DOI QR코드

DOI QR Code

Engineered biomaterials for development of nucleic acid vaccines

  • Yang, Jun (National Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences) ;
  • Li, Yan (National Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences) ;
  • Jin, Shubin (CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, National Center for Nanoscience and Technology) ;
  • Xu, Jing (CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, National Center for Nanoscience and Technology) ;
  • Wang, Paul C (Laboratory of Molecular Imaging, Department of Radiology, Howard University) ;
  • Liang, Xing-Jie (CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, National Center for Nanoscience and Technology) ;
  • Zhang, Xin (National Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences)
  • Received : 2014.08.23
  • Accepted : 2014.12.23
  • Published : 2015.03.31

Abstract

Nucleic acid vaccines have attracted many attentions since they have presented some superiority over traditional vaccines. However, they could only induce moderate immunogenicity. The route and formulation of nucleic acid vaccines have strong effects on the immune response and efficiency. Numerous biomaterials are used as a tool to enhance the immunogenicity of antigens. They deliver the antigens into the cells through particle- and non-particle-mediated pathway. However, challenges remain due to lack of comprehensive understanding of the actions of these biomaterials as a carrier/adjuvant. Herein, this review focuses on the evolution of biomaterials used for nucleic acid vaccines, discusses the advantages and disadvantages for gene delivery and immunostimulation of variety of structures of the biomaterials, in order to provide new thought on rational design of carrier/adjuvant and better understanding of mechanism of action in both immunostimulatory and delivery methods.

Keywords

Acknowledgement

Supported by : National Natural Science Foundation of China

References

  1. Jenner E. An inquiry into the causes and effects of the variolae vaccinae, a disease discovered in some of the western counties of England, particularly Gloucestershire, and known by the name of the cow pox. 1798, New York: General Books.
  2. Behbehani AM. The smallpox story: life and death of an old disease. Microbiol Rev. 1983;47(4):455-509.
  3. Peek LJ, Middaugh CR, Berkland C. Nanotechnology in vaccine delivery. Adv Drug Deliv Rev. 2008;60(8):915-28. https://doi.org/10.1016/j.addr.2007.05.017
  4. Kubba AK, Taylor P, Graneek B, Strobel S. Non-responders to hepatitis B vaccination: a review. Commun Dis Public Health. 2003;6:106-12.
  5. Plotkin SA. Vaccines: past, present and future. Nat Med. 2005;11(4 Suppl):S5-11.
  6. Plotkin SA, Orenstein WA, Offit PA. Vaccines. Philadelphia: Saunders; 2008.
  7. Laddy DJ, Weiner DB. From plasmids to protection: a review of DNA vaccines against infectious diseases. Int Rev Immunol. 2006;25(3-4):99-123. https://doi.org/10.1080/08830180600785827
  8. Chiarella P, Massi E, Robertis MD, Fazio VM, Signori E. Strategies for effective naked-DNA vaccination against infectious diseases. Recent Pat Antiinfect Drug Discov. 2008;3(2):93-101. https://doi.org/10.2174/157489108784746623
  9. Rice J, Ottensmeier CH, Stevenson FK. DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer. 2008;8(2):108-20. https://doi.org/10.1038/nrc2326
  10. Stevenson FK, Ottensmeier CH, Johnson P, Zhu D, Buchan SL, McCann KJ, et al. DNA vaccines to attack cancer. Proc Natl Acad Sci U S A. 2004;101 Suppl 2:14646-52. https://doi.org/10.1073/pnas.0404896101
  11. Ferrera F, Lacava A, Rizzi M, Hahn BH, Indiveri F, Filaci G. Gene vaccination for the induction of immune tolerance. Ann N Y Acad Sci. 2007;1110:99-111. https://doi.org/10.1196/annals.1423.012
  12. Richard W, Sandra S, Elisabeth R, Fatima F, Josef T. Prophylactic mRNA vaccination against allergy. Curr Opin Allergy Clin Immunol. 2010;10(6):567-74. https://doi.org/10.1097/ACI.0b013e32833fd5b6
  13. Sardesai NY, Weiner DB. Electroporation delivery of DNA vaccines: prospects for success. Curr Opin Immunol. 2011;23(3):421-9. https://doi.org/10.1016/j.coi.2011.03.008
  14. Porgador A, Irvine KR, Iwasaki A, Barber BH, Restifo NP, Germain RN. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J Exp Med. 1998;188(6):1075-82. https://doi.org/10.1084/jem.188.6.1075
  15. Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat Rev Genet. 2008;9(10):776-88. https://doi.org/10.1038/nrg2432
  16. Ledgerwood JE, Pierson TC, Hubka SA, Desai N, Rucker S, Gordon IJ, et al. A West Nile virus DNA vaccine utilizing a modified promoter induces neutralizing antibody in younger and older healthy adults in a phase I clinical trial. J Infect Dis. 2011;203(10):1396-404. https://doi.org/10.1093/infdis/jir054
  17. Martin JE, Pierson TC, Hubka S, Rucker S, Gordon IJ, Enama ME, et al. A West Nile virus DNA vaccine induces neutralizing antibody in healthy adults during a phase 1 clinical trial. J Infect Dis. 2007;196(12):1732-40. https://doi.org/10.1086/523650
  18. Liu MA, Ulmer JB. Human clinical trials of plasmid DNA vaccines. Adv Genet. 2005;55:25-40. https://doi.org/10.1016/S0065-2660(05)55002-8
  19. Buchan S, Gronevik E, Mathiesen I, King CA, Stevenson FK, Rice J. Electroporation as a "prime/boost" strategy for naked DNA vaccination against a tumor antigen. J Immunol. 2005;174(10):6292-8. https://doi.org/10.4049/jimmunol.174.10.6292
  20. Johansson DX, Ljungberg K, Kakoulidou M, Liljestrom P. Intradermal electroporation of naked replicon RNA elicits strong immune responses. PLoS One. 2012;7(1):e29732. https://doi.org/10.1371/journal.pone.0029732
  21. Yang J, Liu H, Zhang X. Design, preparation and application of nucleic acid delivery carriers. Biotechnol Adv. 2014;32(4):804-917. https://doi.org/10.1016/j.biotechadv.2013.11.004
  22. Mora-Solano C, Collier JH. Engaging adaptive immunity with biomaterials. J Mater Chem B Mater Biol Med. 2014;2(17):2409-21. https://doi.org/10.1039/C3TB21549K
  23. Rodriguez-Gascon A, Pozo-Rodriguez A, Solinis MA. Development of nucleic acid vaccines: use of self-amplifying RNA in lipid nanoparticles. Int J Nanomedicine. 2014;9:1833-43.
  24. Marrack P, McKee AS, Munks MW. Towards an understanding of the adjuvant action of aluminium. Nat Rev Immunol. 2009;9(4):287-93. https://doi.org/10.1038/nri2510
  25. Ulmer JB, DeWitt CM, Chastain M, Friedman A, Donnelly JJ, McClements WL, et al. Enhancement of DNA vaccine potency using conventional aluminum adjuvants. Vaccine. 2000;18:18-28.
  26. Wang S, Liu X, Fisher K, Smith JG, Chen F, Tobery TW, et al. Enhanced type I immune response to a hepatitis B DNA vaccine by formulation with calcium- or aluminum phosphate. Vaccine. 2000;18:1227-35. https://doi.org/10.1016/S0264-410X(99)00391-6
  27. Correia-Pintoa JF, Csaba N, Alonso MJ. Vaccine delivery carriers: insights and future perspectives. Int J Pharm. 2013;440(1):27-38. https://doi.org/10.1016/j.ijpharm.2012.04.047
  28. Tomljenovic L, Shaw CA. Aluminum vaccine adjuvants: are they safe? Curr Med Chem. 2011;18(17):2630-7. https://doi.org/10.2174/092986711795933740
  29. Chakravarthy KV, Bonoiu AC, Davis WG, Ranjan P, Ding H, Hu R, et al. Gold nanorod delivery of an ssRNA immune activator inhibits pandemic H1N1 influenza viral replication. Proc Natl Acad Sci U S A. 2010;107(22):10172-7. https://doi.org/10.1073/pnas.0914561107
  30. Salem AK, Searson PC, Leong KW. Multifunctional nanorods for gene delivery. Nat Mater. 2003;2(10):668-71. https://doi.org/10.1038/nmat974
  31. Almeida JPM, Figueroa ER, Drezek RA. Gold nanoparticle mediated cancer immunotherapy. Nanomedicine. 2014;10(3):503-14. https://doi.org/10.1016/j.nano.2013.09.011
  32. Xu L, Liu Y, Chen Z, Li W, Liu Y, Wang L, et al. Surface-Engineered Gold Nanorods: Promising DNA Vaccine Adjuvant for HIV-1 Treatment. Nano Lett. 2012;12:2003-12. https://doi.org/10.1021/nl300027p
  33. Grant EV, Thomas M, Fortune J, Klibanov AM, Letvin NL. Enhancement of plasmid DNA immunogenicity with linear polyethylenimine. Eur J Immunol. 2012;42:2937-48. https://doi.org/10.1002/eji.201242410
  34. Patnaik S, Gupta KC. Novel polyethylenimine-derived nanoparticles for in vivo gene delivery. Expert Opin Drug Deliv. 2013;10(2):215-28. https://doi.org/10.1517/17425247.2013.744964
  35. Huang R, Liu S, Shao K, Han L, Ke W, Liu Y, et al. Evaluation and mechanism studies of PEGylated dendrigraft poly-L-lysines as novel gene delivery vectors. Nanotechnology. 2010;21(26):265101-11. https://doi.org/10.1088/0957-4484/21/26/265101
  36. Hofman J, Buncek M, Haluza R, Ludvik S, Ledvina M, Cigler P. In vitro transfection mediated by dendrigraft poly(L-lysines): the effect of structure and molecule size. Macromol Biosci. 2013;13(2):167-76. https://doi.org/10.1002/mabi.201200303
  37. Little SR, Lynn DM, Puram SV, Langer R. Formulation and characterization of poly (beta amino ester) microparticles for genetic vaccine delivery. J Control Release. 2005;107(3):449-62. https://doi.org/10.1016/j.jconrel.2005.04.022
  38. Little SR, Lynn DM, Ge Q, Anderson DG, Puram SV, Chen J, et al. Poly-beta amino ester-containing microparticles enhance the activity of nonviral genetic vaccines. Proc Natl Acad Sci U S A. 2004;101(26):9534-9. https://doi.org/10.1073/pnas.0403549101
  39. Shen Y, Tang H, Zhan Y, Kirk EAV, Murdoch WJ. Degradable Poly(${\beta}$-amino ester) nanoparticles for cancer cytoplasmic drug delivery. Nanomedicine. 2009;5:192-201. https://doi.org/10.1016/j.nano.2008.09.003
  40. Zhang B, Ma X, Murdoch W, Radosz M, Shen Y. Bioreducible poly(amido amine)s with different branching degrees as gene delivery vectors. Biotechnol Bioeng. 2013;110:990-8. https://doi.org/10.1002/bit.24772
  41. Huang B, Kukowska-Latallo JF, Tang S, Zong H, Johnson KB, Desai A, et al. The facile synthesis of multifunctional PAMAM dendrimer conjugates through copper-free click chemistry. Bioorg Med Chem Lett. 2012;22(9):3152-6. https://doi.org/10.1016/j.bmcl.2012.03.052
  42. Zhang X, Sharma KK, Boeglin M, Ogier J, Mainard D, Voegel J-C, et al. Transfection ability and intracellular DNA pathway of nanostructured gene-delivery systems. Nano Lett. 2008;8(8):2432-6. https://doi.org/10.1021/nl801379y
  43. Ma Y-F, Yang Y-W. Delivery of DNA-based cancer vaccine with polyethylenimine. Eur J Pharm Sci. 2010;40(2):75-83. https://doi.org/10.1016/j.ejps.2010.02.009
  44. Akinc A, Thomas M, Klibanov AM, Langer R. Exploring polyethyleniminemediated DNA transfection and the proton sponge hypothesis. J Gene Med. 2005;7(5):657-63. https://doi.org/10.1002/jgm.696
  45. Negash T, Liman M, Rautenschlein S. Mucosal application of cationic poly(d, l-lactide-co-glycolide) microparticles as carriers of DNA vaccine and adjuvants to protect chickens against infectious bursal disease. Vaccine. 2013;31:3656-62. https://doi.org/10.1016/j.vaccine.2013.06.011
  46. Zhou X, Liu B, Yu X, Zha X, Zhang X, Chen Y, et al. Controlled release of PEI/DNA complexes from mannose-bearing chitosan microspheres as a potent delivery system to enhance immune response to HBV DNA vaccine. J Control Release. 2007;121(3):200-7. https://doi.org/10.1016/j.jconrel.2007.05.018
  47. Li M, Jiang Y, Xu C, Zhang Z, Sun X. Enhanced immune response against HIV-1 induced by a heterologous DNA prime-adenovirus boost vaccination using mannosylated polyethyleneimine as DNA vaccine adjuvant. Int J Nanomedicine. 2013;8:1843-54.
  48. Sun X, Chen S, Han J, Zhang Z. Mannosylated biodegradable polyethyleneimine for targeted DNA delivery to dendritic cells. Int J Nanomedicine. 2012;7:2929-42.
  49. Mannisto M, Vanderkerken S, Toncheva V, Elomaa M, Ruponen M, Schacht E, et al. Structure-activity relationships of poly(L-lysines): effects of pegylation and molecular shape on physicochemical and biological properties in gene delivery. J Control Release. 2002;83(1):169-82. https://doi.org/10.1016/S0168-3659(02)00178-5
  50. Green JJ, Zugates GT, Tedford NC, Huang Y-H, Griffith LG, Lauffenburger DA, et al. Combinatorial modification of degradable polymers enables transfection of human cells comparable to adenovirus. Adv Mater. 2007;19:2836-42. https://doi.org/10.1002/adma.200700371
  51. Liu Z, Lv D, Liu S, Gong J, Wang D, Xiong M, et al. Alginic acid-coated chitosan nanoparticles loaded with legumain DNA vaccine: effect against breast cancer in mice. PLoS One. 2013;8(4):e60190. https://doi.org/10.1371/journal.pone.0060190
  52. Yao W, Peng Y, Du M, Luo J, Zong L. Preventative vaccine-loaded mannosylated chitosan nanoparticles intended for nasal mucosal delivery enhance immune responses and potent tumor immunity. Mol Pharmaceutics. 2013;10:2904-14. https://doi.org/10.1021/mp4000053
  53. Feng G, Jiang Q, Xia M, Lu Y, Qiu W, Zhao D, et al. Enhanced immune response and protective effects of nano-chitosan-based DNA vaccine encoding T cell epitopes of Esat-6 and FL against mycobacterium tuberculosis infection. PLoS One. 2013;8(4):e61135. https://doi.org/10.1371/journal.pone.0061135
  54. Rudra JS, Tian YF, Jung JP, Collier JH. A self-assembling peptide acting as an immune adjuvant. Proc Natl Acad Sci U S A. 2010;107(2):622-7. https://doi.org/10.1073/pnas.0912124107
  55. Rudra JS, Sun T, Bird KC, Daniels MD, Gasiorowski JZ, Chong AS, et al. Modulating Adaptive Immune Responses to Peptide Self-Assemblies. ACS Nano. 2012;6(2):1557-64. https://doi.org/10.1021/nn204530r
  56. Cui J, Rose RD, Best JP, Johnston APR, Alcantara S, Liang K, et al. Mechanically tunable, self-adjuvanting nanoengineered polypeptide particles. Adv Mater. 2013;25(25):3468-72. https://doi.org/10.1002/adma.201300981
  57. Tian Y, Wang H, Liu Y, Mao L, Chen W, Zhu Z, et al. A peptide-based nanofibrous hydrogel as a promising DNA nanovector for optimizing the efficacy of HIV vaccine. Nano Lett. 2014;14:1439-45. https://doi.org/10.1021/nl404560v
  58. Minigo G, Scholzen A, Tang CK, Hanley JC, Kalkanidis M, Pietersz GA, et al. Poly-l-lysine-coated nanoparticles: a potent delivery system to enhance DNA vaccine efficacy. Vaccine. 2007;25:1316-27. https://doi.org/10.1016/j.vaccine.2006.09.086
  59. Henriksen-Lacey M, Korsholm KS, Andersen P, Perrie Y, Christensen D. Liposomal vaccine delivery systems. Expert Opin Drug Deliv. 2011;8(4):505-19. https://doi.org/10.1517/17425247.2011.558081
  60. Un K, Kawakami S, Suzuki R, Maruyama K, Yamashita F, Hashida M. Development of an ultrasound-responsive and mannose-modified gene carrier for DNA vaccine therapy. Biomaterials. 2010;31:7813-26. https://doi.org/10.1016/j.biomaterials.2010.06.058
  61. Perrie Y, Frederik PM, Gregoriadis G. Liposome-mediated DNA vaccination: the effect of vesicle composition. Vaccine. 2001;19:3301-10. https://doi.org/10.1016/S0264-410X(00)00432-1
  62. Watson DS, Endsley AN, Huang L. Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cellmediated immune responses to liposome associated antigens. Vaccine. 2012;30(13):2256-72. https://doi.org/10.1016/j.vaccine.2012.01.070
  63. Ginn SL, Alexander IE, Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2012 - an update. J Gene Med. 2013;15:65-77. https://doi.org/10.1002/jgm.2698
  64. Stopeck AT, Jones A, Hersh EM, Thompson JA, Finucane DM, Gutheil JC, et al. Phase II study of direct intralesional gene transfer of allovectin-7, an HLA-B7/beta2-microglobulin DNA-liposome complex, in patients with metastatic melanoma. Clin Cancer Res. 2001;7(8):2285-91.
  65. DeMuth PC, Min Y, Huang B, Kramer JA, Miller AD, Barouch DH, et al. Polymer multilayer tattooing for enhanced DNA vaccination. Nat Mater. 2013;12(4):367-76. https://doi.org/10.1038/nmat3550
  66. Pollard C, Rejman J, Haes WD, Verrier B, Gulck EV, Naessens T, et al. Type I IFN counteracts the induction of antigen-specific immune responses by lipid-based delivery of mRNA vaccines. Mol Ther. 2013;21(1):251-9. https://doi.org/10.1038/mt.2012.202
  67. Geall AJ, Verma A, Otten GR, Shaw CA, Hekele A, Banerjee K, et al. Nonviral delivery of self-amplifying RNA vaccines. Proc Natl Acad Sci U S A. 2012;109(36):14604-9. https://doi.org/10.1073/pnas.1209367109

Cited by

  1. Phage Particles as Vaccine Delivery Vehicles: Concepts, Applications and Prospects vol.16, pp.18, 2015, https://doi.org/10.7314/apjcp.2015.16.18.8019
  2. Immunological properties of gold nanoparticles vol.8, pp.3, 2015, https://doi.org/10.1039/c6sc03631g
  3. A Novel Molecular Design for a Hybrid Phage-DNA Construct Against DKK1 vol.60, pp.11, 2015, https://doi.org/10.1007/s12033-018-0115-2
  4. Polymeric nanostructure vaccines: applications and challenges vol.17, pp.7, 2015, https://doi.org/10.1080/17425247.2020.1776259
  5. Biomaterials and nanomaterials for sustained release vaccine delivery vol.13, pp.6, 2021, https://doi.org/10.1002/wnan.1735