Structurally flexible triethanolamine-core poly(amidoamine) dendrimers as effective nanovectors to deliver RNAi-based therapeutics

Biotechnology Advances

Volumn 32, Issue 4, 2014, Pages 844-852

  Liu, Xiaoxuan ^a,b,c,d   Liu, Cheng ^e,f   Catapano, Carlo V ^g   Peng, Ling ^e   Zhou, Jiehua ^h   Rocchi, Palma ^a,b,c,d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT PAOLI CALMETTES   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d CNRS   (France)

^e AIX MARSEILLE UNIVERSITÉ   (France)

^f WUHAN UNIVERSITY   (China)

^g INSTITUTE OF ONCOLOGY RESEARCH   (Switzerland)

^h CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Dendrimer; Gene silencing; Nanovector; RNA interference; RNAi therapeutics

Indexed keywords

DENDRIMERS; ETHANOLAMINES; NUCLEIC ACIDS; TRIETHANOLAMINE;

DELIVERY SYSTEMS; DISEASE MODELS; GENE SILENCING; NANOVECTOR; NUCLEIC ACID DELIVERIES; POLYAMIDOAMINE DENDRIMERS; RNA INTERFERENCE; RNAI THERAPEUTICS;

FUNCTIONAL POLYMERS;

DISEASE TREATMENT; GENETIC ENGINEERING; NANOTECHNOLOGY; POLYMER; RNA;

DENDRIMER; ETHANOLAMINE DERIVATIVE; MICRORNA; PAMAM STARBURST; POLYAMIDOAMINE; POLYAMINE; SMALL INTERFERING RNA; TRIETHANOLAMINE;

ANIMAL; CHEMISTRY; HUMAN; METABOLISM; MOUSE; NANOMEDICINE; NANOTECHNOLOGY; PROCEDURES; RNA INTERFERENCE;

ANIMALS; DENDRIMERS; ETHANOLAMINES; HUMANS; MICE; MICRORNAS; NANOMEDICINE; NANOTECHNOLOGY; POLYAMINES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84899472253     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2013.08.001     Document Type: Article

References (87)

1. Acunzo J., Katsogiannou M., Rocchi P. Small heat shock proteins HSP27 (HspB1), alphaB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. Int J Biochem Cell Biol 2012, 44:1622-1631.
2. Alabi C., Vegas A., Anderson D. Attacking the genome: emerging siRNA nanocarriers from concept to clinic. Curr Opin Pharmacol 2012, 12:427-433.
3. Amarzguioui M., Rossi J.J. Principles of Dicer substrate (d-siRNA) design and function. Methods Mol Biol 2008, 442:3-10.
4. Amarzguioui M., Lundberg P., Cantin E., Hagstrom J., Behlke M.A., Rossi J.J. Rational design and in vitro and in vivo delivery of Dicer substrate siRNA. Nat Protoc 2006, 1:508-517.
5. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
6. Anderson J., Banerjea A., Akkina R. Bispecific short hairpin siRNA constructs targeted to CD4, CXCR4, and CCR5 confer HIV-1 resistance. Oligonucleotides 2003, 13:303-312.
7. Bader A.G., Brown D., Winkler M. The promise of microRNA replacement therapy. Cancer Res 2010, 70:7027-7030.
8. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
9. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
10. Behr J.P. The proton sponge: a trick to enter cells the viruses did not exploit. Chimia 1997, 51:34-36.
11. Berkhout B., ter Brake O. Towards a durable RNAi gene therapy for HIV-AIDS. Expert Opin Biol Ther 2009, 9:161-170.
12. Bolcato-Bellemin A.L., Bonnet M.E., Creusat G., Erbacher P., Behr J.P. Sticky overhangs enhance siRNA-mediated gene silencing. Proc Natl Acad Sci U S A 2007, 104:16050-16055.
13. Bouillon C., Tintaru A., Monnier V., Charles L., Quéléver G., Peng L. Synthesis of poly(amino)ester dendrimers via active cyanomethyl ester intermediates. J Org Chem 2010, 75:8685-8688.
14. Boussif O., Lezoualc'h F., Zanta M., Mergny M., Scherman D., Demeneix B., et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A 1995, 92:7297-7301.
15. Brass A.L., Dykxhoorn D.M., Benita Y., Yan N., Engelman A., Xavier R.J., et al. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319:921-926.
16. Brault L., Gasser C., Bracher F., Huber K., Knapp S., Schwaller J. PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers. Haematologica 2010, 95:1004-1015.
17. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat Rev Cancer 2006, 6:857-866.
18. Castanotto D., Rossi J.J. The promises and pitfalls of RNA-interference-based therapeutics. Nature 2009, 457:426-433.
19. Christ F., Thys W., De Rijck J., Gijsbers R., Albanese A., Arosio D., et al. Transportin-SR2 imports HIV into the nucleus. Curr Biol 2008, 18:1192-1202.
20. Cornford P.A., Dodson A.R., Parsons K.F., Desmond A.D., Woolfenden A., Fordham M., et al. Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res 2000, 60:7099-7105.
21. Couto L.B., High K.A. Viral vector-mediated RNA interference. Curr Opin Pharmacol 2010, 10:534-542.
22. de Fougerolles A., Vornlocher H.P., Maraganore J., Lieberman J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Discov 2007, 6:443-453.
23. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006, 6:259-269.
24. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
25. Fusi A., Procopio G., Della Torre S., Ricotta R., Bianchini G., Salvioni R., et al. Treatment options in hormone-refractory metastatic prostate carcinoma. Tumori 2004, 90:535-546.
26. Gallagher E., Gapstur R. Hormone-refractory prostate cancer: a shifting paradigm in treatment. Clin J Oncol Nurs 2006, 10:233-240.
27. Godlewski J., Newton H.B., Chiocca E.A., Lawler S.E. MicroRNAs and glioblastoma; the stem cell connection. Cell Death Differ 2010, 17:221-228.
28. Guillot-Nieckowski M., Eisler S., Diederich F. Dendritic vectors for gene transfection. New J Chem 2007, 31:1111-1127.
29. Haensler J., Szoka F.C. Polyamidoamine cascade polymers mediate efficient transfection of cells in culture. Bioconjug Chem 1993, 4:372-379.
30. Hannon G.J. RNA interference. Nature 2002, 418:244-251.
31. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004, 5:522-531.
32. Huntzinger E., Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011, 12:99-110.
33. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010, 60:277-300.
34. Kan Z., Jaiswal B.S., Stinson J., Janakiraman V., Bhatt D., Stern H.M., et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010, 466:869-873.
35. Kanasty R.L., Whitehead K.A., Vegas A.J., Anderson D.G. Action and reaction: the biological response to siRNA and its delivery vehicles. Mol Ther 2012, 20:513-524.
36. Kiessling M.K., Oberholzer P.A., Mondal C., Karpova M.B., Zipser M.C., Lin W.M., et al. High-throughput mutation profiling of CTCL samples reveals KRAS and NRAS mutations sensitizing tumors toward inhibition of the RAS/RAF/MEK signaling cascade. Blood 2011, 117:2433-2440.
37. Kim D.H., Behlke M.A., Rose S.D., Chang M.S., Choi S., Rossi J.J. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat Biotechnol 2005, 23:222-226.
38. Lang M.F., Yang S., Zhao C., Sun G., Murai K., Wu X., et al. Genome-wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells. PLoS One 2012, 7:e36248.
39. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
40. Liu X.X., Rocchi P., Qu F.Q., Zheng S.Q., Liang Z.C., Gleave M., et al. PAMAM dendrimers mediate siRNA delivery to target Hsp27 and produce potent antiproliferative effects on prostate cancer cells. ChemMedChem 2009, 4:1302-1310.
41. Liu X., Wu J., Yammine M., Zhou J., Posocco P., Viel S., et al. Structurally flexible triethanolamine core PAMAM dendrimers are effective nanovectors for DNA transfection in vitro and in vivo to the mouse thymus. Bioconjugate Chem 2011, 22:2461-2473.
42. Liu X., Liu C., Laurini E., Posocco P., Pricl S., Qu F., et al. Efficient delivery of sticky siRNA and potent gene silencing in a prostate cancer model using a generation 5 triethanolamine-core PAMAM dendrimer. Mol Pharmaceutics 2012, 9:470-481.
43. Liu X., Rocchi P., Peng L. Dendrimers as non-viral vectors for siRNA delivery. New J Chem 2012, 36:256-263.
44. Liu X., Posocco P., Liu C., Yu T., Wang Q., Dal Col V., et al. Poly(amidoamine) dendrimes as non-viral vectors for the delivery of RNA therapeutics. Dendrimers in biomedical applications 2013, 73-83. RSC publishing. V. Cena, B. Klajnert, L. Peng (Eds.).
45. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007, 114:97-109.
46. Martinez M.A. Progress in the therapeutic applications of siRNAs against HIV-1. Methods Mol Biol 2009, 487:343-368.
47. Mignani S., El Kazzouli S., Bousmina M., Majoral J.P. Expand classical drug administration ways by emerging routes using dendrimer drug delivery systems: a concise overview. Adv Drug Deliv Rev 2013, 10.1016/j.addr.2013.01.001.
48. Nekhai S., Jeang K.T. Transcriptional and post-transcriptional regulation of HIV-1 gene expression: role of cellular factors for Tat and Rev. Future Microbiol 2006, 1:417-426.
49. Novina C.D., Murray M.F., Dykxhoorn D.M., Beresford P.J., Riess J., Lee S.K., et al. siRNA-directed inhibition of HIV-1 infection. Nat Med 2002, 8:681-686.
50. Pasquinelli A.E. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012, 13:271-282.
51. Pham J.W., Pellino J.L., Lee Y.S., Carthew R.W., Sontheimer E.J. A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 2004, 117:83-94.
52. Posocco P., Liu X., Laurini E., Marson D., Chen C., Liu C., et al. Impact of siRNA overhangs for dendrimer-mediated siRNA delivery and gene silencing. Mol Pharm 2013, 10:3262-3273.
53. Quéléver G., Bouillon C., Moreno P., Tintaru A., Charles L., Pricl S., et al. Poly(aminoester) dendrimers: design, synthesis and characterization. Dendrimers in biomedical applications 2013, 167-178. RSC publishing. V. Cena, B. Klajnert, L. Peng (Eds.).
54. Ravina M., Paolicelli P., Seijo B., Sanchez A. Knocking down gene expression with dendritic vectors. Mini Rev Med Chem 2010, 10:73-86.
55. Reebye V., Sætrom P., Mintz P.J., Huang K.W., Swiderski P., Peng L., et al. A novel RNA oligonucleotide improves liver function and inhibits liver carcinogenesis in vivo. Hepatology 2013, [in press]. 10.1002/hep.26669.
56. Rocchi P., So A., Kojima S., Signaevsky M., Beraldi E., Fazli L., et al. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res 2004, 64:6595-6602.
57. Rocchi P., Beraldi E., Ettinger S., Fazli L., Vessella R.L., Nelson C., et al. Increased Hsp27 after androgen ablation facilitates androgen-independent progression in prostate cancer via signal transducers and activators of transcription 3-mediated suppression of apoptosis. Cancer Res 2005, 65:11083-11093.
58. Rocchi P., Jugpal P., So A., Sinneman S., Ettinger S., Fazli L., et al. Small interference RNA targeting heat-shock protein 27 inhibits the growth of prostatic cell lines and induces apoptosis via caspase-3 activation in vitro. BJU Int 2006, 98:1082-1089.
59. Rose S.D., Kim D.H., Amarzguioui M., Heidel J.D., Collingwood M.A., Davis M.E., et al. Functional polarity is introduced by Dicer processing of short substrate RNAs. Nucleic Acids Res 2005, 33:4140-4156.
60. Rossi J.J. RNAi as a treatment for HIV-1 infection. Biotechniques 2006, 25-29. [Suppl.].
61. Rossi J.J., June C.H., Kohn D.B. Genetic therapies against HIV. Nat Biotechnol 2007, 25:1444-1454.
62. Scherer L., Rossi J.J., Weinberg M.S. Progress and prospects: RNA-based therapies for treatment of HIV infection. Gene Ther 2007, 14:1057-1064.
63. Schroeder A., Levins C.G., Cortez C., Langer R., Anderson D.G. Lipid-based nanotherapeutics for siRNA delivery. J Intern Med 2010, 267:9-21.
64. Shen X.C., Zhou J., Liu X., Wu J., Qu F., Zhang Z.L., et al. Importance of size-to-charge ratio in construction of stable and uniform nanoscale RNA/dendrimer complexes. Org Biomol Chem 2007, 5:3674-3681.
65. Shen H., Sun T., Ferrari M. Nanovector delivery of siRNA for cancer therapy. Cancer Gene Ther 2012, 19:367-373.
66. Silber J., Lim D.A., Petritsch C., Persson A.I., Maunakea A.K., Yu M., et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 2008, 6:14.
67. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., et al. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
68. Soifer H.S., Rossi J.J., Saetrom P. MicroRNAs in disease and potential therapeutic applications. Mol Ther 2007, 15:2070-2079.
69. 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, 432:173-178.
70. Stavridi F., Karapanagiotou E.M., Syrigos K.N. Targeted therapeutic approaches for hormone-refractory prostate cancer. Cancer Treat Rev 2010, 36:122-130.
71. Tan S.J., Kiatwuthinon P., Roh Y.H., Kahn J.S., Luo D. Engineering nanocarriers for siRNA delivery. Small 2011, 7:841-856.
72. Tang M.X., Redemann C.T., Szoka F.C. In vitro gene delivery by degraded polyamidoamine dendrimers. Bioconjug Chem 1996, 7:703-714.
73. Tannock I.F., de Wit R., Berry W.R., Horti J., Pluzanska A., Chi K.N., et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004, 351:1502-1512.
74. Tomalia D.A., Baker H., Dewald J., Hall M., Kallos G., Martin S., et al. A new class of polymers: starburst-dendritic macromolecules. Polym J 1985, 17:117-132.
75. Tomalia D.A., Naylor A.M., Goddard W.A. Starburst dendrimers: molecular-level control of size, shape, surface chemistry, topology, and flexibility from atoms to macroscopic matter. Angew Chem Int Ed Engl 1990, 29:138-175.
76. Tomari Y., Matranga C., Haley B., Martinez N., Zamore P.D. A protein sensor for siRNA asymmetry. Science 2004, 306:1377-1380.
77. Tseng Y.C., Mozumdar S., Huang L. Lipid-based systemic delivery of siRNA. Adv Drug Deliv Rev 2009, 61:721-731.
78. Vögtle F., Richardt G., Werner N. Dendrimer chemistry: concepts, syntheses, properties, applications 2009, Wiley-VCH.
79. Wagner E. Polymers for siRNA delivery: inspired by viruses to be targeted, dynamic, and precise. Acc Chem Res 2012, 45:1005-1013.
80. Wang Y., Quéléver G., Peng L. The seemingly trivial yet challenging synthesis of poly(aminoester) dendrimers. Curr Med Chem 2012, 19:5011-5028.
81. Whitehead K.A., Langer R., Anderson D.G. Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 2009, 8:129-138.
82. Wu J., Zhou J., Qu F., Bao P., Zhang Y., Peng L. Polycationic dendrimers interact with RNA molecules: polyamine dendrimers inhibit the catalytic activity of Candida ribozymes. Chem Commun 2005, 313-315.
83. Wu Y., Wang Y.Y., Nakamoto Y., Li Y.Y., Baba T., Kaneko S., et al. Accelerated hepatocellular carcinoma development in mice expressing the Pim-3 transgene selectively in the liver. Oncogene 2010, 29:2228-2237.
84. Zhou J., Wu J., Hafdi N., Behr J.P., Erbacher P., Peng L. PAMAM dendrimers for efficient siRNA delivery and potent gene silencing. Chem Commun 2006, 2362-2364.
85. Zhou J., Swiderski P., Li H., Zhang J., Neff C.P., Akkina R., et al. Selection, characterization and application of new RNA HIV gp 120 aptamers for facile delivery of Dicer substrate siRNAs into HIV infected cells. Nucleic Acids Res 2009, 37:3094-3109.
86. Zhou J., Neff C.P., Liu X., Zhang J., Li H., Smith D.D., et al. Systemic administration of combinatorial dsiRNAs via nanoparticles efficiently suppresses HIV-1 infection in humanized mice. Mol Ther 2011, 19:2228-2238.
87. Zoubeidi A., Gleave M. Small heat shock proteins in cancer therapy and prognosis. Int J Biochem Cell Biol 2012, 44:1646-1656.