Structure-based design of dendritic peptide bolaamphiphiles for siRNA delivery

ACS Central Science

Volumn 1, Issue 6, 2015, Pages 303-312

  Zeng, Hanxiang ^a   Johnson, Mark E ^a   Oldenhuis, Nathan J ^a   Tiambeng, Timothy N ^a   Guan, Zhibin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVITY; CELL CULTURE; EFFICIENCY; LIPOSOMES; NUCLEIC ACIDS; PEPTIDES; VECTORS;

BIOMATERIAL APPLICATION; LIPOFECTAMINE RNAIMAX; NUCLEIC ACID DELIVERIES; SELF ASSEMBLED NANOSTRUCTURES; SMALL INTERFERING RNA (SIRNA); STRUCTURE PROPERTY RELATIONSHIPS; STRUCTURE-BASED DESIGNS; TRANSFECTION EFFICIENCY;

RNA;

EID: 84949742176     PISSN: 23747943     EISSN: 23747951     Source Type: Journal    
DOI: 10.1021/acscentsci.5b00233     Document Type: Article

References (56)

1. Sahin, Ö.; Löbke, C.; Korf, U.; Appelhans, H.; Sültmann, H.; Poustka, A.; Wiemann, S.; Arlt, D. Combinatorial RNAi for quantitative protein network analysis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 6579-6584.
2. Dietzl, G.; Chen, D.; Schnorrer, F.; Su, K.-C.; Barinova, Y.; Fellner, M.; Gasser, B.; Kinsey, K.; Oppel, S.; Scheiblauer, S.; Couto, A.; Marra, V.; Keleman, K.; Dickson, B. J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448, 151-156.
3. Chen, T.; Heller, E.; Beronja, S.; Oshimori, N.; Stokes, N.; Fuchs, E. An RNA interference screen uncovers a new molecule in stem cell self-renewal and long-term regeneration. Nature 2012, 485, 104-108.
4. Castanotto, D.; Rossi, J. J. The promises and pitfalls of RNAinterference- based therapeutics. Nature 2009, 457, 426-433.
5. de Fougerolles, A.; Vornlocher, H.-P.; Maraganore, J.; Lieberman, J. Interfering with disease: A progress report on siRNA-based therapeutics. Nat. Rev. Drug Discovery 2007, 6, 443-453.
6. Whitehead, K. A.; Langer, R.; Anderson, D. G. Knocking down barriers: Advances in siRNA delivery. Nat. Rev. Drug Discovery 2009, 8, 129-138.
7. Mitragotri, S.; Burke, P. A.; Langer, R. Overcoming the challenges in administering biopharmaceuticals: Formulation and delivery strategies. Nat. Rev. Drug Discovery 2014, 13, 655-672.
8. Kanasty, R.; Dorkin, J. R.; Vegas, A.; Anderson, D. Delivery materials for siRNA therapeutics. Nat. Mater. 2013, 12, 967-977.
9. Malone, R. W.; Felgner, P. L.; Verma, I. M. Cationic liposomemediated RNA transfection. Proc. Natl. Acad. Sci. U. S. A. 1989, 86, 6077-6081.
10. Love, K. T.; Mahon, K. P.; Levins, C. G.; Whitehead, K. A.; Querbes, W.; Dorkin, J. R.; Qin, J.; Cantley, W.; Qin, L. L.; Racie, T.; Frank-Kamenetsky, M.; Yip, K. N.; Alvarez, R.; Sah, D. W. Y.; de Fougerolles, A.; Fitzgerald, K.; Koteliansky, V.; Akinc, A.; Langer, R.; Anderson, D. G. Lipid-like materials for low-dose, in vivo gene silencing. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 1864-1869.
11. Semple, S. C.; Akinc, A.; Chen, J.; Sandhu, A. P.; Mui, B. L.; Cho, C. K.; Sah, D. W. Y.; Stebbing, D.; Crosley, E. J.; Yaworski, E.; Hafez, I. M.; Dorkin, J. R.; Qin, J.; Lam, K.; Rajeev, K. G.; Wong, K. F.; Jeffs, L. B.; Nechev, L.; Eisenhardt, M. L.; Jayaraman, M.; Kazem, M.; Maier, M. A.; Srinivasulu, M.; Weinstein, M. J.; Chen, Q.; Alvarez, R.; Barros, S. A.; De, S.; Klimuk, S. K.; Borland, T.; Kosovrasti, V.; Cantley, W. L.; Tam, Y. K.; Manoharan, M.; Ciufolini, M. A.; Tracy, M. A.; de Fougerolles, A.; MacLachlan, I.; Cullis, P. R.; Madden, T. D.; Hope, M. J. Rational design of cationic lipids for siRNA delivery. Nat. Biotechnol. 2010, 28, 172-176.
12. Crombez, L.; Aldrian-Herrada, G.; Konate, K.; Nguyen, Q. N.; McMaster, G. K.; Brasseur, R.; Heitz, F.; Divita, G. A New Potent Secondary Amphipathic Cell-penetrating Peptide for siRNA Delivery Into Mammalian Cells. Mol. Ther. 2009, 17, 95-103.
13. Eguchi, A.; Dowdy, S. F. siRNA delivery using peptide transduction domains. Trends Pharmacol. Sci. 2009, 30, 341-345.
14. Won, Y.-W.; Adhikary, P. P.; Lim, K. S.; Kim, H. J.; Kim, J. K.; Kim, Y.-H. Oligopeptide complex for targeted non-viral gene delivery to adipocytes. Nat. Mater. 2014, 13, 1157-1164.
15. Kumar, P.; Wu, H.; McBride, J. L.; Jung, K.-E.; Hee Kim, M.; Davidson, B. L.; Kyung Lee, S.; Shankar, P.; Manjunath, N. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007, 448, 39-43.
16. Davis, M. E.; Zuckerman, J. E.; Choi, C. H. J.; Seligson, D.; Tolcher, A.; Alabi, C. A.; Yen, Y.; Heidel, J. D.; Ribas, A. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 2010, 464, 1067-1070.
17. Rozema, D. B.; Lewis, D. L.; Wakefield, D. H.; Wong, S. C.; Klein, J. J.; Roesch, P. L.; Bertin, S. L.; Reppen, T. W.; Chu, Q.; Blokhin, A. V.; Hagstrom, J. E.; Wolff, J. A. Dynamic PolyConjugates for targeted in vivo delivery of siRNA to hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 12982-12987.
18. Tschiche, A.; Malhotra, S.; Haag, R. Nonviral gene delivery with dendritic self-assembling architectures. Nanomedicine 2014, 9, 667- 693.
19. Kulkarni, A.; DeFrees, K.; Hyun, S.-H.; Thompson, D. H. Pendant Polymer: Amino-ß-Cyclodextrin: SiRNA Guest: Host Nanoparticles as Efficient Vectors for Gene Silencing. J. Am. Chem. Soc. 2012, 134, 7596-7599.
20. Wu, J.; Huang, W.; He, Z. Dendrimers as carriers for siRNA delivery and gene silencing: A review. Sci. World J. [Online] 2013, 630654. 10.1155/2013/630654
21. Yu, T.; Liu, X.; Bolcato-Bellemin, A.-L.; Wang, Y.; Liu, C.; Erbacher, P.; Qu, F.; Rocchi, P.; Behr, J.-P.; Peng, L. An Amphiphilic Dendrimer for Effective Delivery of Small Interfering RNA and Gene Silencing In Vitro and In Vivo. Angew. Chem., Int. Ed. 2012, 51, 8478- 8484.
22. Giljohann, D. A.; Seferos, D. S.; Prigodich, A. E.; Patel, P. C.; Mirkin, C. A. Gene Regulation with Polyvalent siRNA-Nanoparticle Conjugates. J. Am. Chem. Soc. 2009, 131, 2072-2073.
23. Kim, S. T.; Chompoosor, A.; Yeh, Y.-C.; Agasti, S. S.; Solfiell, D. J.; Rotello, V. M. Dendronized Gold Nanoparticles for siRNA Delivery. Small 2012, 8, 3253-3256.
24. Dokka, S.; Toledo, D.; Shi, X.; Castranova, V.; Rojanasakul, Y. Oxygen Radical-Mediated Pulmonary Toxicity Induced by Some Cationic Liposomes. Pharm. Res. 2000, 17, 521-525.
25. Landesman-Milo, D.; Peer, D. Toxicity profiling of several common RNAi-based nanomedicines: A comparative study. Drug Delivery Transl. Res. 2014, 4, 96-103.
26. Lv, H. T.; Zhang, S. B.; Wang, B.; Cui, S. H.; Yan, J. Toxicity of cationic lipids and cationic polymers in gene delivery. J. Controlled Release 2006, 114, 100-109.
27. Tabernero, J.; Shapiro, G. I.; LoRusso, P. M.; Cervantes, A.; Schwartz, G. K.; Weiss, G. J.; Paz-Ares, L.; Cho, D. C.; Infante, J. R.; Alsina, M.; Gounder, M. M.; Falzone, R.; Harrop, J.; White, A. C. S.; Toudjarska, I.; Bumcrot, D.; Meyers, R. E.; Hinkle, G.; Svrzikapa, N.; Hutabarat, R. M.; Clausen, V. A.; Cehelsky, J.; Nochur, S. V.; Gamba- Vitalo, C.; Vaishnaw, A. K.; Sah, D. W. Y.; Gollob, J. A.; Burris, H. A. First-in-Humans Trial of an RNA Interference Therapeutic Targeting VEGF and KSP in Cancer Patients with Liver Involvement. Cancer Discovery 2013, 3, 406-417.
28. Wong, S. C.; Klein, J. J.; Hamilton, H. L.; Chu, Q.; Frey, C. L.; Trubetskoy, V. S.; Hegge, J.; Wakefield, D.; Rozema, D. B.; Lewis, D. L. 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, 380-390.
29. Gilleron, J.; Querbes, W.; Zeigerer, A.; Borodovsky, A.; Marsico, G.; Schubert, U.; Manygoats, K.; Seifert, S.; Andree, C.; Stoter, M.; Epstein-Barash, H.; Zhang, L.; Koteliansky, V.; Fitzgerald, K.; Fava, E.; Bickle, M.; Kalaidzidis, Y.; Akinc, A.; Maier, M.; Zerial, M. Imagebased analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol. 2013, 31, 638-646.
30. Shete, H. K.; Prabhu, R. H.; Patravale, V. B. Endosomal Escape: A Bottleneck in Intracellular Delivery. J. Nanosci. Nanotechnol. 2014, 14, 460-474.
31. Hafez, I. M.; Maurer, N.; Cullis, P. R. On the mechanism whereby cationic lipids promote intracellular delivery of polynucleic acids. Gene Ther. 2001, 8, 1188-1196.
32. Knudsen, K. B.; Northeved, H.; Kumar EK, P.; Permin, A.; Gjetting, T.; Andresen, T. L.; Larsen, S.; Wegener, K. M.; Lykkesfeldt, J.; Jantzen, K.; Loft, S.; Moller, P.; Roursgaard, M. In vivo toxicity of cationic micelles and liposomes. Nanomedicine 2015, 11, 467-477.
33. Hunter, A. C. Molecular hurdles in polyfectin design and mechanistic background to polycation induced cytotoxicity. Adv. Drug Delivery Rev. 2006, 58, 1523-1531.
34. Dong, Y. Z.; Love, K. T.; Dorkin, J. R.; Sirirungruang, S.; Zhang, Y. L.; Chen, D. L.; Bogorad, R. L.; Yin, H.; Chen, Y.; Vegas, A. J.; Alabi, C. A.; Sahay, G.; Olejnik, K. T.; Wang, W. H.; Schroeder, A.; Lytton-Jean, A. K. R.; Siegwart, D. J.; Akinc, A.; Barnes, C.; Barros, S. A.; Carioto, M.; Fitzgerald, K.; Hettinger, J.; Kumar, V.; Novobrantseva, T. I.; Qin, J. N.; Querbes, W.; Koteliansky, V.; Langer, R.; Anderson, D. G. Lipopeptide nanoparticles for potent and selective siRNA delivery in rodents and nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 3955-3960.
35. Nuraje, N.; Bai, H. Y.; Su, K. Bolaamphiphilic molecules: Assembly and applications. Prog. Polym. Sci. 2013, 38, 302-343.
36. Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 2007, 5, 316-323.
37. Jain, N.; Goldschmidt, V.; Oncul, S.; Arntz, Y.; Duportail, G.; Mely, Y.; Klymchenko, A. S. Lactose-ornithine bolaamphiphiles for efficient gene delivery in vitro. Int. J. Pharm. 2012, 423, 392-400.
38. Khan, M.; Ang, C. Y.; Wiradharma, N.; Yong, L. K.; Liu, S. Q.; Liu, L. H.; Gao, S. J.; Yang, Y. Y. Diaminododecane-based cationic bolaamphiphile as a non-viral gene delivery carrier. Biomaterials 2012, 33, 4673-4680.
39. Kim, T., Afonin, K. A., Viard, M., Koyfman, A. Y., Sparks, S., Heldman, E., Grinberg, S., Linder, C., Blumenthal, R. P., Shapiro, B. A. In Silico, In Vitro, and In Vivo Studies Indicate the Potential Use of Bolaamphiphiles for Therapeutic siRNAs Delivery. Mol. Ther.--Nucleic Acids 2013, 2, e80. 10.1038/mtna.2013.5
40. Popov, M.; Abu Hammad, I.; Bachar, T.; Grinberg, S.; Linder, C.; Stepensky, D.; Heldman, E. Delivery of analgesic peptides to the brain by nano-sized bolaamphiphilic vesicles made of monolayer membranes. Eur. J. Pharm. Biopharm. 2013, 85, 381-389.
41. Zeng, H.; Little, H. C.; Tiambeng, T. N.; Williams, G. A.; Guan, Z. Multifunctional Dendronized Peptide Polymer Platform for Safe and Effective siRNA Delivery. J. Am. Chem. Soc. 2013, 135, 4962- 4965.
42. Saito, H.; Shinoda, W.; Mikami, M. Enhanced Hydrophobicity of Fluorinated Lipid Bilayer: A Molecular Dynamics Study. J. Phys. Chem. B 2008, 112, 11305-11309.
43. Dafik, L.; Kalsani, V.; Leung, A. K. L.; Kumar, K. Fluorinated Lipid Constructs Permit Facile Passage of Molecular Cargo into Living Cells. J. Am. Chem. Soc. 2009, 131, 12091-12093.
44. Klein, E.; Leborgne, C.; Ciobanu, M.; Klein, J.; Frisch, B.; Pons, F.; Zuber, G.; Scherman, D.; Kichler, A.; Lebeau, L. Nucleic acid transfer with hemifluorinated polycationic lipids. Biomaterials 2010, 31, 4781-4788.
45. Wang, M., Liu, H., Li, L., Cheng, Y. A fluorinated dendrimer achieves excellent gene transfection efficacy at extremely low nitrogen to phosphorus ratios. Nat. Commun. 2014, 5. 10.1038/ncomms4053
46. Saito, H.; Shinoda, W.; Mikami, M. Fluorination effects on structure and dynamics of phospholipid bilayer: A molecular dynamics study. Chem. Phys. Lett. 2009, 468, 260-263.
47. Son, S.; Namgung, R.; Kim, J.; Singha, K.; Kim, W. J. Bioreducible Polymers for Gene Silencing and Delivery. Acc. Chem. Res. 2012, 45, 1100-1112.
48. Hartgerink, J. D.; Beniash, E.; Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 2001, 294, 1684-1688.
49. Silva, G. A.; Czeisler, C.; Niece, K. L.; Beniash, E.; Harrington, D. A.; Kessler, J. A.; Stupp, S. I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004, 303, 1352-1355.
50. Deshayes, S.; Konate, K.; Rydström, A.; Crombez, L.; Godefroy, C.; Milhiet, P.-E.; Thomas, A.; Brasseur, R.; Aldrian, G.; Heitz, F.; Munoz-Morris, M. A.; Devoisselle, J.-M.; Divita, G. Self-Assembling Peptide-Based Nanoparticles for siRNA Delivery in Primary Cell Lines. Small 2012, 8, 2184-2188.
51. Liu, X. F.; Wang, T. Y.; Liu, M. H. Interfacial Assembly of a Series of Cinnamoyl-Containing Bolaamphiphiles: Spacer-Controlled Packing, Photochemistry, and Odd-Even Effect. Langmuir 2012, 28, 3474-3482.
52. Khalil, I. A.; Kogure, K.; Akita, H.; Harashima, H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol. Rev. 2006, 58, 32-45.
53. Ivanov, A. In Exocytosis and Endocytosis; Ivanov, A., Ed.; Humana Press: 2008; Vol. 440, p 15.
54. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Sizedependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 2004, 377, 159-169.
55. Rehman, Z. u.; Zuhorn, I. S.; Hoekstra, D. How cationic lipids transfer nucleic acids into cells and across cellular membranes: Recent advances. J. Controlled Release 2013, 166, 46-56.
56. Wang, M.; Cheng, Y. The effect of fluorination on the transfection efficacy of surface-engineered dendrimers. Biomaterials 2014, 35, 6603-6613.