Nanogels for intracellular delivery of biotherapeutics

Journal of Controlled Release

Volumn 259, Issue , 2017, Pages 16-28

  Li, Dandan ^a   van Nostrum, Cornelus F ^a   Mastrobattista, Enrico ^a   Vermonden, Tina ^a   Hennink, Wim E ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Biotherapeutics; Intracellular delivery; Nanogels; Stimuli responsive

Indexed keywords

CELL MEMBRANES;

BIOTHERAPEUTICS; CELL INTERNALIZATION; CHEMICAL DEGRADATION; HYDROPHILIC POLYMERS; INTRACELLULAR DELIVERY; NANOGELS; STIMULI-RESPONSIVE; THREE-DIMENSIONAL NETWORKS;

NANOSTRUCTURED MATERIALS;

ANTIBODY; BIOLOGICAL PRODUCT; CHITOSAN; ENZYME; FREE RADICAL; MACROGOL; NANOCARRIER; NANOPARTICLE; NUCLEIC ACID; PEPTIDES AND PROTEINS; POLYMER; POLYMETHACRYLIC ACID; SMALL INTERFERING RNA; NANOMATERIAL;

ARTICLE; BIOLOGICAL THERAPY; CELL MEMBRANE; CELL SURFACE; CYTOSOL; DISULFIDE BOND; DRUG DEGRADATION; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; GEL; HUMAN; HYDROGEL; INTERNALIZATION; INTRACELLULAR SPACE; NANOGEL; NONHUMAN; PARTICLE SIZE; POLYMERIZATION; PRIORITY JOURNAL; ADMINISTRATION AND DOSAGE; ANIMAL; CHEMISTRY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL THERAPY; BIOLOGICAL TRANSPORT; DRUG DELIVERY SYSTEMS; GELS; HUMANS; NANOSTRUCTURES; PARTICLE SIZE;

EID: 85009212532     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.12.020     Document Type: Article

References (177)

1. Leader, B., Baca, Q.J., Golan, D.E., Protein therapeutics: a summary and pharmacological classification. Nat. Rev. Drug Discov. 7 (2008), 21–39.
2. Torchilin, V., Intracellular delivery of protein and peptide therapeutics. Drug Discov. Today 5 (2008), e95–e103.
3. Naldini, L., Gene therapy returns to centre stage. Nature 526 (2015), 351–360.
4. Amigorena, S., Savina, A., Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22 (2010), 109–117.
5. Sarisozen, C., Torchilin, V.P., Intracellular delivery of proteins and peptides. Drug Deliv., 2016, 576–622.
6. Lächelt, U., Wagner, E., Nucleic acid therapeutics using polyplexes: a journey of 50 years (and beyond). Chem. Rev. 115 (2015), 11043–11078.
7. Benne, N., van Duijn, J., Kuiper, J., Jiskoot, W., Slütter, B., Orchestrating immune responses: how size, shape and rigidity affect the immunogenicity of particulate vaccines. J. Control. Release 234 (2016), 124–134.
8. Couvreur, P., Nanoparticles in drug delivery: past, present and future. Adv. Drug Deliv. Rev. 65 (2013), 21–23.
9. Blanco, E., Shen, H., Ferrari, M., Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotechnol. 33 (2015), 941–951.
10. Manzoor, A.A., Lindner, L.H., Landon, C.D., Park, J.-Y., Simnick, A.J., Dreher, M.R., Das, S., Hanna, G., Park, W., Chilkoti, A., Koning, G.A., ten Hagen, T.L.M., Needham, D., Dewhirst, M.W., Overcoming limitations in nanoparticle drug delivery: triggered, intravascular release to improve drug penetration into tumors. Cancer Res. 72 (2012), 5566–5575.
11. Saraiva, C., Praça, C., Ferreira, R., Santos, T., Ferreira, L., Bernardino, L., Nanoparticle-mediated brain drug delivery: overcoming blood–brain barrier to treat neurodegenerative diseases. J. Control. Release 235 (2016), 34–47.
12. Kanapathipillai, M., Brock, A., Ingber, D.E., Nanoparticle targeting of anti-cancer drugs that alter intracellular signaling or influence the tumor microenvironment. Adv. Drug Deliv. Rev. 79–80 (2014), 107–118.
13. Suk, J.S., Xu, Q., Kim, N., Hanes, J., Ensign, L.M., PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv. Drug Deliv. Rev. 99 (2016), 28–51.
14. Fang, J., Nakamura, H., Maeda, H., The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 63 (2011), 136–151.
15. Azzopardi, E.A., Ferguson, E.L., Thomas, D.W., The enhanced permeability retention effect: a new paradigm for drug targeting in infection. J. Antimicrob. Chemother. 68 (2012), 257–274.
16. Xu, S., Olenyuk, B.Z., Okamoto, C.T., Hamm-Alvarez, S.F., Targeting receptor-mediated endocytotic pathways with nanoparticles: rationale and advances. Adv. Drug Deliv. Rev. 65 (2013), 121–138.
17. van der Meel, R., Vehmeijer, L.J.C., Kok, R.J., Storm, G., van Gaal, E.V.B., Ligand-targeted particulate nanomedicines undergoing clinical evaluation: current status. Adv. Drug Deliv. Rev. 65 (2013), 1284–1298.
18. Danhier, F., Ansorena, E., Silva, J.M., Coco, R., Le Breton, A., Préat, V., PLGA-based nanoparticles: an overview of biomedical applications. J. Control. Release 161 (2012), 505–522.
19. Allen, T.M., Cullis, P.R., Liposomal drug delivery systems: from concept to clinical applications. Adv. Drug Deliv. Rev. 65 (2013), 36–48.
20. Liong, M., Lu, J., Kovochich, M., Xia, T., Ruehm, S.G., Nel, A.E., Tamanoi, F., Zink, J.I., Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano 2 (2008), 889–896.
21. Gong, J., Chen, M., Zheng, Y., Wang, S., Wang, Y., Polymeric micelles drug delivery system in oncology. J. Control. Release 159 (2012), 312–323.
22. Chacko, R.T., Ventura, J., Zhuang, J., Thayumanavan, S., Polymer nanogels: a versatile nanoscopic drug delivery platform. Adv. Drug Deliv. Rev. 64 (2012), 836–851.
23. Eetezadi, S., Ekdawi, S.N., Allen, C., The challenges facing block copolymer micelles for cancer therapy: in vivo barriers and clinical translation. Adv. Drug Deliv. Rev. 91 (2015), 7–22.
24. Nochi, T., Yuki, Y., Takahashi, H., Sawada, S.-i., Mejima, M., Kohda, T., Harada, N., Kong, I.G., Sato, A., Kataoka, N., Tokuhara, D., Kurokawa, S., Takahashi, Y., Tsukada, H., Kozaki, S., Akiyoshi, K., Kiyono, H., Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nat. Mater. 9 (2010), 572–578.
25. Peppas, N.A., Hilt, J.Z., Khademhosseini, A., Langer, R., Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv. Mater. 18 (2006), 1345–1360.
26. Buwalda, S.J., Boere, K.W.M., Dijkstra, P.J., Feijen, J., Vermonden, T., Hennink, W.E., Hydrogels in a historical perspective: from simple networks to smart materials. J. Control. Release 190 (2014), 254–273.
27. Jiang, Y., Chen, J., Deng, C., Suuronen, E.J., Zhong, Z., Click hydrogels, microgels and nanogels: emerging platforms for drug delivery and tissue engineering. Biomaterials 35 (2014), 4969–4985.
28. Vermonden, T., Censi, R., Hennink, W.E., Hydrogels for protein delivery. Chem. Rev. 112 (2012), 2853–2888.
29. Censi, R., Di Martino, P., Vermonden, T., Hennink, W.E., Hydrogels for protein delivery in tissue engineering. J. Control. Release 161 (2012), 680–692.
30. Annabi, N., Tamayol, A., Uquillas, J.A., Akbari, M., Bertassoni, L.E., Cha, C., Camci-Unal, G., Dokmeci, M.R., Peppas, N.A., Khademhosseini, A., Rational design and applications of hydrogels in regenerative medicine. Adv. Mater. 26 (2014), 85–124.
31. Lee, K.Y., Mooney, D.J., Hydrogels for tissue engineering. Chem. Rev. 101 (2001), 1869–1880.
32. Sasaki, Y., Akiyoshi, K., Nanogel engineering for new nanobiomaterials: from chaperoning engineering to biomedical applications. Chem. Rec. 10 (2010), 366–376.
33. Thomann-Harwood, L.J., Kaeuper, P., Rossi, N., Milona, P., Herrmann, B., McCullough, K.C., Nanogel vaccines targeting dendritic cells: contributions of the surface decoration and vaccine cargo on cell targeting and activation. J. Control. Release 166 (2013), 95–105.
34. Zhang, H., Zhai, Y., Wang, J., Zhai, G., New progress and prospects: the application of nanogel in drug delivery. Mater. Sci. Eng. C 60 (2016), 560–568.
35. Li, Y., Maciel, D., Rodrigues, J., Shi, X., Tomás, H., Biodegradable polymer nanogels for drug/nucleic acid delivery. Chem. Rev. 115 (2015), 8564–8608.
36. Wu, H.-Q., Wang, C., Biodegradable smart nanogels: a new platform for targeting drug delivery and biomedical diagnostics. Langmuir 32 (2016), 6211–6225.
37. Soni, K.S., Desale, S.S., Bronich, T.K., Nanogels: an overview of properties, biomedical applications and obstacles to clinical translation. J. Control. Release 240 (2016), 109–126.
38. Zhang, X., Malhotra, S., Molina, M., Haag, R., Micro- and nanogels with labile crosslinks - from synthesis to biomedical applications. Chem. Soc. Rev. 44 (2015), 1948–1973.
39. Yang, H., Wang, Q., Huang, S., Xiao, A., Li, F., Gan, L., Yang, X., Smart pH/redox dual-responsive nanogels for on-demand intracellular anticancer drug release. ACS Appl. Mater. Interfaces 8 (2016), 7729–7738.
40. Shirangi, M., Sastre Toraño, J., Sellergren, B., Hennink, W.E., Somsen, G.W., van Nostrum, C.F., Methyleneation of peptides by N,N,N,N-tetramethylethylenediamine (TEMED) under conditions used for free radical polymerization: a mechanistic study. Bioconjug. Chem. 26 (2015), 90–100.
41. Cadée, J.A., van Steenbergen, M.J., Versluis, C., Heck, A.J.R., Underberg, W.J.M., den Otter, W., Jiskoot, W., Hennink, W.E., Oxidation of recombinant human interleukin-2 by potassium peroxodisulfate. Pharm. Res. 18 (2001), 1461–1467.
42. Gregoritza, M., Goepferich, A.M., Brandl, F.P., Polyanions effectively prevent protein conjugation and activity loss during hydrogel cross-linking. J. Control. Release 238 (2016), 92–102.
43. Hammer, N., Brandl, F.P., Kirchhof, S., Messmann, V., Goepferich, A.M., Protein compatibility of selected cross-linking reactions for hydrogels. Macromol. Biosci. 15 (2015), 405–413.
44. Raemdonck, K., Naeye, B., Hogset, A., Demeester, J., De Smedt, S.C., Biodegradable dextran nanogels as functional carriers for the intracellular delivery of small interfering RNA. J. Control. Release 148 (2010), e95–e96.
45. Toita, S., Sawada, S.-i., Akiyoshi, K., Polysaccharide nanogel gene delivery system with endosome-escaping function: Co-delivery of plasmid DNA and phospholipase A2. J. Control. Release 155 (2011), 54–59.
46. Raemdonck, K., Van Thienen, T.G., Vandenbroucke, R.E., Sanders, N.N., Demeester, J., De Smedt, S.C., Dextran microgels for time-controlled delivery of sirna. Adv. Funct. Mater. 18 (2008), 993–1001.
47. Nuhn, L., Kaps, L., Diken, M., Schuppan, D., Zentel, R., Reductive decationizable block copolymers for stimuli-responsive mRNA delivery. Macromol. Rapid Commun. 37 (2016), 924–933.
48. Nuhn, L., Braun, L., Overhoff, I., Kelsch, A., Schaeffel, D., Koynov, K., Zentel, R., Degradable cationic nanohydrogel particles for stimuli-responsive release of siRNA. Macromol. Rapid Commun. 35 (2014), 2057–2064.
49. Raemdonck, K., Naeye, B., Buyens, K., Vandenbroucke, R.E., Høgset, A., Demeester, J., De Smedt, S.C., Biodegradable dextran nanogels for RNA interference: focusing on endosomal escape and intracellular siRNA delivery. Adv. Funct. Mater. 19 (2009), 1406–1415.
50. Nagahama, K., Ouchi, T., Ohya, Y., Biodegradable nanogels prepared by self-assembly of poly(L-lactide)-grafted dextran: entrapment and release of proteins. Macromol. Biosci. 8 (2008), 1044–1052.
51. Rader, R.A., (Re)defining biopharmaceutical. Nat. Biotechnol. 26 (2008), 743–751.
52. Kinch, M.S., An overview of FDA-approved biologics medicines. Drug Discov. Today 20 (2015), 393–398.
53. Fosgerau, K., Hoffmann, T., Peptide therapeutics: current status and future directions. Drug Discov. Today 20 (2015), 122–128.
54. Couzin-Frankel, J., Cancer immunotherapy. Science 342 (2013), 1432–1433.
55. Manohar, A., Ahuja, J., Crane, J.K., Immunotherapy for infectious diseases: past, present, and future. Immunol. Investig. 44 (2015), 731–737.
56. Chan, A.C., Carter, P.J., Therapeutic antibodies for autoimmunity and inflammation. Nat. Rev. Immunol. 10 (2010), 301–316.
57. Nathan, D.G., Orkin, S.H., Musings on genome medicine: enzyme-replacement therapy of the lysosomal storage diseases. Genome Med. 1 (2009), 1–3.
58. Guermonprez, P., Valladeau, J., Zitvogel, L., Thery, C., Amigorena, S., Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20 (2002), 621–667.
59. Joffre, O.P., Segura, E., Savina, A., Amigorena, S., Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12 (2012), 557–569.
60. Roche, P.A., Furuta, K., The ins and outs of MHC class II-mediated antigen processing and presentation. Nat. Rev. Immunol. 15 (2015), 203–216.
61. Tahara, Y., Akiyoshi, K., Current advances in self-assembled nanogel delivery systems for immunotherapy. Adv. Drug Deliv. Rev. 95 (2015), 65–76.
62. Sahay, G., Alakhova, D.Y., Kabanov, A.V., Endocytosis of nanomedicines. J. Control. Release 145 (2010), 182–195.
63. Kou, L., Sun, J., Zhai, Y., He, Z., The endocytosis and intracellular fate of nanomedicines: implication for rational design. Asian J. Pharm. Sci. 8 (2013), 1–10.
64. Shete, H.K., Prabhu, R.H., Patravale, V.B., Endosomal escape: a bottleneck in intracellular delivery. J. Nanosci. Nanotechnol. 14 (2014), 460–474.
65. Martens, T.F., Remaut, K., Demeester, J., De Smedt, S.C., Braeckmans, K., Intracellular delivery of nanomaterials: how to catch endosomal escape in the act. Nano Today 9 (2014), 344–364.
66. Varkouhi, A.K., Scholte, M., Storm, G., Haisma, H.J., Endosomal escape pathways for delivery of biologicals. J. Control. Release 151 (2011), 220–228.
67. Akinc, A., Battaglia, G., Exploiting endocytosis for nanomedicines. Cold Spring Harb. Perspect. Biol., 5, 2013, a016980.
68. Wang, S.H., Lee, C.W., Chiou, A., Wei, P.K., Size-dependent endocytosis of gold nanoparticles studied by three-dimensional mapping of plasmonic scattering images. J. Nanobiotechnol., 8, 2010, 33.
69. Rejman, J., Oberle, V., Zuhorn, I.S., Hoekstra, D., Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 377 (2004), 159–169.
70. Zhang, S., Li, J., Lykotrafitis, G., Bao, G., Suresh, S., Size-dependent endocytosis of nanoparticles. Adv. Mater. 21 (2009), 419–424.
71. Shang, L., Nienhaus, K., Nienhaus, G.U., Engineered nanoparticles interacting with cells: size matters. J. Nanobiotechnol., 12, 2014, 5.
72. Nuhn, L., Vanparijs, N., De Beuckelaer, A., Lybaert, L., Verstraete, G., Deswarte, K., Lienenklaus, S., Shukla, N.M., Salyer, A.C.D., Lambrecht, B.N., Grooten, J., David, S.A., De Koker, S., De Geest, B.G., pH-Degradable imidazoquinoline-ligated nanogels for lymph node-focused immune activation. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 8098–8103.
73. Nuhn, L., Tomcin, S., Miyata, K., Mailänder, V., Landfester, K., Kataoka, K., Zentel, R., Size-dependent knockdown potential of siRNA-loaded cationic nanohydrogel particles. Biomacromolecules 15 (2014), 4111–4121.
74. Ryu, J.-H., Bickerton, S., Zhuang, J., Thayumanavan, S., Ligand-decorated nanogels: fast one-pot synthesis and cellular targeting. Biomacromolecules 13 (2012), 1515–1522.
75. Abolmaali, S.S., Tamaddon, A.M., Mohammadi, S., Amoozgar, Z., Dinarvand, R., Chemically crosslinked nanogels of PEGylated poly ethyleneimine (l-histidine substituted) synthesized via metal ion coordinated self-assembly for delivery of methotrexate: cytocompatibility, cellular delivery and antitumor activity in resistant cells. Mater. Sci. Eng. C 62 (2016), 897–907.
76. Hamidi, M., Azadi, A., Rafiei, P., Hydrogel nanoparticles in drug delivery. Adv. Drug Deliv. Rev. 60 (2008), 1638–1649.
77. Raemdonck, K., Demeester, J., De Smedt, S., Advanced nanogel engineering for drug delivery. Soft Matter 5 (2009), 707–715.
78. Yallapu, M.M., Jaggi, M., Chauhan, S.C., Design and engineering of nanogels for cancer treatment. Drug Discov. Today 16 (2011), 457–463.
79. Iversen, T.-G., Skotland, T., Sandvig, K., Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano Today 6 (2011), 176–185.
80. Bareford, L.M., Swaan, P.W., Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59 (2007), 748–758.
81. Li, D., Sun, F., Bourajjaj, M., Chen, Y., Pieters, E.H., Chen, J., van den Dikkenberg, J.B., Lou, B., Camps, M.G.M., Ossendorp, F., Hennink, W.E., Vermonden, T., van Nostrum, C.F., Strong in vivo antitumor responses induced by an antigen immobilized in nanogels via reducible bonds. Nanoscale, 2016.
82. Li, L., Raghupathi, K., Yuan, C., Thayumanavan, S., Surface charge generation in nanogels for activated cellular uptake at tumor-relevant pH. Chem. Sci. 4 (2013), 3654–3660.
83. Vinogradov, S.V., Bronich, T.K., Kabanov, A.V., Nanosized cationic hydrogels for drug delivery: preparation, properties and interactions with cells. Adv. Drug Deliv. Rev. 54 (2002), 135–147.
84. Urakami, H., Hentschel, J., Seetho, K., Zeng, H., Chawla, K., Guan, Z., Surfactant-free synthesis of biodegradable, biocompatible, and stimuli-responsive cationic nanogel particles. Biomacromolecules 14 (2013), 3682–3688.
85. Li, R.-Q., Wu, W., Song, H.-Q., Ren, Y., Yang, M., Li, J., Xu, F.-J., Well-defined reducible cationic nanogels based on functionalized low-molecular-weight PGMA for effective pDNA and siRNA delivery. Acta Biomater. 41 (2016), 282–292.
86. Vandamme, T.F., Brobeck, L., Poly(amidoamine) dendrimers as ophthalmic vehicles for ocular delivery of pilocarpine nitrate and tropicamide. J. Control. Release 102 (2005), 23–38.
87. Chiu, Y.-L., Ho, Y.-C., Chen, Y.-M., Peng, S.-F., Ke, C.-J., Chen, K.-J., Mi, F.-L., Sung, H.-W., The characteristics, cellular uptake and intracellular trafficking of nanoparticles made of hydrophobically-modified chitosan. J. Control. Release 146 (2010), 152–159.
88. Nam, H.Y., Kwon, S.M., Chung, H., Lee, S.-Y., Kwon, S.-H., Jeon, H., Kim, Y., Park, J.H., Kim, J., Her, S., Oh, Y.-K., Kwon, I.C., Kim, K., Jeong, S.Y., Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J. Control. Release 135 (2009), 259–267.
89. Vinogradov, S.V., Kohli, E., Zeman, A.D., Cross-linked polymeric nanogel formulations of 5′-triphosphates of nucleoside analogues: role of the cellular membrane in drug release. Mol. Pharm. 2 (2005), 449–461.
90. Liang, K., Ng, S., Lee, F., Lim, J., Chung, J.E., Lee, S.S., Kurisawa, M., Targeted intracellular protein delivery based on hyaluronic acid–green tea catechin nanogels. Acta Biomater. 33 (2016), 142–152.
91. Yang, C., Wang, X., Yao, X., Zhang, Y., Wu, W., Jiang, X., Hyaluronic acid nanogels with enzyme-sensitive cross-linking group for drug delivery. J. Control. Release 205 (2015), 206–217.
92. Eckmann, D.M., Composto, R.J., Tsourkas, A., Muzykantov, V.R., Nanogel carrier design for targeted drug delivery. J. Mater. Chem. B 2 (2014), 8085–8097.
93. Steichen, S.D., Caldorera-Moore, M., Peppas, N.A., A review of current nanoparticle and targeting moieties for the delivery of cancer therapeutics. Eur. J. Pharm. Sci. 48 (2013), 416–427.
94. Bazak, R., Houri, M., El Achy, S., Kamel, S., Refaat, T., Cancer active targeting by nanoparticles: a comprehensive review of literature. J. Cancer Res. Clin. Oncol. 141 (2015), 769–784.
95. Dehaini, D., Fang, R.H., Zhang, L., Biomimetic strategies for targeted nanoparticle delivery. Bioeng. Transl. Med. 1 (2016), 30–46.
96. Ye, Y., Yu, J., Gu, Z., Versatile protein nanogels prepared by in situ polymerization. Macromol. Chem. Phys. 217 (2016), 333–343.
97. Soni, G., Yadav, K.S., Nanogels as potential nanomedicine carrier for treatment of cancer: a mini review of the state of the art. Saudi Pharm. J. 24 (2016), 133–139.
98. Schafer, F.Q., Buettner, G.R., Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30 (2001), 1191–1212.
99. Roberts, M.J., Bentley, M.D., Harris, J.M., Chemistry for peptide and protein PEGylation. Adv. Drug Deliv. Rev. 64 (2012), 116–127 (Supplement).
100. Zhang, S., Gao, H., Bao, G., Physical principles of nanoparticle cellular endocytosis. ACS Nano 9 (2015), 8655–8671.
101. Yameen, B., Choi, W.I., Vilos, C., Swami, A., Shi, J., Farokhzad, O.C., Insight into nanoparticle cellular uptake and intracellular targeting. J. Control. Release 190 (2014), 485–499.
102. Tammam, S.N., Azzazy, H.M.E., Lamprecht, A., How successful is nuclear targeting by nanocarriers?. J. Control. Release 229 (2016), 140–153.
103. Hwang, C., Sinskey, A., Lodish, H., Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257 (1992), 1496–1502.
104. Appenzeller-Herzog, C., Glutathione- and non-glutathione-based oxidant control in the endoplasmic reticulum. J. Cell Sci. 124 (2011), 847–855.
105. Brülisauer, L., Gauthier, M.A., Leroux, J.-C., Disulfide-containing parenteral delivery systems and their redox-biological fate. J. Control. Release 195 (2014), 147–154.
106. Saito, G., Swanson, J.A., Lee, K.-D., Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv. Drug Deliv. Rev. 55 (2003), 199–215.
107. Arunachalam, B., Phan, U.T., Geuze, H.J., Cresswell, P., Enzymatic reduction of disulfide bonds in lysosomes: characterization of a gamma-interferon-inducible lysosomal thiol reductase (GILT). Proc. Natl. Acad. Sci. 97 (2000), 745–750.
108. Phan, U.T., Arunachalam, B., Cresswell, P., Gamma-interferon-inducible lysosomal thiol reductase (GILT): maturation, activity, and mechanism of action. J. Biol. Chem. 275 (2000), 25907–25914.
109. Gainey, D., Short, S., McCoy, K.L., Intracellular location of cysteine transport activity correlates with productive processing of antigen disulfide. J. Cell. Physiol. 168 (1996), 248–254.
110. Short, S., Merkel, B.J., Caffrey, R., McCoy, K.L., Defective antigen processing correlates with a low level of intracellular glutathione. Eur. J. Immunol. 26 (1996), 3015–3020.
111. Dunn, S.S., Tian, S., Blake, S., Wang, J., Galloway, A.L., Murphy, A., Pohlhaus, P.D., Rolland, J.P., Napier, M.E., DeSimone, J.M., Reductively responsive siRNA-conjugated hydrogel nanoparticles for gene silencing. J. Am. Chem. Soc. 134 (2012), 7423–7430.
112. Hong, C.A., Kim, J.S., Lee, S.H., Kong, W.H., Park, T.G., Mok, H., Nam, Y.S., Reductively dissociable siRNA-polymer hybrid nanogels for efficient targeted gene silencing. Adv. Funct. Mater. 23 (2013), 316–322.
113. Li, D., Kordalivand, N., Fransen, M.F., Ossendorp, F., Raemdonck, K., Vermonden, T., Hennink, W.E., van Nostrum, C.F., Reduction-sensitive dextran nanogels aimed for intracellular delivery of antigens. Adv. Funct. Mater. 25 (2015), 2993–3003.
114. Watts, J.K., Deleavey, G.F., Damha, M.J., Chemically modified siRNA: tools and applications. Drug Discov. Today 13 (2008), 842–855.
115. Cheng, R., Feng, F., Meng, F., Deng, C., Feijen, J., Zhong, Z., Glutathione-responsive nano-vehicles as a promising platform for targeted intracellular drug and gene delivery. J. Control. Release 152 (2011), 2–12.
116. Zhao, M., Biswas, A., Hu, B., Joo, K.-I., Wang, P., Gu, Z., Tang, Y., Redox-responsive nanocapsules for intracellular protein delivery. Biomaterials 32 (2011), 5223–5230.
117. Mishina, M., Minamihata, K., Moriyama, K., Nagamune, T., Peptide tag-induced horseradish peroxidase-mediated preparation of a streptavidin-immobilized redox-sensitive hydrogel. Biomacromolecules 17 (2016), 1978–1984.
118. Lee, H., Mok, H., Lee, S., Oh, Y.K., Park, T.G., Target-specific intracellular delivery of siRNA using degradable hyaluronic acid nanogels. J. Control. Release 119 (2007), 245–252.
119. Mok, H., Park, T.G., PEG-assisted DNA solubilization in organic solvents for preparing cytosol specifically degradable PEG/DNA nanogels. Bioconjug. Chem. 17 (2006), 1369–1372.
120. Shi, B., Zhang, H., Qiao, S.Z., Bi, J., Dai, S., Intracellular microenvironment-responsive label-free autofluorescent nanogels for traceable gene delivery. Adv. Healthc. Mater. 3 (2014), 1839–1848.
121. Shrivats, A.R., Mishina, Y., Averick, S., Matyjaszewski, K., Hollinger, J.O., In vivo GFP knockdown by cationic nanogel-sirna polyplexes. Bioengineering 2 (2015), 160–175.
122. Novo, L., van Gaal, E.V.B., Mastrobattista, E., van Nostrum, C.F., Hennink, W.E., Decationized crosslinked polyplexes for redox-triggered gene delivery. J. Control. Release 169 (2013), 246–256.
123. Novo, L., Mastrobattista, E., van Nostrum, C.F., Hennink, W.E., Targeted decationized polyplexes for cell specific gene delivery. Bioconjug. Chem. 25 (2014), 802–812.
124. Nguyen, D.H., Hoon Choi, J., Ki Joung, Y., Dong Park, K., Disulfide-crosslinked heparin-pluronic nanogels as a redox-sensitive nanocarrier for intracellular protein delivery. J. Bioact. Compat. Polym. 26 (2011), 287–300.
125. Choi, J.H., Jang, J.Y., Joung, Y.K., Kwon, M.H., Park, K.D., Intracellular delivery and anti-cancer effect of self-assembled heparin-pluronic nanogels with RNase A. J. Control. Release 147 (2010), 420–427.
126. Merkel, B.J., Mandel, R., Ryser, H.J., McCoy, K.L., Characterization of fibroblasts with a unique defect in processing antigens with disulfide bonds. J. Immunol. 154 (1995), 128–136.
127. Pisoni, R.L., Acker, T.L., Lisowski, K.M., Lemons, R.M., Thoene, J.G., A cysteine-specific lysosomal transport system provides a major route for the delivery of thiol to human fibroblast lysosomes: possible role in supporting lysosomal proteolysis. J. Cell Biol. 110 (1990), 327–335.
128. Nguyen, J., Bernert, R., In, K., Kang, P., Sebastiao, N., Hu, C., Hastings, K.T., Gamma-interferon-inducible lysosomal thiol reductase is upregulated in human melanoma. Melanoma Res. 26 (2016), 125–137.
129. Xiang, Y.-J., Guo, M.-M., Zhou, C.-J., Liu, L., Han, B., Kong, L.-Y., Gao, Z.-C., Ma, Z.-B., Wang, L., Feng, M., Chen, H.-Y., Jia, G.-T., Gao, D.-Z., Zhang, Q., Li, L., Li, Y.-Y., Yu, Z.-G., Absence of gamma-interferon-inducible lysosomal thiol reductase (GILT) is associated with poor disease-free survival in breast cancer patients. PLoS ONE, 9, 2014, e109449.
130. Chen, W., Zheng, M., Meng, F., Cheng, R., Deng, C., Feijen, J., Zhong, Z., In situ forming reduction-sensitive degradable nanogels for facile loading and triggered intracellular release of proteins. Biomacromolecules 14 (2013), 1214–1222.
131. Jiang, X., Wang, X., Cytochrome C-mediated apoptosis. Annu. Rev. Biochem. 73 (2004), 87–106.
132. Balce, D.R., Allan, E.R.O., McKenna, N., Yates, R.M., γ-interferon-inducible lysosomal thiol reductase (GILT) maintains phagosomal proteolysis in alternatively activated macrophages. J. Biol. Chem. 289 (2014), 31891–31904.
133. Collins, D.S., Unanue, E.R., Harding, C.V., Reduction of disulfide bonds within lysosomes is a key step in antigen processing. J. Immunol. 147 (1991), 4054–4059.
134. Jensen, P.E., Antigen unfolding and disulfide reduction in antigen presenting cells. Semin. Immunol. 7 (1995), 347–353.
135. Hastings, K.T., Cresswell, P., Disulfide reduction in the endocytic pathway: immunological functions of gamma-interferon-inducible lysosomal thiol reductase. Antioxid. Redox Signal. 15 (2011), 657–668.
136. West, L.C., Cresswell, P., Expanding roles for GILT in immunity. Curr. Opin. Immunol. 25 (2013), 103–108.
137. Li, P., Luo, Z., Liu, P., Gao, N., Zhang, Y., Pan, H., Liu, L., Wang, C., Cai, L., Ma, Y., Bioreducible alginate-poly(ethylenimine) nanogels as an antigen-delivery system robustly enhance vaccine-elicited humoral and cellular immune responses. J. Control. Release 168 (2013), 271–279.
138. Karimi, M., Eslami, M., Sahandi-Zangabad, P., Mirab, F., Farajisafiloo, N., Shafaei, Z., Ghosh, D., Bozorgomid, M., Dashkhaneh, F., Hamblin, M.R., pH-Sensitive stimulus-responsive nanocarriers for targeted delivery of therapeutic agents. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 8 (2016), 696–716.
139. Kanamala, M., Wilson, W.R., Yang, M., Palmer, B.D., Wu, Z., Mechanisms and biomaterials in pH-responsive tumour targeted drug delivery: a review. Biomaterials 85 (2016), 152–167.
140. Colson, Y.L., Grinstaff, M.W., Biologically responsive polymeric nanoparticles for drug delivery. Adv. Mater. 24 (2012), 3878–3886.
141. Molina, M., Asadian-Birjand, M., Balach, J., Bergueiro, J., Miceli, E., Calderon, M., Stimuli-responsive nanogel composites and their application in nanomedicine. Chem. Soc. Rev. 44 (2015), 6161–6186.
142. Zeng, Z., She, Y., Peng, Z., Wei, J., He, X., Enzyme-mediated in situ formation of pH-sensitive nanogels for proteins delivery. RSC Adv. 6 (2016), 8032–8042.
143. Morimoto, N., Hirano, S., Takahashi, H., Loethen, S., Thompson, D.H., Akiyoshi, K., Self-assembled pH-sensitive cholesteryl pullulan nanogel as a protein delivery vehicle. Biomacromolecules 14 (2013), 56–63.
144. Yan, M., Du, J., Gu, Z., Liang, M., Hu, Y., Zhang, W., Priceman, S., Wu, L., Zhou, Z.H., Liu, Z., Segura, T., Tang, Y., Lu, Y., A novel intracellular protein delivery platform based on single-protein nanocapsules. Nat. Nanotechnol. 5 (2010), 48–53.
145. Shi, L., Khondee, S., Linz, T.H., Berkland, C., Poly(N-vinylformamide) nanogels capable of pH-sensitive protein release. Macromolecules 41 (2008), 6546–6554.
146. Molla, M.R., Marcinko, T., Prasad, P., Deming, D., Garman, S.C., Thayumanavan, S., Unlocking a caged lysosomal protein from a polymeric nanogel with a pH trigger. Biomacromolecules 15 (2014), 4046–4053.
147. Ahmed, M., Narain, R., Intracellular delivery of DNA and enzyme in active form using degradable carbohydrate-based nanogels. Mol. Pharm. 9 (2012), 3160–3170.
148. Oishi, M., Hayashi, H., Itaka, K., Kataoka, K., Nagasaki, Y., pH-Responsive PEGylated nanogels as targetable and low invasive endosomolytic agents to induce the enhanced transfection efficiency of nonviral gene vectors. Colloid Polym. Sci. 285 (2007), 1055–1060.
149. Fleige, E., Quadir, M.A., Haag, R., Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: concepts and applications. Adv. Drug Deliv. Rev. 64 (2012), 866–884.
150. Mura, S., Nicolas, J., Couvreur, P., Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 12 (2013), 991–1003.
151. Lungwitz, U., Breunig, M., Blunk, T., Göpferich, A., Polyethylenimine-based non-viral gene delivery systems. Eur. J. Pharm. Biopharm. 60 (2005), 247–266.
152. Boussif, O., Lezoualc'h, F., Zanta, M.A., Mergny, M.D., Scherman, D., Demeneix, B., Behr, J.P., A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. 92 (1995), 7297–7301.
153. Godbey, W.T., Wu, K.K., Mikos, A.G., Poly(ethylenimine) and its role in gene delivery. J. Control. Release 60 (1999), 149–160.
154. Kim, C., Lee, Y., Lee, S.H., Kim, J.S., Jeong, J.H., Park, T.G., Self-crosslinked polyethylenimine nanogels for enhanced intracellular delivery of siRNA. Macromol. Res. 19 (2011), 166–171.
155. Khaled, S.Z., Cevenini, A., Yazdi, I.K., Parodi, A., Evangelopoulos, M., Corbo, C., Scaria, S., Hu, Y., Haddix, S.G., Corradetti, B., Salvatore, F., Tasciotti, E., One-pot synthesis of pH-responsive hybrid nanogel particles for the intracellular delivery of small interfering RNA. Biomaterials 87 (2016), 57–68.
156. Zhang, X., Zhang, K., Haag, R., Multi-stage, charge conversional, stimuli-responsive nanogels for therapeutic protein delivery. Biomater. Sci. 3 (2015), 1487–1496.
157. Li, Y., Yang, J., Xu, B., Gao, F., Wang, W., Liu, W., Enhanced therapeutic siRNA to tumor cells by a pH-sensitive agmatine–chitosan bioconjugate. ACS Appl. Mater. Interfaces 7 (2015), 8114–8124.
158. Ferrara, N., Gerber, H.-P., LeCouter, J., The biology of VEGF and its receptors. Nat. Med. 9 (2003), 669–676.
159. Drake, C.G., Lipson, E.J., Brahmer, J.R., Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat. Rev. Clin. Oncol. 11 (2014), 24–37.
160. Blattman, J.N., Greenberg, P.D., Cancer immunotherapy: a treatment for the masses. Science 305 (2004), 200–205.
161. Butterfield, L.H., Cancer vaccines. BMJ, 350, 2015, h988.
162. Burgdorf, S., Kautz, A., Böhnert, V., Knolle, P.A., Kurts, C., Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316 (2007), 612–616.
163. Vyas, J.M., Van der Veen, A.G., Ploegh, H.L., The known unknowns of antigen processing and presentation. Nat. Rev. Immunol. 8 (2008), 607–618.
164. Hu, Y., Litwin, T., Nagaraja, A.R., Kwong, B., Katz, J., Watson, N., Irvine, D.J., Cytosolic delivery of membrane-impermeable molecules in dendritic cells using ph-responsive core–shell nanoparticles. Nano Lett. 7 (2007), 3056–3064.
165. Wang, C., Li, P., Liu, L., Pan, H., Li, H., Cai, L., Ma, Y., Self-adjuvanted nanovaccine for cancer immunotherapy: role of lysosomal rupture-induced ROS in MHC class I antigen presentation. Biomaterials 79 (2016), 88–100.
166. Gialeli, C., Theocharis, A.D., Karamanos, N.K., Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278 (2011), 16–27.
167. Jacob, M.P., Extracellular matrix remodeling and matrix metalloproteinases in the vascular wall during aging and in pathological conditions. Biomed. Pharmacother. 57 (2003), 195–202.
168. Gurtner, G.C., Werner, S., Barrandon, Y., Longaker, M.T., Wound repair and regeneration. Nature 453 (2008), 314–321.
169. Das, S.K., Hoefler, G., The role of triglyceride lipases in cancer associated cachexia. Trends Mol. Med. 19 (2013), 292–301.
170. McAtee, C.O., Barycki, J.J., Simpson, M.A., Emerging roles for hyaluronidase in cancer metastasis and therapy. Adv. Cancer Res. 123 (2014), 1–34.
171. Shiomi, T., Lemaître, V., D'Armiento, J., Okada, Y., Matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs in non-neoplastic diseases. Pathol. Int. 60 (2010), 477–496.
172. Roth, D., Piekarek, M., Paulsson, M., Christ, H., Bloch, W., Krieg, T., Davidson, J.M., Eming, S.A., Plasmin modulates vascular endothelial growth factor-a-mediated angiogenesis during wound repair. Am. J. Pathol. 168 (2006), 670–684.
173. Wen, J., Anderson, S.M., Du, J., Yan, M., Wang, J., Shen, M., Lu, Y., Segura, T., Controlled protein delivery based on enzyme-responsive nanocapsules. Adv. Mater. 23 (2011), 4549–4553.
174. Zhu, S., Nih, L., Carmichael, S.T., Lu, Y., Segura, T., Enzyme-responsive delivery of multiple proteins with spatiotemporal control. Adv. Mater. 27 (2015), 3620–3625.
175. Bernardos, A., Mondragón, L., Aznar, E., Marcos, M.D., Martínez-Máñez, R., Sancenón, F., Soto, J., Barat, J.M., Pérez-Payá, E., Guillem, C., Amorós, P., Enzyme-responsive intracellular controlled release using nanometric silica mesoporous supports capped with “saccharides”. ACS Nano 4 (2010), 6353–6368.
176. Lee, J.S., Groothuis, T., Cusan, C., Mink, D., Feijen, J., Lysosomally cleavable peptide-containing polymersomes modified with anti-EGFR antibody for systemic cancer chemotherapy. Biomaterials 32 (2011), 9144–9153.
177. Biswas, A., Joo, K.-I., Liu, J., Zhao, M., Fan, G., Wang, P., Gu, Z., Tang, Y., Endoprotease-mediated intracellular protein delivery using nanocapsules. ACS Nano 5 (2011), 1385–1394.