One-pot synthesis of pH-responsive hybrid nanogel particles for the intracellular delivery of small interfering RNA

Biomaterials

Volumn 87, Issue , 2016, Pages 57-68

  Khaled, Sm Z ^a   Cevenini, Armando ^a,b,c   Yazdi, Iman K ^a,d   Parodi, Alessandro ^a,e   Evangelopoulos, Michael ^a   Corbo, Claudia ^a,e   Scaria, Shilpa ^a   Hu, Ye ^a   Haddix, Seth G ^a   Corradetti, Bruna ^a,f   Salvatore, Francesco ^c,e   Tasciotti, Ennio ^a  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^d UNIVERSITY OF HOUSTON   (United States)

^e IRCCS SDN   (Italy)

^f UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Cancer therapy; Lysosomal escape; Nanoparticles; PH responsive polymer; SiRNA delivery

Indexed keywords

BOND STRENGTH (CHEMICAL); CELL CULTURE; CHEMICAL ANALYSIS; CHEMICAL STABILITY; DISEASES; EMULSIFICATION; EMULSIONS; GENE THERAPY; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; HYDROGELS; LIGHT SCATTERING; NANOPARTICLES; PLASTIC COATINGS; RNA; SILICA; THERMOGRAVIMETRIC ANALYSIS; TITRATION; TRANSMISSION ELECTRON MICROSCOPY;

CANCER THERAPY; HUMAN BREAST CANCER CELLS; INTRAVENOUS ADMINISTRATION; LYSOSOMAL ESCAPE; PH-RESPONSIVE POLYMER; SIRNA DELIVERY; SMALL INTERFERING RNA (SIRNA); ZETA POTENTIAL ANALYSIS;

SYNTHESIS (CHEMICAL);

CHEMOKINE RECEPTOR CXCR4; HYBRID NANOPARTICLE; SILICA NANOPARTICLE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WATER OIL CREAM; CATION; CXCR4 PROTEIN, HUMAN; DELAYED RELEASE FORMULATION; DIETHYLAMINOETHYL METHACRYLATE; METHACRYLIC ACID DERIVATIVE; NANOPARTICLE; POLYMER; SILICON DIOXIDE;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; ENZYMATIC DEGRADATION; HUMAN; HUMAN CELL; HYDROGEL; ONE POT SYNTHESIS; PH; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERMOGRAVIMETRY; ZETA POTENTIAL; ANIMAL; BREAST; BREAST NEOPLASMS; CHEMISTRY; DELAYED RELEASE FORMULATION; FEMALE; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNAI THERAPEUTICS; TUMOR CELL LINE;

ANIMALS; BREAST; BREAST NEOPLASMS; CATIONS; CELL LINE, TUMOR; DELAYED-ACTION PREPARATIONS; FEMALE; HUMANS; METHACRYLATES; MICE, NUDE; NANOPARTICLES; POLYMERS; RECEPTORS, CXCR4; RNA, SMALL INTERFERING; RNAI THERAPEUTICS; SILICON DIOXIDE;

EID: 84959275399     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.01.052     Document Type: Article

References (66)

1. Qiu Y., Park K. Environment-sensitive hydrogels for drug delivery. Adv. Drug Deliv. Rev. 2012, 64:49-60.
2. Parodi A., Corbo C., Cevenini A., Molinaro R., Palomba R., Pandolfi L., Agostini M., Salvatore F., Tasciotti E. Enabling cytoplasmic delivery and organelle targeting by surface modification of nanocarriers. Nanomedicine Lond. 2015, 10(12):1923-1940.
3. Hennink W.E., van Nostrum C.F. Novel crosslinking methods to design hydrogels. Adv. Drug Deliv. Rev. 2012, 64:223-236.
4. Hoffman A.S. Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 2012, 64:18-23.
5. Hamner K.L., Alexander C.M., Coopersmith K., Reishofer D., Provenza C., Maye M.M. Using temperature-sensitive smart polymers to regulate dna-mediated nanoassembly and encoded nanocarrier drug release. Acs Nano 2013, 7(8):7011-7020.
6. Hoffman A.S. Stimuli-responsive polymers: biomedical applications and challenges for clinical translation. Adv. Drug Deliv. Rev. 2013, 65(1):10-16.
7. Wang J., Lu Z., Wientjes M.G., Au J.L.S. Delivery of siRNA therapeutics: barriers and carriers. Aaps J. 2010, 12(4):492-503.
8. Yang J., Deng L.H., Han C.R., Duan J.F., Ma M.G., Zhang X.M., Xu F., Sun R.C. Synthetic and viscoelastic behaviors of silica nanoparticle reinforced poly(acrylamide) core-shell nanocomposite hydrogels. Soft Matter 2013, 9(4):1220-1230.
9. Buwalda S.J., Boere K.W., Dijkstra P.J., Feijen J., Vermonden T., Hennink W.E. Hydrogels in a historical perspective: from simple networks to smart materials. J. Control Release 2014, 190C:254-273.
10. Robinson D.N., Peppas N.A. Preparation and characterization of pH-responsive poly(methacrylic acid-g-ethylene glycol) nanospheres. Macromolecules 2002, 35(9):3668-3674.
11. Thomas J.B., Creecy C.M., McGinity J.W., Peppas N.A. Synthesis and properties of lightly crosslinked poly((meth)acrylic acid) microparticles prepared by free radical precipitation polymerization. Polym. Bull. 2006, 57(1):11-20.
12. Tamura G., Shinohara Y., Tamura A., Sanada Y., Oishi M., Akiba I., Nagasaki Y., Sakurai K., Amemiya Y. Dependence of the swelling behavior of a pH-responsive PEG-modified nanogel on the cross-link density. Polym. J. 2012, 44(3):240-244.
13. Kharlampieva E., Kozlovskaya V., Zavgorodnya O., Lilly G.D., Kotov N.A., Tsukruk V.V. pH-responsive photoluminescent LbL hydrogels with confined quantum dots. Soft Matter 2010, 6(4):800-807.
14. Bennour S., Louzri F. Study of swelling properties and thermal behavior of poly (N, N-dimethylacrylamide-co-maleic acid) based hydrogels. Adv. Chem. 2014, 2014.
15. Bian Q.Q., Xiao Y., Zhou C., Lang M.D. Synthesis, self-assembly, and pH-responsive behavior of (photo-crosslinked) star amphiphilic triblock copolymer. J. Colloid Interface Sci. 2013, 392:141-150.
16. Park C.W., Yang H.M., Lee H.J., Kim J.D. Core-shell nanogel of PEG-poly(aspartic acid) and its pH-responsive release of rh-insulin. Soft Matter 2013, 9(6):1781-1788.
17. Mukhopadhyay P., Sarkar K., Soam S., Kundu P.P. Formulation of pH-responsive carboxymethyl chitosan and alginate beads for the oral delivery of insulin. J. Appl. Polym. Sci. 2013, 129(2):835-845.
18. Kirschner C.M., Anseth K.S. Hydrogels in healthcare: from static to dynamic material microenvironments. Acta Mater. 2013, 61(3):931-944.
19. Yin H., Kanasty R.L., Eltoukhy A.A., Vegas A.J., Dorkin J.R., Anderson D.G. Non-viral vectors for gene-based therapy. Nat. Rev. Genet. 2014, 15(8):541-555.
20. Yang J., Chen J., Pan D., Wan Y., Wang Z. pH-sensitive interpenetrating network hydrogels based on chitosan derivatives and alginate for oral drug delivery. Carbohydr. Polym. 2013, 92(1):719-725.
21. Du H., Liu M., Yang X., Zhai G. The design of pH-sensitive chitosan-based formulations for gastrointestinal delivery. Drug Discov. Today 2015, 20(8):1004-1011.
22. Mironi-Harpaz I., Wang D.Y., Venkatraman S., Seliktar D. Photopolymerization of cell-encapsulating hydrogels: crosslinking efficiency versus cytotoxicity. Acta Biomater. 2012, 8(5):1838-1848.
23. Mazzoccoli J.P., Feke D.L., Baskaran H., Pintauro P.N. Mechanical and cell viability properties of crosslinked low- and high-molecular weight poly(ethylene glycol) diacrylate blends. J. Biomed. Mater. Res. Part A 2010, 93A(2):558-566.
24. Ji J., Shu S., Wang F., Liu J.J., Yu Z.Z. Revisit to the self-assembled hybrid acrylate/silica core-shell structured particles in the presence of unmodified silica particles. Colloids Surfaces A Physicochem. Eng. Aspects 2014, 446:156-162.
25. Sun J.T., Hong C.Y., Pan C.Y. Fabrication of PDEAEMA-coated mesoporous silica nanoparticles and pH-responsive controlled release. J. Phys. Chem. C 2010, 114(29):12481-12486.
26. Marek S.R., Conn C.A., Peppas N.A. Cationic nanogels based on diethylaminoethyl methacrylate. Polymer 2010, 51(6):1237-1243.
27. Liechty W.B., Caldorera-Moore M., Phillips M.A., Schoener C., Peppas N.A. Advanced molecular design of biopolymers for transmucosal and intracellular delivery of chemotherapeutic agents and biological therapeutics. J. Control. Release 2011, 155(2):119-127.
28. Gao Q., Xu Y., Wu D., Sun Y.H., Li X.A. pH-responsive drug release from polymer-coated mesoporous silica spheres. J. Phys. Chem. C 2009, 113(29):12753-12758.
29. Coates J. Interpretation of infrared spectra, a practical approach. Encycl. Anal. Chem. 2000, 10815-10837.
30. Kim D.J., Lee K.B., Chi Y.S., Kim W.J., Paik H.J., Choi I.S. Biomimetic formation of silica thin films by surface-initiated polymerization of 2-(dimethylamino) ethyl methacrylate and silicic acid. Langmuir 2004, 20(19):7904-7906.
31. Gulari E., McKeigue K., Ng K. Raman and FTIR spectroscopy of polymerization: bulk polymerization of methyl methacrylate and styrene. Macromolecules 1984, 17(9):1822-1825.
32. Cokbaglan L., Arsu N., Yagci Y., Jockusch S., Turro N.J. 2-Mercaptothioxanthone as a novel photoinitiator for free radical polymerization. Macromolecules 2003, 36(8):2649-2653.
33. Khaled S.M., Sui R., Charpentier P.A., Rizkalla A.S. Synthesis of TiO2-PMMA nanocomposite: Using methacrylic acid as a coupling agent. Langmuir 2007, 23(7):3988-3995.
34. Huang X.Y., Brittain W.J. Synthesis and characterization of PMMA nanocomposites by suspension and emulsion polymerization. Macromolecules 2001, 34(10):3255-3260.
35. Hackley V.A., Clogston J.D. Measuring the Hydrodynamic Size of Nanoparticles in Aqueous Media Using Batch-mode Dynamic Light Scattering. Characterization of Nanoparticles Intended for Drug Delivery 2007, 35-52. Springer.
36. Amalvy J.I., Wanless E.J., Li Y., Michailidou V., Armes S.P., Duccini Y. Synthesis and characterization of novel pH-responsive microgels based on tertiary amine methacrylates. Langmuir 2004, 20(21):8992-8999.
37. De S.K., Aluru N.R., Johnson B., Crone W.C., Beebe D.J., Moore J. Equilibrium swelling and kinetics of pH-responsive hydrogels: models, experiments, and simulations. J. Microelectromech. Syst. 2002, 11(5):544-555.
38. Ostroha J., Pong M., Lowman A., Dan N. Controlling the collapse/swelling transition in charged hydrogels. Biomaterials 2004, 25(18):4345-4353.
39. Pack D.W., Hoffman A.S., Pun S., Stayton P.S. Design and development of polymers for gene delivery. Nat. Rev. Drug Discov. 2005, 4(7):581-593.
40. Benjaminsen R.V., Mattebjerg M.A., Henriksen J.R., Moghimi S.M., Andresen T.L. The possible "Proton Sponge" effect of polyethylenimine (PEI) does not include change in lysosomal pH. Mol. Ther. 2013, 21(1):149-157.
41. Nel A.E., Madler L., Velegol D., Xia T., Hoek E.M.V., Somasundaran P., Klaessig F., Castranova V., Thompson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8(7):543-557.
42. You Y.Z., Manickam D.S., Zhou Q.H., Oupicky D. Reducible poly(2-dimethylaminoethyl methaerylate): synthesis, cytotoxicity, and gene delivery activity. J. Control. Release 2007, 122(3):217-225.
43. Fisher O.Z., Peppas N.A. Polybasic nanomatrices prepared by UV-initiated photopolymerization. Macromolecules 2009, 42(9):3391-3398.
44. Miller D.K., Griffiths E., Lenard J., Firestone R.A. Cell killing by lysosomotropic detergents. J. Cell Biol. 1983, 97(6):1841-1851.
45. Moreira C., Oliveira H., Pires L.R., Simoes S., Barbosa M.A., Pego A.P. Improving chitosan-mediated gene transfer by the introduction of intracellular buffering moieties into the chitosan backbone. Acta Biomater. 2009, 5(8):2995-3006.
46. Albini A., Mussi V., Parodi A., Ventura A., Principi E., Tegami S., Rocchia M., Francheschi E., Sogno I., Cammarota R., Finzi G., Sessa F., Noonan D.M., Valbusa U. Interactions of single-wall carbon nanotubes with endothelial cells. Nanomedicine 2009r, 6(2):277-288.
47. Parodi A., Quattrocchi N., van de Ven A.L., Chiappini C., Evangelopoulos M., Martinez J.O., Brown B.S., Khaled S.Z., Yazdi I.K., Enzo M.V., Isenhart L., Ferrari M., Tasciotti E. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 2013, 8(1):61-68.
48. Liang Z.X., Yoon Y.H., Votaw J., Goodman M.M., Williams L., Shim H. Silencing of CXCR4 blocks breast cancer metastasis. Cancer Res. 2005, 65(3):967-971.
49. Lee H., Lytton-Jean A.K., Chen Y., Love K.T., Park A.I., Karagiannis E.D., Sehgal A., Querbes W., Zurenko C.S., Jayaraman M., Peng C.G., Charisse K., Borodovsky A., Manoharan M., Donahoe J.S., Truelove J., Nahrendorf M., Langer R., Anderson D.G. Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat. Nanotechnol. 2012, 7(6):389-393.
50. Arima H., Tsutsumi T., Yoshimatsu A., Ikeda H., Motoyama K., Higashi T., Hirayama F., Uekama K. Inhibitory effect of siRNA complexes with polyamidoamine dendrimer/alpha-cyclodextrin conjugate (generation 3, G3) on endogenous gene expression. Eur. J. Pharm. Sci. 2011, 44(3):375-384.
51. Cun D., Foged C., Yang M., Frokjaer S., Nielsen H.M. Preparation and characterization of poly(DL-lactide-co-glycolide) nanoparticles for siRNA delivery. Int. J. Pharm. 2010, 390(1):70-75.
52. Naito M., Ishii T., Matsumoto A., Miyata K., Miyahara Y., Kataoka K. A phenylboronate-functionalized polyion complex micelle for ATP-triggered release of siRNA. Angew. Chem. Int. Ed. Engl. 2012, 51(43):10751-10755.
53. Hu Y., Atukorale P.U., Lu J.J., Moon J.J., Um S.H., Cho E.C., Wang Y., Chen J., Irvine D.J. Cytosolic delivery mediated via electrostatic surface binding of protein, virus, or siRNA cargos to pH-responsive core-shell gel particles. Biomacromolecules 2009, 10(4):756-765.
54. Convertine A.J., Diab C., Prieve M., Paschal A., Hoffman A.S., Johnson P.H., Stayton P.S. pH-responsive polymeric micelle carriers for siRNA drugs. Biomacromolecules 2010, 11(11):2904-2911.
55. Prencipe G., Tabakman S.M., Welsher K., Liu Z., Goodwin A.P., Zhang L., Henry J., Dai H.J. PEG branched polymer for functionalization of nanomaterials with ultralong blood circulation. J. Am. Chem. Soc. 2009, 131(13):4783-4787.
56. Gref R., Domb A., Quellec P., Blunk T., Muller R.H., Verbavatz J.M., Langer R. The controlled intravenous delivery of drugs using PEG-coated sterically stabilized nanospheres. Adv. Drug Deliv. Rev. 2012, 64:316-326.
57. Trewyn B.G., Slowing I.I., Giri S., Chen H.T., Lin V.S.Y. Synthesis and functionalization of a mesoporous silica nanoparticle based on the sol-gel process and applications in controlled release. Accounts Chem. Res. 2007, 40(9):846-853.
58. Yamamoto H., Shigematsu H., Nomura M., Lockwood W.W., Sato M., Okumura N., Soh J., Suzuki M., Wistuba I.I., Fong K.M., Lee H., Toyooka S., Date H., Lam W.L., Minna J.D., Gazdar A.F. PIK3CA mutations and copy number gains in human lung cancers. Cancer Res. 2008, 68(17):6913-6921.
59. Chen Y.Y., Takita J., Choi Y.L., Kato M., Ohira M., Sanada M., Wang L.L., Soda M., Kikuchi A., Igarashi T., Nakagawara A., Hayashi Y., Mano H., Ogawa S. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008, 455(7215). 971-U956.
60. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65(1-2):55-63.
61. Borenfreund E., Puerner J.A. Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol. Lett. 1985, 24(2-3):119-124.
62. Riddell R.J., Clothier R.H., Balls M. An evaluation of three in vitro cytotoxicity assays. Food Chem. Toxicol. 1986, 24(6-7):469-471.
63. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3(6):1101-1108.
64. Parodi A., Haddix S.G., Taghipour N., Scaria S., Taraballi F., Cevenini A., Yazdi I.K., Corbo C., Palomba R., Khaled S.Z., Martinez J.O., Brown B.S., Isenhart L., Tasciotti E. Bromelain surface modification increases the diffusion of silica nanopartides in the tumor extracellular matrix. Acs Nano 2014, 8(10):9874-9883.
65. Martinez J.O., Boada C., Yazdi I.K., Evangelopoulos M., Brown B.S., Liu X.W., Ferrari M., Tasciotti E. Short and long term, in vitro and in vivo correlations of cellular and tissue responses to mesoporous silicon nanovectors. Small 2013, 9(9-10):1722-1733.
66. Minardi S., Pandolfi L., Taraballi F., De Rosa E., Yazdi I.K., Liu X.W., Ferrari M., Tasciotti E. PLGA-mesoporous silicon microspheres for the in vivo controlled temporospatial delivery of proteins. Acs Appl. Mater. Interfaces 2015, 7(30):16364-16373.