutics. AAPS J. 2009;11(1):195-203.
3. Juliano R, Alam MR, Dixit V, et al. Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides. Nucleic Acids Res. 2008;36(12):4158-4171.
4. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov. 2010;9(10):775-789.
5. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol. 2008;9(1):47-59.
6. Lessene G, Czabotar PE, Colman PM. BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov. 2008;7(12):989-1000.
7. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352(8):804-815.
8. Pleyer L, Egle A, Hartmann TN, et al. Molecular and cellular mechanisms of CLL: novel therapeutic approaches. Nat Rev Clin Oncol. 2009;6(7):405-418.
9. Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with In vitro and In vivo chemoresponses. Blood. 1998;91(9):3379-3389.
10. Cheson BD. Oblimersen for the treatment of patients with chronic lymphocytic leukemia. Ther Clin Risk Manag. 2007;3(5):855-870.
11. O'Brien SM, Cunningham CC, Golenkov AK, et al. Phase I to II multicenter study of oblimersen sodium, a Bcl-2 antisense oligonucleotide, in patients with advanced chronic lymphocytic leukemia. J Clin Oncol. 2005;23(30):7697-7702.
12. Marcucci G, Stock W, Dai G, et al. Phase I study of oblimersen sodium, an antisense to Bcl-2, in untreated older patients with acute myeloid leukemia: pharmacokinetics, pharmacodynamics, and clinical activity. J Clin Oncol. 2005;23(15):3404-3411.
13. O'Brien S, Moore JO, Boyd TE, et al. Randomized phase III trial of fludarabine plus cyclophosphamide with or without oblimersen sodium (Bcl-2 antisense) in patients with relapsed or refractory chronic lymphocytic leukemia. J Clin Oncol. 2007;25(9):1114-1120.
14. O'Brien S, Moore JO, Boyd TE, et al. 5-year survival in patients with relapsed or refractory chronic lymphocytic leukemia in a randomized, phase III trial of fludarabine plus cyclophosphamide with or without oblimersen. J Clin Oncol. 2009;27(31):5208-5212.
15. Vogler M, Butterworth M, Majid A, et al. Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood. 2009;113(18):4403-4413.
16. Jahrsdörfer B, Jox R, Muhlenhoff L, et al. Modulation of malignant B cell activation and apoptosis by bcl-2 antisense ODN and immunostimulatory CpG ODN. J Leukoc Biol. 2002;72(1):83-92.
17. Agrawal S, Kandimalla ER. Role of Toll-like receptors in antisense and siRNA [corrected]. Nat Biotechnol. 2004;22(12):1533-1537.
18. Gekeler V, Gimmnich P, Hofmann HP, et al. G3139 and other CpG-containing immunostimulatory phosphorothioate oligodeoxynucleotides are potent suppressors of the growth of human tumor xenografts in nude mice. Oligonucleotides. 2006;16(1):83-93.
19. Kim R, Emi M, Matsuura K, et al. Antisense and nonantisense effects of antisense Bcl-2 on multiple roles of Bcl-2 as a chemosensitizer in cancer therapy. Cancer Gene Ther. 2007;14(1):1-11.
20. Yang X, Koh CG, Liu S, et al. Transferrin receptor-targeted lipid nanoparticles for delivery of an antisense oligodeoxyribonucleotide against Bcl-2. Mol Pharm. 2009;6(1):221-230.
21. Liang X, Moseman EA, Farrar MA, et al. Toll-like receptor 9 signaling by CpG-B oligodeoxynucleotides induces an apoptotic pathway in human chronic lymphocytic leukemia B cells. Blood. 2010;115(24):5041-5052.
22. Rozková D, Novotna L, Pytlik R, et al. Toll-like receptors on B-CLL cells: expression and functional consequences of their stimulation. Int J Cancer. 2010;126(5):1132-1143.
23. Hertlein ETG, Sass EJ, Hessler JD, et al. Milatuzumab immunoliposomes induce cell death in CLL by promoting accumulation of CD74 on the surface of B cells. Blood. 2010;116(14):2554-2558.
24. Chiu GN, Edwards LA, Kapanen AI, et al. Modulation of cancer cell survival pathways using multivalent liposomal therapeutic antibody constructs. Mol Cancer Ther. 2007;6(3):844-855.
25. Weiss A, Preston TC, Popov J et al. Selective recognition of rituximab-functionalized gold nanoparticles by lymphoma cells studied with 3D imaging. J Phys Chem C. 2009;113(47):20252-20258.
26. Jahrsdörfer B, Hartmann G, Racila E, et al. CpG DNA increases primary malignant B cell expression of costimulatory molecules and target antigens. J Leukoc Biol. 2001;69(1):81-88.
27. Barchet W, Wimmenauer V, Schlee M, et al. Accessing the therapeutic potential of immunostimulatory nucleic acids. Curr Opin Immunol. 2008;20(4):389-395.
28. Peng SL. Signaling in B cells via Toll-like receptors. Curr Opin Immunol. 2005;17(3):230-236.
29. Krieg AM. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov. 2006;5(6):471-484.
30. Viatour P, Bentires-Alj M, Chariot A, et al. NFkappa B2/p100 induces Bcl-2 expression. Leukemia. 2003;17(7):1349-1356.
31. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441(7092):431-436.
32. Pedersen IM, Buhl AM, Klausen P, et al. The chimeric anti-CD20 antibody rituximab induces apoptosis in B-cell chronic lymphocytic leukemia cells through a p38 mitogen activated protein-kinase-dependent mechanism. Blood. 2002;99(4):1314-1319.
33. Zhao X, Lapalombella R, Joshi T, et al. Targeting CD37-positive lymphoid malignancies with a novel engineered small modular immunopharmaceutical. Blood. 2007;110(7):2569-2577.
34. Pan X, Chen L, Liu S, et al. Antitumor activity of G3139 lipid nanoparticles (LNPs). Mol Pharm. 2009;6(1):211-220.
35. Wacheck V, Krepler C, Strommer S, et al. Antitumor effect of G3139 Bcl-2 antisense oligonucleotide is independent of its immune stimulation by CpG motifs in SCID mice. Antisense Nucleic Acid Drug Dev. 2002;12(6):359-367.
36. Lai JC, Benimetskaya L, Khvorova A, et al. Phosphorothioate oligodeoxynucleotides and G3139 induce apoptosis in 518A2 melanoma cells. Mol Cancer Ther. 2005;4(2):305-315.
37. Lai JC, Tan W, Benimetskaya L, et al. A pharmacologic target of G3139 in melanoma cells may be the mitochondrial VDAC. Proc Natl Acad Sci U SA. 2006;103(19):7494-7499.
38. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 2008;8(8):594-606.
39. Guiducci C, Ott G, Chan JH, et al. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J Exp Med. 2006;203(8):1999-2008.
40. Vollmer J, Weeratna RD, Jurk M, et al. Oligodeoxynucleotides lacking CpG dinucleotides mediate Toll-like receptor 9 dependent T helper type 2 biased immune stimulation. Immunology. 2004;113(2):212-223.
41. Castro JE, Prada CE, Aguillon RA, et al. Thymidine-phosphorothioate oligonucleotides induce activation and apoptosis of CLL cells independently of CpG motifs or BCL-2 gene interference. Leukemia. 2006;20(4):680-688.
42. Kleinman ME, Yamada K, Takeda A, et al. Sequence- and target-independent angiogenesis suppression by siRNA via TLR3. Nature. 2008;452(7187):591-597.
43. Lapalombella R, Yu B, Triantafillou G, et al. Lenalidomide down-regulates the CD20 antigen and antagonizes direct and antibody-dependent cellular cytotoxicity of rituximab on primary chronic lymphocytic leukemia cells. Blood. 2008;112(13):5180-5189.