Hepatic RNA interference: delivery by synthetic vectors

Schmidt C. RNAi momentum fizzles as pharma shifts priorities. Nat Biotechnol. 2011;29(2):93–4. Sinha G. Interest resparks in RNAi. Nat Biotech. 2012;30(11):1012. Huang L, Liu Y. In vivo delivery of RNAi with lipid-based nanoparticles. Annu Rev Biomed Eng. 2011;13:507–30. Bertrand JR, Pottier M, Vekris A, Opolon P, Maksimenko A, Malvy C. Comparison of antisense oligonucleotides and siRNAs in cell culture and in vivo. Biochem Biophys Res Commun. 2002;296(4):1000–4. Pecot CV, Calin GA, Coleman RL, Lopez-Berestein G, Sood AK. RNA interference in the clinic: challenges and future directions. Nat Rev Cancer. 2011;11(1):59–67. Bartlett DW, Davis ME. Insights into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent imaging. Nucleic Acids Res. 2006;34(1):322–33. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell. 2005;123(4):607–20. Kim DH, Rossi JJ. Strategies for silencing human disease using RNA interference. Nat Rev Genet. 2007;8(3):173–84. Baker M. RNA interference: homing in on delivery. Nature. 2010;464(7292):1225–8. doi:10.1038/4641225a. Kim DH, Behlke MA, Rose SD, Chang MS, Choi S, Rossi JJ. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat Biotechnol. 2005;23(2):222–6. 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. 2012;18(3):557–68. Sledz CA, Holko M, de Veer MJ, Silverman RH, Williams BR. Activation of the interferon system by short-interfering RNAs. Nature cell biology. 2003;5(9):834–9. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, et al. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol. 2003;21(6):635–7. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nature reviews Drug discovery. 2009;8(2):129–38. Pan Q, Ramakrishnaiah V, Henry S, Fouraschen S, de Ruiter PE, Kwekkeboom J, et al. Hepatic cell-to-cell transmission of small silencing RNA can extend the therapeutic reach of RNA interference (RNAi). Gut. 2012;61(9):1330–9. Liu F, Song YK, Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene therapy. 1999;6(7):1258–66. Geary RS, Yu RZ, Watanabe T, Henry SP, Hardee GE, Chappell A, et al. Pharmacokinetics of a tumor necrosis factor-alpha phosphorothioate 2′-O-(2-methoxyethyl) modified antisense oligonucleotide: comparison across species. Drug metabolism and disposition: the biological fate of chemicals. 2003;31(11):1419–28. Khatsenko O, Morgan R, Truong L, York-Defalco C, Sasmor H, Conklin B, et al. Absorption of antisense oligonucleotides in rat intestine: effect of chemistry and length. Antisense & Nucleic Acid Drug Development. 2000;10(1):35–44. Graff JR, Konicek BW, Vincent TM, Lynch RL, Monteith D, Weir SN, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Investig. 2007;117(9):2638–48. Soutschek J, Akinc A, Bramlage B, Charisse K, Constien R, Donoghue M, et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature. 2004;432(7014):173–8. Wang Y, Chen P, Shen J. The development and characterization of a glutathione-sensitive cross-linked polyethylenimine gene vector. Biomaterials. 2006;27(30):5292–8. Lungwitz U, Breunig M, Blunk T, Gopferich A. Polyethylenimine-based non-viral gene delivery systems. Eur J Pharm Biopharm. 2005;60(2):247–66. Doi Y, Katafuchi A, Fujiwara Y, Hitomi K, Tainer JA, Ide H, et al. Synthesis and characterization of oligonucleotides containing 2′-fluorinated thymidine glycol as inhibitors of the endonuclease III reaction. Nucleic Acids Res. 2006;34(5):1540–51. Jannot G, Vasquez-Rifo A, Simard MJ. Argonaute pull-down and RISC analysis using 2′-O-methylated oligonucleotides affinity matrices. Methods Mol Biol. 2011;725:233–49. doi:10.1007/978-1-61779-046-1_16. Verheggen I, Van Aerschot A, Toppet S, Snoeck R, Janssen G, Balzarini J, et al. Synthesis and antiherpes virus activity of 1,5-anhydrohexitol nucleosides. J Med Chem. 1993;36(14):2033–40. Egholm M, Buchardt O, Nielsen PE, Berg RH. Peptide nucleic acids (PNA). Oligonucleotide analogs with an achiral peptide backbone. J Am Chem Soc. 1992;114(5):1895–7. Mitchell JA, Paul-Clark MJ, Clarke GW, McMaster SK, Cartwright N. Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J Endocrinol. 2007;193(3):323–30. Prakash TP, Bhat B. 2′-Modified oligonucleotides for antisense therapeutics. Current topics in medicinal chemistry. 2007;7(7):641–9. Sonawane ND, Szoka Jr FC, Verkman AS. Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes. J Biol Chem. 2003;278(45):44826–31. Hafez IM, Maurer N, Cullis PR. On the mechanism whereby cationic lipids promote intracellular delivery of polynucleic acids. Gene therapy. 2001;8(15):1188–96. Choi HS, Liu W, Misra P, Tanaka E, Zimmer JP, Itty Ipe B, et al. Renal clearance of quantum dots. Nat Biotechnol. 2007;25(10):1165–70. Raouane M, Desmaele D, Urbinati G, Massaad-Massade L, Couvreur P. Lipid Conjugated Oligonucleotides: A Useful Strategy for Delivery. Bioconjugate chemistry. 2012. Jäschke A. Oligonucleotide-Poly(ethylene glycol) Conjugates: Synthesis, Properties, and Applications. Poly(ethylene glycol). ACS Symposium Series, vol 680: American Chemical Society; 1997. p. 265–83. Prakash TP, Allerson CR, Dande P, Vickers TA, Sioufi N, Jarres R, et al. Positional effect of chemical modifications on short interference RNA activity in mammalian cells. J Med Chem. 2005;48(13):4247–53. Wolfrum C, Shi S, Jayaprakash KN, Jayaraman M, Wang G, Pandey RK, et al. Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat Biotechnol. 2007;25(10):1149–57. Liu D, Mori A, Huang L. Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes. Biochim Biophys Acta. 1992;1104(1):95–101. Merkel TJ, Jones SW, Herlihy KP, Kersey FR, Shields AR, Napier M et al. Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proceedings of the National Academy of Sciences. 2011. doi:10.1073/pnas.1010013108 Li H, LaBean TH, Leong KW. Nucleic acid-based nanoengineering: novel structures for biomedical applications. Interface Focus. 2011;1(5):702–24. Erben CM, Goodman RP, Turberfield AJ. Single-molecule protein encapsulation in a rigid DNA cage. Angew Chem Int Ed. 2006;45(44):7414–7. Lo PK, Karam P, Aldaye FA, McLaughlin CK, Hamblin GD, Cosa G, et al. Loading and selective release of cargo in DNA nanotubes with longitudinal variation. Nat Chem. 2010;2(4):319–28. Zhou J, Shu Y, Guo P, Smith DD, Rossi JJ. Dual functional RNA nanoparticles containing phi29 motor pRNA and anti-gp120 aptamer for cell-type specific delivery and HIV-1 inhibition. Methods. 2011;54(2):284–94. Goodman RP, Heilemann M, Doose S, Erben CM, Kapanidis AN, Turberfield AJ. Reconfigurable, braced, three-dimensional DNA nanostructures. Nat Nano. 2008;3(2):93–6. Lee H, Lytton-Jean AKR, Chen Y, Love KT, Park AI, Karagiannis ED, et al. Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat Nano. 2012;7(6):389–93. Crispe IN. Hepatic T, cells and liver tolerance. Nat Rev Immunol. 2003;3(1):51–62. Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp Hepatol. 2002;1(1):1. Romero EL, Morilla MJ, Regts J, Koning GA, Scherphof GL. On the mechanism of hepatic transendothelial passage of large liposomes. FEBS Lett. 1999;448(1):193–6. Matsui K, Yoshimoto T, Tsutsui H, Hyodo Y, Hayashi N, Hiroishi K, et al. Propionibacterium acnes treatment diminishes CD4+ NK1.1+ T cells but induces type I T cells in the liver by induction of IL-12 and IL-18 production from Kupffer cells. J Immunol. 1997;159(1):97–106. Fiore G, Galetta V, Piazzolla G, Angarano I, Jirillo E, Schiraldi O, et al. CD45RA and CD45RO isoform expression on intrahepatic T-lymphocytes in chronic hepatitis C. Microbios. 1997;92(371):73–82. Gossmann J, Lohler J, Utermohlen O, Lehmann-Grube F. Murine hepatitis caused by lymphocytic choriomeningitis virus. II. Cells involved in pathogenesis. Lab Invest. 1995;72(5):559–70. Guebre-Xabier M, Yang S, Lin HZ, Schwenk R, Krzych U, Diehl AM. Altered hepatic lymphocyte subpopulations in obesity-related murine fatty livers: potential mechanism for sensitization to liver damage. Hepatology. 2000;31(3):633–40. Sato Y, Murase K, Kato J, Kobune M, Sato T, Kawano Y, et al. Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone. Nat Biotechnol. 2008;26(4):431–42. Friedman SL. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J Biol Chem. 2000;275(4):2247–50. Dunn MA, Lok ASF, Negro F, Schilsky ML, Tavill AS, Caldwell SH, et al. Schiff's diseases of the liver, 11th ed.; Schiff ER, Maddrey WC, Sorrell MF, editors. Oxford: Wiley; 2012. Tomita K, Tamiya G, Ando S, Ohsumi K, Chiyo T, Mizutani A, et al. Tumour necrosis factor α signalling through activation of Kupffer cells plays an essential role in liver fibrosis of non-alcoholic steatohepatitis in mice. Gut. 2006;55(3):415–24. Torchilin VP, Omelyanenko VG, Papisov MI, Bogdanov Jr AA, Trubetskoy VS, Herron JN, et al. Poly(ethylene glycol) on the liposome surface: on the mechanism of polymer-coated liposome longevity. Biochimica et Biophysica Acta (BBA) - Biomembranes. 1994;1195(1):11–20. Lee H, de Vries AH, Marrink SJ, Pastor RW. A coarse-grained model for polyethylene oxide and polyethylene glycol: conformation and hydrodynamics. J Phys Chem B. 2009;113(40):13186–94. Li SD, Huang L. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol Pharm. 2006;3(5):579–88. Li J, Chen YC, Tseng YC, Mozumdar S, Huang L. Biodegradable calcium phosphate nanoparticle with lipid coating for systemic siRNA delivery. J Contr Release. 2010;142(3):416–21. Li SD, Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol Pharm. 2008;5(4):496–504. Liu Y.; Nieh M.P.; Heller W.; Hu Y.; Huang L. Nanoparticle delivery to hepatocytes requires a compact, non-brush conformation of the polyethylene glycol coating. Drug Carriers in Medicine and Biology, Gordon Research Conferences: Waterville Valley, NH; 2012 Knop K, Hoogenboom R, Fischer D, Schubert US. Poly(ethylene glycol) in drug delivery: pros and cons as well as potential alternatives. Angew Chem. 2010;49(36):6288–308. Shiraishi K, Hamano M, Ma H, Kawano K, Maitani Y, Aoshi T, et al. Hydrophobic blocks of PEG-conjugates play a significant role in the accelerated blood clearance (ABC) phenomenon. J Contr Release. 2013;165(3):183–90. Romberg B, Oussoren C, Snel CJ, Carstens MG, Hennink WE, Storm G. Pharmacokinetics of poly(hydroxyethyl-l-asparagine)-coated liposomes is superior over that of PEG-coated liposomes at low lipid dose and upon repeated administration. Biochim Biophys Acta. 2007;1768(3):737–43. Cho CS, Kobayashi A, Takei R, Ishihara T, Maruyama A, Akaike T. Receptor-mediated cell modulator delivery to hepatocyte using nanoparticles coated with carbohydrate-carrying polymers. Biomaterials. 2001;22(1):45–51. Zhang XQ, Wang XL, Zhang PC, Liu ZL, Zhuo RX, Mao HQ, et al. Galactosylated ternary DNA/polyphosphoramidate nanoparticles mediate high gene transfection efficiency in hepatocytes. J Contr Release. 2005;102(3):749–63. Kim TH, Park IK, Nah JW, Choi YJ, Cho CS. Galactosylated chitosan/DNA nanoparticles prepared using water-soluble chitosan as a gene carrier. Biomaterials. 2004;25(17):3783–92. Rozema DB, Lewis DL, Wakefield DH, Wong SC, Klein JJ, Roesch PL, et al. Dynamic PolyConjugates for targeted in vivo delivery of siRNA to hepatocytes. Proc Natl Acad Sci U S A. 2007;104(32):12982–7. Rensen PC, Herijgers N, Netscher MH, Meskers SC, van Eck M, van Berkel TJ. Particle size determines the specificity of apolipoprotein E-containing triglyceride-rich emulsions for the LDL receptor versus hepatic remnant receptor in vivo. Journal of lipid research. 1997;38(6):1070–84. Choi YH, Liu F, Park JS, Kim SW. Lactose-poly(ethylene glycol)-grafted poly-L-lysine as hepatoma cell-targeted gene carrier. Bioconjugate chemistry. 1998;9(6):708–18. Rensen PC, Sliedregt LA, Ferns M, Kieviet E, van Rossenberg SM, van Leeuwen SH, et al. Determination of the upper size limit for uptake and processing of ligands by the asialoglycoprotein receptor on hepatocytes in vitro and in vivo. J Biol Chem. 2001;276(40):37577–84. Lee YC, Townsend RR, Hardy MR, Lonngren J, Arnarp J, Haraldsson M, et al. Binding of synthetic oligosaccharides to the hepatic Gal/GalNAc lectin. Dependence on fine structural features. J Biol Chem. 1983;258(1):199–202. Thomas G, Loriette C, Pepin D, Chambaz J, Bereziat G. Selective channelling of arachidonic and linoleic acids into glycerolipids of rat hepatocytes in primary culture. Biochem J. 1988;256(2):641–7. Pandey NR, Renwick J, Misquith A, Sokoll K, Sparks DL. Linoleic acid-enriched phospholipids act through peroxisome proliferator-activated receptors alpha to stimulate hepatic apolipoprotein A-I secretion. Biochemistry. 2008;47(6):1579–87. Cheong SJ, Lee CM, Kim SL, Jeong HJ, Kim EM, Park EH, et al. Superparamagnetic iron oxide nanoparticles-loaded chitosan-linoleic acid nanoparticles as an effective hepatocyte-targeted gene delivery system. Int J Pharm. 2009;372(1–2):169–76. Wang B, He C, Tang C, Yin C. Effects of hydrophobic and hydrophilic modifications on gene delivery of amphiphilic chitosan based nanocarriers. Biomaterials. 2011;32(20):4630–8. 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. 2010;18(7):1357–64. Rahman YE, Cerny EA, Patel KR, Lau EH, Wright BJ. Differential uptake of liposomes varying in size and lipid composition by parenchymal and kupffer cells of mouse liver. Life Sci. 1982;31(19):2061–71. Popielarski SR, Hu-Lieskovan S, French SW, Triche TJ, Davis ME. A nanoparticle-based model delivery system to guide the rational design of gene delivery to the liver. 2. In vitro and in vivo uptake results. Bioconjug Chem. 2005;16(5):1071–80. Yue Y, Jin F, Deng R, Cai J, Dai Z, Lin MCM, et al. Revisit complexation between DNA and polyethylenimine—effect of length of free polycationic chains on gene transfection. J Control Release. 2011;152(1):143–51. Xu Y, Szoka Jr FC. Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry. 1996;35(18):5616–23. Ross R, Harker L. Hyperlipidemia and atherosclerosis. Science. 1976;193(4258):1094–100. Lacoste L, Lam JY, Hung J, Letchacovski G, Solymoss CB, Waters D. Hyperlipidemia and coronary disease. Correction of the increased thrombogenic potential with cholesterol reduction. Circulation. 1995;92(11):3172–7. Rashid S, Curtis DE, Garuti R, Anderson NN, Bashmakov Y, Ho YK, et al. Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc Natl Acad Sci U S A. 2005;102(15):5374–9. 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. 2008;105(33):11915–20. Lee A-H, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science. 2008;320(5882):1492–6. Love KT, Mahon KP, Levins CG, Whitehead KA, Querbes W, Dorkin JR, et al. Lipid-like materials for low-dose, in vivo gene silencing. Proc Natl Acad Sci U S A. 2010;107(5):1864–9. Edvardsson U, Ljungberg A, Linden D, William-Olsson L, Peilot-Sjogren H, Ahnmark A, et al. PPARalpha activation increases triglyceride mass and adipose differentiation-related protein in hepatocytes. J Lipid Res. 2006;47(2):329–40. Stuart MJ, Gerrard JM, White JG. Effect of cholesterol on production of thromboxane b2 by platelets in vitro. N Engl J Med. 1980;302(1):6–10. Baigude H, McCarroll J, Yang CS, Swain PM, Rana TM. Design and creation of new nanomaterials for therapeutic RNAi. ACS Chem Biol. 2007;2(4):237–41. Zimmermann TS, Lee AC, Akinc A, Bramlage B, Bumcrot D, Fedoruk MN, et al. RNAi-mediated gene silencing in non-human primates. Nature. 2006;441(7089):111–4. Akinc A, Zumbuehl A, Goldberg M, Leshchiner ES, Busini V, Hossain N, et al. A combinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat Biotechnol. 2008;26(5):561–9. Wong SC, Klein JJ, Hamilton HL, Chu Q, Frey CL, Trubetskoy VS, et al. Co-injection of a targeted, reversibly masked endosomolytic polymer dramatically improves the efficacy of cholesterol-conjugated small interfering RNAs in vivo. Nucleic Acid Ther. 2012;22(6):380–90. Wooddell CI, Rozema DB, Hossbach M, John M, Hamilton HL, Chu Q et al. Hepatocyte-targeted RNAi therapeutics for the treatment of chronic hepatitis b virus infection. Mol Ther. 2013; 21(5):973–85. Semple SC, Akinc A, Chen J, Sandhu AP, Mui BL, Cho CK, et al. Rational design of cationic lipids for siRNA delivery. Nat Biotechnol. 2010;28(2):172–6. Marzano A, Angelucci E, Andreone P, Brunetto M, Bruno R, Burra P, et al. Prophylaxis and treatment of hepatitis B in immunocompromised patients. Dig Liver Dis. 2007;39(5):397–408. Nunez M, Soriano V. Management of patients co-infected with hepatitis B virus and HIV. Lancet Infect Dis. 2005;5(6):374–82. Shlomai A, Shaul Y. Inhibition of hepatitis B virus expression and replication by RNA interference. Hepatology. 2003;37(4):764–70. Morrissey DV, Lockridge JA, Shaw L, Blanchard K, Jensen K, Breen W, et al. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat Biotechnol. 2005;23(8):1002–7. Epiphanio S, Mikolajczak SA, Goncalves LA, Pamplona A, Portugal S, Albuquerque S, et al. Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection. Cell Host Microbe. 2008;3(5):331–8. Musso G, Gambino R, Cassader M. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Prog Lipid Res. 2009;48(1):1–26. Abumrad N, Harmon C, Ibrahimi A. Membrane transport of long-chain fatty acids: evidence for a facilitated process. J Lipid Res. 1998;39(12):2309–18. Van Nieuwenhoven FA, Verstijnen CP, Abumrad NA, Willemsen PH, Van Eys GJ, Van der Vusse GJ, et al. Putative membrane fatty acid translocase and cytoplasmic fatty acid-binding protein are co-expressed in rat heart and skeletal muscles. Biochem Biophys Res Commun. 1995;207(2):747–52. Degrace P, Moindrot B, Mohamed I, Gresti J, Du ZY, Chardigny JM, et al. Upregulation of liver VLDL receptor and FAT/CD36 expression in LDLR−/− apoB100/100 mice fed trans-10, cis-12 conjugated linoleic acid. J Lipid Res. 2006;47(12):2647–55. Lee S, Yang SC, Kao C-Y, Pierce RH, Murthy N. Solid polymeric microparticles enhance the delivery of siRNA to macrophages in vivo. Nucleic Acids Res. 2009;37(22):e145. Vaishnaw AK, Gollob J, Gamba-Vitalo C, Hutabarat R, Sah D, Meyers R, et al. A status report on RNAi therapeutics. Silence. 2010;1(1):14. doi:10.1186/1758-907X-1-14. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806–11.