Pieter Cullis’ quest for a lipid-based, fusogenic delivery system for nucleic acid therapeutics: success with siRNA so what about mRNA?

References

• Coelho T , Adams D , Silva A , et al . Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N Engl J Med 2013;369:819–29.
   PubMed Web of Science ®Google Scholar
• Butler JS , Chan A , Costelha S , et al . Preclinical evaluation of RNAi as a treatment for transthyretin-mediated amyloidosis. Amyloid 2016;23:1–10.
   Web of Science ®Google Scholar
• Cullis PR , Hope MJ. Effects of fusogenic agent on membrane structure of erythrocyte ghosts and the mechanism of membrane fusion. Nature 1978;271:672–4.
   PubMed Web of Science ®Google Scholar
• Cullis PR , De Kruijff B , Hope MJ , et al . Phospholipids and membrane transport. Can J Biochem 1980;58:1091–100.
   PubMedGoogle Scholar
• Verkleij AJ , Van Echteld CJ , Gerritsen WJ , et al . The lipidic particle as an intermediate structure in membrane fusion processes and bilayer to hexagonal HII transitions. Biochim Biophys Acta 1980;600:620–4.
   PubMed Web of Science ®Google Scholar
• Hope MJ , Cullis PR. The role of nonbilayer lipid structures in the fusion of human erythrocytes induced by lipid fusogens. Biochim Biophys Acta 1981;640:82–90.
   PubMed Web of Science ®Google Scholar
• Tilcock CP , Cullis PR. The polymorphic phase behavior of mixed phosphatidylserine-phosphatidylethanolamine model systems as detected by 31P-NMR. Biochim Biophys Acta 1981;641:189–201.
   PubMed Web of Science ®Google Scholar
• Bally MB , Tilcock CP , Hope MJ , Cullis PR. Polymorphism of phosphatidylethanolamine-phosphatidylserine model systems: influence of cholesterol and Mg2+ on Ca2+-triggered bilayer to hexagonal (HII) transitions. Can J Biochem Cell Biol 1983;61:346–52.
   PubMedGoogle Scholar
• Verkleij AJ , Leunissen-Bijvelt J , De Kruijff B , et al . Non-bilayer structures in membrane fusion. Ciba Found Symp 1984;103: 45–59.
   PubMedGoogle Scholar
• Cullis PR , De Kruijff B , Verkleij AJ , Hope MJ. Lipid polymorphism and membrane fusion. Biochem Soc Trans 1986a;14:242–5.
   PubMed Web of Science ®Google Scholar
• Cullis PR , Hope MJ , Tilcock CP. Lipid polymorphism and the roles of lipids in membranes. Chem Phys Lipids 1986b;40:127–44.
   PubMed Web of Science ®Google Scholar
• Hope MJ , Walker DC , Cullis PR. Ca2+ and pH induced fusion of small unilamellar vesicles consisting of phosphatidylethanolamine and negatively charged phospholipids: a freeze fracture study. Biochem Biophys Res Commun 1983;110:15–22.
   PubMed Web of Science ®Google Scholar
• Hope MJ , Bally MB , Webb G , Cullis PR. Production of large unilamellar vesicles by a rapid extrusion procedure: characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim Biophys Acta 1985;812:55–65.
   PubMed Web of Science ®Google Scholar
• Olson F , Hunt CA , Szoka FC , et al . Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. Biochim Biophys Acta 1979;557:9–23.
   PubMed Web of Science ®Google Scholar
• Szoka F , Olson F , Heath T , et al . Preparation of unilamellar liposomes of intermediate size (0.1-0.2 mumol) by a combination of reverse phase evaporation and extrusion through polycarbonate membranes. Biochim Biophys Acta 1980;601:559–71.
   PubMed Web of Science ®Google Scholar
• Mayer LD , Hope MJ , Cullis PR. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim Biophys Acta 1986b;858:161–8.
   PubMed Web of Science ®Google Scholar
• Mayer LD , Bally MB , Hope MJ , Cullis PR. Uptake of antineoplastic agents into large unilamellar vesicles in response to a membrane potential. Biochim Biophys Acta 1985a;816:294–302.
   PubMed Web of Science ®Google Scholar
• Mayer LD , Bally MB , Hope MJ , Cullis PR. Uptake of dibucaine into large unilamellar vesicles in response to a membrane potential. J Biol Chem 1985b;260:802–8.
   PubMed Web of Science ®Google Scholar
• Mayer LD , Bally MB , Hope MJ , Cullis PR. Techniques for encapsulating bioactive agents into liposomes. Chem Phys Lipids 1986a;40: 333–45.
   PubMed Web of Science ®Google Scholar
• Madden TD , Harrigan PR , Tai LC , et al . The accumulation of drugs within large unilamellar vesicles exhibiting a proton gradient: a survey. Chem Phys Lipids 1990;53:37–46.
   PubMed Web of Science ®Google Scholar
• Allen TM , Cullis PR. Liposomal drug delivery systems: from concept to clinical applications . Adv Drug Deli. Rev 2013;65:36–48.
   PubMed Web of Science ®Google Scholar
• Waterhouse DN , Madden TD , Cullis PR , et al . Preparation, characterization, and biological analysis of liposomal formulations of vincristine. Methods Enzymol 2005;391:40–57.
   PubMed Web of Science ®Google Scholar
• Felgner PL , Gadek TR , Holm M , et al . Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure . Proc Natl Acad Sci USA 1987;84:7413–17.
   PubMed Web of Science ®Google Scholar
• Maurer N , Mori A , Palmer L , et al . Lipid-based systems for the intracellular delivery of genetic drugs. Mol Membr Biol 1999;16:129–40.
   PubMed Web of Science ®Google Scholar
• Wheeler JJ , Palmer L , Ossanlou M , et al . Stabilized plasmid-lipid particles: construction and characterization. Gene Ther 1999;6:271–81.
   PubMed Web of Science ®Google Scholar
• Bailey AL , Cullis PR. Modulation of membrane fusion by asymmetric transbilayer distributions of amino lipids. Biochemistry 1994;33:12573–80.
   PubMed Web of Science ®Google Scholar
• Bailey AL , Cullis PR. Membrane fusion with cationic liposomes: effects of target membrane lipid composition. Biochemistry 1997;36:1628–34.
   PubMed Web of Science ®Google Scholar
• Behr JP . Gene transfer with synthetic cationic amphiphiles: prospects for gene therapy . Bioconjug Chem 1994;5:382–9.
   PubMed Web of Science ®Google Scholar
• Hafez IM , Cullis PR. Roles of lipid polymorphism in intracellular delivery . Adv Drug Deliv Rev 2001;47:139–48.
   PubMed Web of Science ®Google Scholar
• Hafez IM , Maurer N , Cullis PR. On the mechanism whereby cationic lipids promote intracellular delivery of polynucleic acids. Gene Ther 2001;8:1188–96.
   PubMed Web of Science ®Google Scholar
• Akinc A , Goldberg M , Qin J , et al . Development of lipidoid-siRNA formulations for systemic delivery to the liver. Mol Ther 2009;17:872–9.
   PubMed Web of Science ®Google Scholar
• Semple SC , Akinc A , Chen J , et al . Rational design of cationic lipids for siRNA delivery . Nat. Biotechnol 2010;28:172–6.
   PubMed Web of Science ®Google Scholar
• Heyes J , Palmer L , Bremner K , Maclachlan I. Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids. J Control Release 2005;107:276–87.
   PubMed Web of Science ®Google Scholar
• Jayaraman M , Ansell SM , Mui BL , et al . Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo . Angew Chem Int Ed Engl 2012;51:8529–33.
   PubMed Web of Science ®Google Scholar
• Weissman D , Kariko K. mRNA: fulfilling the promise of gene therapy. Mol Ther 2015;23:1416–7.
   PubMed Web of Science ®Google Scholar
• Phua KK. Towards targeted delivery systems: ligand conjugation strategies for mRNA nanoparticle tumor vaccines. J Immunol Res 2015;2015:680620.
   PubMed Web of Science ®Google Scholar
• Weissman D. mRNA transcript therapy. Expert Rev Vaccines 2015;14:265–81.
   PubMed Web of Science ®Google Scholar
• Kariko K , Muramatsu H , Ludwig J , Weissman D. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA. Nucleic Acids Res 2011;39:e142.
   PubMed Web of Science ®Google Scholar
• Kormann MS , Hasenpusch G , Aneja MK , et al . Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 2011;29:154–7.
   PubMed Web of Science ®Google Scholar
• Antony JS , Dewerth A , Haque A , et al . Modified mRNA as a new therapeutic option for pediatric respiratory diseases and hemoglobinopathies. Mol Cell Pediatr 2015;2:11
   PubMedGoogle Scholar
• Warren L , Manos PD , Ahfeldt T , et al . Highly efficient reprograming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7:618–30.
   PubMed Web of Science ®Google Scholar
• Zangi L , Lui KO , Von Gise A , et al . Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol 2013;31:898–907.
   PubMed Web of Science ®Google Scholar
• Li C , Qi R , Singleterry R , et al . Simultaneous gene editing by injection of mRNAs encoding transcription activator-like effector nucleases into mouse zygotes. Mol Cell Biol 2014;34:1649–58.
   PubMed Web of Science ®Google Scholar
• Mahiny AJ , Dewerth A , Mays LE , et al . In vivo genome editing using nuclease-encoding mRNA corrects SP-B deficiency. Nat Biotechnol 2015;33:584–6.
   PubMed Web of Science ®Google Scholar
• Mcivor RS. Therapeutic delivery of mRNA: the medium is the message. Mol Ther 2011;19:822–3.
   PubMed Web of Science ®Google Scholar
• Boczkowski D , Nair SK , Snyder D , Gilboa E. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 1996;184:465–72.
   PubMed Web of Science ®Google Scholar
• Van Lint S , Heirman C , Thielemans K , Breckpot K. mRNA: From a chemical blueprint for protein production to an off-the-shelf therapeutic. Hum Vaccin Immunother 2013;9:265–74.
   PubMed Web of Science ®Google Scholar
• Bowie AG , Unterholzner L . Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 2008;8:911–22.
   PubMed Web of Science ®Google Scholar
• Kariko K , Weissman D. Naturally occurring nucleoside modifications suppress the immunostimulatory activity of RNA: implication for therapeutic RNA development. Curr Opin Drug Discov Devel 2007;10:523–32.
   PubMedGoogle Scholar
• Anderson BR , Muramatsu H , Nallagatla SR , et al . Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Res 2010;38:5884–92.
   PubMed Web of Science ®Google Scholar
• Thess A , Grund S , Mui BL , et al . Sequence-engineered mRNA Without Chemical Nucleoside Modifications Enables an Effective Protein Therapy in Large Animals. Mol Ther 2015;23:1456–64.
   PubMed Web of Science ®Google Scholar
• Lorenz C , Fotin-Mleczek M , Roth G , et al . Protein expression from exogenous mRNA: uptake by receptor-mediated endocytosis and trafficking via the lysosomal pathway. RNA Biol 2011;8:627–36.
   PubMed Web of Science ®Google Scholar
• Phua KK , Leong KW , Nair SK. 2013; Transfection efficiency and transgene expression kinetics of mRNA delivered in naked and nanoparticle format. J Control Release 166: 227–33.
   PubMed Web of Science ®Google Scholar
• Sorrentino S , Naddeo M , Russo A , D'alessio G. Degradation of double-stranded RNA by human pancreatic ribonuclease: crucial role of noncatalytic basic amino acid residues. Biochemistry 2003;42:10182–90.
   PubMed Web of Science ®Google Scholar
• Kanasty R , Dorkin JR , Vegas A , Anderson D. Delivery materials for siRNA therapeutics. Nat Mater 2013;12:967–77.
   PubMed Web of Science ®Google Scholar
• Nair JK , Willoughby JL , Chan A , et al . Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J Am Chem Soc 2014;136:16958–61.
   PubMed Web of Science ®Google Scholar
• Pardi N , Tuyishime S , Muramatsu H , et al . Expression kinetics of nucleoside-modified mRNA delivered in lipid nanoparticles to mice by various routes. J Control Release 2015;217:345–51.
   PubMed Web of Science ®Google Scholar