A Glu-urea-Lys Ligand-conjugated Lipid Nanoparticle/siRNA System Inhibits Androgen Receptor Expression In Vivo

Molecular Therapy Nucleic Acids

Volumn 5, Issue , 2016, Pages e348-

  Lee, Justin B ^a   Zhang, Kaixin ^b   Tam, Yuen Yi C ^a   Quick, Joslyn ^a   Tam, Ying K ^a   Lin, Paulo JC ^a   Chen, Sam ^a   Liu, Yan ^a   Nair, Jayaprakash K ^c   Zlatev, Ivan ^c   Rajeev, Kallanthottathil G ^c   Manoharan, Muthiah ^c   Rennie, Paul S ^b   Cullis, Pieter R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER PROSTATE CENTRE   (Canada)

^c ALNYLAM PHARMACEUTICALS   (United States)

Author keywords

androgen receptor; lipid nanoparticles; liposomes; prostate cancer; prostate specific membrane antigen; siRNA

Indexed keywords

ANDROGEN RECEPTOR; GLUTAMIC ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LIPID NANOPARTICLE; LYSINE; MACROGOL; MESSENGER RNA; NANOPARTICLE; PROSTATE SPECIFIC ANTIGEN; PROSTATE SPECIFIC MEMBRANE ANTIGEN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UREA; GLUTAMATE UREA LYSINE; LIGAND; NANOCARRIER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG TARGETING; DRUG UPTAKE; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; LNCAP CELL LINE; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NANOENCAPSULATION; NONHUMAN; OPSONIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROSTATE CANCER; SONOGASHIRA REACTION; TUMOR XENOGRAFT; TUNEL ASSAY; ZETA POTENTIAL; ANTINEOPLASTIC ACTIVITY; DRUG CONJUGATION; DRUG FORMULATION; DRUG POTENCY; SERUM; TUMOR CELL;

EID: 85015163851     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2016.43     Document Type: Article

References (48)

1. 1 Lee, JB, Zhang, K, Tam, YY, Tam, YK, Belliveau, NM, Sung, VY, et al. Lipid nanoparticle siRNA systems for silencing the androgen receptor in human prostate cancer in vivo. Int J Cancer 131 (2012), E781–E790.
2. 2 Semple, SC, Akinc, A, Chen, J, Sandhu, AP, Mui, BL, Cho, CK, et al. Rational design of cationic lipids for siRNA delivery. Nat Biotechnol 28 (2010), 172–176.
3. 3 Akinc, A, Querbes, W, De, S, Qin, J, Frank-Kamenetsky, M, Jayaprakash, KN, et al. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol Ther 18 (2010), 1357–1364.
4. 4 Jayaraman, M, Ansell, SM, Mui, BL, Tam, YK, Chen, J, Du, X, et al. Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew Chem Int Ed Engl 51 (2012), 8529–8533.
5. 5 Longmuir, KJ, Robertson, RT, Haynes, SM, Baratta, JL, Waring, AJ, Effective targeting of liposomes to liver and hepatocytes in vivo by incorporation of a Plasmodium amino acid sequence. Pharm Res 23 (2006), 759–769.
6. 6 Cullis, PR, Chonn, A, Semple, SC, Interactions of liposomes and lipid-based carrier systems with blood proteins: Relation to clearance behaviour in vivo. Adv Drug Deliv Rev 32 (1998), 3–17.
7. 7 Mahley, RW, Huang, Y, Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. J Clin Invest 117 (2007), 94–98.
8. 8 Rungta, RL, Choi, HB, Lin, PJ, Ko, RW, Ashby, D, Nair, J, et al. Lipid nanoparticle delivery of siRNA to silence neuronal gene expression in the brain. Mol Ther Nucleic Acids, 2, 2013, e136.
9. 9 Frank-Kamenetsky, M, Grefhorst, A, Anderson, NN, Racie, TS, Bramlage, B, Akinc, A, et al. Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholesterol in rodents and LDL cholesterol in nonhuman primates. Proc Natl Acad Sci USA 105 (2008), 11915–11920.
10. 10 Foster, DJ, Barros, S, Duncan, R, Shaikh, S, Cantley, W, Dell, A, et al. Comprehensive evaluation of canonical versus Dicer-substrate siRNA in vitro and in vivo. RNA 18 (2012), 557–568.
11. 11 Maeda, H, Wu, J, Sawa, T, Matsumura, Y, Hori, K, Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 65 (2000), 271–284.
12. 12 Maeda, H, The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv Enzyme Regul 41 (2001), 189–207.
13. 13 Ambegia, E, Ansell, S, Cullis, P, Heyes, J, Palmer, L, MacLachlan, I, Stabilized plasmid-lipid particles containing PEG-diacylglycerols exhibit extended circulation lifetimes and tumor selective gene expression. Biochim Biophys Acta 1669 (2005), 155–163.
14. 14 Mui, BL, Tam, YK, Jayaraman, M, Ansell, SM, Du, X, Tam, YY, et al. Influence of polyethylene glycol lipid desorption rates on pharmacokinetics and pharmacodynamics of siRNA lipid nanoparticles. Mol Ther Nucleic Acids, 2, 2013, e139.
15. 15 Banerjee, R, Tyagi, P, Li, S, Huang, L, Anisamide-targeted stealth liposomes: a potent carrier for targeting doxorubicin to human prostate cancer cells. Int J Cancer 112 (2004), 693–700.
16. 16 Chono, S, Li, SD, Conwell, CC, Huang, L, An efficient and low immunostimulatory nanoparticle formulation for systemic siRNA delivery to the tumor. J Control Release 131 (2008), 64–69.
17. 17 Li, SD, Chono, S, Huang, L, Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J Control Release 126 (2008), 77–84.
18. 18 Tam, YY, Chen, S, Zaifman, J, Tam, YK, Lin, PJ, Ansell, S, et al. Small molecule ligands for enhanced intracellular delivery of lipid nanoparticle formulations of siRNA. Nanomedicine 9 (2013), 665–674.
19. 19 Holmes, EH, Greene, TG, Tino, WT, Boynton, AL, Aldape, HC, Misrock, SL, et al. Analysis of glycosylation of prostate-specific membrane antigen derived from LNCaP cells, prostatic carcinoma tumors, and serum from prostate cancer patients. Prostate Suppl 7 (1996), 25–29.
20. 20 Liu, H, Rajasekaran, AK, Moy, P, Xia, Y, Kim, S, Navarro, V, et al. Constitutive and antibody-induced internalization of prostate-specific membrane antigen. Cancer Res 58 (1998), 4055–4060.
21. 21 Kularatne, SA, Wang, K, Santhapuram, HK, Low, PS, Prostate-specific membrane antigen targeted imaging and therapy of prostate cancer using a PSMA inhibitor as a homing ligand. Mol Pharm 6 (2009), 780–789.
22. 22 Kularatne, SA, Venkatesh, C, Santhapuram, HK, Wang, K, Vaitilingam, B, Henne, WA, et al. Synthesis and biological analysis of prostate-specific membrane antigen-targeted anticancer prodrugs. J Med Chem 53 (2010), 7767–7777.
23. 23 Thomas, M, Kularatne, SA, Qi, L, Kleindl, P, Leamon, CP, Hansen, MJ, et al. Ligand-targeted delivery of small interfering RNAs to malignant cells and tissues. Ann N Y Acad Sci 1175 (2009), 32–39.
24. 24 Banerjee, SR, Foss, CA, Castanares, M, Mease, RC, Byun, Y, Fox, JJ, et al. Synthesis and evaluation of technetium-99m- and rhenium-labeled inhibitors of the prostate-specific membrane antigen (PSMA). J Med Chem 51 (2008), 4504–4517.
25. 25 Maresca, KP, Hillier, SM, Femia, FJ, Keith, D, Barone, C, Joyal, JL, et al. A series of halogenated heterodimeric inhibitors of prostate specific membrane antigen (PSMA) as radiolabeled probes for targeting prostate cancer. J Med Chem 52 (2009), 347–357.
26. 26 McEnaney, PJ, Parker, CG, Zhang, AX, Spiegel, DA, Antibody-recruiting molecules: an emerging paradigm for engaging immune function in treating human disease. ACS Chem Biol 7 (2012), 1139–1151.
27. 27 Murelli, RP, Zhang, AX, Michel, J, Jorgensen, WL, Spiegel, DA, Chemical control over immune recognition: a class of antibody-recruiting small molecules that target prostate cancer. J Am Chem Soc 131 (2009), 17090–17092.
28. 28 Zhang, AX, Murelli, RP, Barinka, C, Michel, J, Cocleaza, A, Jorgensen, WL, et al. A remote arene-binding site on prostate specific membrane antigen revealed by antibody-recruiting small molecules. J Am Chem Soc 132 (2010), 12711–12716.
29. 29 He, W, Kularatne, SA, Kalli, KR, Prendergast, FG, Amato, RJ, Klee, GG, et al. Quantitation of circulating tumor cells in blood samples from ovarian and prostate cancer patients using tumor-specific fluorescent ligands. Int J Cancer 123 (2008), 1968–1973.
30. 30 Cheng, H, Snoek, R, Ghaidi, F, Cox, ME, Rennie, PS, Short hairpin RNA knockdown of the androgen receptor attenuates ligand-independent activation and delays tumor progression. Cancer Res 66 (2006), 10613–10620.
31. 31 Haupenthal, J, Baehr, C, Zeuzem, S, Piiper, A, RNAse A-like enzymes in serum inhibit the anti-neoplastic activity of siRNA targeting polo-like kinase 1. Int J Cancer 121 (2007), 206–210.
32. 32 Behlke, MA, Chemical modification of siRNAs for in vivo use. Oligonucleotides 18 (2008), 305–319.
33. 33 Belliveau, NM, Huft, J, Lin, PJ, Chen, S, Leung, AK, Leaver, TJ, et al. Microfluidic synthesis of highly potent limit-size lipid nanoparticles for in vivo delivery of siRNA. Mol Ther Nucleic Acids, 1, 2012, e37.
34. 34 Yoshioka, H, Surface modification of haemoglobin-containing liposomes with polyethylene glycol prevents liposome aggregation in blood plasma. Biomaterials 12 (1991), 861–864.
35. 35 Chen, S, Tam, YYC, Lin, PJC, Sung, MMH, Tam, YK, Cullis, PRC, Influence of particle size on the in vivo potency of lipid nanoparticle formulations of siRNA. J Control Release 235 (2016), 236–244.
36. 36 Madani, H, Thompson, AS, Threadgill, MD, An expedient synthesis of 7-O-functionalised pyrrolo[2,1-c][1,4]benzodiazepine-5,11-diones. Tetrahedron 58 (2002), 8107–8111.
37. 37 Sonogashira, K, Development of Pd–Cu catalyzed cross-coupling of terminal acetylenes with sp2-carbon halides. J Organometallic Chem 653 (2002), 46–49.
38. 38 Kaighn, ME, Narayan, KS, Ohnuki, Y, Lechner, JF, Jones, LW, Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 17 (1979), 16–23.
39. 39 Chonn, A, Semple, SC, Cullis, PR, Association of blood proteins with large unilamellar liposomes in vivo. Relation to circulation lifetimes. J Biol Chem 267 (1992), 18759–18765.
40. 40 Park, YS, Maruyama, K, Huang, L, Some negatively charged phospholipid derivatives prolong the liposome circulation in vivo. Biochim Biophys Acta 1108 (1992), 257–260.
41. 41 Scholzen, T, Gerdes, J, The Ki-67 protein: from the known and the unknown. J Cell Physiol 182 (2000), 311–322.
42. 42 Kawano, K, Maitani, Y, Effects of polyethylene glycol spacer length and ligand density on folate receptor targeting of liposomal Doxorubicin in vitro. J Drug Deliv, 2011, 2011, 160967.
43. 43 Reiter, RE, Gu, Z, Watabe, T, Thomas, G, Szigeti, K, Davis, E, et al. Prostate stem cell antigen: a cell surface marker overexpressed in prostate cancer. Proc Natl Acad Sci USA 95 (1998), 1735–1740.
44. 44 Cabral, H, Matsumoto, Y, Mizuno, K, Chen, Q, Murakami, M, Kimura, M, et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat Nanotechnol 6 (2011), 815–823.
45. 45 Nair, JK, Willoughby, JL, Chan, A, Charisse, K, Alam, MR, Wang, Q, et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J Am Chem Soc 136 (2014), 16958–16961.
46. 46 Maier, MA, Jayaraman, M, Matsuda, S, Liu, J, Barros, S, Querbes, W, et al. Biodegradable lipids enabling rapidly eliminated lipid nanoparticles for systemic delivery of RNAi therapeutics. Mol Ther 21 (2013), 1570–1578.
47. 47 Horoszewicz, JS, Leong, SS, Kawinski, E, Karr, JP, Rosenthal, H, Chu, TM, et al. LNCaP model of human prostatic carcinoma. Cancer Res 43 (1983), 1809–1818.
48. 48 Snoek, R, Cheng, H, Margiotti, K, Wafa, LA, Wong, CA, Wong, EC, et al. In vivo knockdown of the androgen receptor results in growth inhibition and regression of well-established, castration-resistant prostate tumors. Clin Cancer Res 15 (2009), 39–47.