Suppression of Hepatic Inflammation via Systemic siRNA Delivery by Membrane-Disruptive and Endosomolytic Helical Polypeptide Hybrid Nanoparticles

ACS Nano

Volumn 10, Issue 2, 2016, Pages 1859-1870

  He, Hua ^a   Zheng, Nan ^b   Song, Ziyuan ^b   Kim, Kyung Hoon ^b   Yao, Catherine ^b   Zhang, Rujing ^b   Zhang, Chenglin ^a   Huang, Yuhui ^a   Uckun, Fatih M ^c   Cheng, Jianjun ^b   Zhang, Yanfeng ^d   Yin, Lichen ^a  

^a SOOCHOW UNIVERSITY   (China)

^b University of Illinois at Urbana Champaign   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

anti inflammation therapy; endosomal escape; helical polypeptide; membrane disruption; siRNA delivery; TNF

Indexed keywords

DISEASES; PATHOLOGY; POLYPEPTIDES; RNA;

ANTI-INFLAMMATION; ENDOSOMAL ESCAPES; HELICAL POLYPEPTIDES; MEMBRANE DISRUPTION; SIRNA DELIVERY;

GENE THERAPY;

ANTIINFLAMMATORY AGENT; NANOPARTICLE; PEPTIDE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR;

ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; DRUG EFFECTS; ENDOSOME; GENETICS; HEPATITIS; LIVER; MACROPHAGE; MALE; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; ENDOSOMES; HEPATITIS; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; NANOPARTICLES; PEPTIDES; RNA, SMALL INTERFERING; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84960146233     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b05470     Document Type: Article

References (55)

1. Ye, C. T.; Choi, J. G.; Abraham, S.; Wu, H. Q.; Diaz, D.; Terreros, D.; Shankar, P.; Manjunath, N. Human Macrophage and Dendritic Cell-Specific Silencing of High-Mobility Group Protein B1 Ameliorates Sepsis in a Humanized Mouse Model Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 21052-21057 10.1073/pnas.1216195109
2. Un, K.; Kawakami, S.; Yoshida, M.; Higuchi, Y.; Suzuki, R.; Maruyama, K.; Yamashita, F.; Hashida, M. Efficient Suppression of Murine Intracellular Adhesion Molecule-1 Using Ultrasound-Responsive and Mannose-Modified Lipoplexes Inhibits Acute Hepatic Inflammation Hepatology 2012, 56, 259-269 10.1002/hep.25607
3. Nie, H.; Zheng, Y. X.; Li, R. S.; Guo, T. B.; He, D. Y.; Fang, L.; Liu, X. B.; Xiao, L. B.; Chen, X.; Wan, B. et al. Phosphorylation of FOXP3 Controls Regulatory T Cell Function and Is Inhibited by TNF-alpha in Rheumatoid Arthritis Nat. Med. 2013, 19, 322-328 10.1038/nm.3085
4. Kirman, I.; Whelan, R. L.; Nielsen, O. H. Infliximab: Mechanism of Action Beyond TNF-alpha Neutralization in Inflammatory Bowel Disease Eur. J. Gastroenterol. Hepatol. 2004, 16, 639-641 10.1097/01.meg.0000108345.41221.c2
5. Keane, J.; Gershon, S.; Wise, R. P.; Mirabile-Levens, E.; Kasznica, J.; Schwieterman, W. D.; Siegel, J. N.; Braun, M. M. Tuberculosis Associated with Infliximab, a Tumor Necrosis Factor (alpha)-Neutralizing Agent N. Engl. J. Med. 2001, 345, 1098-1104 10.1056/NEJMoa011110
6. 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 10.1038/nature08956
7. Lee, H.; Lytton-Jean, A. K. R.; Chen, Y.; Love, K. T.; Park, A. I.; Karagiannis, E. D.; Sehgal, A.; Querbes, W.; Zurenko, C. S.; Jayaraman, M. et al. Molecularly Self-Assembled Nucleic Acid Nanoparticles for Targeted In Vivo siRNA Delivery Nat. Nanotechnol. 2012, 7, 389-393 10.1038/nnano.2012.73
8. Woodrow, K. A.; Cu, Y.; Booth, C. J.; Saucier-Sawyer, J. K.; Wood, M. J.; Saltzman, W. M. Intravaginal Gene Silencing using Biodegradable Polymer Nanoparticles Densely Loaded with Small-Interfering RNA Nat. Mater. 2009, 8, 526-533 10.1038/nmat2444
9. Lee, S. J.; Huh, M. S.; Lee, S. Y.; Min, S.; Lee, S.; Koo, H.; Chu, J. U.; Lee, K. E.; Jeon, H.; Choi, Y. et al. Tumor-Homing Poly-siRNA/Glycol Chitosan Self-Cross-Linked Nanoparticles for Systemic siRNA Delivery in Cancer Treatment Angew. Chem., Int. Ed. 2012, 51, 7203-7207 10.1002/anie.201201390
10. Dassie, J. P.; Liu, X. Y.; Thomas, G. S.; Whitaker, R. M.; Thiel, K. W.; Stockdale, K. R.; Meyerholz, D. K.; McCaffrey, A. P.; McNamara, J. O.; Giangrande, P. H. Systemic Administration of Optimized Aptamer-siRNA Chimeras Promotes Regression of PSMA-Expressing Tumors Nat. Biotechnol. 2009, 27, 839-846 10.1038/nbt.1560
11. Wei, H.; Schellinger, J. G.; Chu, D. S. H.; Pun, S. H. Neuron-Targeted Copolymers with Sheddable Shielding Blocks Synthesized Using a Reducible, RAFT-ATRP Double-Head Agent J. Am. Chem. Soc. 2012, 134, 16554-16557 10.1021/ja3085803
12. Kozielski, K. L.; Tzeng, S. Y.; De Mendoza, B. A. H.; Green, J. J. Bioreducible Cationic Polymer-Based Nanoparticles for Efficient and Environmentally Triggered Cytoplasmic siRNA Delivery to Primary Human Brain Cancer Cells ACS Nano 2014, 8, 3232-3241 10.1021/nn500704t
13. Tranter, M.; Liu, Y. M.; He, S. W.; Gulick, J.; Ren, X. P.; Robbins, J.; Jones, W. K.; Reineke, T. M. In Vivo Delivery of Nucleic Acids via Glycopolymer Vehicles Affords Therapeutic Infarct Size Reduction In Vivo Mol. Ther. 2012, 20, 601-608 10.1038/mt.2011.267
14. Li, J.; Yu, X.; Wang, Y.; Yuan, Y.; Xiao, H.; Cheng, D.; Shuai, X. A Reduction and pH Dual-Sensitive Polymeric Vector for Long-Circulating and Tumor-Targeted siRNA Delivery Adv. Mater. 2014, 26, 8217-8224 10.1002/adma.201403877
15. Nelson, C. E.; Kim, A. J.; Adolph, E. J.; Gupta, M. K.; Yu, F.; Hocking, K. M.; Davidson, J. M.; Guelcher, S. A.; Duvall, C. L. Tunable Delivery of siRNA from a Biodegradable Scaffold to Promote Angiogenesis In Vivo Adv. Mater. 2014, 26, 607-614 10.1002/adma.201303520
16. Howard, K. A.; Paludan, S. R.; Behlke, M. A.; Besenbacher, F.; Deleuran, B.; Kjems, J. Chitosan/siRNA Nanoparticle-mediated TNF-alpha Knockdown in Peritoneal Macrophages for Anti-inflammatory Treatment in a Murine Arthritis Model Mol. Ther. 2009, 17, 162-168 10.1038/mt.2008.220
17. Kim, S. S.; Ye, C. T.; Kumar, P.; Chiu, I.; Subramanya, S.; Wu, H. Q.; Shankar, P.; Manjunath, N. Targeted Delivery of siRNA to Macrophages for Anti-inflammatory Treatment Mol. Ther. 2010, 18, 993-1001 10.1038/mt.2010.27
18. Wilson, D. S.; Dalmasso, G.; Wang, L. X.; Sitaraman, S. V.; Merlin, D.; Murthy, N. Orally Delivered Thioketal Nanoparticles Loaded with TNF-alpha-siRNA Target Inflammation and Inhibit Gene Expression in the Intestines Nat. Mater. 2010, 9, 923-928 10.1038/nmat2859
19. Lee, S.; Yang, S. C.; Kao, C. Y.; Pierce, R. H.; Murthy, N. Solid Polymeric Microparticles Enhance the Delivery of siRNA to Macrophages In Vivo Nucleic Acids Res. 2009, 37, e145 10.1093/nar/gkp758
20. Kriegel, C.; Amiji, M. Oral TNF-alpha Gene Silencing using a Polymeric Microsphere-Based Delivery System for the Treatment of Inflammatory Bowel Disease J. Controlled Release 2011, 150, 77-86 10.1016/j.jconrel.2010.10.002
21. Yang, X. Z.; Du, J. Z.; Dou, S.; Mao, C. Q.; Long, H. Y.; Wang, J. Sheddable Ternary Nanoparticles for Tumor Acidity-Targeted siRNA Delivery ACS Nano 2012, 6, 771-781 10.1021/nn204240b
22. Shim, M. S.; Wong, S.; Kwon, Y. J. siRNA as a Conventional Drug in the Clinic? Challenges and Current Technologies Drug Discovery Today: Technol. 2012, 9, e167-e173 10.1016/j.ddtec.2012.01.003
23. Roy, K.; Mao, H. Q.; Huang, S. K.; Leong, K. W. Oral Gene Delivery with Chitosan-DNA Nanoparticles Generates Immunologic Protection in a Murine Model of Peanut Allergy Nat. Med. 1999, 5, 387-391 10.1038/7385
24. Zheng, D.; Giljohann, D. A.; Chen, D. L.; Massich, M. D.; Wang, X. Q.; Iordanov, H.; Mirkin, C. A.; Paller, A. S. Topical Delivery of siRNA-Based Spherical Nucleic Acid Nanoparticle Conjugates for Gene Regulation Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 11975-11980 10.1073/pnas.1118425109
25. Tezgel, A. O.; Gonzalez-Perez, G.; Telfer, J. C.; Osborne, B. A.; Minter, L. M.; Tew, G. N. Novel Protein Transduction Domain Mimics as Nonviral Delivery Vectors for siRNA Targeting NOTCH1 in Primary Human T cells Mol. Ther. 2013, 21, 201-209 10.1038/mt.2012.209
26. 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. et al. Lipid-Like Materials for Low-Dose, In Vivo Gene Silencing Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 1864-1869 10.1073/pnas.0910603106
27. van Asbeck, A. H.; Beyerle, A.; McNeill, H.; Bovee-Geurts, P. H. M.; Lindberg, S.; Verdurmen, W. P. R.; Hällbrink, M.; Langel, Ü.; Heidenreich, O.; Brock, R. Molecular Parameters of siRNA-Cell Penetrating Peptide Nanocomplexes for Efficient Cellular Delivery ACS Nano 2013, 7, 3797-3807 10.1021/nn305754c
28. Meade, B. R.; Dowdy, S. F. Enhancing the Cellular Uptake of siRNA Duplexes Following Noncovalent Packaging with Protein Transduction Domain Peptides Adv. Drug Delivery Rev. 2008, 60, 530-536 10.1016/j.addr.2007.10.004
29. Ruzza, P.; Calderan, A.; Guiotto, A.; Osler, A.; Borin, G. Tat Cell-Penetrating Peptide Has the Characteristics of a Poly(proline) II Helix in Aqueous Solution and in SDS Micelles J. Pept. Sci. 2004, 10, 423-426 10.1002/psc.558
30. Daniels, D. S.; Schepartz, A. Intrinsically Cell-Permeable Miniature Proteins Based on a Minimal Cationic PPII Motif J. Am. Chem. Soc. 2007, 129, 14578-14579 10.1021/ja0772445
31. Stewart, K. M.; Horton, K. L.; Kelley, S. O. Cell-Penetrating Peptides as Delivery Vehicles for Biology and Medicine Org. Biomol. Chem. 2008, 6, 2242-2255 10.1039/b719950c
32. Meade, B. R.; Dowdy, S. F. Exogenous siRNA Delivery Using Peptide Transduction Domains/Cell Penetrating Peptides Adv. Drug Delivery Rev. 2007, 59, 134-140 10.1016/j.addr.2007.03.004
33. Gooding, M.; Browne, L. P.; Quinteiro, F. M.; Selwood, D. L. siRNA Delivery: From Lipids to Cell-penetrating Peptides and Their Mimics Chem. Biol. Drug Des. 2012, 80, 787-809 10.1111/cbdd.12052
34. Johnson, R. N.; Chu, D. S. H.; Shi, J.; Schellinger, J. G.; Carlson, P. M.; Pun, S. H. HPMA-Oligolysine Copolymers for Gene Delivery: Optimization of Peptide Length and Polymer Molecular Weight J. Controlled Release 2011, 155, 303-311 10.1016/j.jconrel.2011.07.009
35. Meyer, M.; Philipp, A.; Oskuee, R.; Schmidt, C.; Wagner, E. Breathing Life into Polycations: Functionalization with pH-Responsive Endosomolytic Peptides and Polyethylene Glycol Enables siRNA Delivery J. Am. Chem. Soc. 2008, 130, 3272-3273 10.1021/ja710344v
36. Lu, H.; Wang, J.; Bai, Y. G.; Lang, J. W.; Liu, S. Y.; Lin, Y.; Cheng, J. J. Ionic Polypeptides with Unusual Helical Stability Nat. Commun. 2011, 2, 206 10.1038/ncomms1209
37. Gabrielson, N. P.; Lu, H.; Yin, L. C.; Li, D.; Wang, F.; Cheng, J. J. Reactive and Bioactive Cationic a-Helical Polypeptide Template for Nonviral Gene Delivery Angew. Chem., Int. Ed. 2012, 51, 1143-1147 10.1002/anie.201104262
38. Katas, H.; Alpar, H. O. Development and Characterisation of Chitosan Nanoparticles for siRNA Delivery J. Controlled Release 2006, 115, 216-225 10.1016/j.jconrel.2006.07.021
39. Zhang, Y. F.; Lu, H.; Lin, Y.; Cheng, J. J. Water-Soluble Polypeptides with Elongated, Charged Side Chains Adopt Ultrastable Helical Conformations Macromolecules 2011, 44, 6641-6644 10.1021/ma201678r
40. Tang, D. W.; Yu, S. H.; Ho, Y. C.; Mi, F. L.; Kuo, P. L.; Sung, H. W. Heparinized Chitosan/Poly(gamma-glutamic acid) Nanoparticles For Multi-Functional Delivery of Fibroblast Growth Factor and Heparin Biomaterials 2010, 31, 9320-9332 10.1016/j.biomaterials.2010.08.058
41. Ter-Avetisyan, G.; Tuennemann, G.; Nowak, D.; Nitschke, M.; Herrmann, A.; Drab, M.; Cardoso, M. C. Cell Entry of Arginine-Rich Peptides Is Independent of Endocytosis J. Biol. Chem. 2009, 284, 3370-3378 10.1074/jbc.M805550200
42. 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 10.1124/pr.58.1.8
43. Zhao, X.; Yin, L.; Ding, J.; Tang, C.; Gu, S.; Yin, C.; Mao, Y. Thiolated Trimethyl Chitosan Nanocomplexes as Gene Carriers with High In Vitro and In Vivo Transfection Efficiency J. Controlled Release 2010, 144, 46-54 10.1016/j.jconrel.2010.01.022
44. McLendon, P. M.; Fichter, K. M.; Reineke, T. M. Poly(glycoamidoamine) Vehicles Promote pDNA Uptake through Multiple Routes and Efficient Gene Expression via Caveolae-Mediated Endocytosis Mol. Pharmaceutics 2010, 7, 738-750 10.1021/mp900282e
45. Akinc, A.; Zumbuehl, A.; Goldberg, M.; Leshchiner, E. S.; Busini, V.; Hossain, N.; Bacallado, S. A.; Nguyen, D. N.; Fuller, J.; Alvarez, R. et al. A Combinatorial Library of Lipid-Like Materials for Delivery of RNAi Therapeutics Nat. Biotechnol. 2008, 26, 561-569 10.1038/nbt1402
46. Lichtman, S. N.; Wang, J.; Lemasters, J. J. LPS Receptor CD14 Participates in Release of TNF-alpha in RAW 264.7 and Peritoneal Cells but not in Kupffer Cells Am. J. Physiol.-Gastr. L 1998, 275, G39-G46
47. Park, J. H.; Kim, K. H.; Lee, W. R.; Han, S. M.; Park, K. K. Protective Effect of Melittin on Inflammation and Apoptosis in Acute Liver Failure Apoptosis 2012, 17, 61-69 10.1007/s10495-011-0659-0
48. Zuckerman, J. E.; Choi, C. H. J.; Han, H.; Davis, M. E. Polycation-siRNA Nanoparticles Can Disassemble at the Kidney Glomerular Basement Membrane Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 3137-3142 10.1073/pnas.1200718109
49. Sanada, T.; Takaesu, G.; Mashima, R.; Yoshida, R.; Kobayashi, T.; Yoshimura, A. FLN29 Deficiency Reveals Its Negative Regulatory Role in the Toll-like Receptor (TLR) and Retinoic Acid-Inducible Gene I (RIG-I)-Like Helicase Signaling Pathway J. Biol. Chem. 2008, 283, 33858-33864 10.1074/jbc.M806923200
50. Nakama, T.; Hirono, S.; Moriuchi, A.; Hasuike, S.; Nagata, K.; Hori, T.; Ido, A.; Hayashi, K.; Tsubouchi, K. Etoposide Prevents Apoptosis in Mouse Liver with D-Galactosamine/Lipopolysaccharide-Induced Fulminant Hepatic Failure Resulting in Reduction of Lethality Hepatology 2001, 33, 1441-1450 10.1053/jhep.2001.24561
51. Miller, S. I.; Ernst, R. K.; Bader, M. W. LPS, TLR4 and Infectious Disease Diversity Nat. Rev. Microbiol. 2005, 3, 36-46 10.1038/nrmicro1068
52. Lu, H.; Bai, Y. G.; Wang, J.; Gabrielson, N. P.; Wang, F.; Lin, Y.; Cheng, J. J. Ring-Opening Polymerization of Gamma-(4-Vinylbenzyl)-L-Glutamate N-Carboxyanhydride for the Synthesis of Functional Polypeptides Macromolecules 2011, 44, 6237-6240 10.1021/ma201164n
53. Yin, L. C.; Tang, H. Y.; Kim, K. H.; Zheng, N.; Song, Z. Y.; Gabrielson, N. P.; Lu, H.; Cheng, J. J. Light-Responsive Helical Polypeptides Capable of Reducing Toxicity and Unpacking DNA: Toward Nonviral Gene Delivery Angew. Chem., Int. Ed. 2013, 52, 9182-9186 10.1002/anie.201302820
54. Takemoto, H.; Ishii, A.; Miyata, K.; Nakanishi, M.; Oba, M.; Ishii, T.; Yamasaki, Y.; Nishiyama, N.; Kataoka, K. Polyion Complex Stability and Gene Silencing Efficiency with a siRNA-Grafted Polymer Delivery System Biomaterials 2010, 31, 8097-8105 10.1016/j.biomaterials.2010.07.015
55. Tang, L.; Fan, T. M.; Borst, L. B.; Cheng, J. J. Synthesis and Biological Response of Size-Specific, Monodisperse Drug-Silica Nanoconjugates ACS Nano 2012, 6, 3954-3966 10.1021/nn300149c