Abstract
The potential of oligonucleotides is exceptional in therapeutics because of their high safety, potency, and specificity compared to conventional therapeutic agents. However, many obstacles, such as low in vivo stability and poor cellular uptake, have hampered their clinical success. Use of polymeric carriers can be an effective approach for overcoming the biological barriers and thereby maximizing the therapeutic efficacy of the oligonucleotides due to the availability of highly tunable synthesis and functional modification of various polymers. As loaded in the polymeric carriers, the therapeutic oligonucleotides, such as antisense oligonucleotides, small interfering RNAs, microRNAs, and even messenger RNAs, become nuclease-resistant by bypassing renal filtration and can be efficiently internalized into disease cells. In this review, we introduced a variety of systematic combinations between the therapeutic oligonucleotides and the synthetic polymers, including the uses of highly functionalized polymers responding to a wide range of endogenous and exogenous stimuli for spatiotemporal control of oligonucleotide release. We also presented intriguing characteristics of oligonucleotides suitable for targeted therapy and immunotherapy, which can be fully supported by versatile polymeric carriers.
Keywords: nucleic acid, gene delivery, polymeric carrier, stimuli-responsive system, immunotherapy
Footnotes
Acknowledgment: This work was supported by the National Research Foundation of Korea (NRF) grant [NRF-2017R1C1B3012050], and figures were prepared using BioRender. Com for scientific illustrations.
Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
These authors equally contributed to this work.
References
- (1).Walls A C, Park Y-J, Tortorici M A, Wall A, McGuire A T, Veesler D. Cell. 2020;181:281. doi: 10.1016/j.cell.2020.02.058. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (2).Wallace D C. Annu. Rev. Genet. 2005;39:359. doi: 10.1146/annurev.genet.39.110304.095751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (3).Blauwkamp T A, Thair S, Rosen M J, Blair L, Lindner M S, Vilfan I D, Kawli T, Christians F C, Venkatasubrahmanyam S, Wall G D. Nat. Microbiol. 2019;4:663. doi: 10.1038/s41564-018-0349-6. [DOI] [PubMed] [Google Scholar]
- (4).Chapman S J, Hill A V S. Nat. Rev. Genet. 2012;13:175. doi: 10.1038/nrg3114. [DOI] [PubMed] [Google Scholar]
- (5).Stephenson M L, Zamecnik P C. Proc. Natl. Acad. Sci. 1978;75:285. doi: 10.1073/pnas.75.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (6).Nishiyama N, Kataoka K. Pharmacol. Ther. 2006;112:630. doi: 10.1016/j.pharmthera.2006.05.006. [DOI] [PubMed] [Google Scholar]
- (7).Tsui N B, Ng E K, Lo Y D. Clin. Chem. 2002;48:1647. doi: 10.1093/clinchem/48.10.1647. [DOI] [PubMed] [Google Scholar]
- (8).Iversen F, Yang C, Dagnæs-Hansen F, Schaffert D H, Kjems J, Gao S. Theranostics. 2013;3:201. doi: 10.7150/thno.5743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (9).Panyam J, Labhasetwar V. Adv. Drug Deliv. Rev. 2003;55:329. doi: 10.1016/S0169-409X(02)00228-4. [DOI] [PubMed] [Google Scholar]
- (10).Cabral H, Miyata K, Osada K, Kataoka K. Chem. Rev. 2018;118:6844. doi: 10.1021/acs.chemrev.8b00199. [DOI] [PubMed] [Google Scholar]
- (11).Roberts T C, Langer R, Wood M J A. Nat. Rev. Drug Discov. 2020;19:673. doi: 10.1038/s41573-020-0075-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (12).Luther D C, Huang R, Jeon T, Zhang X, Lee Y-W, Nagaraj H, Rotello V M. Adv. Drug Deliv. Rev. 2020;156:188. doi: 10.1016/j.addr.2020.06.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (13).Cutler J I, Auyeung E, Mirkin C A. J. Am. Chem. Soc. 2012;134:1376. doi: 10.1021/ja209351u. [DOI] [PubMed] [Google Scholar]
- (14).Thambi T, Li Y, Lee D S. J. Control. Release. 2017;267:57. doi: 10.1016/j.jconrel.2017.08.006. [DOI] [PubMed] [Google Scholar]
- (15).Park H, Lee K Y, Lee S J, Park K E, Park W H. Macromol. Res. 2007;15:238. doi: 10.1007/BF03218782. [DOI] [Google Scholar]
- (16).Ashraf S, Park H-K, Park H, Lee S-H. Macromol. Res. 2016;24:297. doi: 10.1007/s13233-016-4052-2. [DOI] [Google Scholar]
- (17).Kumari A, Yadav S K, Yadav S C. Colloids Surf. B. 2010;75:1. doi: 10.1016/j.colsurfb.2009.09.001. [DOI] [PubMed] [Google Scholar]
- (18).Alfei S, Castellaro S. Macromol. Res. 2017;25:1172. doi: 10.1007/s13233-017-5160-3. [DOI] [Google Scholar]
- (19).Kim J H, Oh Y T, Lee K S, Yun J M, Park B T, Oh K T. Macromol. Res. 2011;19:453. doi: 10.1007/s13233-011-0502-z. [DOI] [Google Scholar]
- (20).Wang C, Ravi S, Martinez G V, Chinnasamy V, Raulji P, Howell M, Davis Y, Mallela J, Seehra M S, Mohapatra S. J. Control. Release. 2012;163:82. doi: 10.1016/j.jconrel.2012.04.030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (21).H. J. Zhang, X. Zhao, L. J. Chen, C. X. Yang, and X. P. Yan, Talanta, 219, (2020). [DOI] [PubMed]
- (22).Verma I M, Somia N. Nature. 1997;389:239. doi: 10.1038/38410. [DOI] [PubMed] [Google Scholar]
- (23).Boussif O, Lezoualc’h F, Zanta M A, Mergny M D, Scherman D, Demeneix B, Behr J P. Proc. Natl. Acad. Sci. 1995;92:7297. doi: 10.1073/pnas.92.16.7297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (24).Carthew R W, Sontheimer E J. Cell. 2009;136:642. doi: 10.1016/j.cell.2009.01.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (25).Esquela-Kerscher A, Slack F J. Nat. Rev. Cancer. 2006;6:259. doi: 10.1038/nrc1840. [DOI] [PubMed] [Google Scholar]
- (26).Hill A B, Chen M, Chen C-K, Pfeifer B A, Jones C H. Trends Biotechnol. 2016;34:91. doi: 10.1016/j.tibtech.2015.11.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (27).Yoo H, Jo H, Oh S S. Mater. Adv. 2020;1:2663. doi: 10.1039/D0MA00639D. [DOI] [Google Scholar]
- (28).Liu J, Cao Z, Lu Y. Chem. Rev. 2009;109:1948. doi: 10.1021/cr030183i. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (29).Ellington A D, Szostak J W. Nature. 1990;346:818. doi: 10.1038/346818a0. [DOI] [PubMed] [Google Scholar]
- (30).Park S V, Yang J-S, Jo H, Kang B, Oh S S, Jung G Y. Biotechnol. Adv. 2019;37:107452. doi: 10.1016/j.biotechadv.2019.107452. [DOI] [PubMed] [Google Scholar]
- (31).Willner I, Shlyahovsky B, Zayats M, Willner B. Chem. Soc. Rev. 2008;37:1153. doi: 10.1039/b718428j. [DOI] [PubMed] [Google Scholar]
- (32).Kim T, Nam K, Kim Y M, Yang K, Roh Y H. ACS Nano. 2021;15:1942. doi: 10.1021/acsnano.0c08905. [DOI] [PubMed] [Google Scholar]
- (33).Mintzer M A, Simanek E E. Chem. Rev. 2009;109:259. doi: 10.1021/cr800409e. [DOI] [PubMed] [Google Scholar]
- (34).Danhier F, Feron O, Préat V. J. Control. Release. 2010;148:135. doi: 10.1016/j.jconrel.2010.08.027. [DOI] [PubMed] [Google Scholar]
- (35).Kessenbrock K, Plaks V, Werb Z. Cell. 2010;141:52. doi: 10.1016/j.cell.2010.03.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (36).Park G, Kang B, Park S V, Lee D, Seung Nucleic Acids Res. 2021;49:4919. doi: 10.1093/nar/gkab285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (37).Setten R L, Rossi J J, Han S-P. Nat. Rev. Drug Discov. 2019;18:421. doi: 10.1038/s41573-019-0017-4. [DOI] [PubMed] [Google Scholar]
- (38).Tsui N B Y, Ng E K O, Lo Y M D. Clin. Chem. 2002;48:1647. doi: 10.1093/clinchem/48.10.1647. [DOI] [PubMed] [Google Scholar]
- (39).Kawabata K, Takakura Y, Hashida M. Pharm. Res. 1995;12:825. doi: 10.1023/A:1016248701505. [DOI] [PubMed] [Google Scholar]
- (40).Moret I, Esteban Peris J, Guillem V M, Benet M, Revert F, Dasí F, Crespo A, Aliño S F. J. Control. Release. 2001;76:169. doi: 10.1016/S0168-3659(01)00415-1. [DOI] [PubMed] [Google Scholar]
- (41).Cho K C, Choi S H, Park T G. Macromol. Res. 2006;14:348. doi: 10.1007/BF03219093. [DOI] [Google Scholar]
- (42).Benjaminsen R V, Mattebjerg M A, Henriksen J R, Moghimi S M, Andresen T L. Mol. Ther. 2013;21:149. doi: 10.1038/mt.2012.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (43).Creixell M, Peppas N A. Nano Today. 2012;7:367. doi: 10.1016/j.nantod.2012.06.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (44).Krishnamachari Y, Salem A K. Adv. Drug Deliv. Rev. 2009;61:205. doi: 10.1016/j.addr.2008.12.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (45).Jung H, Kim S A, Lee E, Mok H. Macromol. Res. 2015;23:449. doi: 10.1007/s13233-015-3060-y. [DOI] [Google Scholar]
- (46).Kang L, Gao Z, Huang W, Jin M, Wang Q. Acta Pharm. Sin. B. 2015;5:169. doi: 10.1016/j.apsb.2015.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (47).Krieg A M. Nat. Rev. Drug Discov. 2006;5:471. doi: 10.1038/nrd2059. [DOI] [PubMed] [Google Scholar]
- (48).Li N, Zhao L, Qi L, Li Z, Luan Y. Prog. Polym. Sci. 2016;58:1. doi: 10.1016/j.progpolymsci.2015.10.009. [DOI] [Google Scholar]
- (49).Wang Y, Gao S, Ye W-H, Yoon H S, Yang Y-Y. Nat. Mater. 2006;5:791. doi: 10.1038/nmat1737. [DOI] [PubMed] [Google Scholar]
- (50).Sun M, Wang K, Oupický D. Adv. Healthc. Mater. 2018;7:1701070. doi: 10.1002/adhm.201701070. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (51).Gao Y, Wei M, Li X, Xu W, Ahiabu A, Perdiz J, Liu Z, Serpe M J. Macromol. Res. 2017;25:513. doi: 10.1007/s13233-017-5088-7. [DOI] [Google Scholar]
- (52).Gerweck L E, Seetharaman K. Cancer Res. 1996;56:1194. [PubMed] [Google Scholar]
- (53).Wang F, Lu C-H, Willner I. Chem. Rev. 2014;114:2881. doi: 10.1021/cr400354z. [DOI] [PubMed] [Google Scholar]
- (54).Kang B, Park S V, Soh H T, Oh S S. ACS Sens. 2019;4:2802. doi: 10.1021/acssensors.9b01503. [DOI] [PubMed] [Google Scholar]
- (55).Cho M, Soo Oh S, Nie J, Stewart R, Eisenstein M, Chambers J, Marth J D, Walker F, Thomson J A, Soh H T. Proc. Natl. Acad. Sci. 2013;110:18460. doi: 10.1073/pnas.1315866110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (56).Keefe A D, Pai S, Ellington A. Nat. Rev. Drug Discov. 2010;9:537. doi: 10.1038/nrd3141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (57).Zhuang Y, Deng H, Su Y, He L, Wang R, Tong G, He D, Zhu X. Biomacromolecules. 2016;17:2050. doi: 10.1021/acs.biomac.6b00262. [DOI] [PubMed] [Google Scholar]
- (58).Maruyama A. Adv. Drug Deliv. Rev. 2001;52:227. doi: 10.1016/S0169-409X(01)00208-3. [DOI] [PubMed] [Google Scholar]
- (59).Kwak M, Herrmann A. Angew. Chem. Int. Ed. 2010;49:8574. doi: 10.1002/anie.200906820. [DOI] [PubMed] [Google Scholar]
- (60).S. M. Hammond, A. Aartsma-Rus, S. Alves, S. E. Borgos, R. A. M. Buijsen, R. W. J. Collin, G. Covello, M. A. Denti, L. R. Desviat, L. Echevarría, C. Foged, G. Gaina, A. Garanto, A. T. Goyenvalle, M. Guzowska, I. Holod-nuka, D. R. Jones, S. Krause, T. Lehto, M. Montolio, W. Van Roon-Mom, and V. Arechavala-Gomeza, EMBO Mol. Med., 13 (2021). [DOI] [PMC free article] [PubMed]
- (61).Yin H, Kanasty R L, Eltoukhy A A, Vegas A J, Dorkin J R, Anderson D G. Nat. Rev. Genet. 2014;15:541. doi: 10.1038/nrg3763. [DOI] [PubMed] [Google Scholar]
- (62).Lächelt U, Wagner E. Chem. Rev. 2015;115:11043. doi: 10.1021/cr5006793. [DOI] [PubMed] [Google Scholar]
- (63).Dowdy S F. Nat. Biotechnol. 2017;35:222. doi: 10.1038/nbt.3802. [DOI] [PubMed] [Google Scholar]
- (64).Piotrowski-Daspit A S, Kauffman A C, Bracaglia L G, Saltzman W M. Adv. Drug Deliv. Rev. 2020;156:119. doi: 10.1016/j.addr.2020.06.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (65).Zamecnik P C, Stephenson M L. Proc. Natl. Acad. Sci. 1978;75:280. doi: 10.1073/pnas.75.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (66).Watts J K, Corey D R. J. Pathol. 2012;226:365. doi: 10.1002/path.2993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (67).Bennett C F. Annu. Rev. Med. 2019;70:307. doi: 10.1146/annurev-med-041217-010829. [DOI] [PubMed] [Google Scholar]
- (68).Chirila T V, Rakoczy P E, Garrett K L, Lou X, Constable I J. Biomaterials. 2002;23:321. doi: 10.1016/S0142-9612(01)00125-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (69).Juliano R L. Nucleic Acids Res. 2016;44:6518. doi: 10.1093/nar/gkw236. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (70).Merdan T, KopečEk J, Kissel T. Adv. Drug Deliv. Rev. 2002;54:715. doi: 10.1016/S0169-409X(02)00046-7. [DOI] [PubMed] [Google Scholar]
- (71).Fattal E, Barratt G. Br. J. Pharmacol. 2009;157:179. doi: 10.1111/j.1476-5381.2009.00148.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (72).De Rosa G, Quaglia F, Bochot A, Ungaro F, Fattal E. Biomacromolecules. 2003;4:529. doi: 10.1021/bm025684c. [DOI] [PubMed] [Google Scholar]
- (73).Dheur S, Dias N, Van Aerschot A, Herdewijn P, Bettinger T, Remy J-S, Hélène C, Saison-Behmoaras E T. Antisense Nucleic Acid Drug Dev. 1999;9:515. doi: 10.1089/oli.1.1999.9.515. [DOI] [PubMed] [Google Scholar]
- (74).Falzarano M S, Passarelli C, Ferlini A. Nucleic Acid Ther. 2014;24:87. doi: 10.1089/nat.2013.0450. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (75).Akhtar S, Hughes M D, Khan A, Bibby M, Hussain M, Nawaz Q, Double J, Sayyed P. Adv. Drug Deliv. Rev. 2000;44:3. doi: 10.1016/S0169-409X(00)00080-6. [DOI] [PubMed] [Google Scholar]
- (76).Jain R A. Biomaterials. 2000;21:2475. doi: 10.1016/S0142-9612(00)00115-0. [DOI] [PubMed] [Google Scholar]
- (77).Lewis K J, Irwin W J, Akhtar S. J. Drug Target. 1998;5:291. doi: 10.3109/10611869808995882. [DOI] [PubMed] [Google Scholar]
- (78).Dorsett Y, Tuschl T. Nat. Rev. Drug Discov. 2004;3:318. doi: 10.1038/nrd1345. [DOI] [PubMed] [Google Scholar]
- (79).Whitehead K A, Langer R, Anderson D G. Nat. Rev. Drug Discov. 2009;8:129. doi: 10.1038/nrd2742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (80).Bertrand J-R, Pottier M, Vekris A, Opolon P, Maksimenko A, Malvy C. Biochem. Biophys. Res. Commun. 2002;296:1000. doi: 10.1016/S0006-291X(02)02013-2. [DOI] [PubMed] [Google Scholar]
- (81).Kim D H, Rossi J J. Nat. Rev. Genet. 2007;8:173. doi: 10.1038/nrg2006. [DOI] [PubMed] [Google Scholar]
- (82).Tatiparti K, Sau S, Kashaw S, Iyer A. Nanomaterials. 2017;7:77. doi: 10.3390/nano7040077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (83).Alexis F, Pridgen E, Molnar L K, Farokhzad O C. Mol. Pharm. 2008;5:505. doi: 10.1021/mp800051m. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (84).Mao S, Neu M, Germershaus O, Merkel O, Sitterberg J, Bakowsky U, Kissel T. Bioconjug. Chem. 2006;17:1209. doi: 10.1021/bc060129j. [DOI] [PubMed] [Google Scholar]
- (85).Walker G F, Fella C, Pelisek J, Fahrmeir J, Boeckle S, Ogris M, Wagner E. Mol. Ther. 2005;11:418. doi: 10.1016/j.ymthe.2004.11.006. [DOI] [PubMed] [Google Scholar]
- (86).Hoon Jeong J, Christensen L V, Yockman J W, Zhong Z, Engbersen J F J, Jong Kim W, Feijen J, Wan Kim S. Biomaterials. 2007;28:1912. doi: 10.1016/j.biomaterials.2006.12.019. [DOI] [PubMed] [Google Scholar]
- (87).Lam J K W, Chow M Y T, Zhang Y, Leung S W S. Mol. Ther. Nucleic Acids. 2015;4:e252. doi: 10.1038/mtna.2015.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (88).Friedman R C, Farh K K H, Burge C B, Bartel D P. Genome Res. 2008;19:92. doi: 10.1101/gr.082701.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (89).Calin G A, Sevignani C, Dumitru C D, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce C M. Proc. Natl. Acad. Sci. 2004;101:2999. doi: 10.1073/pnas.0307323101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (90).Wang H, Jiang Y, Peng H, Chen Y, Zhu P, Huang Y. Adv. Drug Deliv. Rev. 2015;81:142. doi: 10.1016/j.addr.2014.10.031. [DOI] [PubMed] [Google Scholar]
- (91).Ibrahim A F, Weirauch U, Thomas M, Grünweller A, Hartmann R K, Aigner A. Cancer Res. 2011;71:5214. doi: 10.1158/0008-5472.CAN-10-4645. [DOI] [PubMed] [Google Scholar]
- (92).Kowalski P S, Rudra A, Miao L, Anderson D G. Mol. Ther. 2019;27:710. doi: 10.1016/j.ymthe.2019.02.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (93).Lorenz C, Fotin-Mleczek M, Roth G, Becker C, Dam T C, Verdurmen W P R, Brock R, Probst J, Schlake T. RNA Biol. 2011;8:627. doi: 10.4161/rna.8.4.15394. [DOI] [PubMed] [Google Scholar]
- (94).Cheng C, Convertine A J, Stayton P S, Bryers J D. Biomaterials. 2012;33:6868. doi: 10.1016/j.biomaterials.2012.06.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (95).Y. Wang, Z. Zhang, J. Luo, X. Han, Y. Wei, and X. Wei, Mol. Cancer, 20 (2021). [DOI] [PMC free article] [PubMed]
- (96).Yin H, Kauffman K J, Anderson D G. Nat. Rev. Drug Discov. 2017;16:387. doi: 10.1038/nrd.2016.280. [DOI] [PubMed] [Google Scholar]
- (97).Capasso Palmiero U, Kaczmarek J C, Fenton O S, Anderson D G. Adv. Healthc. Mater. 2018;7:1800249. doi: 10.1002/adhm.201800249. [DOI] [PubMed] [Google Scholar]
- (98).Cordeiro R A, Serra A, Coelho J F J, Faneca H. J. Control. Release. 2019;310:155. doi: 10.1016/j.jconrel.2019.08.024. [DOI] [PubMed] [Google Scholar]
- (99).Patton J S, Byron P R. Nat. Rev. Drug Discov. 2007;6:67. doi: 10.1038/nrd2153. [DOI] [PubMed] [Google Scholar]
- (100).Densmore C L, Orson F M, Xu B, Kinsey B M, Waldrep J C, Hua P, Bhogal B, Knight V. Mol. Ther. 2000;1:180. doi: 10.1006/mthe.1999.0021. [DOI] [PubMed] [Google Scholar]
- (101).Patel A K, Kaczmarek J C, Bose S, Kauffman K J, Mir F, Heartlein M W, Derosa F, Langer R, Anderson D G. Adv. Mater. 2019;31:1805116. doi: 10.1002/adma.201805116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (102).Jiang Y, Gaudin A, Zhang J, Agarwal T, Song E, Kauffman A C, Tietjen G T, Wang Y, Jiang Z, Cheng C J, Saltzman W M. Biomaterials. 2018;176:122. doi: 10.1016/j.biomaterials.2018.05.043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (103).Zhou J, Liu J, Cheng C J, Patel T R, Weller C E, Piepmeier J M, Jiang Z, Saltzman W M. Nat. Mater. 2012;11:82. doi: 10.1038/nmat3187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (104).Li Y, Gao J, Zhang C, Cao Z, Cheng D, Liu J, Shuai X. Top. Curr. Chem. 2017;375:27. doi: 10.1007/s41061-017-0119-6. [DOI] [PubMed] [Google Scholar]
- (105).Bus T, Traeger A, Schubert U S. J. Mater. Chem. B. 2018;6:6904. doi: 10.1039/C8TB00967H. [DOI] [PubMed] [Google Scholar]
- (106).Takemoto H, Miyata K, Nishiyama N, Kataoka K. Adv. Genet. 2014;88:289. doi: 10.1016/B978-0-12-800148-6.00010-9. [DOI] [PubMed] [Google Scholar]
- (107).Liu J, Huang Y, Kumar A, Tan A, Jin S, Mozhi A, Liang X-J. Biotechnol. Adv. 2014;32:693. doi: 10.1016/j.biotechadv.2013.11.009. [DOI] [PubMed] [Google Scholar]
- (108).Y.-B. Hu, E. B. Dammer, R.-J. Ren, and G. Wang, Transl. Neurodegener., 4 (2015). [DOI] [PMC free article] [PubMed]
- (109).Suk J S, Xu Q, Kim N, Hanes J, Ensign L M. Adv. Drug Deliv. Rev. 2016;99:28. doi: 10.1016/j.addr.2015.09.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (110).Xu C-F, Zhang H-B, Sun C-Y, Liu Y, Shen S, Yang X-Z, Zhu Y-H, Wang J. Biomaterials. 2016;88:48. doi: 10.1016/j.biomaterials.2016.02.031. [DOI] [PubMed] [Google Scholar]
- (111).Degors I M S, Wang C, Rehman Z U, Zuhorn I S. Acc. Chem. Res. 2019;52:1750. doi: 10.1021/acs.accounts.9b00177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (112).Itaka K, Ishii T, Hasegawa Y, Kataoka K. Biomaterials. 2010;31:3707. doi: 10.1016/j.biomaterials.2009.11.072. [DOI] [PubMed] [Google Scholar]
- (113).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. Adv. Mater. 2014;26:607. doi: 10.1002/adma.201303520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (114).Mi P. Theranostics. 2020;10:4557. doi: 10.7150/thno.38069. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (115).Cheng R, Feng F, Meng F, Deng C, Feijen J, Zhong Z. J. Control. Release. 2011;152:2. doi: 10.1016/j.jconrel.2011.01.030. [DOI] [PubMed] [Google Scholar]
- (116).Gerald, Tamas Cell. 2015;163:560. doi: 10.1016/j.cell.2015.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (117).Chang Y, Yang K, Wei P, Huang S, Pei Y, Zhao W, Pei Z. Angew. Chem. Int. Ed. 2014;53:13126. doi: 10.1002/anie.201407272. [DOI] [PubMed] [Google Scholar]
- (118).Ganta S, Devalapally H, Shahiwala A, Amiji M. J. Control. Release. 2008;126:187. doi: 10.1016/j.jconrel.2007.12.017. [DOI] [PubMed] [Google Scholar]
- (119).Choi S, Lee K-D. J. Control. Release. 2008;131:70. doi: 10.1016/j.jconrel.2008.07.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (120).Kam N W S, Liu Z, Dai H. J. Am. Chem. Soc. 2005;127:12492. doi: 10.1021/ja053962k. [DOI] [PubMed] [Google Scholar]
- (121).Matsumoto S, Christie R J, Nishiyama N, Miyata K, Ishii A, Oba M, Koyama H, Yamasaki Y, Kataoka K. Biomacromolecules. 2009;10:119. doi: 10.1021/bm800985e. [DOI] [PubMed] [Google Scholar]
- (122).Jiang H-L, Islam M A, Xing L, Firdous J, Cao W, He Y-J, Zhu Y, Cho K-H, Li H-S, Cho C-S. Top. Curr. Chem. 2017;375:34. doi: 10.1007/s41061-017-0124-9. [DOI] [PubMed] [Google Scholar]
- (123).Peng Q, Zhong Z, Zhuo R. Bioconjug. Chem. 2008;19:499. doi: 10.1021/bc7003236. [DOI] [PubMed] [Google Scholar]
- (124).Li Y, Maciel D, Rodrigues J, Shi X, Tomás H. Chem. Rev. 2015;115:8564. doi: 10.1021/cr500131f. [DOI] [PubMed] [Google Scholar]
- (125).Nam K, Park J W, Bark H, Han J, Nah J-W, Jang M-K, Kim S W. Macromol. Res. 2014;22:370. doi: 10.1007/s13233-014-2052-7. [DOI] [Google Scholar]
- (126).Kawagishi H, Finkel T. Nat. Med. 2014;20:711. doi: 10.1038/nm.3625. [DOI] [PubMed] [Google Scholar]
- (127).Mittal M, Siddiqui M R, Tran K, Reddy S P, Malik A B. Antioxid. Redox Signal. 2014;20:1126. doi: 10.1089/ars.2012.5149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (128).Burgoyne J R, Oka S-I, Ale-Agha N, Eaton P. Antioxid. Redox Signal. 2013;18:1042. doi: 10.1089/ars.2012.4817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (129).Shim M S, Xia Y. Angew. Chem. Int. Ed. 2013;52:6926. doi: 10.1002/anie.201209633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (130).Wilson D S, Dalmasso G, Wang L, Sitaraman S V, Merlin D, Murthy N. Nat. Mater. 2010;9:923. doi: 10.1038/nmat2859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (131).Xu X, Saw P E, Tao W, Li Y, Ji X, Bhasin S, Liu Y, Ayyash D, Rasmussen J, Huo M, Shi J, Farokhzad O C. Adv. Mater. 2017;29:1700141. doi: 10.1002/adma.201700141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (132).Li Y, Bai H, Wang H, Shen Y, Tang G, Ping Y. Nanoscale. 2018;10:203. doi: 10.1039/C7NR06689A. [DOI] [PubMed] [Google Scholar]
- (133).De La Rica R, Aili D, Stevens M M. Adv. Drug Deliv. Rev. 2012;64:967. doi: 10.1016/j.addr.2012.01.002. [DOI] [PubMed] [Google Scholar]
- (134).Hu J, Zhang G, Liu S. Chem. Soc. Rev. 2012;41:5933. doi: 10.1039/c2cs35103j. [DOI] [PubMed] [Google Scholar]
- (135).Yingyuad P, Mével M, Prata C, Furegati S, Kontogiorgis C, Thanou M, Miller A D. Bioconjug. Chem. 2013;24:343. doi: 10.1021/bc300419g. [DOI] [PubMed] [Google Scholar]
- (136).Wang C, Chen Q, Wang Z, Zhang X. Angew. Chem. Int. Ed. 2010;49:8612. doi: 10.1002/anie.201004253. [DOI] [PubMed] [Google Scholar]
- (137).Hu Q, Katti P S, Gu Z. Nanoscale. 2014;6:12273. doi: 10.1039/C4NR04249B. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (138).Wang H-X, Yang X-Z, Sun C-Y, Mao C-Q, Zhu Y-H, Wang J. Biomaterials. 2014;35:7622. doi: 10.1016/j.biomaterials.2014.05.050. [DOI] [PubMed] [Google Scholar]
- (139).Bergers G, Brekken R, McMahon G, Vu T H, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D. Nat. Cell Biol. 2000;2:737. doi: 10.1038/35036374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (140).Yong V W, Power C, Forsyth P, Edwards D R. Nat. Rev. Neurosci. 2001;2:502. doi: 10.1038/35081571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (141).Qiu N, Liu X, Zhong Y, Zhou Z, Piao Y, Miao L, Zhang Q, Tang J, Huang L, Shen Y. Adv. Mater. 2016;28:10613. doi: 10.1002/adma.201603095. [DOI] [PubMed] [Google Scholar]
- (142).Raza A, Hayat U, Rasheed T, Bilal M, Iqbal H M N. J. Mater. Res. Technol. 2019;8:1497. doi: 10.1016/j.jmrt.2018.03.007. [DOI] [Google Scholar]
- (143).Kono K, Ozawa T, Yoshida T, Ozaki F, Ishizaka Y, Maruyama K, Kojima C, Harada A, Aoshima S. Biomaterials. 2010;31:7096. doi: 10.1016/j.biomaterials.2010.05.045. [DOI] [PubMed] [Google Scholar]
- (144).Karino T, Koga S, Maeta M. Jpn. J. Surg. 1988;18:276. doi: 10.1007/BF02471444. [DOI] [PubMed] [Google Scholar]
- (145).Song C W, Park H J, Lee C K, Griffin R. Int. J. Hyperth. 2005;21:761. doi: 10.1080/02656730500204487. [DOI] [PubMed] [Google Scholar]
- (146).Kong G, Anyarambhatla G, Petros W P, Braun R D, Colvin O M, Needham D, Dewhirst M W. Cancer Res. 2000;60:6950. [PubMed] [Google Scholar]
- (147).Lindner L H, Eichhorn M E, Eibl H, Teichert N, Schmitt-Sody M, Issels R D, Dellian M. Clin. Cancer Res. 2004;10:2168. doi: 10.1158/1078-0432.CCR-03-0035. [DOI] [PubMed] [Google Scholar]
- (148).Twaites B R, De Las Heras Alarcón C, Lavigne M, Saulnier A, Pennadam S S, Cunliffe D, Górecki D C, Alexander C. J. Control. Release. 2005;108:472. doi: 10.1016/j.jconrel.2005.08.009. [DOI] [PubMed] [Google Scholar]
- (149).Roy D, Brooks W L A, Sumerlin B S. Chem. Soc. Rev. 2013;42:7214. doi: 10.1039/c3cs35499g. [DOI] [PubMed] [Google Scholar]
- (150).Pasparakis G, Tsitsilianis C. Polymer. 2020;211:123146. doi: 10.1016/j.polymer.2020.123146. [DOI] [Google Scholar]
- (151).Haq M A, Su Y, Wang D. Mater. Sci. Eng. C. 2017;70:842. doi: 10.1016/j.msec.2016.09.081. [DOI] [PubMed] [Google Scholar]
- (152).Seo J-W, Shin U S. Macromol. Res. 2015;23:1073. doi: 10.1007/s13233-015-3143-9. [DOI] [Google Scholar]
- (153).Zintchenko A, Ogris M, Wagner E. Bioconjug. Chem. 2006;17:766. doi: 10.1021/bc050292z. [DOI] [PubMed] [Google Scholar]
- (154).Schwerdt A, Zintchenko A, Concia M, Roesen N, Fisher K, Lindner L H, Issels R, Wagner E, Ogris M. Hum. Gene Ther. 2008;19:1283. doi: 10.1089/hum.2008.064. [DOI] [PubMed] [Google Scholar]
- (155).Cao P, Sun X, Liang Y, Gao X, Li X, Li W, Song Z, Li W, Liang G. Nanomedicine. 2015;10:1585. doi: 10.2217/nnm.15.20. [DOI] [PubMed] [Google Scholar]
- (156).Hernot S, Klibanov A L. Adv. Drug Deliv. Rev. 2008;60:1153. doi: 10.1016/j.addr.2008.03.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (157).Ferrara K, Pollard R, Borden M. Annu. Rev. Biomed. Eng. 2007;9:415. doi: 10.1146/annurev.bioeng.8.061505.095852. [DOI] [PubMed] [Google Scholar]
- (158).Shapiro G, Wong A W, Bez M, Yang F, Tam S, Even L, Sheyn D, Ben-David S, Tawackoli W, Pelled G, Ferrara K W, Gazit D. J. Control. Release. 2016;223:157. doi: 10.1016/j.jconrel.2015.12.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (159).Meng F, Zhong Z, Feijen J. Biomacromolecules. 2009;10:197. doi: 10.1021/bm801127d. [DOI] [PubMed] [Google Scholar]
- (160).Yan N D, Keller W, Scully N M, Lean D R S, Dillon P J. Nature. 1996;381:141. doi: 10.1038/381141a0. [DOI] [Google Scholar]
- (161).Ash C, Dubec M, Donne K, Bashford T. Lasers Med. Sci. 2017;32:1909. doi: 10.1007/s10103-017-2317-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (162).Liu G, Liu W, Dong C-M. Polym Chem. 2013;4:3431. doi: 10.1039/c3py21121e. [DOI] [Google Scholar]
- (163).Shin J, Sung J, Kang M, Xie X, Lee B, Lee K M, White T J, Leal C, Sottos N R, Braun P V, Cahill D G. Proc. Natl. Acad. Sci. 2019;116:5973. doi: 10.1073/pnas.1817082116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (164).Park J Y, Umashankar M, Huh D S. Macromol. Res. 2016;24:350. doi: 10.1007/s13233-016-4046-0. [DOI] [Google Scholar]
- (165).Li Y, Yang J, Sun L, Wang W, Liu W. J. Mater. Chem. B. 2014;2:3868. doi: 10.1039/c4tb00294f. [DOI] [PubMed] [Google Scholar]
- (166).Duan S, Cao D, Li X, Zhu H, Lan M, Tan Z, Song Z, Zhu R, Yin L, Chen Y. Biomaterials Science. 2020;8:290. doi: 10.1039/C9BM01452G. [DOI] [PubMed] [Google Scholar]
- (167).Deng X, Zheng N, Song Z, Yin L, Cheng J. Biomaterials. 2014;35:5006. doi: 10.1016/j.biomaterials.2014.03.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (168).Nalluri S K M, Voskuhl J, Bultema J B, Boekema E J, Ravoo B J. Angew. Chem. Int. Ed. 2011;50:9747. doi: 10.1002/anie.201103707. [DOI] [PubMed] [Google Scholar]
- (169).Shim M S, Kwon Y J. Adv. Drug Deliv. Rev. 2012;64:1046. doi: 10.1016/j.addr.2012.01.018. [DOI] [PubMed] [Google Scholar]
- (170).Shubayev V I, Pisanic T R, Jin S. Adv. Drug Deliv. Rev. 2009;61:467. doi: 10.1016/j.addr.2009.03.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (171).Lo Y-L, Chou H-L, Liao Z-X, Huang S-J, Ke J-H, Liu Y-S, Chiu C-C, Wang L-F. Nanoscale. 2015;7:8554. doi: 10.1039/C5NR01404B. [DOI] [PubMed] [Google Scholar]
- (172).Han X, Xu K, Taratula O, Farsad K. Nanoscale. 2019;11:799. doi: 10.1039/C8NR07769J. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (173).Park T, Jeong J, Kim S. Adv. Drug Deliv. Rev. 2006;58:467. doi: 10.1016/j.addr.2006.03.007. [DOI] [PubMed] [Google Scholar]
- (174).Brannon-Peppas L, Blanchette J O. Adv. Drug Deliv. Rev. 2004;56:1649. doi: 10.1016/j.addr.2004.02.014. [DOI] [PubMed] [Google Scholar]
- (175).Chiu S-J, Ueno N T, Lee R J. J. Control. Release. 2004;97:357. doi: 10.1016/j.jconrel.2004.03.019. [DOI] [PubMed] [Google Scholar]
- (176).Mitra A, Mulholland J, Nan A, McNeill E, Ghandehari H, Line B R. J. Control. Release. 2005;102:191. doi: 10.1016/j.jconrel.2004.09.023. [DOI] [PubMed] [Google Scholar]
- (177).Yang L, Sun H, Liu Y, Hou W, Yang Y, Cai R, Cui C, Zhang P, Pan X, Li X, Li L, Sumerlin B S, Tan W. Angew. Chem. 2018;130:17294. doi: 10.1002/ange.201809753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (178).Mignani S, Shi X, Ceña V, Majoral J-P. Drug Discov. Today. 2020;25:1065. doi: 10.1016/j.drudis.2020.03.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (179).Oh S S, Lee B F, Leibfarth F A, Eisenstein M, Robb M J, Lynd N A, Hawker C J, Soh H T. J. Am. Chem. Soc. 2014;136:15010. doi: 10.1021/ja5079464. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (180).Alibolandi M, Taghdisi S M, Ramezani P, Hosseini Shamili F, Farzad S A, Abnous K, Ramezani M. Int. J. Pharm. 2017;519:352. doi: 10.1016/j.ijpharm.2017.01.044. [DOI] [PubMed] [Google Scholar]
- (181).Sanmamed M F, Chen L. Cell. 2018;175:313. doi: 10.1016/j.cell.2018.09.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (182).Xing L, Zhou T-J, Fan Y-T, He Y-J, Pang T, Cho K-H, Lu J-J, Jiang H-L, Cho C-S. Macromol. Res. 2019;27:215. doi: 10.1007/s13233-019-7042-3. [DOI] [Google Scholar]
- (183).June C H, O’Connor R S, Kawalekar O U, Ghassemi S, Milone M C. Science. 2018;359:1361. doi: 10.1126/science.aar6711. [DOI] [PubMed] [Google Scholar]
- (184).Vollmer J, Krieg A M. Adv. Drug Deliv. Rev. 2009;61:195. doi: 10.1016/j.addr.2008.12.008. [DOI] [PubMed] [Google Scholar]
- (185).Kumar M, Keller B, Makalou N, Sutton R E. Hum. Gene Ther. 2001;12:1893. doi: 10.1089/104303401753153947. [DOI] [PubMed] [Google Scholar]
- (186).Olden B R, Cheng Y, Yu J L, Pun S H. J. Control. Release. 2018;282:140. doi: 10.1016/j.jconrel.2018.02.043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (187).Sharma P, Hu-Lieskovan S, Wargo J A, Ribas A. Cell. 2017;168:707. doi: 10.1016/j.cell.2017.01.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (188).June C H, Sadelain M. N. Engl. J. Med. 2018;379:64. doi: 10.1056/NEJMra1706169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (189).Wilson J T, Keller S, Manganiello M J, Cheng C, Lee C-C, Opara C, Convertine A, Stayton P S. ACS Nano. 2013;7:3912. doi: 10.1021/nn305466z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (190).Kundu A, Nandi S, Nandi A K. Prog. Mater. Sci. 2017;88:136. doi: 10.1016/j.pmatsci.2017.04.001. [DOI] [Google Scholar]
- (191).Mi Y, Hagan C T, Vincent B G, Wang A Z. Adv. Sci. 2019;6:1801847. doi: 10.1002/advs.201801847. [DOI] [PMC free article] [PubMed] [Google Scholar]
- (192).Lv H, Zhang S, Wang B, Cui S, Yan J. J. Control. Release. 2006;114:100. doi: 10.1016/j.jconrel.2006.04.014. [DOI] [PubMed] [Google Scholar]
- (193).Duncan R, Vicent M J. Adv. Drug Deliv. Rev. 2013;65:60. doi: 10.1016/j.addr.2012.08.012. [DOI] [PubMed] [Google Scholar]