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Cited by 261RNA Interference and Gene DeliveryNanoparticle-Based Drug DeliveryImmunotherapy and Immune Responses

Next‐Generation Vaccines: Nanoparticle‐Mediated DNA and mRNA Delivery

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Ho, William, Gao, Mingzhu, Li, Fengqiao, Li, Zhongyu, Zhang, Xue‐Qing, Xu, Xiaoyang·2021·Advanced Healthcare Materials
DOI 10.1002/adhm.202001812PMC PMC7995055
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Abstract

Nucleic acid vaccines are a method of immunization aiming to elicit immune responses akin to live attenuated vaccines. In this method, DNA or messenger RNA (mRNA) sequences are delivered to the body to generate proteins, which mimic disease antigens to stimulate the immune response. Advantages of nucleic acid vaccines include stimulation of both cell‐mediated and humoral immunity, ease of design, rapid adaptability to changing pathogen strains, and customizable multiantigen vaccines. To combat the SARS‐CoV‐2 pandemic, and many other diseases, nucleic acid vaccines appear to be a promising method. However, aid is needed in delivering the fragile DNA/mRNA payload. Many delivery strategies have been developed to elicit effective immune stimulation, yet no nucleic acid vaccine has been FDA‐approved for human use. Nanoparticles (NPs) are one of the top candidates to mediate successful DNA/mRNA vaccine delivery due to their unique properties, including unlimited possibilities for formulations, protective capacity, simultaneous loading, and delivery potential of multiple DNA/mRNA vaccines. This review will summarize the many varieties of novel NP formulations for DNA and mRNA vaccine delivery as well as give the reader a brief synopsis of NP vaccine clinical trials. Finally, the future perspectives and challenges for NP‐mediated nucleic acid vaccines will be explored.

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  • mRNA therapies must be encapsulated into safe, stable, and effective delivery vehicles to preserve the cargo from degradation and prevent immunogenicity.

    “mRNA therapies must be encapsulated into safe, stable, and effective delivery vehicles to preserve the cargo from degradation and prevent immunogenicity.”

    From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [8]

  • The main obstacle to the delivery of mRNA lies in its intrinsic instability and inability to penetrate the cellular lipid bilayer.

    “The main obstacle to the delivery of mRNA lies in its intrinsic instability and inability to penetrate the cellular lipid bilayer.”

    From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [8]

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References 172 · Cited by 261

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  1. C. Zhang, G. Maruggi, H. Shan, J. Li, Front. Immunol. 2019, 10, 594.
  2. H. Bedford, D. Elliman, BMJ 2000, 320, 240.
  3. I. Amanna, M. K. Slifka, Viral Immunol. 2005, 18, 307.
  4. J. Ehreth, Vaccine 2003, 21, 596.
  5. B. Ferraro, M. P. Morrow, N. A. Hutnick, T. H. Shin, C. E. Lucke, D. B. Weiner, Clin. Infect. Dis. 2011, 53, 296.
  6. S. Han, Clin. Exp. Vaccine Res. 2015, 4, 46.
  7. T. T. Le, Z. Andreadakis, A. Kumar, R. G. Roman, S. Tollefsen, M. Saville, S. Mayhew, Nat. Rev. Drug Discovery 2020, 19, 667.
  8. N. Pardi, M. J. Hogan, F. W. Porter, D. Weissman, Nat. Rev. Drug Discovery 2018, 17, 261.
  9. N. Pardi, K. Parkhouse, E. Kirkpatrick, M. McMahon, S. J. Zost, B. L. Mui, Y. K. Tam, K. Karikó, C. J. Barbosa, T. D. Madden, M. J. Hope, F. Krammer, S. E. Hensley, D. Weissman, Nat. Commun. 2018, 9, 3361.
  10. F. Krammer, P. Palese, Nat. Rev. Drug Discovery 2015, 14, 167.
  11. S. A. Hudu, S. H. Shinkafi, U. Shuaibu, Int. J. Pharm. Pharm. Sci. 2016, 8, 19.
  12. M. F. Bachmann, G. T. Jennings, Nat. Rev. Immunol. 2010, 10, 787.
  13. F. R. Vogel, N. Sarver, Clin. Microbiol. Rev. 1995, 8, 406.
  14. R. P. Deering, S. Kommareddy, J. B. Ulmer, L. A. Brito, A. J. Geall, Expert Opin. Drug Delivery 2014, 11, 885.
  15. C. Coban, S. Koyama, F. Takeshita, S. Akira, K. J. Ishii, Hum. Vaccines 2008, 4, 453.
  16. P. A. Krieg, D. Melton, Nucleic Acids Res. 1984, 12, 7057.
  17. T. Schlake, A. Thess, M. Fotin-Mleczek, K.-J. Kallen, RNA Biol. 2012, 9, 1319.
  18. A. S. Espeseth, P. J. Cejas, M. P. Citron, D. Wang, D. J. DiStefano, C. Callahan, G. O. Donnell, J. D. Galli, R. Swoyer, S. Touch, Z. Wen, J. Antonello, L. Zhang, J. A. Flynn, K. S. Cox, D. C. Freed, K. A. Vora, K. Bahl, A. H. Latham, J. S. Smith, M. E. Gindy, G. Ciaramella, D. Hazuda, C. A. Shaw, A. J. Bett, npj Vaccines 2020, 5, 16.
  19. L. Li, N. Petrovsky, Expert Rev. Vaccines 2016, 15, 313.
  20. L. Cheng, P. R. Ziegelhoffer, N.-S. Yang, Proc. Natl. Acad. Sci. USA 1993, 90, 4455.
  21. M. Manthorpe, F. Cornefert-Jensen, J. Hartikka, J. Felgner, A. Run- dell, M. Margalith, V. Dwarki, Hum. Gene Ther. 1993, 4, 419.
  22. S. Wang, D. J. Farfan-Arribas, S. Shen, W. C. Te-hui, A. Hirsch, F. He, S. Lu, Vaccine 2006, 24, 4531.
  23. T. Vanniasinkam, S. Reddy, H. Ertl, Virology 2006, 344, 412.
  24. Z. Wang, N. Day, P. Trifillis, M. Kiledjian, Mol. Cell. Biol. 1999, 19, 4552.
  25. B. R. Anderson, H. Muramatsu, S. R. Nallagatla, P. C. Bevilacqua, L. H. Sansing, D. Weissman, K. Kariko, Nucleic Acids Res. 2010, 38, 5884.
  26. O. Andries, S. Mc Cafferty, S. C. De Smedt, R. Weiss, N. N. Sanders, T. Kitada, J. Controlled Release 2015, 217, 337.
  27. N. Pardi, H. Muramatsu, D. Weissman, K. Karikó, in Synthetic Mes- senger RNA and Cell Metabolism Modulation, (Eds: P. Rabinovich) Springer, New York 2013, p. 29.
  28. J. B. Ulmer, P. W. Mason, A. Geall, C. W. Mandl, Vaccine 2012, 30, 4414.
  29. K. C. McCullough, P. Milona, L. Thomann-Harwood, T. Démoulins, P. Englezou, R. Suter, N. Ruggli, Vaccines 2014, 2, 735.
  30. A. M. Reichmuth, M. A. Oberli, A. Jaklenec, R. Langer, D. Blankschtein, Ther. Delivery 2016, 7, 319.
  31. D. Hobernik, M. Bros, Int. J. Mol. Sci. 2018, 19, 3605.
  32. K. Karikó, H. Muramatsu, F. A. Welsh, J. Ludwig, H. Kato, S. Akira, D. Weissman, Mol. Ther. 2008, 16, 1833.
  33. M. A. Liu, Vaccines 2019, 7, 37.
  34. F. Dieli, Clin. Exp. Immunol. 2003, 134, 178.
  35. D. J. Shedlock, D. B. Weiner, J. Leukocyte Biol. 2000, 68, 793.
  36. A. Porgador, K. R. Irvine, A. Iwasaki, B. H. Barber, N. P. Restifo, R. N. Germain, J. Exp. Med. 1998, 188, 1075.
  37. L. Y. Y. Lee, L. Izzard, A. C. Hurt, Front. Immunol. 2018, 9, 1568.
  38. D. Baxter, Occup. Med. 2007, 57, 552.
  39. S. H. T. Jorritsma, E. J. Gowans, B. Grubor-Bauk, D. K. Wijesundara, Vaccine 2016, 34, 5488.
  40. F. Steinhagen, T. Kinjo, C. Bode, D. M. Klinman, Vaccine 2011, 29, 3341.
  41. A. S. Cordeiro, M. J. Alonso, Pharm. Pat. Anal. 2016, 5, 49.
  42. K. E. Kester, D. G. Heppner Jr, P. Moris, O. Ofori-Anyinam, U. Krzych, N. Tornieporth, D. McKinney, M. Delchambre, C. F. Ocken- house, G. Voss, Vaccine 2014, 32, 6683.
  43. R. H. Behrens, J. P. Cramer, T. Jelinek, H. Shaw, F. von Sonnenburg, D. Wilbraham, T. Weinke, D. J. Bell, E. Asturias, H. L. E. Pauwells, Lancet Infect. Dis. 2014, 14, 197.
  44. J. M. Lynch, D. E. Briles, D. W. Metzger, Infect. Immun. 2003, 71, 4780.
  45. D. J. Glover, H. J. Lipps, D. A. Jans, Nat. Rev. Genet. 2005, 6, 299.
  46. S. Hacein-Bey-Abina, F. L.e Deist, F. Carlier, C. Bouneaud, C. Hue, J.-P. De Villartay, A. J. Thrasher, N. Wulffraat, R. Sorensen, S. Dupuis- Girod, N. Engl. J. Med. 2002, 346, 1185.
  47. K. L. Molnar-Kimber, D. H. Sterman, M. Chang, E. H. Kang, M. El- Bash, M. Lanuti, A. Elshami, K. Gelfand, J. M. Wilson, L. R. Kaiser, Hum. Gene Ther. 1998, 9, 2121.
  48. S. Jenks, J. Natl. Cancer Inst. 2000, 92, 98.
  49. J. Bonadio, E. Smiley, P. Patil, S. Goldstein, Nat. Med. 1999, 5, 753.
  50. T. Ohno, D. Gordon, H. San, V. J. Pompili, M. J. Imperiale, G. J. Nabel, E. G. Nabel, Science 1994, 265, 781.
  51. K. A. Whitehead, R. Langer, D. G. Anderson, Nat. Rev. Drug Discovery 2009, 8, 129.
  52. A. Chrastina, K. A. Massey, J. E. Schnitzer, Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2011, 3, 421.
  53. C. N. Fries, E. J. Curvino, J.-L. Chen, S. R. Permar, G. G. Fouda, J. H. Collier, Nat. Nanotechnol. 2020, 15, 1.
  54. S. T. Reddy, A. J. Van Der Vlies, E. Simeoni, V. Angeli, G. J. Randolph, C. P. O'Neil, L. K. Lee, M. A. Swartz, J. A. Hubbell, Nat. Biotechnol. 2007, 25, 1159.
  55. X. Xu, W. Ho, X. Zhang, N. Bertrand, O. Farokhzad, Trends Mol. Med. 2015, 21, 223.
  56. H. Yin, R. L. Kanasty, A. A. Eltoukhy, A. J. Vegas, J. R. Dorkin, D. G. Anderson, Nat. Rev. Genet. 2014, 15, 541.
  57. C. H. Jones, C.-K. Chen, A. Ravikrishnan, S. Rane, B. A. Pfeifer, Mol. Pharmaceutics 2013, 10, 4082.
  58. D. Fischer, Y. Li, B. Ahlemeyer, J. Krieglstein, T. Kissel, Biomaterials 2003, 24, 1121.
  59. A. J. Mukalel, R. S. Riley, R. Zhang, M. J. Mitchell, Cancer Lett. 2019, 458, 102.
  60. M. A. Oberli, A. M. Reichmuth, J. R. Dorkin, M. J. Mitchell, O. S. Fenton, A. Jaklenec, D. G. Anderson, R. Langer, D. Blankschtein, Nano Lett. 2017, 17, 1326.
  61. C. Pollard, S. De Koker, X. Saelens, G. Vanham, J. Grooten, Trends Mol. Med. 2013, 19, 705.
  62. C. Voshavar, R. C. R. Meka, S. Samanta, S. Marepally, A. Chaudhuri, J. Med. Chem. 2017, 60, 1605.
  63. X.-Z. Yang, S. Dou, T.-M. Sun, C.-Q. Mao, H.-X. Wang, J. Wang, J. Controlled Release 2011, 156, 203.
  64. S. Shen, C.-Q. Mao, X.-Z. Yang, X.-J. Du, Y. Liu, Y.-H. Zhu, J. Wang, Mol. Pharmaceutics 2014, 11, 2612.
  65. C.-F. Xu, H.-B. Zhang, C.-Y. Sun, Y. Liu, S. Shen, X.-Z. Yang, Y.-H. Zhu, J. Wang, Biomaterials 2016, 88, 48.
  66. Y.-L. Luo, C.-F. Xu, H.-J. Li, Z.-T. Cao, J. Liu, J.-L. Wang, X.-J. Du, X.-Z. Yang, Z. Gu, J. Wang, ACS Nano 2018, 12, 994.
  67. Y.-N. Fan, M. Li, Y.-L. Luo, Q. Chen, L. Wang, H.-B. Zhang, S. Shen, Z. Gu, J. Wang, Biomater. Sci. 2018, 6, 3009.
  68. B. Li, X. Luo, B. Deng, J. Wang, D. W. McComb, Y. Shi, K. M. L. Gaensler, X. Tan, A. L. Dunn, B. A. Kerlin, Y. Dong, Nano Lett. 2015, 15, 8099.
  69. C. Zeng, X. Hou, J. Yan, C. Zhang, W. Li, W. Zhao, S. Du, Y. Dong, Adv. Mater. 2020, 32, 2004452.
  70. B. S. Graham, M. S. A. Gilman, J. S. McLellan, Annu. Rev. Med. 2019, 70, 91.
  71. J. S. McLellan, M. Chen, S. Leung, K. W. Graepel, X. Du, Y. Yang, T. Zhou, U. Baxa, E. Yasuda, T. Beaumont, Science 2013, 340, 1113.
  72. M. C. Crank, T. J. Ruckwardt, M. Chen, K. M. Morabito, E. Phung, P. J. Costner, L. A. Holman, S. P. Hickman, N. M. Berkowitz, I. J. Gordon, Science 2019, 365, 505.
  73. J. Pallesen, N. Wang, K. S. Corbett, D. Wrapp, R. N. Kirchdoerfer, H. L. Turner, C. A. Cottrell, M. M. Becker, L. Wang, W. Shi, Proc. Natl. Acad. Sci. USA 2017, 114, E7348.
  74. A. C. Walls, M. A. Tortorici, B.-J. Bosch, B. Frenz, P. J. Rottier, F. Di- Maio, F. A. Rey, D. Veesler, Nature 2016, 531, 114.
  75. R. N. Kirchdoerfer, C. A. Cottrell, N. Wang, J. Pallesen, H. M. Yassine, H. L. Turner, K. S. Corbett, B. S. Graham, J. S. McLellan, A. B. Ward, Nature 2016, 531, 118.
  76. L. A. Jackson, E. J. Anderson, N. G. Rouphael, P. C. Roberts, M. Makhene, R. N. Coler, M. P. McCullough, J. D. Chappell, M. R. Deni- son, L. J. Stevens, N. Engl. J. Med. 2020, 383, 1920.
  77. M. Jayaraman, S. M. Ansell, B. L. Mui, Y. K. Tam, J. Chen, X. Du, D. Butler, L. Eltepu, S. Matsuda, J. K. Narayanannair, Angew. Chem. 2012, 124, 8657.
  78. P. F. McKay, K. Hu, A. K. Blakney, K. Samnuan, J. C. Brown, R. Penn, J. Zhou, C. R. Bouton, P. Rogers, K. Polra, P. J. C. Lin, C. Barbosa, Y. K. Tam, W. S. Barclay, R. J. Shattock, Nat. Commun. 2020, 11, 3523.
  79. K. Gurpreet, S. Singh, Indian J. Pharm. Sci. 2018, 80, 781.
  80. L. A. Brito, M. Chan, C. A. Shaw, A. Hekele, T. Carsillo, M. Schaefer, J. Archer, A. Seubert, G. R. Otten, C. W. Beard, Mol. Ther. 2014, 22, 2118.
  81. M. M. Samsa, L. C. Dupuy, C. W. Beard, C. M. Six, C. S. Schmaljohn, P. W. Mason, A. J. Geall, J. B. Ulmer, D. Yu, Mol. Ther. 2019, 27, 850.
  82. H. Y. Xue, S. Liu, H. L. Wong, Nanomedicine 2014, 9, 295.
  83. H. Y. Xue, P. Guo, W.-C. Wen, H. L. Wong, Curr. Pharm. Des. 2015, 21, 3140.
  84. B. Nagavarma, H. K. Yadav, A. Ayaz, L. Vasudha, H. J. A. J. P. C. R. Shivakumar, Asian J. Pharmaceutical Clinical Res. 2012, 5, 16.
  85. J. M. Chan, P. M. Valencia, L. Zhang, R. Langer, O. C. Farokhzad, Methods Mol. Biol. 2010, 624, 163.
  86. Z. W. Wu, C. T. Chien, C. Y. Liu, J. Y. Yan, S. Y. Lin, J. Drug Targeting 2012, 20, 551.
  87. N. A. Nikitenko, V. S. Prassolov, Acta Nat. 2013, 5, 35.
  88. C. Sun, T. Tang, H. Uludag, J. E. Cuervo, Biophys. J. 2011, 100, 2754.
  89. J. Suh, H.-j. Paik, B. K. Hwang, Bioorg. Chem. 1994, 22, 318.
  90. M. Tang, F. Szoka, Gene Ther. 1997, 4, 823.
  91. L. Palmerston Mendes, J. Pan, V. P. Torchilin, Molecules 2017, 22, 1401.
  92. D. Kaur, K. Jain, N. K. Mehra, P. Kesharwani, N. K. Jain, J. Nanopart. Res. 2016, 18, 146.
  93. D. S. Katti, S. Lakshmi, R. Langer, C. T. Laurencin, Adv. Drug Delivery Rev. 2002, 54, 933.
  94. J. Yoo, D. J. Kuruvilla, S. R. D'Mello, A. K. Salem, N. B. Bowden, Macromolecules 2012, 45, 2292.
  95. E. I. Wafa, J. H. Wilson-Welder, R. L. Hornsby, J. E. Nally, S. M. Geary, N. B. Bowden, A. K. Salem, Biomacromolecules 2020, 21, 534.
  96. A. Makkouk, V. B. Joshi, A. Wongrakpanich, C. D. Lemke, B. P. Gross, A. K. Salem, G. J. Weiner, AAPS J. 2015, 17, 184.
  97. Z. Li, W. Ho, X. Bai, F. Li, Y.-J. Chen, X.-Q. Zhang, X. Xu, J. Controlled Release 2020, 322, 622.
  98. J. S. Chahal, O. F. Khan, C. L. Cooper, J. S. McPartlan, J. K. Tsosie, L. D. Tilley, S. M. Sidik, S. Lourido, R. Langer, S. Bavari, Proc. Natl. Acad. Sci. USA 2016, 113, E4133.
  99. J.-F. Nicolas, B. Guy, Expert Rev. Vaccines 2008, 7, 1201.
  100. Y.-C. Kim, F.-S. Quan, D.-G. Yoo, R. W. Compans, S.-M. Kang, M. R. Prausnitz, Vaccine 2009, 27, 6932.
  101. H. S. Gill, J. Söderholm, M. R. Prausnitz, M. Sällberg, Gene Ther. 2010, 17, 811.
  102. H. Seok, J. Y. Noh, D. Y. Lee, S. J. Kim, C. S. Song, Y. C. Kim, J. Con- trolled Release 2017, 265, 66.
  103. S. Dhakal, S. Ghimire, S. Renu, K. A. Ross, Y. S. Lakshmanappa, B. T. Hogshead, P. Bernardo, C. W. Lee, M. J. Wannemuehler, B. Narasimhan, G. J. Renukaradhya, Vet. Microbiol. 2019, 237, 108401.
  104. H. Shirota, D. M. Klinman, in Immunopotentiators in Modern Vac- cines, 2nd ed. (Eds: V. E. J. C. Schijns, D. T. O'Hagan), Academic Press, San Diego, CA 2017, p. 163.
  105. M. P. Torres, B. M. Vogel, B. Narasimhan, S. K. Mallapragada, J. Biomed. Mater. Res., Part A 2006, 76, 102.
  106. H.-W. Yang, L. Ye, X. D. Guo, C. Yang, R. W. Compans, M. R. Praus- nitz, Adv. Healthcare Mater. 2017, 6, 1600750.
  107. A.-J. Choi, C.-J. Kim, Y.-J. Cho, J.-K. Hwang, C.-T. J. F. Kim, Food Bio- process Technol. 2011, 4, 1119.
  108. S. K. Nitta, K. Numata, Int. J. Mol. Sci. 2013, 14, 1629.
  109. A. Kumar, A. Vimal, A. Kumar, Int. J. Biol. Macromol. 2016, 91, 615.
  110. C. Shi, Y. Zhu, X. Ran, M. Wang, Y. Su, T. Cheng, J. Surg. Res. 2006, 133, 185.
  111. A. Vila, A. Sánchez, K. Janes, I. Behrens, T. Kissel, J. L. V. Jato, M. J. Alonso, Eur. J. Pharm. Biopharm. 2004, 57, 123.
  112. F. Khademi, R.-A. Taheri, A. Yousefi Avarvand, H. Vaez, A. A. Momtazi-Borojeni, S. Soleimanpour, Microb. Pathog. 2018, 121, 218.
  113. K. Zhao, J. Han, Y. Zhang, L. Wei, S. Yu, X. Wang, Z. Jin, Y. Wang, Mol. Pharmaceutics 2018, 15, 226.
  114. J. Necas, L. Bartosikova, P. Brauner, J. Kolar, Vet. Med. 2008, 53, 397.
  115. J. A. Burdick, G. D. Prestwich, Adv. Mater. 2011, 23, H41.
  116. J. G. Rho, H. S. Han, J. H. Han, H. Lee, W. H. Lee, S. Kwon, S. Heo, J. Yoon, H. H. Shin, E.-Y. Lee, J. Controlled Release 2018, 279, 89.
  117. S. Ganesh, A. K. Iyer, D. V. Morrissey, M. M. Amiji, Biomaterials 2013, 34, 3489.
  118. H. S. Han, J. Lee, H. R. Kim, S. Y. Chae, M. Kim, G. Saravanakumar, H. Y. Yoon, D. G. You, H. Ko, K. Kim, J. Controlled Release 2013, 168, 105.
  119. H. Yu, Y. Zou, Y. Wang, X. Huang, G. Huang, B. D. Sumer, D. A. Boothman, J. Gao, ACS Nano 2011, 5, 9246.
  120. T.-H. Tran, R. Rastogi, J. Shelke, M. M. Amiji, Sci. Rep. 2015, 5, 16632.
  121. B. Shi, M. Zheng, W. Tao, R. Chung, D. Jin, D. Ghaffari, O. C. Farokhzad, Biomacromolecules 2017, 18, 2231.
  122. D. Ulkoski, A. Bak, J. T. Wilson, V. R. Krishnamurthy, Expert Opin. Drug Delivery 2019, 16, 1149.
  123. L. Peng, E. Wagner, Biomacromolecules 2019, 20, 3613.
  124. Y. Ding, Z. Jiang, K. Saha, C. S. Kim, S. T. Kim, R. F. Landis, V. M. Rotello, Mol. Ther. 2014, 22, 1075.
  125. M. C. Daniel, D. Astruc, Chem. Rev. 2004, 104, 293.
  126. S. H. Ku, K. Kim, K. Choi, S. H. Kim, I. C. Kwon, Adv. Healthcare Mater. 2014, 3, 1182.
  127. D. A. Giljohann, D. S. Seferos, W. L. Daniel, M. D. Massich, P. C. Patel, C. A. Mirkin, Angew. Chem., Int. Ed. 2010, 49, 3280.
  128. R. R. Meka, S. Mukherjee, C. R. Patra, A. Chaudhuri, Nanoscale 2019, 11, 7931.
  129. D. Tarn, C. E. Ashley, M. Xue, E. C. Carnes, J. I. Zink, C. J. Brinker, Acc. Chem. Res. 2013, 46, 792.
  130. J. E. Lee, N. Lee, T. Kim, J. Kim, T. Hyeon, Acc. Chem. Res. 2011, 44, 893.
  131. M. An, M. Li, J. Xi, H. Liu, ACS Appl. Mater. Interfaces 2017, 9, 23466.
  132. S. P. Kasturi, I. Skountzou, R. A. Albrecht, D. Koutsonanos, T. Hua, H. I. Nakaya, R. Ravindran, S. Stewart, M. Alam, M. Kwissa, F. Villinger, N. Murthy, J. Steel, J. Jacob, R. J. Hogan, A. García-Sastre, R. Compans, B. Pulendran, Nature 2011, 470, 543.
  133. I. Pal, J. D. Ramsey, Adv. Drug Delivery Rev. 2011, 63, 909.
  134. X. Wang, X. Li, A. Ito, Y. Watanabe, Y. Sogo, N. M. Tsuji, T. Ohno, Angew. Chem. 2016, 128, 1931.
  135. H. Song, Y. Yang, J. Tang, Z. Gu, Y. Wang, M. Zhang, C. Yu, Adv. Ther. 2020, 3, 1900154.
  136. H. Song, M. Yu, Y. Lu, Z. Gu, Y. Yang, M. Zhang, J. Fu, C. Yu, J. Appl. Chem. Sci. 2017, 139, 18247.
  137. I. Fratoddi, I. Venditti, C. Cametti, M. Russo, J. Mater. Chem. B 2014, 2, 4204.
  138. R. Arvizo, R. Bhattacharya, P. Mukherjee, Expert Opin. Drug Delivery 2010, 7, 753.
  139. W. Cha, R. Fan, Y. Miao, Y. Zhou, C. Qin, X. Shan, X. Wan, J. Li, Molecules 2017, 22, 782.
  140. J. L. Paris, M. Vallet-Regí, Pharmaceutics 2020, 12, 526.
  141. W. Li, M. D. Joshi, S. Singhania, K. H. Ramsey, A. K. Murthy, Vaccines 2014, 2, 515.
  142. M. Grau, P. R. Walker, M. Derouazi, Cell. Mol. Life Sci. 2018, 75, 2887.
  143. V. K. Udhayakumar, A. De Beuckelaer, J. McCaffrey, C. M. Mc- Crudden, J. L. Kirschman, D. Vanover, L. Van Hoecke, K. Roose, K. Deswarte, B. G. De Geest, S. Lienenklaus, P. J. Santangelo, J. Grooten, H. O. McCarthy, S. De Koker, Adv. Healthcare Mater. 2017, 6, 1601412.
  144. V. Pavot, N. Rochereau, C. Primard, C. Genin, E. Perouzel, T. Lioux, S. Paul, B. Verrier, J. Controlled Release 2013, 167, 60.
  145. J. Rességuier, E. Delaune, A.-L. Coolen, J.-P. Levraud, P. Boudinot, D. L.e Guellec, B. Verrier, Front. Immunol. 2017, 8, 190.
  146. A.-L. Coolen, C. Lacroix, P. Mercier-Gouy, E. Delaune, C. Monge, J.-Y. Exposito, B. Verrier, Biomaterials 2019, 195, 23.
  147. L. A. Palomares, O. T. Ramírez, Biochem. Eng. J. 2009, 45, 158.
  148. A. Salvador, M. Igartua, R. M. Hernández, J. L. Pedraz, J. Drug De- livery 2011, 2011, 181646.
  149. M. J. Rohovie, M. Nagasawa, J. R. Swartz, Bioeng. Transl. Med. 2017, 2, 43.
  150. M. Kerkmann, S. Rothenfusser, V. Hornung, A. Towarowski, M. Wag- ner, A. Sarris, T. Giese, S. Endres, G. Hartmann, J. Immunol. 2003, 170, 4465.
  151. Y. Cheng, C. D. Lemke-Miltner, W. Wongpattaraworakul, Z. Wang, C. H. F. Chan, A. K. Salem, G. J. Weiner, A. L. Simons, J. Immunother. Cancer 2020, 8, e000940.
  152. T. Lehto, K. Ezzat, M. J. A. Wood, S. E.l Andaloussi, Adv. Drug Delivery Rev. 2016, 106, 172.
  153. M. L. Hovlid, J. L. Lau, K. Breitenkamp, C. J. Higginson, B. Laufer, M. Manchester, M. Finn, ACS Nano 2014, 8, 8003.
  154. A. Roldao, M. C. Mellado, L. R. Castilho, M. J. Carrondo, P. M. Alves, Expert Rev. Vaccines 2010, 9, 1149.
  155. N. Kushnir, S. J. Streatfield, V. Yusibov, Vaccine 2012, 31, 58.
  156. A. V. Kroll, Y. Jiang, J. Zhou, M. Holay, R. H. Fang, L. Zhang, Adv. Biosyst. 2019, 3, 1800219.

Authors
Ho, W., Gao, M., Li, F., Li, Z., Zhang, X., & Xu, X.
Affiliations
  • New Jersey Institute of Technology (US)
  • Shanghai Jiao Tong University (CN)
Corresponding author
  • Zhang, Xue‐Qing
  • Xu, Xiaoyang
ORCID
Venue
Advanced Healthcare Materials
Publisher
Wiley
Published
2021-01-18
Volume
10
Issue
8
Pages
e2001812-e2001812
ISSN
  • 2192-2640 (ISSN-L)
  • 2192-2659
DOI
10.1002/adhm.202001812
PMC
PMC7995055
OpenAlex
W3121264726
Cited by
261
References
172
Citations by year
2026: 27 · 2025: 46 · 2024: 53 · 2023: 51 · 2022: 51 · 2021: 33
FWCI
4.93
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Healthcare Materials (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • American Heart Association (19AIREA34380849)
  • National Science Foundation (2001606)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
  • Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords
nucleic acid vaccines, DNA vaccine, mRNA vaccines, nanoparticle delivery, vaccine delivery systems, COVID-19 vaccines, clinical trials, vaccine formulation
MeSH terms
COVID-19, SARS-CoV-2, DNA, Humans, RNA, Messenger, Vaccines, Nanoparticles

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