In vivo electroporation of minicircle DNA as a novel method of vaccine delivery to enhance HIV-1-specific immune responses

Journal of Virology

Volumn 88, Issue 4, 2014, Pages 1924-1934

  Wang, Qingtao ^a   Jiang, Wei ^a   Chen, Yuhai ^a   Liu, Pengyu ^a   Sheng, Chunjie ^a   Chen, Shuai ^a   Zhang, Hui ^d   Pan, Changchuan ^e   Gao, Shijuan ^a   Huang, Wenlin ^a,b,c  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^c Science Park   (China)

^d SUN YAT SEN UNIVERSITY   (China)

^e SICHUAN CANCER HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; DNA, KINETOPLAST; DRUG DELIVERY SYSTEMS; ELECTROPORATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; IMMUNITY, HUMORAL; IMMUNOHISTOCHEMISTRY; LUCIFERASES; MICE; MICE, INBRED BALB C; REAL-TIME POLYMERASE CHAIN REACTION; VACCINES, DNA;

EID: 84893498955     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02757-13     Document Type: Article

References (63)

1. Plotkin SA. 1999. Vaccination against the major infectious diseases. C. R. Acad. Sci. III 322:943-951.
2. Liu MA, Wahren B, Karlsson Hedestam GB. 2006. DNA vaccines: recent developments and future possibilities. Hum. Gene Ther. 17:1051-1061. http://dx.doi.org/10.1089/hum.2006.17.1051.
3. Saha R, Killian S, Donofrio RS. 2011. DNA vaccines: a mini review. Recent Pat. DNAGene Seq. 5:92-96. http://dx.doi.org/10.2174/187221511796392114.
4. Fioretti D, Iurescia S, Fazio VM, Rinaldi M. 2010. DNA vaccines: developing new strategies against cancer. J. Biomed. Biotechnol. 2010:174378. http://dx.doi.org/10.1155/2010/174378.
5. Toda M, Kasai M, Hosokawa H, Nakano N, Taniguchi Y, Inouye S, Kaminogawa S, Takemori T, Sakaguchi M. 2002. DNA vaccine using invariant chain gene for delivery of CD4 T cell epitope peptide derived from Japanese cedar pollen allergen inhibits allergen-specific IgE response. Eur. J. Immunol. 32:1631-1639. http://dx.doi.org/10.1002/1521-4141(200206)32:6<1631::AID-IMMU1631>3.0.CO;2-O.
6. Wingard JB, Anderson B, Weissman D. 2008. Induction of HIV-specific T and B cell responses with a replicating and conditionally infectious lentiviral vaccine. Eur. J. Immunol. 38:1310-1320. http://dx.doi.org/10.1002/eji.200738069.
7. MacGregor RR, Boyer JD, Ugen KE, Lacy KE, Gluckman SJ, Bagarazzi ML, Chattergoon MA, Baine Y, Higgins TJ, Ciccarelli RB, Coney LR, Ginsberg RS, Weiner DB. 1998. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J. Infect. Dis. 178:92-100. http://dx.doi.org/10.1086/515613.
8. Kutzler MA, Weiner DB. 2008. DNA vaccines: ready for prime time? Nat. Rev. Genet. 9:776-788. http://dx.doi.org/10.1038/nrg2432.
9. Garmory HS, Brown KA, Titball RW. 2003. DNA vaccines: improving expression of antigens. Genet. Vaccines Ther. 1:2. http://dx.doi.org/10.1186/1479-0556-1-2.
10. Luckay A, Sidhu MK, Kjeken R, Megati S, Chong SY, Roopchand V, Garcia-Hand D, Abdullah R, Braun R, Montefiori DC, Rosati M, Felber BK, Pavlakis GN, Mathiesen I, Israel ZR, Eldridge JH, Egan MA. 2007. Effect of plasmid DNA vaccine design and in vivo electroporation on the resulting vaccine-specific immune responses in rhesus macaques. J. Virol. 81:5257-5269. http://dx.doi.org/10.1128/JVI.00055-07.
11. Ivory C, Chadee K. 2004. DNA vaccines: designing strategies against parasitic infections. Genet. Vaccines Ther. 2:17. http://dx.doi.org/10.1186/1479-0556-2-17.
12. Radcliffe JN, Roddick JS, Friedmann PS, Stevenson FK, Thirdborough SM. 2006. Prime-boost with alternating DNA vaccines designed to engage different antigen presentation pathways generates high frequencies of peptide-specific CD8+ T cells. J. Immunol. 177:6626-6633.
13. Bigger BW, Tolmachov O, Collombet JM, Fragkos M, Palaszewski I, Coutelle C. 2001. An araC-controlled bacterial cre expression system to produce DNA minicircle vectors for nuclear and mitochondrial gene therapy. J. Biol. Chem. 276:23018-23027. http://dx.doi.org/10.1074/jbc.M010873200.
14. Darquet AM, Cameron B, Wils P, Scherman D, Crouzet J. 1997. A new DNA vehicle for nonviral gene delivery: supercoiled minicircle. Gene Ther. 4:1341-1349. http://dx.doi.org/10.1038/sj.gt.3300540.
15. Chen ZY, He CY, Ehrhardt A, Kay MA. 2003. Minicircle DNA vectors devoid of bacterial DNA result in persistent and high-level transgene expression in vivo. Mol. Ther. 8:495-500. http://dx.doi.org/10.1016/S1525-0016(03)00168-0.
16. Yoon CS, Jung HS, Kwon MJ, Lee SH, Kim CW, Kim MK, Lee M, Park JH. 2009. Sonoporation of the minicircle-VEGF(165) for wound healing of diabetic mice. Pharm. Res. 26:794-801. http://dx.doi.org/10.1007/s11095-008-9778-x.
17. Chang CW, Christensen LV, Lee M, Kim SW. 2008. Efficient expression of vascular endothelial growth factor using minicircleDNAfor angiogenic gene therapy. J. Control. Release 125:155-163. http://dx.doi.org/10.1016/j.jconrel.2007.10.014.
18. Huang M, Chen Z, Hu S, Jia F, Li Z, Hoyt G, Robbins RC, Kay MA, Wu JC. 2009. Novel minicircle vector for gene therapy in murine myocardial infarction. Circulation 120:S230-S237. http://dx.doi.org/10.1161/CIRCULATIONAHA.108.841155.
19. Jia F, Wilson KD, Sun N, Gupta DM, Huang M, Li Z, Panetta NJ, Chen ZY, Robbins RC, Kay MA, Longaker MT, Wu JC. 2010. A nonviral minicircle vector for deriving human iPS cells. Nat. Methods 7:197-199. http://dx.doi.org/10.1038/nmeth.1426.
20. Wu J, Xiao X, Zhao P, Xue G, Zhu Y, Zhu X, Zheng L, Zeng Y, Huang W. 2006. Minicircle-IFNγ induces antiproliferative and antitumoral effects in human nasopharyngeal carcinoma. Clin. Cancer Res. 12:4702-4713. http://dx.doi.org/10.1158/1078-0432.CCR-06-0520.
21. Zuo Y, Wu J, Xu Z, Yang S, Yan H, Tan L, Meng X, Ying X, Liu R, Kang T, Huang W. 2011. Minicircle-oriP-IFNγ: a novel targeted gene therapeutic system for EBV positive human nasopharyngeal carcinoma. PLoS One 6:e19407. http://dx.doi.org/10.1371/journal.pone.0019407.
22. Jiang WZ, Jin NY, Li ZJ, Zhang LS. 2004. Study on the immunogenicity of HIV-1 gag vaccine. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 20:272-273. (In Chinese.).
23. Ribeiro SP, Rosa DS, Fonseca SG, Mairena EC, Postol E, Oliveira SC, Guilherme L, Kalil J, Cunha-Neto E. 2010. A vaccine encoding conserved promiscuous HIV CD4 epitopes induces broad T cell responses in mice transgenic to multiple common HLA class II molecules. PLoS One 5:e11072. http://dx.doi.org/10.1371/journal.pone.0011072.
24. Lu S, Wang S, Grimes-Serrano JM. 2008. Current progress of DNA vaccine studies in humans. Expert Rev. Vaccines 7:175-191. http://dx.doi.org/10.1586/14760584.7.2.175.
25. Dujardin N, Preat V. 2004. Delivery of DNA to skin by electroporation. Methods Mol. Biol. 245:215-226. http://dx.doi.org/10.1007/978-1-59745-194-9_16.
26. Hartikka J, Sukhu L, Buchner C, Hazard D, Bozoukova V, Margalith M, Nishioka WK, Wheeler CJ, Manthorp M, Sawdey M. 2001. Electroporation-facilitated delivery of plasmid DNA in skeletal muscle: plasmid dependence of muscle damage and effect of poloxamer 188. Mol. Ther. 4:407-415. http://dx.doi.org/10.1006/mthe.2001.0483.
27. Shimao K, Takayama T, Enomoto K, Saito T, Nagai S, Miyazaki J, Ogawa K, Tahara H. 2005. Cancer gene therapy using in vivo electroporation of Flt3-ligand. Int. J. Oncol. 27:457-463.
28. Tamura T, Sakata T. 2003. Application of in vivo electroporation to cancer gene therapy. Curr. Gene Ther. 3:59-64. http://dx.doi.org/10.2174/1566523033347462.
29. Tollefsen S, Tjelle T, Schneider J, Harboe M, Wiker H, Hewinson G, Huygen K, Mathiesen I. 2002. Improved cellular and humoral immune responses against Mycobacterium tuberculosis antigens after intramuscular DNA immunisation combined with muscle electroporation. Vaccine 20:3370-3378. http://dx.doi.org/10.1016/S0264-410X(02)00289-X.
30. Zhang L, Nolan E, Kreitschitz S, Rabussay DP. 2002. Enhanced delivery of naked DNA to the skin by non-invasive in vivo electroporation. Biochim. Biophys. Acta 1572:1-9. http://dx.doi.org/10.1016/S0304-4165 (02)00270-2.
31. Liu J, Kjeken R, Mathiesen I, Barouch DH. 2008. Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J. Virol. 82:5643-5649. http://dx.doi.org/10.1128/JVI.02564-07.
32. Roos AK, Eriksson F, Timmons JA, Gerhardt J, Nyman U, Gudmundsdotter L, Brave A, Wahren B, Pisa P. 2009. Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. PLoS One 4:e7226. http://dx.doi.org/10.1371/journal.pone.0007226.
33. Bodles-Brakhop AM, Heller R, Draghia-Akli R. 2009. Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol. Ther. 17:585-592. http://dx.doi.org/10.1038/mt.2009.5.
34. Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK, Munster PN, Sullivan DM, Ugen KE, Messina JL, Heller R. 2008. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J. Clin. Oncol. 26:5896-5903.
35. Raska M, Moldoveanu Z, Novak J, Hel Z, Novak L, Bozja J, Compans RW, Yang C, Mestecky J. 2008. Delivery of DNA HIV-1 vaccine to the liver induces high and long-lasting humoral immune responses. Vaccine 26:1541-1551. http://dx.doi.org/10.1016/j.vaccine.2008.01.035.
36. Roos AK, Moreno S, Leder C, Pavlenko M, King A, Pisa P. 2006. Enhancement of cellular immune response to a prostate cancer DNA vaccine by intradermal electroporation. Mol. Ther. 13:320-327. http://dx.doi.org/10.1016/j.ymthe.2005.08.005.
37. Kay MA, He CY, Chen ZY. 2010. A robust system for production of minicircleDNAvectors. Nat. Biotechnol. 28:1287-1289. http://dx.doi.org/10.1038/nbt.1708.
38. Ahlén G, Soderholm J, Tjelle T, Kjeken R, Frelin L, Hoglund U, Blomberg P, Fons M, Mathiesen I, Sallberg M. 2007. In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J. Immunol. 179:4741-4753.
39. Dupuis M, Denis-Mize K, Woo C, Goldbeck C, Selby MJ, Chen M, Otten GR, Ulmer JB, Donnelly JJ, Ott G, McDonald DM. 2000. Distribution ofDNAvaccines determines their immunogenicity after intramuscular injection in mice. J. Immunol. 165:2850-2858.
40. Mehendale S, Thakar M, Sahay S, Kumar M, Shete A, Sathyamurthi P, Verma A, Kurle S, Shrotri A, Gilmour J, Goyal R, Dally L, Sayeed E, Zachariah D, Ackland J, Kochhar S, Cox JH, Excler JL, Kumaraswami V, Paranjape R, Ramanathan VD. 2013. Safety and immunogenicity of DNA and MVA HIV-1 subtype C vaccine prime-boost regimens: a phase I randomised trial in HIV-uninfected Indian volunteers. PLoS One 8:e55831. http://dx.doi.org/10.1371/journal.pone.0055831.
41. O'Connell RJ, Kim JH, Corey L, Michael NL. 2012. Human immunodeficiency virus vaccine trials. Cold Spring Harb Perspect Med. 2:a007351. http://dx.doi.org/10.1101/cshperspect.a007351.
42. Excler JL, Tomaras GD, Russell ND. 2013. Novel directions in HIV-1 vaccines revealed from clinical trials. Curr. Opin. HIV AIDS 8:420-430. http://dx.doi.org/10.1097/COH.0b013e3283632c26.
43. Pitisuttithum P, Rerks-Ngarm S, Bussaratid V, Dhitavat J, Maekanantawat W, Pungpak S, Suntharasamai P, Vanijanonta S, Nitayapan S, Kaewkungwal J, Benenson M, Morgan P, O'Connell RJ, Berenberg J, Gurunathan S, Francis DP, Paris R, Chiu J, Stablein D, Michael NL, Excler JL, Robb ML, Kim JH. 2011. Safety and reactogenicity of canary-pox ALVAC-HIV (vCP1521) and HIV-1 gp120 AIDSVAX B/E vaccination in an efficacy trial in Thailand. PLoS One 6:e27837. http://dx.doi.org/10.1371/journal.pone.0027837.
44. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, Benenson M, Gurunathan S, Tartaglia J, McNeil JG, Francis DP, Stablein D, Birx DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361: 2209-2220. http://dx.doi.org/10.1056/NEJMoa0908492.
45. Cai Y, Rodriguez S, Hebel H. 2009. DNA vaccine manufacture: scale and quality. Expert Rev. Vaccines 8:1277-1291. http://dx.doi.org/10.1586/erv.09.84.
46. Barouch DH. 2008. Challenges in the development of an HIV-1 vaccine. Nature 455:613-619. http://dx.doi.org/10.1038/nature07352.
47. Hokey DA, Weiner DB. 2006. DNA vaccines for HIV: challenges and opportunities. Springer Semin. Immunopathol. 28:267-279. http://dx.doi.org/10.1007/s00281-006-0046-z.
48. Hartikka J, Sawdey M, Cornefert-Jensen F, Margalith M, Barnhart K, Nolasco M, Vahlsing HL, Meek J, Marquet M, Hobart P, Norman J, Manthorpe M. 1996. An improved plasmid DNA expression vector for direct injection into skeletal muscle. Hum. Gene Ther. 7:1205-1217. http://dx.doi.org/10.1089/hum.1996.7.10-1205.
49. Valera A, Perales JC, Hatzoglou M, Bosch F. 1994. Expression of the neomycin-resistance (neo) gene induces alterations in gene expression and metabolism. Hum. Gene Ther. 5:449-456. http://dx.doi.org/10.1089/hum.1994.5.4-449.
50. Chen ZY, Riu E, He CY, Xu H, Kay MA. 2008. Silencing of episomal transgene expression in liver by plasmid bacterial backbone DNA is independent of CpG methylation. Mol. Ther. 16:548-556. http://dx.doi.org/10.1038/sj.mt.6300399.
51. Bloquel C, Bourges JL, Touchard E, Berdugo M, BenEzra D, Behar-Cohen F. 2006. Non-viral ocular gene therapy: potential ocular therapeutic avenues. Adv. Drug Deliv Rev. 58:1224-1242. http://dx.doi.org/10.1016/j.addr.2006.07.023.
52. Faurez F, Dory D, Le Moigne V, Gravier R, Jestin A. 2010. Biosafety of DNA vaccines: new generation of DNA vectors and current knowledge on the fate of plasmids after injection. Vaccine 28:3888-3895. http://dx.doi.org/10.1016/j.vaccine.2010.03.040.
53. Molnar MJ, Gilbert R, Lu Y, Liu AB, Guo A, Larochelle N, Orlopp K, Lochmuller H, Petrof BJ, Nalbantoglu J, Karpati G. 2004. Factors influencing the efficacy, longevity, and safety of electroporation-assisted plasmid-based gene transfer into mouse muscles. Mol. Ther. 10:447-455. http://dx.doi.org/10.1016/j.ymthe.2004.06.642.
54. Gracey Maniar LE, Maniar JM, Chen ZY, Lu J, Fire AZ, Kay MA. 2013. Minicircle DNA vectors achieve sustained expression reflected by active chromatin and transcriptional level. Mol. Ther. 21:131-138. http://dx.doi.org/10.1038/mt.2012.244.
55. Zhang X, Epperly MW, Kay MA, Chen ZY, Dixon T, Franicola D, Greenberger BA, Komanduri P, Greenberger JS. 2008. Radioprotection in vitro and in vivo by minicircle plasmid carrying the human manganese superoxide dismutase transgene. Hum. Gene Ther. 19:820-826. http://dx.doi.org/10.1089/hum.2007.141.
56. Klinman DM, Yamshchikov G, Ishigatsubo Y. 1997. Contribution of CpG motifs to the immunogenicity of DNA vaccines. J. Immunol. 158: 3635-3639.
57. Sato Y, Roman M, Tighe H, Lee D, Corr M, Nguyen MD, Silverman GJ, Lotz M, Carson DA, Raz E. 1996. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273:352-354. http://dx.doi.org/10.1126/science.273.5273.352.
58. Fuller DH, Loudon P, Schmaljohn C. 2006. Preclinical and clinical progress of particle-mediatedDNAvaccines for infectious diseases. Methods 40:86-97. http://dx.doi.org/10.1016/j.ymeth.2006.05.022.
59. Eriksson F, Totterman T, Maltais AK, Pisa P, Yachnin J. 2013. DNA vaccine coding for the rhesus prostate specific antigen delivered by intradermal electroporation in patients with relapsed prostate cancer. Vaccine 31:3843-3848. http://dx.doi.org/10.1016/j.vaccine.2013.06.063.
60. Rabussay DP, Nanda GS, Goldfarb PM. 2002. Enhancing the effectiveness of drug-based cancer therapy by electroporation (electropermeabilization). Technol. Cancer Res. Treat. 1:71-82.
61. Grønevik E, von Steyern FV, Kalhovde JM, Tjelle TE, Mathiesen I. 2005. Gene expression and immune response kinetics using electroporation-mediatedDNAdelivery to muscle. J. Gene Med. 7:218-227. http://dx.doi.org/10.1002/jgm.650.
62. Chiarella P, Massi E, De Robertis M, Sibilio A, Parrella P, Fazio VM, Signori E. 2008. Electroporation of skeletal muscle induces danger signal release and antigen-presenting cell recruitment independently of DNA vaccine administration. Expert Opin. Biol. Ther. 8:1645-1657. http://dx.doi.org/10.1517/14712598.8.11.1645.
63. Dietz WM, Skinner NE, Hamilton SE, Jund MD, Heitfeld SM, Litterman AJ, Hwu P, Chen ZY, Salazar AM, Ohlfest JR, Blazar BR, Pennell CA, Osborn MJ. 2013. Minicircle DNA is superior to plasmid DNA in eliciting antigen-specific CD8(+) T-cell responses. Mol. Ther. 21:1526-1535. http://dx.doi.org/10.1038/mt.2013.85.